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Spatial- and Valence-Matched Neutralizing DNA Nanostructure Blocks Wild-Type SARS-CoV-2 and Omicron Variant Infection

  • Shuang Wan
    Shuang Wan
    The MOE Key Laboratory of Spectrochemical Analysis & Instrumentation, Key Laboratory of Chemical Biology of Fujian Province, State Key Laboratory of Physical Chemistry of Solid Surfaces, Department of Chemical Biology, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen, 361005, China
    More by Shuang Wan
  • Siwen Liu
    Siwen Liu
    State Key Laboratory for Emerging Infectious Diseases and InnoHK Centre for Infectious Diseases, Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China
    More by Siwen Liu
  • Miao Sun
    Miao Sun
    The MOE Key Laboratory of Spectrochemical Analysis & Instrumentation, Key Laboratory of Chemical Biology of Fujian Province, State Key Laboratory of Physical Chemistry of Solid Surfaces, Department of Chemical Biology, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen, 361005, China
    More by Miao Sun
  • Jialu Zhang
    Jialu Zhang
    The MOE Key Laboratory of Spectrochemical Analysis & Instrumentation, Key Laboratory of Chemical Biology of Fujian Province, State Key Laboratory of Physical Chemistry of Solid Surfaces, Department of Chemical Biology, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen, 361005, China
    Institute of Molecular Medicine, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200127, China
    More by Jialu Zhang
  • Xinyu Wei
    Xinyu Wei
    The MOE Key Laboratory of Spectrochemical Analysis & Instrumentation, Key Laboratory of Chemical Biology of Fujian Province, State Key Laboratory of Physical Chemistry of Solid Surfaces, Department of Chemical Biology, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen, 361005, China
    More by Xinyu Wei
  • Ting Song
    Ting Song
    The MOE Key Laboratory of Spectrochemical Analysis & Instrumentation, Key Laboratory of Chemical Biology of Fujian Province, State Key Laboratory of Physical Chemistry of Solid Surfaces, Department of Chemical Biology, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen, 361005, China
    More by Ting Song
  • Yuhao Li
    Yuhao Li
    The MOE Key Laboratory of Spectrochemical Analysis & Instrumentation, Key Laboratory of Chemical Biology of Fujian Province, State Key Laboratory of Physical Chemistry of Solid Surfaces, Department of Chemical Biology, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen, 361005, China
    More by Yuhao Li
  • Xinyang Liu
    Xinyang Liu
    The MOE Key Laboratory of Spectrochemical Analysis & Instrumentation, Key Laboratory of Chemical Biology of Fujian Province, State Key Laboratory of Physical Chemistry of Solid Surfaces, Department of Chemical Biology, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen, 361005, China
    More by Xinyang Liu
  • Honglin Chen*
    Honglin Chen
    State Key Laboratory for Emerging Infectious Diseases and InnoHK Centre for Infectious Diseases, Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China
    *Email: [email protected]
    More by Honglin Chen
  • Chaoyong James Yang*
    Chaoyong James Yang
    The MOE Key Laboratory of Spectrochemical Analysis & Instrumentation, Key Laboratory of Chemical Biology of Fujian Province, State Key Laboratory of Physical Chemistry of Solid Surfaces, Department of Chemical Biology, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen, 361005, China
    Institute of Molecular Medicine, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200127, China
    *Email: [email protected]
  • , and 
  • Yanling Song*
    Yanling Song
    The MOE Key Laboratory of Spectrochemical Analysis & Instrumentation, Key Laboratory of Chemical Biology of Fujian Province, State Key Laboratory of Physical Chemistry of Solid Surfaces, Department of Chemical Biology, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen, 361005, China
    *Email: [email protected]
    More by Yanling Song
Cite this: ACS Nano 2022, 16, 9, 15310–15317
Publication Date (Web):September 8, 2022
https://doi.org/10.1021/acsnano.2c06803
Copyright © 2022 American Chemical Society

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    Abstract

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    Natural ligand–receptor interactions that play pivotal roles in biological events are ideal models for design and assembly of artificial recognition molecules. Herein, aiming at the structural characteristics of the spike trimer and infection mechanism of SARS-CoV-2, we have designed a DNA framework-guided spatial-patterned neutralizing aptamer trimer for SARS-CoV-2 neutralization. The ∼5.8 nm tetrahedral DNA framework affords precise spatial organization and matched valence as four neutralizing aptamers (MATCH-4), which matches with nanometer precision the topmost surface of SARS-CoV-2 spike trimer, enhancing the interaction between MATCH-4 and spike trimer. Moreover, the DNA framework provides a dimensionally complementary nanoscale barrier to prevent the spike trimer–ACE2 interaction and the conformational transition, thereby inhibiting SARS-CoV-2–host cell fusion and infection. As a result, the spatial- and valence-matched MATCH-4 ensures improved binding affinity and neutralizing activity against SARS-CoV-2 and its varied mutant strains, particularly the current Omicron variant, that are evasive of the majority of existing neutralizing antibodies. In addition, because neutralizing aptamers specific to other targets can be evolved and assembled, the present design has the potential to inhibit other wide-range and emerging pathogens.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsnano.2c06803.

    • Yield analysis of TDF, MATCH-n assembly; TEM images of the MATCH-n assembled with quantitative AuNPs; the RMSD for each assembly; docking complexes of 1–3-aptamer binding with SARS-CoV-2 RBD; time-lapse, live confocal imaging; stability analysis of MATCH-4; H&E staining images; serum levels of IFN-α in mice; MATCH-n binding to white blood cells; and sequences of oligonucleotides (PDF)

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    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    This article is cited by 2 publications.

    1. Divita Mathur, Angelica Rose Galvan, Christopher M. Green, Kevin Liu, Igor L. Medintz. Uptake and stability of DNA nanostructures in cells: a cross-sectional overview of the current state of the art. Nanoscale 2023, 15 (6) , 2516-2528. https://doi.org/10.1039/D2NR05868E
    2. Jingran Chen, Ying Li, Zhen Liu. Functional nucleic acids as potent therapeutics against SARS-CoV-2 infection. Cell Reports Physical Science 2023, 4 (2) , 101249. https://doi.org/10.1016/j.xcrp.2023.101249

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