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Enhanced Apoptosis by Functionalized Highly Reduced Graphene Oxide and Gold Nanocomposites in MCF-7 Breast Cancer Cells

  • Syed Farooq Adil
    Syed Farooq Adil
    Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
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    Orcidhttps://orcid.org/0000-0002-2768-1235
  • , 
  • Mohammed Rafi Shaik
    Mohammed Rafi Shaik
    Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
    More by Mohammed Rafi Shaik
    Orcidhttps://orcid.org/0000-0003-2937-317X
  • , 
  • Fahd A. Nasr
    Fahd A. Nasr
    Medicinal, Aromatic and Poisonous Plants Research Center, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia
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  • , 
  • Ali S. Alqahtani
    Ali S. Alqahtani
    Medicinal, Aromatic and Poisonous Plants Research Center, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia
    Department of Pharmacognosy, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia
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    Orcidhttps://orcid.org/0000-0002-1034-7441
  • , 
  • Mohammad Z. Ahmed
    Mohammad Z. Ahmed
    Medicinal, Aromatic and Poisonous Plants Research Center, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia
    Department of Pharmacognosy, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia
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  • , 
  • Wajhul Qamar
    Wajhul Qamar
    Department of Pharmacology and Toxicology, Central Laboratory, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia
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  • , 
  • Mufsir Kuniyil
    Mufsir Kuniyil
    Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
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    Orcidhttps://orcid.org/0000-0001-8038-1381
  • , 
  • Adibah Almutairi
    Adibah Almutairi
    Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
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  • , 
  • Abdulrahman Alwarthan
    Abdulrahman Alwarthan
    Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
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  • , 
  • Mohammed Rafiq H. Siddiqui
    Mohammed Rafiq H. Siddiqui
    Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
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    Orcidhttps://orcid.org/0000-0002-4703-0333
  • , 
  • Mohammad Rafe Hatshan*
    Mohammad Rafe Hatshan
    Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
    *Email: [email protected]
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  • , and 
  • Mujeeb Khan*
    Mujeeb Khan
    Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
    *Email: [email protected]
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    Orcidhttps://orcid.org/0000-0002-4088-6913
Cite this: ACS Omega 2021, 6, 23, 15147–15155
Publication Date (Web):June 4, 2021
https://doi.org/10.1021/acsomega.1c01377

Copyright © 2021 The Authors. Published by American Chemical Society. This publication is licensed under

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Abstract

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Graphene nanocomposites have gained significant interest in a variety of biological applications due to their unique properties. Herein, we have studied the apoptosis-inducing ability and anticancer properties of functionalized highly reduced graphene oxide (HRG) and gold nanoparticles (Au NPs)-based nanocomposites (AP-HRG-Au). Samples were prepared under facile conditions via simple stirring and ultrasonication. All the samples were tested for their anticancer properties against different human cancer cell lines including lung (A549), liver (HepG2), and breast (MCF-7) cancer cells using doxorubicin as a positive control. In order to enhance the solubility and bioavailability of the sample, HRG was functionalized with 1-aminopyrene (1-AP) as a stabilizing ligand. The ligand also facilitated the homogeneous growth of Au NPs on the surface of HRG by offering chemically specific binding sites. The synthesis of nanocomposites and the surface functionalization of HRG were confirmed by UV–Vis, powder X-ray diffraction, and Fourier transform infrared spectroscopy. The structure and morphology of the as-prepared nanocomposites were established by high-resolution transmission electron microscopy. Because of the functionalization, the AP-HRG-Au nanocomposite exhibited enhanced physical stability and high dispersibility. A comparative anticancer study of pristine HRG, nonfunctionalized HRG-Au, and 1-AP-functionalized AP-HRG-Au nanocomposites revealed the enhanced apoptosis ability of functionalized nanocomposites compared to the nonfunctionalized sample, whereas the pristine HRG did not show any anticancer ability against all tested cell lines. Both HRG-Au and AP-HRG-Au have induced a concentration-dependent reduction in cell viability in all tested cell lines after 48 h of exposure, with a significantly higher response in MCF-7 cells compared to the remaining cells. Therefore, MCF-7 cells were selected to perform detailed investigations using apoptosis assay, cell cycle analysis, and reactive oxygen species measurements. These results suggest that AP-HRG-Au induces enhanced apoptosis in human breast cancer cells.

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1. Introduction

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Nowadays, increasing cases of multidrug resistant diseases are a cause of serious concern among scientists and medical professionals, which demands immediate solutions, including the development of novel therapeutic agents. (1,2) Among these ailments, cancer is one of the deadliest diseases requiring a challenging task of developing innovative therapeutic strategies. (3) Besides resistance to the drugs, the therapeutic treatment of cancer also involves a major obstacle, which is the development of undesired side effects and complications. In this regard, the strategy for inducing apoptosis using novel therapeutic agents has gained considerable attention in cancer treatment. (4) Over the past decades, a variety of nanomaterials have shown great potential in clinical studies as anticancer drugs, drug carriers, or diagnostic tools. (5,6) From the diverse range of nanomaterials, graphene nanocomposites have gained specific attention due to the excellent physicochemical properties of graphene like the large surface area, superb electrical and electronic properties, and its unique two-dimensional geometry, which offer flexible platform for the immobilization of various substances, including drugs, biomolecules, etc. (7−9)
So far, various studies have highlighted the potential applications of graphene-based materials in cancer therapy, including the benefits of functionalized graphene-based nanocomposites for specific targeting of affected cells to overcome drug resistance and minimize the side effects. (10) Especially, the fabrication of graphene nanocomposites involving metallic nanoparticles remarkably enhances the anticancer properties of the material due to the synergistic effect and unique physicochemical properties of the combined materials. (11) Recently, metallic nanoparticles comprising silver and gold have been incorporated on the surface of graphene to attain graphene nanocomposites for unique biological applications like bio-imaging and cancer detection and therapy. (12,13) Particularly, gold offers several benefits over other nanoparticles owing to its distinctive physicochemical properties like surface plasmon resonance (SPR) and the capability to bind a variety of biomolecules. (14−16) However, metallic nanoparticle (NP)-based graphene composites generally suffer from aggregation owing to the strong van der Waals interactions, low density, and inhomogeneous distribution of inorganic nanoparticles on the surface, which adversely affect their properties for potential applications. (17) This is typically avoided through the surface functionalization of graphene. (18)
Commonly, graphene oxide (GO), an oxidized derivative of graphene, has been one of the most promising carbonaceous materials for cancer therapy due to its versatile surface chemistry, which allows easy functionalization of materials and high water dispersibility. (19,20) However, the random presence of a large number of oxygenated groups on the surface of GO limits the prospects of homogeneous and controlled functionalization of the material, which is beneficial in extracting the full potential of graphene-based materials in biological applications. (21) To overcome this, another derivative of graphene, such as highly reduced graphene oxide (HRG), can be applied, which consists of similar graphitic domains, defects, and residual oxygenated groups on the surface but in far lesser number than GO. (22) The surface properties of HRG can also be further improved through both covalent and noncovalent functionalization to avoid agglomeration and enhance biological properties including the cellular uptakes, etc. (23)
Compared to covalent functionalization, which may disrupt the sp2 structure of the graphene lattice, noncovalent functionalization does not disrupt the structure and retains the electronic properties of the material while simultaneously introducing new chemical groups on the surface. (24,25) Noncovalent functionalization of HRG composites through π–π interactions, hydrogen bonding, van der Waals forces, etc. leads to enhanced dispersibility, binding capacity, biocompatibility, and reactivity of the resulting materials. (26) Among various methods, noncovalent functionalization of HRG through π–π interactions using polycyclic aromatic “π–π stacking” molecules, such as pyrene, anthracene, and coronene as stabilizing agents, has gained interest recently. (27−29) In our previous study, we have developed a novel approach of employing a hard soft acid base concept to prepare HRG palladium (Pd) nanocomposites (HRG-Pd) using 1-aminopyrene (1-AP) as a stabilizing agent. (30) In this case, 1-AP not only stabilized the surface of HRG through noncovalent π–π interactions but also facilitated the homogeneous nucleation and growth of Pd NPs on the surface of HRG.
In this work, we demonstrate the effect of functionalization on the biological properties of graphene and its resulting nanocomposite. For this purpose, we have applied the concept of noncovalent functionalization to homogeneously anchored Au NPs on the surface of HRG. To study the benefits of noncovalent functionalization in biological applications, the in vitro anticancer activity of the as-prepared 1-AP-functionalized HRG and gold (Au) NP-based nanocomposites (AP-HRG-Au) is obtained (Scheme 1). In addition, for the purpose of comparison, the anticancer properties of pristine HRG, functionalized AP-HRG-Au, and nonfunctionalized HRG-Au nanocomposites have also been investigated. All the samples, namely, HRG, HRG-Au, and, AP-HRG-Au, were screened for their antiproliferative effects using an MTT assay against lung (A549), liver (HepG2), and breast (MCF-7) cancer cell lines using doxorubicin as a positive control. To the best of our knowledge, graphene gold nanocomposites have been rarely investigated as therapeutic agents in cancer treatment, and moreover, studies about the benefits of controlled distribution of NPs on the surface substrates in biological applications have not been reported so far.

Scheme 1

Scheme 1. Graphical Representation of the Preparation of Functionalized (AP-HRG-Au) and Nonfunctionalized (HRG-Au) Graphene-Gold Nanocomposites and Their Anticancer Properties
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2. Results and Discussion

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Typically, the agglomeration of nanoparticles in biological systems seriously alters their mobility, size, and surface properties, often complicating their phase behavior and biodistribution. (31) Agglomeration of nanoparticles results in the formation of slow or even immobile materials, which promotes their local accumulation and can significantly affect their overall cellular uptake. (32,33) Aggregation of nanoparticles is typically inhibited through various surface functionalization approaches. In this study, to achieve nonaggregated, homogeneously distributed gold NPs on the surface of graphene, polycyclic aromatic hydrocarbon, namely, 1-aminopyrene (1-AP), is used, which noncovalently functionalizes the sample through π–π interactions. In this case, 1-AP has displayed a dual role, and not only has it stabilized the surface of HRG but its suspended amino group (NH2) also provided active sites for the homogeneous nucleation and growth of gold NPs on the surface of HRG. The biological application of surface-functionalized AP-HRG-Au is demonstrated through a study of anticancer properties of the sample against various cell lines. To investigate the effect of functionalization on its biological properties, the anticancer properties of the functionalized sample (AP-HRG-Au) was compared with its nonfunctionalized counterpart (HRG-Au) and pristine HRG.
Initially, the effect of functionalization of HRG on the dispersion quality of the resulting AP-HRG-Au is assessed and compared with other two samples including pristine HRG and nonfunctionalized HRG-Au. To do this, dispersions of the samples were prepared via sonication by taking 5 mg of each sample in 10 mL of deionized water. Among all the samples, functionalized AP-HRG-Au demonstrated superior dispersion quality, as the dispersion remained stable even after several hours. However, pristine HRG and HRG-Au exhibited poor dispersibility, as the samples settled down after some time (cf. Figure 1).

Figure 1

Figure 1. Digital images of the aqueous dispersions of highly reduced graphene oxide (HRG), nonfunctionalized HRG-Au (gold), and 1-AP-functionalized HRG-Au nanocomposites (AP-HRG-Au). The dispersions were prepared by sonicating 5 mg of each sample in 10 mL of water.

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The functionalization of HRG with 1-AP and the formation of HRG-Au and AP-HRG-Au were initially confirmed by UV analysis. For this, the UV–vis spectra of pristine 1-aminopyrene (1-AP), HRG, Au-HRG, and AP-HRG-Au were compared (cf. Figure 2). 1-AP exhibits three characteristic absorption peaks at ∼242, ∼285, and 360 nm (black line, Figure 2), while the characteristic peak of HRG appears at ∼270 nm (red line, Figure 2). All peaks of 1-AP and HRG exist in AP-HRG-Au (green line, Figure 2), which confirms the successful functionalization of HRG with 1-AP. In addition, the spectrum of AP-HRG-Au also exhibits an absorption peak at ∼540 nm, which is a typical SPR peak of gold nanoparticles, and this points toward the formation of a functionalized HRG-Au nanocomposite. (34) On the other hand, the spectrum of nonfunctionalized HRG-Au (blue line, Figure 2) only exhibits characteristic peaks of HRG and Au NPs. Similarly, the successful functionalization and formation of nanocomposites have also been confirmed by FT-IR spectroscopy by comparing the respective IR spectra of 1-AP, HRG, HRG-Au, and AP-HRG-Au, as shown in Figure 3. The FT-IR spectra of pristine 1-AP (black line, Figure 3) and AP-HRG-Au (green line, Figure 3) closely resemble each other, as majority of IR peaks belonging to 1-AP, such as the IR peaks corresponding to the aromatics of 1-AP between 800 and 1700 cm–1, are also present in the AP-HRG-Au spectrum. Meanwhile, the corresponding IR spectrum of HRG-Au (blue line, Figure 3) demonstrates different characteristics due to the absence 1-AP in the composite. This clearly confirms the functionalization of HRG with 1-AP in AP-HRG-Au.

Figure 2

Figure 2. UV spectra of 1-AP, pristine HRG, nonfunctionalized HRG-Au, and 1-AP-functionalized AP-HRG-Au nanocomposites.

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Figure 3

Figure 3. FT-IR spectra of 1-AP, pristine HRG, nonfunctionalized HRG-Au, and 1-AP-functionalized AP-HRG-Au nanocomposites.

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In addition, XRD analysis also indicated the formation of HRG-Au and AP-HRG-Au nanocomposites besides confirming the crystallinity and phase purity of the samples. The XRD patterns of HRG, HRG-Au, and AP-HRG-Au are shown in Figure 4. Pristine HRG typically exhibits a broad reflection at 22.4° (red line, Figure 4), which is present in the XRD patterns of both HRG-Au (blue line, Figure 4) and AP-HRG-Au (green line, Figure 4). Apart from this reflection, both nanocomposites also demonstrate various reflections in their corresponding XRD patterns, which are similar to the XRD reflections of pure gold nanoparticles. For example, the XRD peaks at 38° (111), 44° (200), 64° (220), and 77° (311) represent Bragg’s reflections of the cubic structure of metallic gold (JCPDS no. 04-0784). The mean size of Au NPs on the surface of HRG in AP-HRG-Au was found to be 3.27 ± 0.02 nm (Table 1), which was calculated using the Debye–Scherrer’s equation (35)
where “hkl” are the Miller indices and “a” is edge lengths

Figure 4

Figure 4. XRD patterns of pristine HRG, nonfunctionalized HRG-Au, and 1-AP-functionalized AP-HRG-Au nanocomposites.

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Table 1. XRD Results and Crystallographic Data of the Au Nanoparticles Existing in the AP-HRG-Au Nanocompositea
2θ (°) FWHM (°) hkl a (nm) sin θ (radian) cos θ (radian) d (nm) D (nm)
38.1 2.6 111 0.4 0.326443 0.9452 0.24 3.22
44.3 2.9 200 0.4 0.3769579 0.92623 0.20 3.28
64.5 3.2 220 0.4 0.5334254 0.845847 0.14 3.29
77.5 3.2 311 0.4 0.6257055 0.780059 0.12 3.22
81.6 2.6 222 0.4 0.6536024 0.756838 0.12 3.32
a

Note: X-ray wavelength λ (nm) = 0.15406.

The size and morphology of Au NPs on the surface of HRG in AP-HRG-Au were determined by HRTEM (high-resolution transmission microscopy), as shown in Figure 5a–c. The prepared composites were subjected to HRTEM analysis by dispersing the prepared composites in hexane and using a sonicator water bath, and then, the dispersed solution was dropped on the TEM grid, which was dried for 6 h at 60 °C in an oven. The size (<4 nm) of spherical-shaped Au NPs can be seen on the surface of HRG in AP-HRG-Au. These NPs are homogeneously and densely distributed on the surface of HRG, which is facilitated by the dual function of 1-AP including the stabilization of HRG and promotion of nucleation and growth of Au NPs. The π–π interactions mediated noncovalent functionalization of HRG involving the pyrenyl ring of 1-AP and the basal plane of HRG, which largely prevented the aggregation of HRG nanosheets, whereas the amino group offered active nucleation sites for the effective growth of NPs. This resulted in considerable enhancement in dispersibility of the nanocomposite (AP-HRG-Au), which improved the biological activity of the sample. In addition, the elemental composition of the as-prepared AP-HRG-Au was also measured by EDX, as shown in Figure 5d. The presence of high carbon content together with oxygen and gold indicates the formation of the AP-HRG-Au nanocomposite.

Figure 5

Figure 5. HRTEM images of a 1-AP-functionalized AP-HRG-Au nanocomposite: (a) overview and (b) magnified images of AP-HRG-Au. (c) EDX spectrum of AP-HRG-Au and (d) particle size distribution graph of AP-HRG-Au.

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2.1. Anticancer Activity

To compare the biological activity of as-prepared HRG, nonfunctionalized HRG-Au, and functionalized AP-HRG-Au, an MTT assay was performed, which assessed the reduction in cell viability by nanocomposites. It was observed that both HRG-Au and AP-HRG-Au induced a concentration-dependent reduction in cell viability in all tested cell lines including lung (A549), liver (HepG2), and breast (MCF-7). However, after 48 h of exposure, a significantly higher response was observed in MCF-7 cells compared to other cells. Notably, HRG did not display any activity against all tested cells, which may be due to the low dispersibility of the sample in aqueous solution and/or due to the absence of gold NPs. The IC50 (concentration reduced the viability of the cells to half) values are shown in Table 2. The dose–response curve for HRG-Au and AP-HRG-Au are presented in Figure 6. Since MCF-7 cells were the most responsive to HRG-Au and AP-HRG-Au, therefore it was selected for the remaining assays.

Figure 6

Figure 6. Effect of (a) 1-AP-functionalized AP-HRG-Au and (b) nonfunctionalized HRG-Au on cell viability after 48 h treatment. The cell viability was determined using an MTT assay. Results are expressed as means ± SD for three replicate values for each concentration.

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Table 2. IC50 Values of Pristine HRG, Nonfunctionalized HRG-Au, Functionalized AP-HRG-Au, and Doxorubicin as a Control
  IC50 values ± SD (μg/mL)
fraction A549 HepG2 MCF-7
HRG      
HRG-Au 72.5. ± 1.5 49.8 ± 1.2 45.6 ± 1.6
AP-HRG-Au 59.7 ± 1.3 47.7 ± 1.6 43.5 ± 1.5
doxorubicin 0.8 ± 0.2 1 ± 0.3 0.9 ± 0.4

2.2. HRG-Au- and AP-HRG-Au-Induced Cell Cycle Arrest

In order to determine whether cell growth inhibition was associated with cell cycle arrest, cell cycle analysis was performed against MCF-7 cells. Upon treatment with AP-HRG-Au and HRG-Au, the percent of cell populations in the G1 phase increased from 50.7 to 62 and 55.1%, respectively. This increase was accompanied by a decrease in the percentage in the phases of G2M and S cell population for AP-HRG-Au and HRG-Au, respectively (Figure 7).

Figure 7

Figure 7. AP-HRG-Au and HRG-Au induces G1 arrest in MCF-7 cells. MCF-7 cells were treated with IC50 concentrations for 48 h. Cells were fixed by ethanol and stained with PI. Cell cycle progression was assessed by flow cytometry.

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2.3. Apoptosis Detection

Flow cytometry was further employed to quantify apoptotic or necrotic death after treatment with AP-HRG-Au and HRG-Au for 48 h. As shown below (Figure 8), approximately 12.2% of the cells stained positive for apoptosis events (5% early apoptosis, +7.2 late apoptosis) after AP-HRG-Au treatment. Cell treatment with HRG-Au also caused changes in the percent of cells undergoing apoptosis compared to the control. A necrotic cell death was also observed after treatment with both particles (Figure 8).

Figure 8

Figure 8. Induction of apoptosis by AP-HRG-Au and HRG-Au in MCF-7 cells. Fluorescence intensity of Annexin V and PI as indication of apoptosis induced by IC50 concentrations of each particle.

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2.4. AHRG and APHRG Stimulate ROS Production

Next, we examined the cellular ROS levels in MCF-7 cells to determine whether AHRG and APHRG induced oxidative stress. It was found that MCF-7 cell populations differ in fluorescence intensity. Nontreated cells displayed low ROS content, while treatment of the cells with AHRG and APHRG leads to an increase in cell number with relatively higher ROS content, which mediated cell damage and initiated apoptotic cell death (Figure 9).

Figure 9

Figure 9. Flow cytometry analysis of ROS generation in MCF-7 cells treated with AP-HRG-Au and HRG-Au for 24 h. MCF-7 cells were treated with IC50 concentrations of both particles for 48 h and then stained as described in the Experimental Details. The left quarter gray dots represent unstained cells, and the right quarter red dots represent stained cells.

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3. Experimental Details

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3.1. Chemicals

Graphite powder (200 mesh) was purchased from Alfa Aesar. 1-Aminopyrene, gold(III) chloride trihydrate, concentrated sulfuric acid, potassium permanganate, sodium nitrate, hydrogen peroxide, hydrazine hydrate, and other organic solvents were purchased from Sigma-Aldrich and used without purification.

3.2. Preparation and Functionalization of HRG with 1-Aminopyrene

HRG was prepared according to the method presented in our previous literature. (36−39) HRG (50 mg) was dispersed in 20 mL of methanol via sonication for 30 min. Separately, 1-AP (50 mg) solution was prepared in methanol (20 mL) using equivalent weight percent of HRG. The HRG dispersion and 1-AP solution were mixed and stirred at room temperature (48 h). After this, stirring was stopped and the mixture was subjected to sonication at a lower temperature (20 °C) for 6 h. The resulting mixture was centrifuged at a lower speed (4000 rpm) for a period of 3 h to remove excess of 1-AP. To remove the remaining unadsorbed content of 1-AP, the as-obtained black powder was again dispersed in 20 mL of fresh methanol and sonicated at a lower temperature (20 °C) for 30 min. Later, the black dispersion was isolated via centrifugation (9000 rpm, 15 min), and the product was separated by simple decanting of suspension. The process continued many times until the leftover liquid turned colorless. Finally, the as-obtained solid was dried overnight in vacuum.

3.3. Preparation of 1-AP-Functionalized Graphene and Gold Composites (AP-HRG-Au)

AP-HRG-Au was prepared using equivalent (1:1 weight ratio) contents of freshly functionalized HRG and gold precursors. To begin with, 10 mg of functionalized HRG was dispersed in 10 mL of ethanol, and separately, 10 mg of HAuCl4·3H2O was dissolved in 10 mL of ethanol. Both the solutions were mixed together and sonicated for 1 h, and subsequently, the product was isolated via centrifugation (9000 rpm). The resulting product was redispersed in 20 mL of deionized water for further use. HRG-Au was also prepared in a similar manner; however, in this case, nonfunctionalized HRG was used instead of functionalized HRG.

3.4. Characterization

The preparations of AP-HRG-Au and HRG-Au nanocomposites were confirmed by UV–vis spectrophotometry (Perkin Elmer Lambda 35 (Waltham, MA, USA)), HRTEM and EDX (JEM 2100F (JEOL, Tokyo, Japan)), FT-IR (Perkin Elmer 1000 FT-IR spectrometer) spectroscopy (Agilent (single quadrupole) MSD-5975C detector, Agilent Technologies Inc., USA; MS was acquired in EI mode (scan range: m/z 45–600, ionization energy: 70 eV)), and XRD (D2 Phaser X-ray diffractometer (Bruker, Germany), Cu Kα radiation (k = 1.5418 A°)).

3.5. Anticancer Activity (MTT Assay)

Pristine HRG, HRG-Au, and AP-HRG-Au were assessed for their anticancer activity in a panel of three human cancer cell lines, namely, lung (A549), liver (HepG2), and breast (MCF-7) using the MTT method as described in a previous study. (40)
Briefly, different concentrations of each sample were added to the cells (5 × 104/well) after 24 h incubation in a 96-well plate and doxorubicin was used as a positive control. After incubation for 48 h, 10 μL of the MTT solution (5 mg/mL, prepared in PBS) was added to each well. The cells were further incubated for another 4 h. Excess medium was removed and replaced by 100 μL of acidified isopropanol in each well to dissolve the formazan crystals. Optical densities were determined using a microplate spectrophotometer (BioTek, USA) at 570 nm. IC50 (50% inhibition of cell growth) was calculated using OriginPro 8.5 software.

3.6. Cell Cycle Analysis

The effects of HRG-Au and AP-HRG-Au on the cell cycle distribution of MCF-7 cells were determined by flow cytometric analysis as earlier reported. (41) Briefly, treated or untreated cells were harvested and washed with cold PBS twice. Following fixation with 70% ethanol at 4 °C for 4 h, cells were stained with freshly prepared DNA-staining solution containing propidium iodide (PI, 50 μg/mL) and RNase A (100 μg/mL). Stained cells were then subjected to analysis using a flow cytometer (flow cytometry, Beckman Coulter, USA). CXP software V. 3.0 was used to determine cell phase distributions.

3.7. Apoptosis Assay (Annexin V-FITC/PI)

Apoptosis detection was performed according to a double stain apoptosis detection kit protocol (BioLegend, CA, USA). In brief, MCF-7 cells were cultured in six-well plates for 24 h before treatment with IC50. After 24 h incubation, treated and control cells were collected and washed with cold PBS. Annexin-binding buffer (1×, 100 μL) was used to resuspend cell pellets, which were then stained with both Annexin V-FITC and propidium iodide (PI) dyes for 15 min in the dark. To this mixture, 400 μL of 1× Annexin buffer was added before analysis using a Cytomics FC500 flow cytometer (Beckman Coulter, USA). Data obtained from the flow cytometer were analyzed using CXP software V. 3.0.

3.8. ROS Measurement

ROS detection reagents (cat. no.: 88-5930, Invitrogen) were utilized to detect the level of ROS in MCF-7 cells. In brief, a working solution (1×) was prepared from ROS assay stain solution. MCF-7 cells were seeded in six-well plates and exposed to HRG-Au and AP-HRG-Au for 48 h. Cells were then harvested and washed twice with PBS and resuspended with 100 μL of working solution. Thereafter, cells were incubated for 60 min and fluorescence was read at 490 nm excitation and 520 nm emission using the Cytomics FC500 flow cytometer (Beckman Coulter, USA).

4. Conclusions

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Herein, we have investigated the apoptosis-induced anticancer activity of 1-AP-functionalized Au-HRG nanocomposite (AP-HRG-Au). The anticancer property of the functionalized nanocomposite is also compared with those of pristine HRG and its nonfunctionalized counterpart. Functionalization of HRG enhanced the aqueous dispersibility of the sample due to the dual role of the 1-AP ligand, which effectively prevented the aggregation of HRG nanosheets and also offered specific nucleation sites for the growth of Au NPs on the surface of graphene. Due to this, functionalized AP-HRG-Au demonstrated slightly better anticancer properties when compared to the nonfunctionalized nanocomposite (HRG-Au). Flow cytometry and the results of ROS generation tests point toward the apoptosis-induced cell death by both AP-HRG-Au and HRG-Au, while the former was found to be more effective against MCF-7 cells.

Author Information

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  • Corresponding Authors
  • Authors
    • Syed Farooq Adil - Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia;  Orcidhttps://orcid.org/0000-0002-2768-1235
    • Mohammed Rafi Shaik - Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia;  Orcidhttps://orcid.org/0000-0003-2937-317X
    • Fahd A. Nasr - Medicinal, Aromatic and Poisonous Plants Research Center, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia
    • Ali S. Alqahtani - Medicinal, Aromatic and Poisonous Plants Research Center, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia;  Department of Pharmacognosy, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia;  Orcidhttps://orcid.org/0000-0002-1034-7441
    • Mohammad Z. Ahmed - Medicinal, Aromatic and Poisonous Plants Research Center, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia;  Department of Pharmacognosy, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia
    • Wajhul Qamar - Department of Pharmacology and Toxicology, Central Laboratory, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia
    • Mufsir Kuniyil - Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia;  Orcidhttps://orcid.org/0000-0001-8038-1381
    • Adibah Almutairi - Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
    • Abdulrahman Alwarthan - Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
    • Mohammed Rafiq H. Siddiqui - Department of Chemistry, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia;  Orcidhttps://orcid.org/0000-0002-4703-0333
  • Notes
    The authors declare no competing financial interest.

Acknowledgments

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The authors extend their appreciation to the Deanship of Scientific Research at King Saud University for funding this work through the Research Group no. RG-1436-032.

References

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This article references 41 other publications.

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    Sanad, Mohamed Fathi; Shalan, Ahmed Esmail; Bazid, Shereen Magdy; Abu Serea, Esraa Samy; Hashem, Elhussein M.; Nabih, Shimaa; Ahsan, Md. Ariful
    RSC Advances (2019), 9 (53), 31021-31029CODEN: RSCACL; ISSN:2046-2069. (Royal Society of Chemistry)
    There is no doubt that cancer is now one of the most formidable diseases in the world; despite all the efforts and research, common treatment routes, including chemotherapy, photodynamic therapy, and photothermal therapy, suffer from different limitations in terms of their efficiency and performance. For this reason, different strategies are being explored to improve the efficiency of the traditional drugs reported to date. In this study, we have redirected the function of one of these drugs (5-fluorouracil, 5-FU) by combining it with a graphene-gold nanocomposite in different molar ratios that has been exceedingly used for biol. research development. The high activity of the graphene-gold material enables it to produce reactive oxygen and ions, which display good anticancer and antioxidant activity through the scavenging of the DPPH, SOD and GPx radicals; in addn., different characterizations have been used to confirm the structure and morphol. of the obtained samples. Highly potent cytotoxicity against the MCF-7 cells was achieved with the drug combination contg. the nanocomposite. All the results, including those obtained via cytometry, indicate that the combination of 5% graphene-gold nanocomposites with 5-FU exhibits a higher antitumor impact and more drug stability than pure 5-FU.
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    Xu, J.; Wang, Y.; Hu, S. Nanocomposites of graphene and graphene oxides: Synthesis, molecular functionalization and application in electrochemical sensors and biosensors. A review. Microchim. Acta 2017, 184, 1– 44,  DOI: 10.1007/s00604-016-2007-0
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    Nanocomposites of graphene and graphene oxides: Synthesis, molecular functionalization and application in electrochemical sensors and biosensors. A review
    Xu, Junhui; Wang, Yazhen; Hu, Shengshui
    Microchimica Acta (2017), 184 (1), 1-44CODEN: MIACAQ; ISSN:0026-3672. (Springer-Verlag GmbH)
    Functionalized nanocomposites based on various type of graphene nanomaterials including graphene, graphene oxides (GOs), and doped graphene (oxides) are widely used as materials for various sensors that can display high sensitivity, selectivity and stability. This review with 347 refs. summarizes advances in the prepn. and functionalization of graphene nanocomposites for the application of electrochem. sensors and biosensors. Following a general introduction into the field, the article is divided into subsections on (a) the synthesis and functionalization of nanocomposites (made from graphene, various kinds of GOs, heteroatom-doped GOs), (b) on methods for functionalization of composites (with other carbon nanomaterials, metal nanoparticles, metal oxide and metal sulfide nanoparticles), (c) on functionalization with inorg. materials including polyoxometalates, hexacyanoferrates, minerals), (d) on functionalization with org. materials such as amino acids, surfactants, org. dyes, ionic liqs., macrocycles (including cyclodextrins, crown ethers and calixarenes), and (e) on functionalization with organometallics and with various other org. compds., (f) on functionalizations with polymers such as conventional polymers, polyelectrolytes, conducting polymers, molecularly imprinted polymers, (g) on functionalization with biomols. including proteins and nucleic acids. Other subsections cover flexible graphene and GO based nanocomposites and 3D composites. Application of graphene and GO nanocomposites are then covered in a in large section that comprises electrochem. sensors and biosensors (based on voltammetry, amperometry, potentiometry, impedimetry, electrochemiluminescence, photoelectrochem., field effect transistors, electrochem. immunosensors) with specific subsections on gas sensors, enzymic biosensors and gene sensors. A concluding section covers current challenges and perspectives of graphene and GO based (bio)sensing. [Figure not available: see fulltext.].
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  18. 18
    Yang, K.; Feng, L.; Hong, H.; Cai, W.; Liu, Z. Preparation and functionalization of graphene nanocomposites for biomedical applications. Nat. Protoc. 2013, 8, 2392– 2403,  DOI: 10.1038/nprot.2013.146
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    18
    Preparation and functionalization of graphene nanocomposites for biomedical applications
    Yang, Kai; Feng, Liangzhu; Hong, Hao; Cai, Weibo; Liu, Zhuang
    Nature Protocols (2013), 8 (12), 2392-2403CODEN: NPARDW; ISSN:1750-2799. (Nature Publishing Group)
    Functionalized nano-graphene- and graphene-based nanocomposites have gained tremendous attention in the area of biomedicine in recent years owing to their biocompatibility, the ease with which they can be functionalized and their properties such as thermal and elec. cond. Potential applications for functionalized nanoparticles range from drug delivery and multimodal imaging to exploitation of the elec. properties of graphene toward the prepn. of biosensing devices. This protocol covers the prepn., functionalization and bioconjugation of various graphene derivs. and nanocomposites. Starting from graphite, the prepns. of graphene oxide (GO), reduced GO (RGO) and magnetic GO-based nanocomposite, as well as how to functionalize them with biocompatible polymers such as polyethylene glycol (PEPEG), are described in detail. We also provide procedures for 125I radiolabeling of PEPEGylated GO and the prepn. of GO-based gene carriers; other bioconjugation approaches including drug loading, antibody conjugation and fluorescent labeling are similar to those described previously and used for bioconjugation of PEPEGylated carbon nanotubes. We hope this article will help researchers in this field to fabricate graphene-based bioconjugates with high reproducibility for various applications in biomedicine. The sample prepn. procedures take various times ranging from 1 to 2 d.
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  19. 19
    Singh, D. P.; Herrera, C. E.; Singh, B.; Singh, S.; Singh, R. K.; Kumar, R. Graphene oxide: An efficient material and recent approach for biotechnological and biomedical applications. Mater. Sci. Eng., C 2018, 86, 173– 197,  DOI: 10.1016/j.msec.2018.01.004
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    Graphene oxide: An efficient material and recent approach for biotechnological and biomedical applications
    Singh, Dinesh Pratap; Herrera, Carlos Eugenio; Singh, Brijesh; Singh, Shipra; Singh, Rajesh Kumar; Kumar, Rajesh
    Materials Science & Engineering, C: Materials for Biological Applications (2018), 86 (), 173-197CODEN: MSCEEE; ISSN:0928-4931. (Elsevier B.V.)
    The two-dimensional (2D) deriv. of graphite termed graphene has widespread applications in various frontiers areas of nanoscience and nanotechnologies. Graphene in its oxidized form named as graphene oxide (GO) has a mixed structure equipped with various oxygen contg. functional groups (epoxy, hydroxyl, carboxylic and carbonyl etc.) provides attachment sites to various biol. mols. including protein, DNA (DNA), RNA (RNA) etc. The attached biol. mols. with the help of functional groups make it a promising candidate in research field of biotechnol. and biomedical applications. The ease of processability and functionalization in aq. soln. due to available functional groups, amphiphilicity, better surface enhanced Raman scattering (SERS), fluorescence and its quenching ability better than graphene make GO a promising candidate for various biol. applications. The amphipathetic nature and high surface area of the GO not only prep. it as a biocompatible, soft and flexible intra/inter cellular carrier but also provides long-term biocompatibility with very low cytotoxicity. Inspite of this, still we lack a very recent review for advanced biol. applications of graphene oxide. This review deals the bio application of GO and the recent advancement as a biosensors, antibacterial agent, early detection of cancer, cancer cell imaging/mapping, targeted drug delivery and gene therapy etc.
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  20. 20
    Zhu, J.; Li, B.; Xu, M.; Liu, R.; Xia, T.; Zhang, Z.; Xu, Y.; Liu, S. Graphene Oxide Promotes Cancer Metastasis through Associating with Plasma Membrane To Promote TGF-β Signaling-Dependent Epithelial–Mesenchymal Transition. ACS Nano 2020, 14, 818– 827,  DOI: 10.1021/acsnano.9b07891
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    20
    Graphene Oxide Promotes Cancer Metastasis through Associating with Plasma Membrane To Promote TGF-β Signaling-Dependent Epithelial-Mesenchymal Transition
    Zhu, Jianqiang; Li, Bin; Xu, Ming; Liu, Rui; Xia, Tian; Zhang, Zhihong; Xu, Yong; Liu, Sijin
    ACS Nano (2020), 14 (1), 818-827CODEN: ANCAC3; ISSN:1936-0851. (American Chemical Society)
    Nanomedicines are being developed to treat diverse diseases; however, inadvertent or unintended health effects has to be considered, esp. for those targeting cancers. For cancers, occurrence of metastasis hints an advanced phase of cancer progression, nanomedicines per se should be evaluated for their effects on existing metastatic tumors and triggering metastases. Graphene based 2D nanomaterials, such as graphene oxide (GO), due to its unique characteristics, has been extensively studied for biomedical applications including cancer therapy. However, the potential effect of GO on metastasis has not been detd. yet. Herein, we found that low-dose GO could induce significant morphol. and structural changes of cellular membrane within cancer cells, suggesting epithelial-mesenchymal transition (EMT), with enhanced invasion/migration and the alterations of representative EMT indicators in GO-treated cells. These changes resulted in enhanced lung metastasis of cancer cells in various metastasis models. The mechanistic investigations unveiled that GO elevated the protein levels of TGF-β receptor, leading to constitutively activated TGF-β-Smad2/3 signaling pathway that drives the EMT. Collectively, our findings enhance the understanding of the unintended side and detrimental effects of GO nanosheets in increasing the progression of metastatic tumors. Thus, the likelihood of pro-EMT effects upon low-dose GO exposure should be considered when developing GO nanomedicines.
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    Silvestrini, S.; De Filippo, C. C.; Vicentini, N.; Menna, E.; Mazzaro, R.; Morandi, V.; Ravotto, L.; Ceroni, P.; Maggini, M. Controlled functionalization of reduced graphene oxide enabled by microfluidic reactors. Chem. Mater. 2018, 30, 2905– 2914,  DOI: 10.1021/acs.chemmater.7b04740
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    Controlled Functionalization of Reduced Graphene Oxide Enabled by Microfluidic Reactors
    Silvestrini, Simone; De Filippo, Christian C.; Vicentini, Nicola; Menna, Enzo; Mazzaro, Raffaello; Morandi, Vittorio; Ravotto, Luca; Ceroni, Paola; Maggini, Michele
    Chemistry of Materials (2018), 30 (9), 2905-2914CODEN: CMATEX; ISSN:0897-4756. (American Chemical Society)
    The authors report the use of microfluidics to functionalize suspended reduced graphene oxide flakes through the addn. of aryl radical, generated in situ by reaction between aryl amines and isopentyl nitrite. Microfluidic enabled a tight control of temp., reaction times, and stoichiometric ratios, making it possible to tune the growth of oligomers on the surface of the flakes, which in turn affects the interactions of the functional material with the surrounding environment. Probably shear stress phenomena within the reactor may play a role in the chem. of graphene materials by providing a const. driving force toward exfoliation of the layered structures. Scale-up of the functionalization process is also reported along with the grafting of dyes based on squaric acid cores. Photophys. characterization of the dye-modified flakes proves that the microfluidic approach is a viable method toward the development of new materials with tailored properties.
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  22. 22
    Khan, M.; Al-Marri, A. H.; Khan, M.; Mohri, N.; Adil, S. F.; Al-Warthan, A.; Siddiqui, M. R. H.; Alkhathlan, H. Z.; Berger, R.; Tremel, W.; Tahir, M. N. Pulicaria glutinosa plant extract: a green and eco-friendly reducing agent for the preparation of highly reduced graphene oxide. RSC Adv. 2014, 4, 24119– 24125,  DOI: 10.1039/C4RA01296H
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    Pulicaria glutinosa plant extract: a green and eco-friendly reducing agent for the preparation of highly reduced graphene oxide
    Khan, Mujeeb; Al-Marri, Abdulhadi H.; Khan, Merajuddin; Mohri, Nils; Adil, Syed Farooq; Al-Warthan, Abdulrahman; Siddiqui, Mohammed Rafiq H.; Alkhathlan, Hamad Z.; Berger, Rudiger; Tremel, Wolfgang; Tahir, Muhammad Nawaz
    RSC Advances (2014), 4 (46), 24119-24125CODEN: RSCACL; ISSN:2046-2069. (Royal Society of Chemistry)
    The environmentally friendly synthesis of nanomaterials using green chem. has attracted tremendous attention in recent years due to its easy handling, low cost, and biocompatibility. Here we demonstrate a facile and efficient route for the synthesis of highly reduced graphene oxide (PE-HRG) by the green redn. of graphene oxide (GRO) using the Pulicaria glutinosa plant ext. (PE). The phytomols. present in the P. glutinosa ext. are not only responsible for the redn. of GRO, but also for the functionalization of the surface of the PE-HRG nanosheets and stabilize them in various solvents, thereby limiting the use of any other external and harmful chem. reductants and surfactants. The effect of PE on the dispersibility of PE-HRG in various solvents was investigated by prepg. PE-HRG with different amts. of PE, and the dispersibility of PE-HRG was compared with that of chem. reduced graphene oxide (CRG). The redn. of GRO was confirmed by UV-visible (UV-vis), Fourier-transform IR (FT-IR), Raman and X-ray photoelectron (XPS) spectroscopies, thermogravimetric anal. (TGA), X-ray powder diffraction (XRD) and transmission electron microscopy (TEM).
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    Tu, Z.; Achazi, K.; Schulz, A.; Mülhaupt, R.; Thierbach, S.; Rühl, E.; Adeli, M.; Haag, R. Combination of surface charge and size controls the cellular uptake of functionalized graphene sheets. Adv. Funct. Mater. 2017, 27, 1701837,  DOI: 10.1002/adfm.201701837
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    Lopez, A.; Liu, J. Covalent and Noncovalent Functionalization of Graphene Oxide with DNA for Smart Sensing. Adv. Intell. Syst. 2020, 2, 2000123,  DOI: 10.1002/aisy.202000123
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    Georgakilas, V.; Otyepka, M.; Bourlinos, A. B.; Chandra, V.; Kim, N.; Kemp, K. C.; Hobza, P.; Zboril, R.; Kim, K. S. Functionalization of graphene: covalent and non-covalent approaches, derivatives and applications. Chem. Rev. 2012, 112, 6156– 6214,  DOI: 10.1021/cr3000412
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    Functionalization of Graphene: Covalent and Non-Covalent Approaches, Derivatives and Applications
    Georgakilas, Vasilios; Otyepka, Michal; Bourlinos, Athanasios B.; Chandra, Vimlesh; Kim, Namdong; Kemp, K. Christian; Hobza, Pavel; Zboril, Radek; Kim, Kwang S.
    Chemical Reviews (Washington, DC, United States) (2012), 112 (11), 6156-6214CODEN: CHREAY; ISSN:0009-2665. (American Chemical Society)
    This comprehensive review covers all modes and methods of graphene functionalization including their classification. The complementary discussions of both exptl. and theor. aspects of graphene functionalization and interaction is presented. The functionalization modes related to chem. of graphene derivs. (graphene oxide, graphane, fluorographene) represent a significant part of the review, which thus considerably exceeds the chem. of pristine graphene. Both covalent functionalization based on binding of org. functionalities like free radicals and dienophiles on pristine graphene and attachment through the chem. of oxygen groups of graphene oxide are comprehensively discussed. The covalent attachments of hydrogen and halogens and, generally, the chem. of graphane and fluorographene are described. Noncovalent functionalization and interactions, which do not disrupt the extended p-conjugation on the graphene surface unlike covalent functionalization, are discussed. The theory of graphene-ligand non-covalent interactions is presented, while various interaction modes (p interactions) are analyzed from both theor. and exptl. viewpoints. The methods of deposition of various nanostructures on graphene are discussed, including a great variety of nanoparticles like noble metals, metal oxides, quantum dots, polymers, and others. The superior properties and applicability of these graphene-nanoparticle composites are extensively analyzed. The specific methods of graphene doping to control the type and concn. of charged carriers are summarized. Selected applications of functionalized graphene, including doped graphene electronic devices, magnetic bilayer intercalates, electronic/spintronic devices, and DNA sequencing devices, green chem., and bio-imaging, are discussed.
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    Georgakilas, V.; Tiwari, J. N.; Kemp, K. C.; Perman, J. A.; Bourlinos, A. B.; Kim, K. S.; Zboril, R. Noncovalent functionalization of graphene and graphene oxide for energy materials, biosensing, catalytic, and biomedical applications. Chem. Rev. 2016, 116, 5464– 5519,  DOI: 10.1021/acs.chemrev.5b00620
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    Noncovalent Functionalization of Graphene and Graphene Oxide for Energy Materials, Biosensing, Catalytic, and Biomedical Applications
    Georgakilas, Vasilios; Tiwari, Jitendra N.; Kemp, K. Christian; Perman, Jason A.; Bourlinos, Athanasios B.; Kim, Kwang S.; Zboril, Radek
    Chemical Reviews (Washington, DC, United States) (2016), 116 (9), 5464-5519CODEN: CHREAY; ISSN:0009-2665. (American Chemical Society)
    A review. This review focuses on noncovalent functionalization of graphene and graphene oxide with various species involving biomols., polymers, drugs, metals and metal oxide-based nanoparticles, quantum dots, magnetic nanostructures, other carbon allotropes (fullerenes, nanodiamonds, and carbon nanotubes), and graphene analogs (MoS2, WS2). A brief description of π-π interactions, van der Waals forces, ionic interactions, and hydrogen bonding allowing noncovalent modification of graphene and graphene oxide is first given. The main part of this Review is devoted to tailored functionalization for applications in drug delivery, energy materials, solar cells, water splitting, biosensing, bioimaging, environmental, catalytic, photocatalytic, and biomedical technologies. A significant part of this Review explores the possibilities of graphene/graphene oxide-based 3D superstructures and their use in lithium-ion batteries. This Review ends with a look at challenges and future prospects of noncovalently modified graphene and graphene oxide.
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    Parviz, D.; Das, S.; Ahmed, H. S. T.; Irin, F.; Bhattacharia, S.; Green, M. J. Dispersions of non-covalently functionalized graphene with minimal stabilizer. ACS Nano 2012, 6, 8857– 8867,  DOI: 10.1021/nn302784m
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    Dispersions of Non-Covalently Functionalized Graphene with Minimal Stabilizer
    Parviz, Dorsa; Das, Sriya; Ahmed, H. S. Tanvir; Irin, Fahmida; Bhattacharia, Sanjoy; Green, Micah J.
    ACS Nano (2012), 6 (10), 8857-8867CODEN: ANCAC3; ISSN:1936-0851. (American Chemical Society)
    We demonstrate that functionalized pyrene derivs. effectively stabilize single- and few-layer graphene flakes in aq. dispersions. The graphene/stabilizer yield obtained by this method is exceptionally high relative to conventional nanomaterial stabilizers such as surfactants or polymers. The mechanism of stabilization by pyrene derivs. is investigated by studying the effects of various parameters on dispersed graphene concn. and stability; these parameters include stabilizer concn., initial graphite concn., soln. pH, and type and no. of functional groups and counterions. The effectiveness of the pyrene derivs. is pH-tunable, as measured by zeta potential, and is also a function of the no. of functional groups, the electronegativity of the functional group, the counterion, the relative polarity between stabilizer and solvent, and the distance from the functional group to the basal plane. Even if the dispersion is destabilized by extreme pH or lyophilization, the graphene does not aggregate because the stabilizer remains adsorbed on the surface. These dispersions also show promise for applications in graphene/polymer nanocomposites (examd. in this paper), org. solar cells, conductive films, and ink-jet-printed electronic devices.
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    Zhu, C.; Kalin, A. J.; Fang, L. Covalent and Noncovalent Approaches to Rigid Coplanar π-Conjugated Molecules and Macromolecules. Acc. Chem. Res. 2019, 52, 1089– 1100,  DOI: 10.1021/acs.accounts.9b00022
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    Covalent and Noncovalent Approaches to Rigid Coplanar π-Conjugated Molecules and Macromolecules
    Zhu, Congzhi; Kalin, Alexander J.; Fang, Lei
    Accounts of Chemical Research (2019), 52 (4), 1089-1100CODEN: ACHRE4; ISSN:0001-4842. (American Chemical Society)
    A review. Mol. conformation and rigidity are essential factors in detg. the properties of individual mols., the assocd. supramol. assemblies, and bulk materials. This correlation is particularly important for π-conjugated mol. and macromol. systems. Within such an individual mol., a coplanar conformation facilitates the delocalization of not only MOs but also charges, excitons, and spins, leading to synergistically ensembled properties of the entire conjugated system. A rigid backbone, meanwhile, imposes a high energy cost to disrupt such a favorable conformation, ensuring the robustness and persistence of coplanarity. From a supramol. and material point of view, coplanarity and rigidity often promote strong intermol. electronic coupling and reduce the energy barrier for the intermol. transport of charges, excitons, and phonons, affording advanced materials properties in bulk. In this context, pursuing a rigid and coplanar mol. conformation often represents one of the primary objectives when designing and synthesizing conjugated mols. for electronic and optical applications. Two general bottom-up strategies-covalent annulation and noncovalent conformational control-are often employed to construct rigid coplanar π systems. These strategies have afforded various classes of such mols. and macromols., including so-called conjugated ladder polymers, graphene nanoribbons, polyacenes, and conformationally locked org. semiconductors. While pursuing these targets, however, one often confronts challenges assocd. with precise synthesis and limited soly. of the rigid coplanar systems, which could further impede their large-scale prepn., characterization, processing, and application. To address these issues, the authors developed and utilized a no. of synthetic methods and mol. engineering approaches to construct and to process rigid coplanar conjugated mols. and macromols. Structure-property correlations of this unique class of org. materials were established, providing important chem. principles for mol. design and materials applications. In this Account, the authors first describe the efforts to synthesize rigid coplanar π systems fused by various types of bonds, including kinetically formed covalent bonds, thermodynamically formed covalent bonds, N→B coordinate bonds, and hydrogen bonds, in order of increasing dynamic character. The subsequent section discusses the characteristic properties of selected examples of these rigid coplanar π systems in comparison with control compds. that are not rigid and coplanar, particularly focusing on the optical, electronic, and electrochem. properties. For systems bridged with noncovalent interactions, active manipulation of the dynamic bonds can tune variable properties at the mol. or collective level. Intermol. interactions, solid-state packing, and processing of several cases are then discussed to lay the foundation for future materials applications of rigid coplanar π conjugated compds.
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    Yu, W.; Sisi, L.; Haiyan, Y.; Jie, L. Progress in the functional modification of graphene/graphene oxide: a review. RSC Adv. 2020, 10, 15328– 15345,  DOI: 10.1039/D0RA01068E
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    Progress in the functional modification of graphene/graphene oxide: a review
    Yu, Wang; Sisi, Li; Haiyan, Yang; Jie, Luo
    RSC Advances (2020), 10 (26), 15328-15345CODEN: RSCACL; ISSN:2046-2069. (Royal Society of Chemistry)
    A review. Graphene and graphene oxide have attracted tremendous interest over the past decade due to their unique and excellent electronic, optical, mech., and chem. properties. This review focuses on the functional modification of graphene and graphene oxide. First, the basic structure, prepn. methods and properties of graphene and graphene oxide are briefly described. Subsequently, the methods for the redn. of graphene oxide are introduced. Next, the functionalization of graphene and graphene oxide is mainly divided into covalent binding modification, non-covalent binding modification and elemental doping. Then, the properties and application prospects of the modified products are summarized. Finally, the current challenges and future research directions are presented in terms of surface functional modification for graphene and graphene oxide.
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    Khan, M.; Shaik, M. R.; Adil, S. F.; Kuniyil, M.; Ashraf, M.; Frerichs, H.; Sarif, M. A.; Siddiqui, M. R. H.; Al-Warthan, A.; Labis, J. P. Facile synthesis of Pd@graphene nanocomposites with enhanced catalytic activity towards Suzuki coupling reaction. Sci. Rep. 2020, 10, 11728,  DOI: 10.1038/s41598-020-68124-w
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    Facile synthesis of Pd@graphene nanocomposites with enhanced catalytic activity towards Suzuki coupling reaction
    Khan, Mujeeb; Shaik, Mohammed Rafi; Adil, Syed Farooq; Kuniyil, Mufsir; Ashraf, Muhammad; Frerichs, Hajo; Sarif, Massih Ahmad; Siddiqui, Mohammed Rafiq H.; Al-Warthan, Abdulrahman; Labis, Joselito P.; Islam, Mohammad Shahidul; Tremel, Wolfgang; Tahir, Muhammad Nawaz
    Scientific Reports (2020), 10 (1), 11728CODEN: SRCEC3; ISSN:2045-2322. (Nature Research)
    A facile and chem. specific method to synthesize highly reduced graphene oxide (HRG) and Pd (HRG@Pd) nanocomposite was presented. The HRG surfaces were tailored with amine groups using 1-aminopyrene (1-AP) as functionalizing mols. The arom. rings of 1-AP sit on the basal planes of HRG through π-π interactions, leaving amino groups outwards (similar like self-assembled monolayer on 2D substrates). The amino groups provide the chem. specific binding sites to the Pd nucleation which subsequently grow into nanoparticles. HRG@Pd nanocomposite demonstrated both uniform distribution of Pd nanoparticles on HRG surface as well as excellent phys. stability and dispersibility. The surface functionalization was confirmed using, UV-visible (UV-Vis), Fourier transform infra-red and Raman spectroscopy. The size and distribution of Pd nanoparticles on the HRG and crystallinity were confirmed using high-resoln. transmission electron microscopy and powder X-ray diffraction and XPS. The catalytic efficiency of highly reduced graphene oxide-pyrene-palladium nanocomposite (HRG-Py-Pd) was tested towards the Suzuki coupling reactions of various aryl halides. The kinetics of the catalytic reaction (Suzuki coupling) using HRG-Py-Pd nanocomposite was monitored using gas chromatog. (GC).
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    Stark, W. J. Nanoparticles in biological systems. Angew. Chem., Int. Ed. 2011, 50, 1242– 1258,  DOI: 10.1002/anie.200906684
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    Nanoparticles in Biological Systems
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  • Abstract

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    Scheme 1

    Scheme 1. Graphical Representation of the Preparation of Functionalized (AP-HRG-Au) and Nonfunctionalized (HRG-Au) Graphene-Gold Nanocomposites and Their Anticancer Properties
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    Figure 1

    Figure 1. Digital images of the aqueous dispersions of highly reduced graphene oxide (HRG), nonfunctionalized HRG-Au (gold), and 1-AP-functionalized HRG-Au nanocomposites (AP-HRG-Au). The dispersions were prepared by sonicating 5 mg of each sample in 10 mL of water.

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    Figure 2

    Figure 2. UV spectra of 1-AP, pristine HRG, nonfunctionalized HRG-Au, and 1-AP-functionalized AP-HRG-Au nanocomposites.

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    Figure 3

    Figure 3. FT-IR spectra of 1-AP, pristine HRG, nonfunctionalized HRG-Au, and 1-AP-functionalized AP-HRG-Au nanocomposites.

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    Figure 4

    Figure 4. XRD patterns of pristine HRG, nonfunctionalized HRG-Au, and 1-AP-functionalized AP-HRG-Au nanocomposites.

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    Figure 5

    Figure 5. HRTEM images of a 1-AP-functionalized AP-HRG-Au nanocomposite: (a) overview and (b) magnified images of AP-HRG-Au. (c) EDX spectrum of AP-HRG-Au and (d) particle size distribution graph of AP-HRG-Au.

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    Figure 6

    Figure 6. Effect of (a) 1-AP-functionalized AP-HRG-Au and (b) nonfunctionalized HRG-Au on cell viability after 48 h treatment. The cell viability was determined using an MTT assay. Results are expressed as means ± SD for three replicate values for each concentration.

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    Figure 7

    Figure 7. AP-HRG-Au and HRG-Au induces G1 arrest in MCF-7 cells. MCF-7 cells were treated with IC50 concentrations for 48 h. Cells were fixed by ethanol and stained with PI. Cell cycle progression was assessed by flow cytometry.

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    Figure 8

    Figure 8. Induction of apoptosis by AP-HRG-Au and HRG-Au in MCF-7 cells. Fluorescence intensity of Annexin V and PI as indication of apoptosis induced by IC50 concentrations of each particle.

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    Figure 9

    Figure 9. Flow cytometry analysis of ROS generation in MCF-7 cells treated with AP-HRG-Au and HRG-Au for 24 h. MCF-7 cells were treated with IC50 concentrations of both particles for 48 h and then stained as described in the Experimental Details. The left quarter gray dots represent unstained cells, and the right quarter red dots represent stained cells.

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    This article references 41 other publications.

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      Xu, Pei-Yao; Kankala, Ranjith Kumar; Pan, Yu-Jing; Yuan, Hui; Wang, Shi-Bin; Chen, Ai-Zheng
      International Journal of Nanomedicine (2018), 13 (), 4685-4698CODEN: IJNNHQ; ISSN:1178-2013. (Dove Medical Press Ltd.)
      In recent times, the co-delivery therapeutics have garnered enormous interest from researchers in the treatment of cancers with multidrug resistance (MDR) due to their efficient delivery of multiple agents, which result in synergistic effects and capable of overcoming all the obstacles of MDR in cancer. However, an efficient delivery platform is required for the conveyance of diverse agents that can successfully devastate MDR in cancer. Initially, short-interfering RNA-loaded chitosan (siRNA-CS) nanoparticles were synthesized using the ionic gelation method. Further, the siRNA-CS nanoparticles and doxorubicin hydrochloride (DOX) were co-loaded in poly-L-lactide porous microparticles (PLLA PMs) (nano-embedded porous microparticles, [NEPMs]) by the supercrit. anti-solvent (SAS) process. The NEPM formulation exhibited an excellent aerodynamic performance and sustained release of DOX, which displayed higher anticancer efficacy in drugresistant cells (human small cell lung cancer, H69AR cell line) than those treated with either free DOX and DOX-PLLA PMs due to the siRNA from CS nanoparticles silenced the MDR gene to DOX therapy. This eco-friendly process provides a convenient way to fabricate such innovative NEPMs co-loaded with a chemotherapeutic agent and a gene, which can devastate MDR in cancer through the co-delivery system.
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    3. 3
      Gao, H.; Bai, Y.; Chen, L.; Fakhri, G. E.; Wang, M. Self-Assembly Nanoparticles for Overcoming Multidrug Resistance and Imaging-Guided Chemo-Photothermal Synergistic Cancer Therapy. Int. J. Nanomed. 2020, 15, 809,  DOI: 10.2147/IJN.S232449
      3
      Self-assembly nanoparticles for overcoming multidrug resistance and imaging-guided chemo-photothermal synergistic cancer therapy
      Gao, Haiyan; Bai, Yan; Chen, Lijuan; Fakhri, Georges Ei; Wang, Meiyun
      International Journal of Nanomedicine (2020), 15 (), 809-819CODEN: IJNNHQ; ISSN:1178-2013. (Dove Medical Press Ltd.)
      The development of multiple drug resistance (MDR) to chemotherapy and single modal therapy remains unsatisfied for the eradication of tumor, which are major obstacles in cancer therapy. This novel system with excellent characteristics for inhibition of P-glycoprotein (P-gp), and for near-IR fluorescence (NIRF) imaging-guided chemo-photothermal therapy (PTT), has been identified as a promising way to MDR and achieve synergistic cancer therapy. In this study, we successfully synthesized a multifunctional theranostic system, which was developed through FDA-approved self-assembling drugs, which contain anticancer drug doxorubicin (Dox), imaging and high photothermal conversion drug indocyanine green (ICG) and P-gp regulator TPGS (the system named T/Dox-ICG). We studied the characterization of T/Dox-ICG NPs, including the TEM, SEM, DLS, UV-vis-NIR, zeta potential, CLSM, in vitro FL imaging, in vitro photothermal effect, in vitro Dox and ICG release. We used CLSM to verify the location of intracellular distribution of Dox in SCG 7901/VCR cells, Western blot was performed to demonstrate the TPGS-mediated inhibition of P-gp. And, the cytotoxicity of materials against SCG 7901/VCR cells was studied by the MTT assay. The TEM showed the T/Dox-ICG NPs had good monodispersity with diams. of 19.03 nm, Dox and ICG could be released constantly from T/Dox-ICG NPs in vitro. In vitro cell expts. demonstrated higher Dox accumulation and retention in the nucleus. Western blot showed TPGS could obviously inhibit the expression of P-gp. In vitro cytotoxicity assay showed more significant cytotoxicity on MDR cells (SCG 7901/VCR) with only 8.75% of cells surviving. MDR cancer therapy indicates that it may be important to develop a safer system that can simultaneously inhibit the drug transporters and monitor the delivery of chemotherapeutic agents, and combination therapy have raised widespread concern on tumor treatment.
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    4. 4
      Lim, B.; Greer, Y.; Lipkowitz, S.; Takebe, N. Novel apoptosis-inducing agents for the treatment of cancer, a new arsenal in the toolbox. Cancers 2019, 11, 1087,  DOI: 10.3390/cancers11081087
      4
      Novel apoptosis-inducing agents for the treatment of cancer, a new arsenal in the toolbox
      Lim, Bora; Greer, Yoshimi; Lipkowitz, Stanley; Takebe, Naoko
      Cancers (2019), 11 (8), 1087CODEN: CANCCT; ISSN:2072-6694. (MDPI AG)
      Evasion from apoptosis is an important hallmark of cancer cells. Alterations of apoptosis pathways are esp. crit. as they confer resistance to conventional anti-cancer therapeutics, e.g., chemotherapy, radiotherapy, and targeted therapeutics. Thus, successful induction of apoptosis using novel therapeutics may be a key strategy for preventing recurrence and metastasis. Inhibitors of anti-apoptotic mols. and enhancers of pro-apoptotic mols. are being actively developed for hematol. malignancies and solid tumors in particular over the last decade. However, due to the complicated apoptosis process caused by a multifaceted connection with cross-talk pathways, protein-protein interaction, and diverse resistance mechanisms, drug development within the category has been extremely challenging. Careful design and development of clin. trials incorporating predictive biomarkers along with novel apoptosis-inducing agents based on rational combination strategies are needed to ensure the successful development of these mols. Here, we review the landscape of currently available direct apoptosis-targeting agents in clin. development for cancer treatment and update the related biomarker advancement to detect and validate the efficacy of apoptosis-targeted therapies, along with strategies to combine them with other agents.
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    5. 5
      Bor, G.; Mat Azmi, I. D.; Yaghmur, A. Nanomedicines for cancer therapy: Current status, challenges and future prospects. Ther. Delivery 2019, 10, 113– 132,  DOI: 10.4155/tde-2018-0062
      5
      Nanomedicines for cancer therapy: current status, challenges and future prospects
      Bor, Gizem; Mat Azmi, Intan Diana; Yaghmur, Anan
      Therapeutic Delivery (2019), 10 (2), 113-132CODEN: TDHEA7; ISSN:2041-5990. (Future Science Ltd.)
      A review. The emergence of nanomedicine as an innovative and promising alternative technol. shows many advantages over conventional cancer therapies and provides new opportunities for early detection, improved treatment, and diagnosis of cancer. Despite the cancer nanomedicines capability of delivering chemotherapeutic agents while providing lower systemic toxicity, it is paramount to consider the cancer complexity and dynamics for bridging the translational bench-to-bedside gap. It is important to conduct appropriate investigations for exploiting the tumor microenvironment, and achieving a more comprehensive understanding of the fundamental biol. processes in cancer and their roles in modulating nanoparticle-protein interactions, blood circulation, and tumor penetration. This review provides an overview of the current cancer nanomedicines, the major challenges, and the future opportunities in this research area.
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    6. 6
      Gu, Z.; Zhu, S.; Yan, L.; Zhao, F.; Zhao, Y. Graphene-based smart platforms for combined Cancer therapy. Adv. Mater. 2019, 31, 1800662,  DOI: 10.1002/adma.201800662
      There is no corresponding record for this reference.
    7. 7
      Reina, G.; González-Domínguez, J. M.; Criado, A.; Vázquez, E.; Bianco, A.; Prato, M. Promises, facts and challenges for graphene in biomedical applications. Chem. Soc. Rev. 2017, 46, 4400– 4416,  DOI: 10.1039/C7CS00363C
      7
      Promises, facts and challenges for graphene in biomedical applications
      Reina, Giacomo; Gonzalez-Dominguez, Jose Miguel; Criado, Alejandro; Vazquez, Ester; Bianco, Alberto; Prato, Maurizio
      Chemical Society Reviews (2017), 46 (15), 4400-4416CODEN: CSRVBR; ISSN:0306-0012. (Royal Society of Chemistry)
      The graphene family has captured the interest and the imagination of an increasing no. of scientists working in different fields, ranging from composites to flexible electronics. In the area of biomedical applications, graphene is esp. involved in drug delivery, biosensing and tissue engineering, with strong contributions to the whole nanomedicine area. Besides the interesting results obtained so far and the evident success, there are still many problems to solve, on the way to the manufg. of biomedical devices, including the lack of standardization in the prodn. of the graphene family members. Control of lateral size, aggregation state (single vs. few layers) and oxidn. state (unmodified graphene vs. oxidized graphenes) is essential for the translation of this material into clin. assays. In this Tutorial Review we critically describe the latest developments of the graphene family materials into the biomedical field. We analyze graphene-based devices starting from graphene synthetic strategies, functionalization and processibility protocols up to the final in vitro and in vivo applications. We also address the toxicol. impact and the limitations in translating graphene materials into advanced clin. tools. Finally, new trends and guidelines for future developments are presented.
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    8. 8
      Salaheldin, T. A.; Loutfy, S. A.; Ramadan, M. A.; Youssef, T.; Mousa, S. A. IR-enhanced photothermal therapeutic effect of graphene magnetite nanocomposite on human liver cancer HepG2 cell model. Int. J. Nanomed. 2019, 14, 4397,  DOI: 10.2147/IJN.S196256
      8
      IR-enhanced photothermal therapeutic effect of graphene magnetite nanocomposite on human liver cancer HepG2 cell model
      Salaheldin, Taher A.; Loutfy, Samah A.; Ramadan, Marwa A.; Youssef, Tareq; Mousa, Shaker A.
      International Journal of Nanomedicine (2019), 14 (), 4397-4412CODEN: IJNNHQ; ISSN:1178-2013. (Dove Medical Press Ltd.)
      Background: Graphene magnetite nanocomposites (G/Fe3O4) exhibit light photothermal conversion upon enhancement by 808 nm IR laser excitation. We evaluated the cytotoxic and photothermal effects of G/Fe3O4 on a HepG2 human liver cancer cell model. Methods: Graphene nanosheets (rGO), magnetite nanoparticles (Fe3O4), and G/Fe3O4 were prepd. by chem. methods and characterized using transmission electron microscopy, Raman spectroscopy, zeta anal., and vibrating sample magnemeter. Results: Treatment of HepG2 with 400 g/mL of rGO, Fe3O4, and G/Fe3O4 showed alteration in cell morphol. after 24 h of cell treatment and revealed toxic effects on cellular DNA. Evaluation of the cytotoxic effects showed mRNA (mRNA) in beta-actin and Bax apoptotic genes, but no expression of mRNA of caspase-3 after 24 h of cell exposure, suggesting the involvement of an intrinsic apoptotic caspase-independent pathway. A photothermal effect was obsd. for G/Fe3O4 after irradn. of the HepG2 cells. A marked decrease was found in cell viability when treated with 10 and 50 g/mL G/Fe3O4 from 40% to 5% after 48 h of cell treatment. Conclusion: Results indicate that G/Fe3O4 nanocomposite was effective at transformation of light into heat and is a promising candidate for cancer therapy.
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    9. 9
      Barrera, C. C.; Groot, H.; Vargas, W. L.; Narváez, D. M. Efficacy and Molecular Effects of a Reduced Graphene Oxide/Fe3O4 Nanocomposite in Photothermal Therapy Against Cancer. Int. J. Nanomed. 2020, 15, 6421,  DOI: 10.2147/IJN.S256760
      There is no corresponding record for this reference.
    10. 10
      Fan, H.-y.; Yu, X.-h.; Wang, K.; Yin, Y.-j.; Tang, Y.-j.; Tang, Y.-l.; Liang, X.-h. Graphene quantum dots (GQDs)-based nanomaterials for improving photodynamic therapy in cancer treatment. Eur. J. Med. Chem. 2019, 182, 111620,  DOI: 10.1016/j.ejmech.2019.111620
      10
      Graphene quantum dots (GQDs)-based nanomaterials for improving photodynamic therapy in cancer treatment
      Fan, Hua-yang; Yu, Xiang-hua; Wang, Ke; Yin, Yi-jia; Tang, Ya-jie; Tang, Ya-ling; Liang, Xin-hua
      European Journal of Medicinal Chemistry (2019), 182 (), 111620CODEN: EJMCA5; ISSN:0223-5234. (Elsevier Masson SAS)
      A review. Graphene quantum dots (GQDs) as novel nanomaterials, have received significant interest in the field of biomedical applications. It is worth noting that a large amt. of research is devoted to GQDs-based nanocomposites for cancer treatment, esp. for photodynamic therapy (PDT), in that they can act not only as more favorable photosensitizers (PSs) but also nanoplatforms for delivering PSs. In this review, the biol. behavior and physicochem. properties of GQDs for PDT are described in detail, and the application of GQDs-based nanocomposites in improved PDT and PDT-based combination therapies is analyzed, which may provide a new strategy for designing efficient PDT systems for cancer treatment.
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    11. 11
      Khan, M.; Tahir, M. N.; Adil, S. F.; Khan, H. U.; Siddiqui, M. R. H.; Al-warthan, A. A.; Tremel, W. Graphene based metal and metal oxide nanocomposites: synthesis, properties and their applications. J. Mater. Chem. A 2015, 3, 18753– 18808,  DOI: 10.1039/C5TA02240A
      11
      Graphene based metal and metal oxide nanocomposites: synthesis, properties and their applications
      Khan, Mujeeb; Tahir, Muhammad Nawaz; Adil, Syed Farooq; Khan, Hadayat Ullah; Siddiqui, M. Rafiq H.; Al-warthan, Abdulrahman A.; Tremel, Wolfgang
      Journal of Materials Chemistry A: Materials for Energy and Sustainability (2015), 3 (37), 18753-18808CODEN: JMCAET; ISSN:2050-7496. (Royal Society of Chemistry)
      A review. Graphene, an atomically thin two-dimensional carbonaceous material, has attracted tremendous attention in the scientific community, due to its exceptional electronic, elec., and mech. properties. Indeed, with the recent explosion of methods for a large-scale synthesis of graphene, the no. of publications related to graphene and other graphene based materials has increased exponentially. Particularly the development of easy prepn. methods for graphene like materials, such as highly reduced graphene oxide (HRG) via redn. of graphite oxide (GO), offers a wide range of possibilities for the prepn. of graphene based inorg. nanocomposites by the incorporation of various functional nanomaterials for a variety of applications. In this review, the current development of graphene based metal and metal oxide nanocomposites, with a detailed account of their synthesis and properties are discussed. Specifically, much attention was given to their wide range of applications in various fields, including electronics, electrochem. and elec. fields. Overall, by the inclusion of various refs., this review covers in detail the aspects of graphene-based inorg. nanocomposites.
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    12. 12
      Zhou, X.; Dorn, M.; Vogt, J.; Spemann, D.; Yu, W.; Mao, Z.; Estrela-Lopis, I.; Donath, E.; Gao, C. A quantitative study of the intracellular concentration of graphene/noble metal nanoparticle composites and their cytotoxicity. Nanoscale 2014, 6, 8535– 8542,  DOI: 10.1039/C4NR01763C
      12
      A quantitative study of the intracellular concentration of graphene/noble metal nanoparticle composites and their cytotoxicity
      Zhou, Xiangyan; Dorn, Marco; Vogt, Jurgen; Spemann, Daniel; Yu, Wei; Mao, Zhengwei; Estrela-Lopis, Irina; Donath, Edwin; Gao, Changyou
      Nanoscale (2014), 6 (15), 8535-8542CODEN: NANOHL; ISSN:2040-3372. (Royal Society of Chemistry)
      Noble-metal nanoparticles (NPs) esp. prepd. from gold and silver have been combined on the surface of graphene to obtain graphene-based nanocomposites for novel functions in enhanced performance in bio-imaging, cancer detection and therapy. However, little is known about their cellular uptake, esp. the intracellular quantity which plays a crit. role in detg. their functions and safety. Therefore, we prepd. covalently conjugated GO/Au and GO/Ag composites by immobilizing Au and Ag nanoparticles on GO sheets pre-functionalized with disulfide bonds, resp. The cellular uptake of these composites was quant. studied by means of an ion beam microscope (IBM) to det. the metal content in human lung cancer cells (A549 cells) and liver hepatocellular carcinoma cells (HepG2 cells). The cell uptake was also studied by inductively coupled plasma mass spectrometry (ICP-MS), which is one of the most sensitive techniques being applied to cell suspensions, for comparison. Toxicity, one of the consequences of cellular uptake of GO based composites, was studied as well. The potential toxicity mechanism was also suggested based on the results of intracellular quantification of the nanomaterials.
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    13. 13
      Khan, M.; Khan, M.; Al-Marri, A. H.; Al-Warthan, A.; Alkhathlan, H. Z.; Siddiqui, M. R. H.; Nayak, V. L.; Kamal, A.; Adil, S. F. Apoptosis inducing ability of silver decorated highly reduced graphene oxide nanocomposites in A549 lung cancer. Int. J. Nanomed. 2016, 11, 873,  DOI: 10.2147/IJN.S100903
      13
      Apoptosis inducing ability of silver decorated highly reduced grapheme oxide nanocomposites in A549 lung cancer
      Khan, Merajuddin; Khan, Mujeeb; Al-Marri, Abdulhadi H.; Al-Warthan, Abdulrahman; Alkhathlan, Hamad Z.; Siddiqui, Mohammed Rafiq H.; Nayak, Vadithe Lakshma; Kamal, Ahmed; Adil, Syed F.
      International Journal of Nanomedicine (2016), 11 (), 873-883CODEN: IJNNHQ; ISSN:1178-2013. (Dove Medical Press Ltd.)
      Recently, graphene and graphene-based materials have been increasingly used for various biol. applications due to their extraordinary physicochem. properties. Here, we demonstrate the anticancer properties and apoptosis-inducing ability of silver doped highly reduced graphene oxide nanocomposites synthesized by employing green approach. These nanocomposites (PGE-HRG-Ag) were synthesized by using Pulicaria glutinosa ext. (PGE) as a reducing agent and were evaluated for their anticancer properties against various human cancer cell lines with tamoxifen as the ref. drug. A correlation between the amt. of Ag nanoparticles on the surface of highly reduced graphene oxide (HRG) and the anticancer activity of nanocomposite was obsd., wherein an increase in the concn. of Ag nanoparticles on the surface of HRG led to the enhanced anticancer activity of the nanocomposite. The nanocomposite PGE-HRG-Ag-2 exhibited more potent cytotoxicity than std. drug in A549 cells, a human lung cancer cell line. A detailed investigation was undertaken and Fluorescence activated cell sorting (FACS) anal. demonstrated that the nanocomposite PGE-HRG-Ag-2 showed G0/G1 phase cell cycle arrest and induced apoptosis in A549 cells. Studies such as, measurement of mitochondrial membrane potential, generation of reactive oxygen species (ROS) and Annexin V-FITC staining assay suggested that this compd. induced apoptosis in human lung cancer cells.
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    14. 14
      Sztandera, K.; Gorzkiewicz, M.; Klajnert-Maculewicz, B. Gold nanoparticles in cancer treatment. Mol. Pharmaceutics 2019, 16, 1– 23,  DOI: 10.1021/acs.molpharmaceut.8b00810
      14
      Gold Nanoparticles in Cancer Treatment
      Sztandera, Krzysztof; Gorzkiewicz, Michal; Klajnert-Maculewicz, Barbara
      Molecular Pharmaceutics (2019), 16 (1), 1-23CODEN: MPOHBP; ISSN:1543-8384. (American Chemical Society)
      Colloidal gold has been studied for its potential application in medicine for centuries. However, synthesis and evaluation of various gold nanoparticles have only recently been met with a wide interest of scientists. Current studies confirm numerous advantages of nanogold over different nanomaterials, primarily due to highly optimized protocols for the prodn. of gold nanoparticles of countless sizes and shapes, featured with unique properties. The possibility to modify the surface of nanogold particles with different targeting and functional compds. significantly broadens the range of their potential biomedical applications, with particular emphasis on cancer treatment. Functionalized gold nanoparticles exhibit good biocompatibility and controllable biodistribution patterns, which make them particularly fine candidates for the basis of innovative therapies. Considering the high amt. of scientific data on nanogold, this review summarizes recent advances in the field of medical application of gold nanoparticles for the therapy of cancer.
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    15. 15
      Turcheniuk, K.; Boukherroub, R.; Szunerits, S. Gold–graphene nanocomposites for sensing and biomedical applications. J. Mater. Chem. B 2015, 3, 4301– 4324,  DOI: 10.1039/C5TB00511F
      15
      Gold-graphene nanocomposites for sensing and biomedical applications
      Turcheniuk, Kostiantyn; Boukherroub, Rabah; Szunerits, Sabine
      Journal of Materials Chemistry B: Materials for Biology and Medicine (2015), 3 (21), 4301-4324CODEN: JMCBDV; ISSN:2050-7518. (Royal Society of Chemistry)
      A review. Recent developments in materials science and nanotechnol. have propelled the development of a plethora of materials with unique chem. and phys. properties for biomedical applications. Graphitic nanomaterials such as carbon nanotubes, fullerenes and, more recently, graphene oxide (GO) and reduced graphene oxide (rGO) have received a great deal of interest in this domain. Besides the exceptional physico-chem. features of these materials, another advantage is that they can be easily produced in good quantities. Moreover, the presence of abundant functional groups on their surface and good biocompatibility make them highly suitable for biomedical applications. Many research groups have utilized GO and rGO nanocargos to effectively deliver insol. drugs, nucleic acids and other mols. into cells for bioimaging and therapeutic purposes. Gold nanostructures (Au NSs), on the other hand, have also attracted great attention owing to their applications in biomedical fields, org. catalysis, etc. Loading of GO and rGO sheets with Au NSs generates a new class of functional materials with improved properties and thus provides new opportunities in the use of such hybrid materials for catalytic biosensing and biomedical applications. This review article is aimed at providing an insight into the important features of gold-graphene nanocomposites, the current research activities related to the different synthetic routes to produce these nanocomposites, and their potential applications in sensing and biomedical therapy, notably photothermal therapy (PTT).
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    16. 16
      Sanad, M. F.; Shalan, A. E.; Bazid, S. M.; Serea, E. S. A.; Hashem, E. M.; Nabih, S.; Ahsan, M. A. A graphene gold nanocomposite-based 5-FU drug and the enhancement of the MCF-7 cell line treatment. RSC Adv. 2019, 9, 31021– 31029,  DOI: 10.1039/C9RA05669F
      16
      A graphene gold nanocomposite-based 5-FU drug and the enhancement of the MCF-7 cell line treatment
      Sanad, Mohamed Fathi; Shalan, Ahmed Esmail; Bazid, Shereen Magdy; Abu Serea, Esraa Samy; Hashem, Elhussein M.; Nabih, Shimaa; Ahsan, Md. Ariful
      RSC Advances (2019), 9 (53), 31021-31029CODEN: RSCACL; ISSN:2046-2069. (Royal Society of Chemistry)
      There is no doubt that cancer is now one of the most formidable diseases in the world; despite all the efforts and research, common treatment routes, including chemotherapy, photodynamic therapy, and photothermal therapy, suffer from different limitations in terms of their efficiency and performance. For this reason, different strategies are being explored to improve the efficiency of the traditional drugs reported to date. In this study, we have redirected the function of one of these drugs (5-fluorouracil, 5-FU) by combining it with a graphene-gold nanocomposite in different molar ratios that has been exceedingly used for biol. research development. The high activity of the graphene-gold material enables it to produce reactive oxygen and ions, which display good anticancer and antioxidant activity through the scavenging of the DPPH, SOD and GPx radicals; in addn., different characterizations have been used to confirm the structure and morphol. of the obtained samples. Highly potent cytotoxicity against the MCF-7 cells was achieved with the drug combination contg. the nanocomposite. All the results, including those obtained via cytometry, indicate that the combination of 5% graphene-gold nanocomposites with 5-FU exhibits a higher antitumor impact and more drug stability than pure 5-FU.
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    17. 17
      Xu, J.; Wang, Y.; Hu, S. Nanocomposites of graphene and graphene oxides: Synthesis, molecular functionalization and application in electrochemical sensors and biosensors. A review. Microchim. Acta 2017, 184, 1– 44,  DOI: 10.1007/s00604-016-2007-0
      17
      Nanocomposites of graphene and graphene oxides: Synthesis, molecular functionalization and application in electrochemical sensors and biosensors. A review
      Xu, Junhui; Wang, Yazhen; Hu, Shengshui
      Microchimica Acta (2017), 184 (1), 1-44CODEN: MIACAQ; ISSN:0026-3672. (Springer-Verlag GmbH)
      Functionalized nanocomposites based on various type of graphene nanomaterials including graphene, graphene oxides (GOs), and doped graphene (oxides) are widely used as materials for various sensors that can display high sensitivity, selectivity and stability. This review with 347 refs. summarizes advances in the prepn. and functionalization of graphene nanocomposites for the application of electrochem. sensors and biosensors. Following a general introduction into the field, the article is divided into subsections on (a) the synthesis and functionalization of nanocomposites (made from graphene, various kinds of GOs, heteroatom-doped GOs), (b) on methods for functionalization of composites (with other carbon nanomaterials, metal nanoparticles, metal oxide and metal sulfide nanoparticles), (c) on functionalization with inorg. materials including polyoxometalates, hexacyanoferrates, minerals), (d) on functionalization with org. materials such as amino acids, surfactants, org. dyes, ionic liqs., macrocycles (including cyclodextrins, crown ethers and calixarenes), and (e) on functionalization with organometallics and with various other org. compds., (f) on functionalizations with polymers such as conventional polymers, polyelectrolytes, conducting polymers, molecularly imprinted polymers, (g) on functionalization with biomols. including proteins and nucleic acids. Other subsections cover flexible graphene and GO based nanocomposites and 3D composites. Application of graphene and GO nanocomposites are then covered in a in large section that comprises electrochem. sensors and biosensors (based on voltammetry, amperometry, potentiometry, impedimetry, electrochemiluminescence, photoelectrochem., field effect transistors, electrochem. immunosensors) with specific subsections on gas sensors, enzymic biosensors and gene sensors. A concluding section covers current challenges and perspectives of graphene and GO based (bio)sensing. [Figure not available: see fulltext.].
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    18. 18
      Yang, K.; Feng, L.; Hong, H.; Cai, W.; Liu, Z. Preparation and functionalization of graphene nanocomposites for biomedical applications. Nat. Protoc. 2013, 8, 2392– 2403,  DOI: 10.1038/nprot.2013.146
      18
      Preparation and functionalization of graphene nanocomposites for biomedical applications
      Yang, Kai; Feng, Liangzhu; Hong, Hao; Cai, Weibo; Liu, Zhuang
      Nature Protocols (2013), 8 (12), 2392-2403CODEN: NPARDW; ISSN:1750-2799. (Nature Publishing Group)
      Functionalized nano-graphene- and graphene-based nanocomposites have gained tremendous attention in the area of biomedicine in recent years owing to their biocompatibility, the ease with which they can be functionalized and their properties such as thermal and elec. cond. Potential applications for functionalized nanoparticles range from drug delivery and multimodal imaging to exploitation of the elec. properties of graphene toward the prepn. of biosensing devices. This protocol covers the prepn., functionalization and bioconjugation of various graphene derivs. and nanocomposites. Starting from graphite, the prepns. of graphene oxide (GO), reduced GO (RGO) and magnetic GO-based nanocomposite, as well as how to functionalize them with biocompatible polymers such as polyethylene glycol (PEPEG), are described in detail. We also provide procedures for 125I radiolabeling of PEPEGylated GO and the prepn. of GO-based gene carriers; other bioconjugation approaches including drug loading, antibody conjugation and fluorescent labeling are similar to those described previously and used for bioconjugation of PEPEGylated carbon nanotubes. We hope this article will help researchers in this field to fabricate graphene-based bioconjugates with high reproducibility for various applications in biomedicine. The sample prepn. procedures take various times ranging from 1 to 2 d.
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    19. 19
      Singh, D. P.; Herrera, C. E.; Singh, B.; Singh, S.; Singh, R. K.; Kumar, R. Graphene oxide: An efficient material and recent approach for biotechnological and biomedical applications. Mater. Sci. Eng., C 2018, 86, 173– 197,  DOI: 10.1016/j.msec.2018.01.004
      19
      Graphene oxide: An efficient material and recent approach for biotechnological and biomedical applications
      Singh, Dinesh Pratap; Herrera, Carlos Eugenio; Singh, Brijesh; Singh, Shipra; Singh, Rajesh Kumar; Kumar, Rajesh
      Materials Science & Engineering, C: Materials for Biological Applications (2018), 86 (), 173-197CODEN: MSCEEE; ISSN:0928-4931. (Elsevier B.V.)
      The two-dimensional (2D) deriv. of graphite termed graphene has widespread applications in various frontiers areas of nanoscience and nanotechnologies. Graphene in its oxidized form named as graphene oxide (GO) has a mixed structure equipped with various oxygen contg. functional groups (epoxy, hydroxyl, carboxylic and carbonyl etc.) provides attachment sites to various biol. mols. including protein, DNA (DNA), RNA (RNA) etc. The attached biol. mols. with the help of functional groups make it a promising candidate in research field of biotechnol. and biomedical applications. The ease of processability and functionalization in aq. soln. due to available functional groups, amphiphilicity, better surface enhanced Raman scattering (SERS), fluorescence and its quenching ability better than graphene make GO a promising candidate for various biol. applications. The amphipathetic nature and high surface area of the GO not only prep. it as a biocompatible, soft and flexible intra/inter cellular carrier but also provides long-term biocompatibility with very low cytotoxicity. Inspite of this, still we lack a very recent review for advanced biol. applications of graphene oxide. This review deals the bio application of GO and the recent advancement as a biosensors, antibacterial agent, early detection of cancer, cancer cell imaging/mapping, targeted drug delivery and gene therapy etc.
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    20. 20
      Zhu, J.; Li, B.; Xu, M.; Liu, R.; Xia, T.; Zhang, Z.; Xu, Y.; Liu, S. Graphene Oxide Promotes Cancer Metastasis through Associating with Plasma Membrane To Promote TGF-β Signaling-Dependent Epithelial–Mesenchymal Transition. ACS Nano 2020, 14, 818– 827,  DOI: 10.1021/acsnano.9b07891
      20
      Graphene Oxide Promotes Cancer Metastasis through Associating with Plasma Membrane To Promote TGF-β Signaling-Dependent Epithelial-Mesenchymal Transition
      Zhu, Jianqiang; Li, Bin; Xu, Ming; Liu, Rui; Xia, Tian; Zhang, Zhihong; Xu, Yong; Liu, Sijin
      ACS Nano (2020), 14 (1), 818-827CODEN: ANCAC3; ISSN:1936-0851. (American Chemical Society)
      Nanomedicines are being developed to treat diverse diseases; however, inadvertent or unintended health effects has to be considered, esp. for those targeting cancers. For cancers, occurrence of metastasis hints an advanced phase of cancer progression, nanomedicines per se should be evaluated for their effects on existing metastatic tumors and triggering metastases. Graphene based 2D nanomaterials, such as graphene oxide (GO), due to its unique characteristics, has been extensively studied for biomedical applications including cancer therapy. However, the potential effect of GO on metastasis has not been detd. yet. Herein, we found that low-dose GO could induce significant morphol. and structural changes of cellular membrane within cancer cells, suggesting epithelial-mesenchymal transition (EMT), with enhanced invasion/migration and the alterations of representative EMT indicators in GO-treated cells. These changes resulted in enhanced lung metastasis of cancer cells in various metastasis models. The mechanistic investigations unveiled that GO elevated the protein levels of TGF-β receptor, leading to constitutively activated TGF-β-Smad2/3 signaling pathway that drives the EMT. Collectively, our findings enhance the understanding of the unintended side and detrimental effects of GO nanosheets in increasing the progression of metastatic tumors. Thus, the likelihood of pro-EMT effects upon low-dose GO exposure should be considered when developing GO nanomedicines.
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    21. 21
      Silvestrini, S.; De Filippo, C. C.; Vicentini, N.; Menna, E.; Mazzaro, R.; Morandi, V.; Ravotto, L.; Ceroni, P.; Maggini, M. Controlled functionalization of reduced graphene oxide enabled by microfluidic reactors. Chem. Mater. 2018, 30, 2905– 2914,  DOI: 10.1021/acs.chemmater.7b04740
      21
      Controlled Functionalization of Reduced Graphene Oxide Enabled by Microfluidic Reactors
      Silvestrini, Simone; De Filippo, Christian C.; Vicentini, Nicola; Menna, Enzo; Mazzaro, Raffaello; Morandi, Vittorio; Ravotto, Luca; Ceroni, Paola; Maggini, Michele
      Chemistry of Materials (2018), 30 (9), 2905-2914CODEN: CMATEX; ISSN:0897-4756. (American Chemical Society)
      The authors report the use of microfluidics to functionalize suspended reduced graphene oxide flakes through the addn. of aryl radical, generated in situ by reaction between aryl amines and isopentyl nitrite. Microfluidic enabled a tight control of temp., reaction times, and stoichiometric ratios, making it possible to tune the growth of oligomers on the surface of the flakes, which in turn affects the interactions of the functional material with the surrounding environment. Probably shear stress phenomena within the reactor may play a role in the chem. of graphene materials by providing a const. driving force toward exfoliation of the layered structures. Scale-up of the functionalization process is also reported along with the grafting of dyes based on squaric acid cores. Photophys. characterization of the dye-modified flakes proves that the microfluidic approach is a viable method toward the development of new materials with tailored properties.
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    22. 22
      Khan, M.; Al-Marri, A. H.; Khan, M.; Mohri, N.; Adil, S. F.; Al-Warthan, A.; Siddiqui, M. R. H.; Alkhathlan, H. Z.; Berger, R.; Tremel, W.; Tahir, M. N. Pulicaria glutinosa plant extract: a green and eco-friendly reducing agent for the preparation of highly reduced graphene oxide. RSC Adv. 2014, 4, 24119– 24125,  DOI: 10.1039/C4RA01296H
      22
      Pulicaria glutinosa plant extract: a green and eco-friendly reducing agent for the preparation of highly reduced graphene oxide
      Khan, Mujeeb; Al-Marri, Abdulhadi H.; Khan, Merajuddin; Mohri, Nils; Adil, Syed Farooq; Al-Warthan, Abdulrahman; Siddiqui, Mohammed Rafiq H.; Alkhathlan, Hamad Z.; Berger, Rudiger; Tremel, Wolfgang; Tahir, Muhammad Nawaz
      RSC Advances (2014), 4 (46), 24119-24125CODEN: RSCACL; ISSN:2046-2069. (Royal Society of Chemistry)
      The environmentally friendly synthesis of nanomaterials using green chem. has attracted tremendous attention in recent years due to its easy handling, low cost, and biocompatibility. Here we demonstrate a facile and efficient route for the synthesis of highly reduced graphene oxide (PE-HRG) by the green redn. of graphene oxide (GRO) using the Pulicaria glutinosa plant ext. (PE). The phytomols. present in the P. glutinosa ext. are not only responsible for the redn. of GRO, but also for the functionalization of the surface of the PE-HRG nanosheets and stabilize them in various solvents, thereby limiting the use of any other external and harmful chem. reductants and surfactants. The effect of PE on the dispersibility of PE-HRG in various solvents was investigated by prepg. PE-HRG with different amts. of PE, and the dispersibility of PE-HRG was compared with that of chem. reduced graphene oxide (CRG). The redn. of GRO was confirmed by UV-visible (UV-vis), Fourier-transform IR (FT-IR), Raman and X-ray photoelectron (XPS) spectroscopies, thermogravimetric anal. (TGA), X-ray powder diffraction (XRD) and transmission electron microscopy (TEM).
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    23. 23
      Tu, Z.; Achazi, K.; Schulz, A.; Mülhaupt, R.; Thierbach, S.; Rühl, E.; Adeli, M.; Haag, R. Combination of surface charge and size controls the cellular uptake of functionalized graphene sheets. Adv. Funct. Mater. 2017, 27, 1701837,  DOI: 10.1002/adfm.201701837
      There is no corresponding record for this reference.
    24. 24
      Lopez, A.; Liu, J. Covalent and Noncovalent Functionalization of Graphene Oxide with DNA for Smart Sensing. Adv. Intell. Syst. 2020, 2, 2000123,  DOI: 10.1002/aisy.202000123
      There is no corresponding record for this reference.
    25. 25
      Georgakilas, V.; Otyepka, M.; Bourlinos, A. B.; Chandra, V.; Kim, N.; Kemp, K. C.; Hobza, P.; Zboril, R.; Kim, K. S. Functionalization of graphene: covalent and non-covalent approaches, derivatives and applications. Chem. Rev. 2012, 112, 6156– 6214,  DOI: 10.1021/cr3000412
      25
      Functionalization of Graphene: Covalent and Non-Covalent Approaches, Derivatives and Applications
      Georgakilas, Vasilios; Otyepka, Michal; Bourlinos, Athanasios B.; Chandra, Vimlesh; Kim, Namdong; Kemp, K. Christian; Hobza, Pavel; Zboril, Radek; Kim, Kwang S.
      Chemical Reviews (Washington, DC, United States) (2012), 112 (11), 6156-6214CODEN: CHREAY; ISSN:0009-2665. (American Chemical Society)
      This comprehensive review covers all modes and methods of graphene functionalization including their classification. The complementary discussions of both exptl. and theor. aspects of graphene functionalization and interaction is presented. The functionalization modes related to chem. of graphene derivs. (graphene oxide, graphane, fluorographene) represent a significant part of the review, which thus considerably exceeds the chem. of pristine graphene. Both covalent functionalization based on binding of org. functionalities like free radicals and dienophiles on pristine graphene and attachment through the chem. of oxygen groups of graphene oxide are comprehensively discussed. The covalent attachments of hydrogen and halogens and, generally, the chem. of graphane and fluorographene are described. Noncovalent functionalization and interactions, which do not disrupt the extended p-conjugation on the graphene surface unlike covalent functionalization, are discussed. The theory of graphene-ligand non-covalent interactions is presented, while various interaction modes (p interactions) are analyzed from both theor. and exptl. viewpoints. The methods of deposition of various nanostructures on graphene are discussed, including a great variety of nanoparticles like noble metals, metal oxides, quantum dots, polymers, and others. The superior properties and applicability of these graphene-nanoparticle composites are extensively analyzed. The specific methods of graphene doping to control the type and concn. of charged carriers are summarized. Selected applications of functionalized graphene, including doped graphene electronic devices, magnetic bilayer intercalates, electronic/spintronic devices, and DNA sequencing devices, green chem., and bio-imaging, are discussed.
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    26. 26
      Georgakilas, V.; Tiwari, J. N.; Kemp, K. C.; Perman, J. A.; Bourlinos, A. B.; Kim, K. S.; Zboril, R. Noncovalent functionalization of graphene and graphene oxide for energy materials, biosensing, catalytic, and biomedical applications. Chem. Rev. 2016, 116, 5464– 5519,  DOI: 10.1021/acs.chemrev.5b00620
      26
      Noncovalent Functionalization of Graphene and Graphene Oxide for Energy Materials, Biosensing, Catalytic, and Biomedical Applications
      Georgakilas, Vasilios; Tiwari, Jitendra N.; Kemp, K. Christian; Perman, Jason A.; Bourlinos, Athanasios B.; Kim, Kwang S.; Zboril, Radek
      Chemical Reviews (Washington, DC, United States) (2016), 116 (9), 5464-5519CODEN: CHREAY; ISSN:0009-2665. (American Chemical Society)
      A review. This review focuses on noncovalent functionalization of graphene and graphene oxide with various species involving biomols., polymers, drugs, metals and metal oxide-based nanoparticles, quantum dots, magnetic nanostructures, other carbon allotropes (fullerenes, nanodiamonds, and carbon nanotubes), and graphene analogs (MoS2, WS2). A brief description of π-π interactions, van der Waals forces, ionic interactions, and hydrogen bonding allowing noncovalent modification of graphene and graphene oxide is first given. The main part of this Review is devoted to tailored functionalization for applications in drug delivery, energy materials, solar cells, water splitting, biosensing, bioimaging, environmental, catalytic, photocatalytic, and biomedical technologies. A significant part of this Review explores the possibilities of graphene/graphene oxide-based 3D superstructures and their use in lithium-ion batteries. This Review ends with a look at challenges and future prospects of noncovalently modified graphene and graphene oxide.
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    27. 27
      Parviz, D.; Das, S.; Ahmed, H. S. T.; Irin, F.; Bhattacharia, S.; Green, M. J. Dispersions of non-covalently functionalized graphene with minimal stabilizer. ACS Nano 2012, 6, 8857– 8867,  DOI: 10.1021/nn302784m
      27
      Dispersions of Non-Covalently Functionalized Graphene with Minimal Stabilizer
      Parviz, Dorsa; Das, Sriya; Ahmed, H. S. Tanvir; Irin, Fahmida; Bhattacharia, Sanjoy; Green, Micah J.
      ACS Nano (2012), 6 (10), 8857-8867CODEN: ANCAC3; ISSN:1936-0851. (American Chemical Society)
      We demonstrate that functionalized pyrene derivs. effectively stabilize single- and few-layer graphene flakes in aq. dispersions. The graphene/stabilizer yield obtained by this method is exceptionally high relative to conventional nanomaterial stabilizers such as surfactants or polymers. The mechanism of stabilization by pyrene derivs. is investigated by studying the effects of various parameters on dispersed graphene concn. and stability; these parameters include stabilizer concn., initial graphite concn., soln. pH, and type and no. of functional groups and counterions. The effectiveness of the pyrene derivs. is pH-tunable, as measured by zeta potential, and is also a function of the no. of functional groups, the electronegativity of the functional group, the counterion, the relative polarity between stabilizer and solvent, and the distance from the functional group to the basal plane. Even if the dispersion is destabilized by extreme pH or lyophilization, the graphene does not aggregate because the stabilizer remains adsorbed on the surface. These dispersions also show promise for applications in graphene/polymer nanocomposites (examd. in this paper), org. solar cells, conductive films, and ink-jet-printed electronic devices.
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    28. 28
      Zhu, C.; Kalin, A. J.; Fang, L. Covalent and Noncovalent Approaches to Rigid Coplanar π-Conjugated Molecules and Macromolecules. Acc. Chem. Res. 2019, 52, 1089– 1100,  DOI: 10.1021/acs.accounts.9b00022
      28
      Covalent and Noncovalent Approaches to Rigid Coplanar π-Conjugated Molecules and Macromolecules
      Zhu, Congzhi; Kalin, Alexander J.; Fang, Lei
      Accounts of Chemical Research (2019), 52 (4), 1089-1100CODEN: ACHRE4; ISSN:0001-4842. (American Chemical Society)
      A review. Mol. conformation and rigidity are essential factors in detg. the properties of individual mols., the assocd. supramol. assemblies, and bulk materials. This correlation is particularly important for π-conjugated mol. and macromol. systems. Within such an individual mol., a coplanar conformation facilitates the delocalization of not only MOs but also charges, excitons, and spins, leading to synergistically ensembled properties of the entire conjugated system. A rigid backbone, meanwhile, imposes a high energy cost to disrupt such a favorable conformation, ensuring the robustness and persistence of coplanarity. From a supramol. and material point of view, coplanarity and rigidity often promote strong intermol. electronic coupling and reduce the energy barrier for the intermol. transport of charges, excitons, and phonons, affording advanced materials properties in bulk. In this context, pursuing a rigid and coplanar mol. conformation often represents one of the primary objectives when designing and synthesizing conjugated mols. for electronic and optical applications. Two general bottom-up strategies-covalent annulation and noncovalent conformational control-are often employed to construct rigid coplanar π systems. These strategies have afforded various classes of such mols. and macromols., including so-called conjugated ladder polymers, graphene nanoribbons, polyacenes, and conformationally locked org. semiconductors. While pursuing these targets, however, one often confronts challenges assocd. with precise synthesis and limited soly. of the rigid coplanar systems, which could further impede their large-scale prepn., characterization, processing, and application. To address these issues, the authors developed and utilized a no. of synthetic methods and mol. engineering approaches to construct and to process rigid coplanar conjugated mols. and macromols. Structure-property correlations of this unique class of org. materials were established, providing important chem. principles for mol. design and materials applications. In this Account, the authors first describe the efforts to synthesize rigid coplanar π systems fused by various types of bonds, including kinetically formed covalent bonds, thermodynamically formed covalent bonds, N→B coordinate bonds, and hydrogen bonds, in order of increasing dynamic character. The subsequent section discusses the characteristic properties of selected examples of these rigid coplanar π systems in comparison with control compds. that are not rigid and coplanar, particularly focusing on the optical, electronic, and electrochem. properties. For systems bridged with noncovalent interactions, active manipulation of the dynamic bonds can tune variable properties at the mol. or collective level. Intermol. interactions, solid-state packing, and processing of several cases are then discussed to lay the foundation for future materials applications of rigid coplanar π conjugated compds.
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    29. 29
      Yu, W.; Sisi, L.; Haiyan, Y.; Jie, L. Progress in the functional modification of graphene/graphene oxide: a review. RSC Adv. 2020, 10, 15328– 15345,  DOI: 10.1039/D0RA01068E
      29
      Progress in the functional modification of graphene/graphene oxide: a review
      Yu, Wang; Sisi, Li; Haiyan, Yang; Jie, Luo
      RSC Advances (2020), 10 (26), 15328-15345CODEN: RSCACL; ISSN:2046-2069. (Royal Society of Chemistry)
      A review. Graphene and graphene oxide have attracted tremendous interest over the past decade due to their unique and excellent electronic, optical, mech., and chem. properties. This review focuses on the functional modification of graphene and graphene oxide. First, the basic structure, prepn. methods and properties of graphene and graphene oxide are briefly described. Subsequently, the methods for the redn. of graphene oxide are introduced. Next, the functionalization of graphene and graphene oxide is mainly divided into covalent binding modification, non-covalent binding modification and elemental doping. Then, the properties and application prospects of the modified products are summarized. Finally, the current challenges and future research directions are presented in terms of surface functional modification for graphene and graphene oxide.
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    30. 30
      Khan, M.; Shaik, M. R.; Adil, S. F.; Kuniyil, M.; Ashraf, M.; Frerichs, H.; Sarif, M. A.; Siddiqui, M. R. H.; Al-Warthan, A.; Labis, J. P. Facile synthesis of Pd@graphene nanocomposites with enhanced catalytic activity towards Suzuki coupling reaction. Sci. Rep. 2020, 10, 11728,  DOI: 10.1038/s41598-020-68124-w
      30
      Facile synthesis of Pd@graphene nanocomposites with enhanced catalytic activity towards Suzuki coupling reaction
      Khan, Mujeeb; Shaik, Mohammed Rafi; Adil, Syed Farooq; Kuniyil, Mufsir; Ashraf, Muhammad; Frerichs, Hajo; Sarif, Massih Ahmad; Siddiqui, Mohammed Rafiq H.; Al-Warthan, Abdulrahman; Labis, Joselito P.; Islam, Mohammad Shahidul; Tremel, Wolfgang; Tahir, Muhammad Nawaz
      Scientific Reports (2020), 10 (1), 11728CODEN: SRCEC3; ISSN:2045-2322. (Nature Research)
      A facile and chem. specific method to synthesize highly reduced graphene oxide (HRG) and Pd (HRG@Pd) nanocomposite was presented. The HRG surfaces were tailored with amine groups using 1-aminopyrene (1-AP) as functionalizing mols. The arom. rings of 1-AP sit on the basal planes of HRG through π-π interactions, leaving amino groups outwards (similar like self-assembled monolayer on 2D substrates). The amino groups provide the chem. specific binding sites to the Pd nucleation which subsequently grow into nanoparticles. HRG@Pd nanocomposite demonstrated both uniform distribution of Pd nanoparticles on HRG surface as well as excellent phys. stability and dispersibility. The surface functionalization was confirmed using, UV-visible (UV-Vis), Fourier transform infra-red and Raman spectroscopy. The size and distribution of Pd nanoparticles on the HRG and crystallinity were confirmed using high-resoln. transmission electron microscopy and powder X-ray diffraction and XPS. The catalytic efficiency of highly reduced graphene oxide-pyrene-palladium nanocomposite (HRG-Py-Pd) was tested towards the Suzuki coupling reactions of various aryl halides. The kinetics of the catalytic reaction (Suzuki coupling) using HRG-Py-Pd nanocomposite was monitored using gas chromatog. (GC).
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    31. 31
      Stark, W. J. Nanoparticles in biological systems. Angew. Chem., Int. Ed. 2011, 50, 1242– 1258,  DOI: 10.1002/anie.200906684
      31
      Nanoparticles in Biological Systems
      Stark, Wendelin J.
      Angewandte Chemie, International Edition (2011), 50 (6), 1242-1258CODEN: ACIEF5; ISSN:1433-7851. (Wiley-VCH Verlag GmbH & Co. KGaA)
      A review. Understanding the behavior of nanoparticles in biol. systems opens up new directions for medical treatments and is essential for the development of safe nanotechnol. This Review discusses mols. and nanoparticles when in contact with cells or whole organisms, with a focus on inorg. materials. The interaction of particles with biol. unravels a series of new mechanisms not found for mols.: altered biodistribution, chem. reactive interfaces, and the combination of solid-state properties and mobility. Externally guided movement of medicaments by using functional nanomagnets brings mechanics into drug design. In subsequent sections, the role of inertness and bioaccumulation is discussed in regard to the long-term safety of nanoparticles.
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    32. 32
      Khan, M.; Khan, S. T.; Khan, M.; Adil, S. F.; Musarrat, J.; Al-Khedhairy, A. A.; Al-Warthan, A.; Siddiqui, M.; Alkhathlan, H. Z. Antibacterial properties of silver nanoparticles synthesized using Pulicaria glutinosa plant extract as a green bioreductant. Int. J. Nanomed. 2014, 9, 3551– 3565,  DOI: 10.2147/IJN.S61983
      32
      Antibacterial properties of silver nanoparticles synthesized using Pulicaria glutinosa plant extract as a green bioreductant
      Khan, Mujeeb; Khan, Shams Tabrez; Khan, Merajuddin; Adil, Syed Farooq; Musarrat, Javed; Al-Khedhairy, Abdulaziz A.; Al-Warthan, Abdulrahman; Siddiqui, Mohammed Rafiq H.; Alkhathlan, Hamad Z.
      International Journal of Nanomedicine (2014), 9 (), 3551-3565CODEN: IJNNHQ; ISSN:1178-2013. (Dove Medical Press Ltd.)
      The antibacterial properties of nanoparticles (NPs) can be significantly enhanced by increasing the wettability or soly. of NPs in aq. medium. In this study, we investigated the effects of the stabilizing agent on the soly. of silver NPs and its subsequent effect on their antimicrobial activities. Silver NPs were prepd. using an aq. soln. of Pulicaria glutinosa plant ext. as bioreductant. The soln. also acts as a capping ligand. During this study, the antimicrobial activities of silver NPs, as well as the plant ext. alone, were tested against Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, and Micrococcus luteus. Silver NPs were prepd. with various concns. of the plant ext. to study its effect on antimicrobial activity. Interestingly, various concns. of P. glutinosa ext. did not show any effect on the growth of tested bacteria; however, a significant effect on the antimicrobial property of plant ext. capped silver NPs (Ag-NPs-PE) was obsd. For instance, the half maximal inhibitory concn. values were found to decrease (from 4% to 21%) with the increasing concns. of plant ext. used for the synthesis of Ag-NPs-PE. These results clearly indicate that the addn. of P. glutinosa exts. enhances the soly. of Ag-NPs-PE and, hence, increases their toxicity against the tested microorganisms.
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    33. 33
      Käkinen, A.; Kahru, A.; Nurmsoo, H.; Kubo, A.-L.; Bondarenko, O. M. Solubility-driven toxicity of CuO nanoparticles to Caco2 cells and Escherichia coli: Effect of sonication energy and test environment. Toxicol. In Vitro 2016, 36, 172– 179,  DOI: 10.1016/j.tiv.2016.08.004
      33
      Solubility-driven toxicity of CuO nanoparticles to Caco2 cells and Escherichia coli: Effect of sonication energy and test environment
      Kakinen, Aleksandr; Kahru, Anne; Nurmsoo, Helen; Kubo, Anna-Liisa; Bondarenko, Olesja M.
      Toxicology In Vitro (2016), 36 (), 172-179CODEN: TIVIEQ; ISSN:0887-2333. (Elsevier Ltd.)
      Due to small size and high surface energy nanoparticles (NPs) tend to agglomerate and ppt. To avoid/diminish that, sonication of NPs stock suspensions prior toxicity testing is often applied. Currently, there is no standardized particle sonication protocol available leading to inconsistent toxicity data, esp. if toxicity is driven by NPs' dissoln. that may be enhanced by sonication. In this study we addressed the effect of sonication on hydrodynamic size (Dh), dissoln. and toxicity of copper oxide (CuO) NPs to mammalian cell line Caco-2 in vitro and bacteria Escherichia coli in the resp. test environments (cell culture MEM medium, bacterial LB medium and deionised (DI) water). NPs were suspended using no sonication, water bath and probe sonication with different energy intensities. Increased sonication energy (i) decreased the Dh of CuO NPs in all three test environments; (ii) increased dissoln. of NPs in MEM medium and their toxicity to Caco-2; (iii) increased dissoln. of NPs in LB medium and their bioavailability to E. coli; and (iv) had no effect on dissoln. and antibacterial effects of NPs in DI water. Thus, to reduce variations in dissoln. and toxicity, we recommend sonication of NPs in DI water following the diln. into suitable test media.
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    34. 34
      Zuber, A.; Purdey, M.; Schartner, E.; Forbes, C.; Van der Hoek, B.; Giles, D.; Abell, A.; Monro, T.; Ebendorff-Heidepriem, H. Detection of gold nanoparticles with different sizes using absorption and fluorescence based method. Sens. Actuator, B 2016, 227, 117– 127,  DOI: 10.1016/j.snb.2015.12.044
      There is no corresponding record for this reference.
    35. 35
      Jayaseelan, C.; Ramkumar, R.; Rahuman, A. A.; Perumal, P. Green synthesis of gold nanoparticles using seed aqueous extract of Abelmoschus esculentus and its antifungal activity. Ind. Crops Prod. 2013, 45, 423– 429,  DOI: 10.1016/j.indcrop.2012.12.019
      35
      Green synthesis of gold nanoparticles using seed aqueous extract of Abelmoschus esculentus and its antifungal activity
      Jayaseelan, Chidambaram; Ramkumar, Rajendiran; Abdul Rahuman, Abdul; Perumal, Pachiappan
      Industrial Crops and Products (2013), 45 (), 423-429CODEN: ICRDEW; ISSN:0926-6690. (Elsevier B.V.)
      In the present work, we describe the synthesis of gold nanoparticles (Au NPs) using seed aq. ext. of Abelmoschus esculentus and its antifungal activity. UV-visible spectroscopy, XRD, FTIR, AFM, FESEM and EDX analyses were performed to ascertain the formation of Au NPs. The synthesized Au NPs were characterized by a peak at 536 nm in the UV-visible spectrum. XRD confirmed the cryst. nature of the nanoparticles of 62 nm size. The XRD peaks at 38°, 44°, 64° and 77° can be indexed to the (1 1 1), (2 0 0), (2 2 0) and (3 1 1) Bragg's reflections of cubic structure of metallic gold, resp. The FTIR result clearly showed that the exts. contg. OH as a functional group act in capping the nanoparticles synthesis. AFM shows the 3D topol. characteristic of Au NPs. FESEM images revealed that all particles were spherical with a narrow size range of 45-75 nm. Antifungal activity of Au NPs were tested against Puccinia graminis tritci, Aspergillus flavus, Aspergillus niger and Candida albicans using std. well diffusion method. The max. zone of inhibition was obsd. in the Au NPs against P. graminis (17 mm) and C. albicans (18 mm). The results suggest that the synthesized Au NPs act as an effective antifungal agent. It is confirmed that Au NPs are capable of rendering high antifungal efficacy and hence has a great potential in the prepn. of drugs used against fungal diseases.
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    36. 36
      Adil, S. F.; Assal, M. E.; Khan, M.; Shaik, M. R.; Kuniyil, M.; Sekou, D.; Dewidar, A. Z.; Al-Warthan, A.; Siddiqui, M. R. H. Eco-Friendly Mechanochemical Preparation of Ag2O–MnO2/Graphene Oxide Nanocomposite: An Efficient and Reusable Catalyst for the Base-Free, Aerial Oxidation of Alcohols. Catalysts 2020, 10, 281,  DOI: 10.3390/catal10030281
      36
      Eco-friendly mechanochemical preparation of Ag2O-MnO2/graphene oxide nanocomposite: an efficient and reusable yst for the base-free, aerial oxidation of alcohols
      Adil, Syed Farooq; Assal, Mohamed E.; Khan, Mujeeb; Shaik, Mohammed Rafi; Kuniyil, Mufsir; Sekou, Doumbia; Dewidar, Ahmed Z.; Al-Warthan, Abdulrahman; Siddiqui, Mohammed Rafiq H.
      Catalysts (2020), 10 (3), 281CODEN: CATACJ; ISSN:2073-4344. (MDPI AG)
      Recently, the development of eco-friendly mechanochem. approaches for the prepn. of novel ysts with enhanced activity and selectivity has gained considerable attention. Herein, we developed a rapid and solvent-less mechanochem. method for the prepn. of mixed metal oxide (Ag2O-MnO2) decorated graphene oxide (GRO)-based nanocomposites (Ag2O-MnO2/(X wt.%)GRO), as the Ag2O-MnO2/(X wt.%)GRO nanocomposite was fabricated by the phys. grinding of freshly prepd. GRO and pre-annealed (300°C) mixed metal oxide nanoparticles (NPs) (Ag2O-MnO2) using an eco-friendly milling procedure. The as-prepd. nanoysts were characterized by using various techniques. Furthermore, the nanocomposites were applied as a heterogeneous yst for the oxidn. of alc. by employing gaseous O2 as an eco-friendly oxidant under base-free conditions. The mechanochem. obtained GRO-based composite exhibited noticeable enhancement in the surface area and ytic performance compared to the pristine Ag2O-MnO2. The results revealed that (1%)Ag2O-MnO2/(5 wt.%)GRO yst exhibited higher specific performance (13.3 mmol.g-1.h-1) with a 100% conversion of benzyl alc. (BnOH) and >99% selectivity towards benzaldehyde (BnH) within 30 min. The enhancement of the activity and selectivity of GRO-based nanoyst was attributed to the presence of various oxygen-contg. functional groups, a large no. of defects, and a high sp. surface area of GRO. In addn., the as-prepd. nanoyst also demonstrated excellent ytic activity towards the conversion of a variety of other alcs. to resp. carbonyls under optimal conditions. Besides, the yst ((1%)Ag2O-MnO2/(5 wt.%)GRO) could be efficiently recycled six times with no noticeable loss in its performance and selectivity.
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    37. 37
      Cote, L. J.; Kim, F.; Huang, J. Langmuir–Blodgett assembly of graphite oxide single layers. J. Am. Chem. Soc. 2008, 131, 1043– 1049
      There is no corresponding record for this reference.
    38. 38
      Hummers, W. S., Jr.; Offeman, R. E. Preparation of Graphitic Oxide. J. Am. Chem. Soc. 1958, 80, 1339– 1339,  DOI: 10.1021/ja01539a017
      38
      Preparation of graphitic oxide
      Hummers, Wm. S., Jr.; Offeman, Richard E.
      Journal of the American Chemical Society (1958), 80 (), 1339CODEN: JACSAT; ISSN:0002-7863.
      See U.S. 2,798,878 (C.A. 51, 15080a).
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    39. 39
      Assal, M. E.; Shaik, M. R.; Kuniyil, M.; Khan, M.; Al-Warthan, A.; Siddiqui, M. R. H.; Khan, S. M. A.; Tremel, W.; Tahir, M. N.; Adil, S. F. A highly reduced graphene oxide/ZrOx–MnCO3 or −Mn2O3 nanocomposite as an efficient catalyst for selective aerial oxidation of benzylic alcohols. RSC Adv. 2017, 7, 55336– 55349,  DOI: 10.1039/C7RA11569E
      39
      A highly reduced graphene oxide/ZrOx-MnCO3 or -Mn2O3 nanocomposite as an efficient catalyst for selective aerial oxidation of benzylic alcohols
      Assal, Mohamed E.; Shaik, Mohammed Rafi; Kuniyil, Mufsir; Khan, Mujeeb; Al-Warthan, Abdulrahman; Siddiqui, Mohammed Rafiq H.; Khan, Sohail M. A.; Tremel, Wolfgang; Tahir, Muhammad Nawaz; Adil, Syed Farooq
      RSC Advances (2017), 7 (87), 55336-55349CODEN: RSCACL; ISSN:2046-2069. (Royal Society of Chemistry)
      Highly reduced graphene oxide (HRG) nanocomposites of manganese carbonate doped with (1%) zirconia (ZrOx) nanoparticles [ZrOx(1%)-MnCO3/(X%)HRG (where X = 0-7)] were prepd. employing a facile co-pptn. method in which the percentage of HRG was varied. Further calcination of the catalyst at 500 °C resulted in the conversion of manganese carbonate to manganese oxide [ZrOx(1%)-Mn2O3/(X%)HRG]. The effect of the inclusion of HRG on the catalytic activity along with its comparative performance between carbonates and their resp. oxides was studied for the liq.-phase selective oxidn. of benzylic alcs. into corresponding aldehydes using mol. oxygen as the eco-friendly oxidizing agent without adding any external additives or bases. The influence of different parameters such as different percentages of HRG, reaction times, calcination temps., catalyst dosages and reaction temps. have also been systematically studied in order to optimize the catalyst compn. and reaction conditions. The inclusion of HRG as a dopant remarkably enhanced the catalytic efficiency of ZrOx-MnCO3 nanocatalysts for the aerobic oxidn. of alcs. The catalyst with compn. ZrOx(1%)-MnCO3/(1%)HRG obtained by calcination at 300 °C exhibited excellent specific activity (60.0 mmol g-1 h-1) with 100% benzyl alc. conversion and more than 99% product selectivity within an extremely short time (4 min). The same catalyst is employed for the oxidn. of a wide range of substituted benzylic and aliph. alcs.
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    40. 40
      Nasr, F. A.; Shahat, A. A.; Alqahtani, A. S.; Ahmed, M. Z.; Qamar, W.; Al-Mishari, A. A.; Almoqbil, A. N. Centaurea bruguierana inhibits cell proliferation, causes cell cycle arrest, and induces apoptosis in human MCF-7 breast carcinoma cells. Mol. Biol. Rep. 2020, 47, 6043– 6051,  DOI: 10.1007/s11033-020-05679-x
      40
      Centaurea bruguierana inhibits cell proliferation, causes cell cycle arrest, and induces apoptosis in human MCF-7 breast carcinoma cells
      Nasr, Fahd A.; Shahat, Abdelaaty A.; Alqahtani, Ali S.; Ahmed, Mohammad Z.; Qamar, Wajhul; Al-Mishari, Abdullah A.; Almoqbil, Abdulaziz N.
      Molecular Biology Reports (2020), 47 (8), 6043-6051CODEN: MLBRBU; ISSN:0301-4851. (Springer)
      Abstr.: Centaurea bruguierana, of the Asteraceae family, has a long history of use in traditional medicines for the treatment of various ailments. However, the anticancer activity and underlying mechanisms have not yet been assessed. The C. bruguierana was extd. with methanol and fractionated into four different fractions. Different cancer cells and one non-cancerous were used to examine the cytotoxic effects of these fractions using MTT assay. The most potent fraction, C. bruguierana Et acetate fraction (CB EtOAc), was explored for its effects on cell cycle progression and apoptosis induction by Hoechst staining and annexin V-PI double staining in MCF-7 cells. The expression of apoptosis-related genes was quantified by RT-PCR. Of all fractions, CB EtOAc was found to have the strongest antiproliferative activity (IC50 = 10 mug/mL) against MCF-7 cells. The antiproliferative activity of the CB EtOAc fraction against MCF-7 was correlated with arrested of cell cycle in the G1 phase, nuclear fragmentation, and the exposure of phosphatidylserine. The induction of apoptosis by CB EtOAc in MCF-7 cells was also assocd. with an increase in the Bax/Bcl-2 ratio and higher expression of caspases. Overall, our results demonstrated that CB EtOAc showed apoptosis-inducing effects, suggesting that C. bruguierana may be a promising source for a novel chemotherapeutic agents for the treatment of breast cancer.
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    41. 41
      Alqahtani, A. S.; Nasr, F. A.; Noman, O. M.; Farooq, M.; Alhawassi, T.; Qamar, W.; El-Gamal, A. Cytotoxic evaluation and anti-angiogenic effects of two furano-sesquiterpenoids from Commiphora myrrh resin. Molecules 2020, 25, 1318,  DOI: 10.3390/molecules25061318
      41
      Cytotoxic Evaluation and Anti-Angiogenic Effects of Two Furano-Sesquiterpenoids from Commiphora myrrh resin
      Alqahtani, Ali S.; Nasr, Fahd A.; Noman, Omar M.; Farooq, Muhammad; Alhawassi, Tariq; Qamar, Wajhul; El-Gamal, Ali
      Molecules (2020), 25 (6), 1318CODEN: MOLEFW; ISSN:1420-3049. (MDPI AG)
      Commiphora myrrh resin (Myrrh) has been used in traditional Arabic medicine to treat various inflammatory diseases. Two furano-sesquiterpenoids, 2-methoxyfuranodiene (CM1) and 2-acetoxyfuranodiene (CM2), were isolated from the chloroform fraction of the ethanolic ext. of Arabic Commiphora myrrh resin. The cytotoxicity of the compds. was evaluated using human liver carcinoma, breast cancer cells (HepG2 and MCF-7, resp.) and normal human umbilical vein endothelial cells (HUVECs) cell lines. The development toxicity and anti-angiogenic activity of both compds. were also evaluated using zebrafish embryos. Cell survival assays demonstrated that both compds. were highly cytotoxic in HepG2 and MCF7 cells, with IC50 values of 3.6 and 4.4 muaM, resp. Both compds. induced apoptosis and caused cell cycle arrest in treated HepG2 cells, which was obsd. using flow cytometric anal. The development toxicity in zebrafish embryos showed the chronic toxicity of both compds. The toxicity was only seen when the embryos remained exposed to the compds. for more than three days. The compd. CM2 showed a significant level of anti-angiogenic activity in transgenic zebrafish embryos at sublethal doses. Thus, we demonstrated the cytotoxic properties of both compds., suggesting that the mol. mechanism of these compds. should be further assessed.
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