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Novel Multifunctional Silver Nanocomposite Serves as a Resistance-Reversal Agent to Synergistically Combat Carbapenem-Resistant Acinetobacter baumannii

  • Xisheng Li
    Xisheng Li
    Department of Laboratory Medicine, The Third Xiangya Hospital, Central South University, Changsha 410013, P. R. China
    More by Xisheng Li
  • , 
  • Rong Gui
    Rong Gui
    Department of Blood Transfusion, The Third Xiangya Hospital, Central South University, Changsha 410013, P. R. China
    More by Rong Gui
  • , 
  • Jian Li
    Jian Li
    Department of Blood Transfusion, The Third Xiangya Hospital, Central South University, Changsha 410013, P. R. China
    More by Jian Li
  • , 
  • Rong Huang
    Rong Huang
    Department of Blood Transfusion, The Third Xiangya Hospital, Central South University, Changsha 410013, P. R. China
    More by Rong Huang
  • , 
  • Yinghui Shang
    Yinghui Shang
    Department of Blood Transfusion, The Third Xiangya Hospital, Central South University, Changsha 410013, P. R. China
    More by Yinghui Shang
  • , 
  • Qiangqiang Zhao
    Qiangqiang Zhao
    Department of Blood Transfusion, The Third Xiangya Hospital, Central South University, Changsha 410013, P. R. China
    More by Qiangqiang Zhao
  • , 
  • Haiting Liu
    Haiting Liu
    Department of Blood Transfusion, The Third Xiangya Hospital, Central South University, Changsha 410013, P. R. China
    More by Haiting Liu
  • , 
  • Haiye Jiang
    Haiye Jiang
    Department of Laboratory Medicine, The Third Xiangya Hospital, Central South University, Changsha 410013, P. R. China
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  • , 
  • Xueling Shang
    Xueling Shang
    Department of Laboratory Medicine, The Third Xiangya Hospital, Central South University, Changsha 410013, P. R. China
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  • , 
  • Xin Wu
    Xin Wu
    Department of Orthopedics, The Third Xiangya Hospital, Central South University, Changsha 410013, P. R. China
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    Orcidhttps://orcid.org/0000-0001-8641-0382
  • , and 
  • Xinmin Nie*
    Xinmin Nie
    Department of Laboratory Medicine, The Third Xiangya Hospital, Central South University, Changsha 410013, P. R. China
    Hunan Engineering Technology Research Center of Optoelectronic Health Detection, Changsha 410000, Hunan, China
    *Email: [email protected]. Phone/Fax: +86-731-8861 8520.
    More by Xinmin Nie
    Orcidhttps://orcid.org/0000-0003-4399-8731
Cite this: ACS Appl. Mater. Interfaces 2021, 13, 26, 30434–30457
Publication Date (Web):June 23, 2021
https://doi.org/10.1021/acsami.1c10309
Copyright © 2021 American Chemical Society
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    Abstract

    Abstract Image

    In the face of the abundant production of various types of carbapenemases, the antibacterial efficiency of imipenem, seen as “the last line of defense”, is weakening. Following, the incidence of carbapenem-resistant Acinetobacter baumannii (CRAB), which can generate antibiotic-resistant biofilms, is increasing. Based on the superior antimicrobial activity of silver nanoparticles against multifarious bacterial strains compared with common antibiotics, we constructed the IPM@AgNPs-PEG-NOTA nanocomposite (silver nanoparticles were coated with SH-PEG-NOTA as well as loaded by imipenem) whose core was a silver nanoparticle to address the current challenge, and IPM@AgNPs-PEG-NOTA was able to function as a novel smart pH-sensitive nanodrug system. Synergistic bactericidal effects of silver nanoparticles and imipenem as well as drug-resistance reversal via protection of the β-ring of carbapenem due to AgNPs-PEG-NOTA were observed; thus, this nanocomposite confers multiple advantages for efficient antibacterial activity. Additionally, IPM@AgNPs-PEG-NOTA not only offers immune regulation and accelerates tissue repair to improve therapeutic efficacy in vivo but also can prevent the interaction of pathogens and hosts. Compared with free imipenem or silver nanoparticles, this platform significantly enhanced antibacterial efficiency while increasing reactive oxygen species (ROS) production and membrane damage, as well as affecting cell wall formation and metabolic pathways. According to the results of crystal violet staining, LIVE/DEAD backlight bacterial viability staining, and real-time quantitative polymerase chain reaction (RT-qPCR), this silver nanocomposite downregulated the levels of ompA expression to prevent formation of biofilms. In summary, this research demonstrated that the IPM@AgNPs-PEG-NOTA nanocomposite is a promising antibacterial agent of security, pH sensitivity, and high efficiency in reversing resistance and synergistically combatting carbapenem-resistant A. baumannii. In the future, various embellishments and selected loads for silver nanoparticles will be the focus of research in the domains of medicine and nanotechnology.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsami.1c10309.

    • Screening of carbapenem-resistant A. baumannii by disk diffusion and modified imipenem-EDTA disk potentiation test (Figure S1); screening of resistance-associated genes (blaNDM, blaIMP, blaIMP) by the PCR assay (Figure S2); flow diagram of SH-PEG2000-NOTA synthesis (Figure S3); mass spectrogram of SH-PEG2000-NOTA (Figure S4); H NMR spectra of SH-PEG2000-NOTA (Figure S5); flow diagram (Figure S6); SEM micrographs of carbapenem-resistant A. baumannii exposed to the respective materials for 12 h (Figure S7); relative percentage of biofilm inhibition by crystal violet assay (Figure S8); percentage of dead MLE-12 cells (Figure S9); viability of MLE-12 cells upon imipenem treatment for 24 h by MTT analysis (Figure S10); viability of MLE-12 cells upon SH-PEG-NOTA treatment for 24 h by MTT analysis (Figure S11); primers for amplification of genes from carbapenem-resistant A. baumannii (Table S1) (PDF)

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    This article is cited by 15 publications.

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