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Customizing Morphology, Size, and Response Kinetics of Matrix Metalloproteinase-Responsive Nanostructures by Systematic Peptide Design

  • Jiye Son
    Jiye Son
    Advanced Science Research Center at The Graduate Center of the City University of New York, 85 Saint Nicholas Terrace, New York, New York 10031, United States
    Department of Chemistry, Brooklyn College, City University of New York, 2900 Bedford Avenue, Brooklyn, New York 11210, United States
    ChemistryPh.D. Programs in , The Graduate Center of the City University of New York, 365 Fifth Avenue, New York, New York 10016, United States
    More by Jiye Son
  • Daniela Kalafatovic
    Daniela Kalafatovic
    Advanced Science Research Center at The Graduate Center of the City University of New York, 85 Saint Nicholas Terrace, New York, New York 10031, United States
  • Mohit Kumar
    Mohit Kumar
    Advanced Science Research Center at The Graduate Center of the City University of New York, 85 Saint Nicholas Terrace, New York, New York 10031, United States
    More by Mohit Kumar
  • Barney Yoo
    Barney Yoo
    Department of Chemistry, Hunter College, City University of New York, 695 Park Avenue, New York, New York 10065, United States
    More by Barney Yoo
  • Mike A. Cornejo
    Mike A. Cornejo
    Department of Chemistry, Brooklyn College, City University of New York, 2900 Bedford Avenue, Brooklyn, New York 11210, United States
    More by Mike A. Cornejo
  • María Contel
    María Contel
    Department of Chemistry, Brooklyn College, City University of New York, 2900 Bedford Avenue, Brooklyn, New York 11210, United States
    Chemistry,  Biochemistry  and  BiologyPh.D. Programs in , The Graduate Center of the City University of New York, 365 Fifth Avenue, New York, New York 10016, United States
    More by María Contel
  • , and 
  • Rein V. Ulijn*
    Rein V. Ulijn
    Advanced Science Research Center at The Graduate Center of the City University of New York, 85 Saint Nicholas Terrace, New York, New York 10031, United States
    ChemistryPh.D. Programs in , The Graduate Center of the City University of New York, 365 Fifth Avenue, New York, New York 10016, United States
    Department of Chemistry, Hunter College, City University of New York, 695 Park Avenue, New York, New York 10065, United States
    *E-mail: [email protected]
    More by Rein V. Ulijn
Cite this: ACS Nano 2019, 13, 2, 1555–1562
Publication Date (Web):January 28, 2019
https://doi.org/10.1021/acsnano.8b07401
Copyright © 2019 American Chemical Society

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    Abstract

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    Overexpression and activation of matrix metalloproteinase-9 (MMP-9) is associated with multiple diseases and can serve as a stimulus to activate nanomaterials for sensing and controlled release. In order to achieve autonomous therapeutics with improved space-time targeting capabilities, several features need to be considered beyond the introduction of an enzyme-cleavable linker into a nanostructure. We introduce guiding principles for a customizable platform using supramolecular peptide nanostructures with three modular components to achieve tunable kinetics and morphology changes upon MMP-9 exposure. This approach enables (1) fine-tuning of kinetics through introduction of ordered/disordered structures, (2) a 12-fold variation in hydrolysis rates achieved by electrostatic (mis)matching of particle and enzyme charge, and (3) selection of enzymatic reaction products that are either cell-killing nanofibers or disintegrate. These guiding principles, which can be rationalized and involve exchange of just a few amino acids, enable systematic customization of enzyme-responsive peptide nanostructures for general use in performance optimization of enzyme-responsive materials.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.8b07401.

    • MMP-9 cleavage studies by LC–MS and characterization of peptides using HRMS, 1H NMR, AFM, TEM, FTIR, ζ-potential, and CAC studies (PDF)

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    Cited By

    This article is cited by 17 publications.

    1. Douglas S. MacPherson, Dhwanit Dave, Salma Kassem, Selma Doganata, Brian M. Zeglis, Rein V. Ulijn. Tuning Supramolecular Chirality in Iodinated Amphiphilic Peptides Through Tripeptide Linker Editing. Biomacromolecules 2024, 25 (4) , 2277-2285. https://doi.org/10.1021/acs.biomac.3c01120
    2. Yaron Marciano, Nazia Nayeem, Dhwanit Dave, Rein V. Ulijn, Maria Contel. N-Acetylation of Biodegradable Supramolecular Peptide Nanofilaments Selectively Enhances Their Proteolytic Stability for Targeted Delivery of Gold-Based Anticancer Agents. ACS Biomaterials Science & Engineering 2023, 9 (6) , 3379-3389. https://doi.org/10.1021/acsbiomaterials.3c00312
    3. Yang Zhou, Qianqian Li, Ye Wu, Xinyu Li, Ya Zhou, Zhu Wang, Hui Liang, Feiqing Ding, Sheng Hong, Nicole F. Steinmetz, Hui Cai. Molecularly Stimuli-Responsive Self-Assembled Peptide Nanoparticles for Targeted Imaging and Therapy. ACS Nano 2023, 17 (9) , 8004-8025. https://doi.org/10.1021/acsnano.3c01452
    4. Yaron Marciano, Virginia del Solar, Nazia Nayeem, Dhwanit Dave, Jiye Son, María Contel, Rein V. Ulijn. Encapsulation of Gold-Based Anticancer Agents in Protease-Degradable Peptide Nanofilaments Enhances Their Potency. Journal of the American Chemical Society 2023, 145 (1) , 234-246. https://doi.org/10.1021/jacs.2c09820
    5. Matthew J. Sis, Zhou Ye, Katherine La Costa, Matthew J. Webber. Energy Landscapes of Supramolecular Peptide–Drug Conjugates Directed by Linker Selection and Drug Topology. ACS Nano 2022, 16 (6) , 9546-9558. https://doi.org/10.1021/acsnano.2c02804
    6. Douglas S. MacPherson, Scott A. McPhee, Brian M. Zeglis, Rein V. Ulijn. The Impact of Tyrosine Iodination on the Aggregation and Cleavage Kinetics of MMP-9-Responsive Peptide Sequences. ACS Biomaterials Science & Engineering 2022, 8 (2) , 579-587. https://doi.org/10.1021/acsbiomaterials.1c01488
    7. Fahmeed Sheehan, Deborah Sementa, Ankit Jain, Mohit Kumar, Mona Tayarani-Najjaran, Daniela Kroiss, Rein V. Ulijn. Peptide-Based Supramolecular Systems Chemistry. Chemical Reviews 2021, 121 (22) , 13869-13914. https://doi.org/10.1021/acs.chemrev.1c00089
    8. Sangpil Kim, Batakrishna Jana, Eun Min Go, Ji Eun Lee, Seongeon Jin, Eun-Koung An, Juyoung Hwang, Youjung Sim, Sehee Son, Dohyun Kim, Chaekyu Kim, Jun-O Jin, Sang Kyu Kwak, Ja-Hyoung Ryu. Intramitochondrial Disulfide Polymerization Controls Cancer Cell Fate. ACS Nano 2021, 15 (9) , 14492-14508. https://doi.org/10.1021/acsnano.1c04015
    9. Mohit Kumar, Jiye Son, Richard H. Huang, Deborah Sementa, Magdelene Lee, Stephen O’Brien, Rein V. Ulijn. In Situ, Noncovalent Labeling and Stimulated Emission Depletion-Based Super-Resolution Imaging of Supramolecular Peptide Nanostructures. ACS Nano 2020, 14 (11) , 15056-15063. https://doi.org/10.1021/acsnano.0c05029
    10. Yejiao Shi, Peter A. Summers, Marina K. Kuimova, Helena S. Azevedo. Unravelling the Enzymatic Degradation Mechanism of Supramolecular Peptide Nanofibers and Its Correlation with Their Internal Viscosity. Nano Letters 2020, 20 (10) , 7375-7381. https://doi.org/10.1021/acs.nanolett.0c02781
    11. Elham Radvar, Yejiao Shi, Salvatore Grasso, Charlotte J. C. Edwards-Gayle, Xitong Liu, Meagan S. Mauter, Valeria Castelletto, Ian W. Hamley, Michael J. Reece, Helena S. Azevedo. Magnetic Field-Induced Alignment of Nanofibrous Supramolecular Membranes: A Molecular Design Approach to Create Tissue-like Biomaterials. ACS Applied Materials & Interfaces 2020, 12 (20) , 22661-22672. https://doi.org/10.1021/acsami.0c05191
    12. Qingxin Yao, Chenlei Wang, Meifang Fu, Luru Dai, Junbai Li, Yuan Gao. Dynamic Detection of Active Enzyme Instructed Supramolecular Assemblies In Situ via Super-Resolution Microscopy. ACS Nano 2020, 14 (4) , 4882-4889. https://doi.org/10.1021/acsnano.0c00883
    13. Wenqi Yu, Rui Liu, Yang Zhou, Huile Gao. Size-Tunable Strategies for a Tumor Targeted Drug Delivery System. ACS Central Science 2020, 6 (2) , 100-116. https://doi.org/10.1021/acscentsci.9b01139
    14. Patrizia Janković, Iva Šantek, Ana Sofia Pina, Daniela Kalafatovic. Exploiting Peptide Self-Assembly for the Development of Minimalistic Viral Mimetics. Frontiers in Chemistry 2021, 9 https://doi.org/10.3389/fchem.2021.723473
    15. Jiali Chen, Yan Zhao, Qingxin Yao, Yuan Gao. Pathological environment directed in situ peptidic supramolecular assemblies for nanomedicines. Biomedical Materials 2021, 16 (2) , 022011. https://doi.org/10.1088/1748-605X/abc2e9
    16. Mengqian Li, Guangkuo Zhao, Wei-Ke Su, Qi Shuai. Enzyme-Responsive Nanoparticles for Anti-tumor Drug Delivery. Frontiers in Chemistry 2020, 8 https://doi.org/10.3389/fchem.2020.00647
    17. Seema Gupta, Indu Singh, Ashwani K. Sharma, Pradeep Kumar. Ultrashort Peptide Self-Assembly: Front-Runners to Transport Drug and Gene Cargos. Frontiers in Bioengineering and Biotechnology 2020, 8 https://doi.org/10.3389/fbioe.2020.00504

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