Complete Mapping of Mutations to the SARS-CoV-2 Spike Receptor-Binding Domain that Escape Antibody Recognition

Cell Host & Microbe - Tập 29 - Trang 44-57.e9 - 2021
Allison J. Greaney1,2, Tyler N. Starr, Pavlo Gilchuk3, Seth J. Zost3, Elad Binshtein3, Andrea N. Loes1,4, Sarah K. Hilton1, John Huddleston5, Rachel Eguia1, Katharine H.D. Crawford1,2, Adam S. Dingens1, Rachel S. Nargi3, Rachel E. Sutton3, Naveenchandra Suryadevara3, Paul W. Rothlauf6,7, Zhuoming Liu6, Sean P.J. Whelan6, Robert H. Carnahan4,8, James E. Crowe4,8,9, Jesse D. Bloom1,2,4
1Basic Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA 98109, USA
2Department of Genome Sciences & Medical Scientist Training Program, University of Washington, Seattle, WA 98195, USA
3Vanderbilt Vaccine Center, Vanderbilt University Medical Center, Nashville, TN 37232, USA
4Howard Hughes Medical Institute, Seattle, WA 98109 USA
5Molecular and Cell Biology, University of Washington, Seattle, WA 98195 USA
6Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63110, USA
7Program in Virology, Harvard Medical School, Boston, MA 02115, USA
8Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232, USA
9Department of Pediatrics, Vanderbilt University Medical Center, Nashville, TN 37232, USA

Tài liệu tham khảo

Addetia, 2020, Neutralizing antibodies correlate with protection from SARS-CoV-2 in humans during a fishery vessel outbreak with high attack rate, J. Clin. Microbiol., 58, e02107-20, 10.1128/JCM.02107-20 Alsoussi, 2020, A Potently Neutralizing Antibody Protects Mice against SARS-CoV-2 Infection, J. Immunol., 205, 915, 10.4049/jimmunol.2000583 Amir, 2013, viSNE enables visualization of high dimensional single-cell data and reveals phenotypic heterogeneity of leukemia, Nat. Biotechnol., 31, 545, 10.1038/nbt.2594 Barnes, 2020, SARS-CoV-2 neutralizing antibody structures inform therapeutic strategies, Nature, 10.1038/s41586-020-2852-1 Barnes, 2020, Structural classification of neutralizing antibodies against the SARS-CoV-2 spike receptor-binding domain suggests vaccine and therapeutic strategies, bioRxiv Baum, 2020, Antibody cocktail to SARS-CoV-2 spike protein prevents rapid mutational escape seen with individual antibodies, Science, 369, 1014, 10.1126/science.abd0831 Baum, 2020, REGN-COV2 antibody cocktail prevents and treats SARS-CoV-2 infection in rhesus macaques and hamsters, bioRxiv Becht, 2018, Dimensionality reduction for visualizing single-cell data using UMAP, Nat. Biotechnol., 37 Bepler, 2019, Positive-unlabeled convolutional neural networks for particle picking in cryo-electron micrographs, Nat. Methods, 16, 1153, 10.1038/s41592-019-0575-8 Bepler, 2020, Topaz-Denoise: general deep denoising models for cryoEM and cryoET, Nat. Commun., 11, 5208, 10.1038/s41467-020-18952-1 Bogan, 1998, Anatomy of hot spots in protein interfaces, J. Mol. Biol., 280, 1, 10.1006/jmbi.1998.1843 Brouwer, 2020, Potent neutralizing antibodies from COVID-19 patients define multiple targets of vulnerability, Science, 369, 643, 10.1126/science.abc5902 Cao, 2020, Potent Neutralizing Antibodies against SARS-CoV-2 Identified by High-Throughput Single-Cell Sequencing of Convalescent Patients’ B Cells, Cell, 182, 73, 10.1016/j.cell.2020.05.025 Case, 2020, Neutralizing Antibody and Soluble ACE2 Inhibition of a Replication-Competent VSV-SARS-CoV-2 and a Clinical Isolate of SARS-CoV-2, Cell Host Microbe, 28, 475, 10.1016/j.chom.2020.06.021 Chen, 2014, Yeast-expressed recombinant protein of the receptor-binding domain in SARS-CoV spike protein with deglycosylated forms as a SARS vaccine candidate, Hum. Vaccin. Immunother., 10, 648, 10.4161/hv.27464 Chi, 2020, A neutralizing human antibody binds to the N-terminal domain of the Spike protein of SARS-CoV-2, Science, 369, 650, 10.1126/science.abc6952 Clackson, 1995, A hot spot of binding energy in a hormone-receptor interface, Science, 267, 383, 10.1126/science.7529940 Crawford, 2020, Protocol and Reagents for Pseudotyping Lentiviral Particles with SARS-CoV-2 Spike Protein for Neutralization Assays, Viruses, 12, 12, 10.3390/v12050513 Crawford, 2020, Dynamics of neutralizing antibody titers in the months after SARS-CoV-2 infection, J. Infect. Dis., jiaa618 Cunningham, 1993, Comparison of a structural and a functional epitope, J. Mol. Biol., 234, 554, 10.1006/jmbi.1993.1611 Dall’Acqua, 1998, A mutational analysis of binding interactions in an antigen-antibody protein-protein complex, Biochemistry, 37, 7981, 10.1021/bi980148j Dieterle, 2020, A Replication-Competent Vesicular Stomatitis Virus for Studies of SARS-CoV-2 Spike-Mediated Cell Entry and Its Inhibition, Cell Host Microbe, 28, 486, 10.1016/j.chom.2020.06.020 Dingens, 2019, An Antigenic Atlas of HIV-1 Escape from Broadly Neutralizing Antibodies Distinguishes Functional and Structural Epitopes, Immunity, 50, 520, 10.1016/j.immuni.2018.12.017 Dingens, 2020, Serological identification of SARS-CoV-2 infections among children visiting a hospital during the initial Seattle outbreak, Nat. Commun., 11, 4378, 10.1038/s41467-020-18178-1 Friedrich, 2004, Extraepitopic compensatory substitutions partially restore fitness to simian immunodeficiency virus variants that escape from an immunodominant cytotoxic-T-lymphocyte response, J. Virol., 78, 2581, 10.1128/JVI.78.5.2581-2585.2004 Gilchuk, 2020, Analysis of a Therapeutic Antibody Cocktail Reveals Determinants for Cooperative and Broad Ebolavirus Neutralization, Immunity, 52, 388, 10.1016/j.immuni.2020.01.001 Gilchuk, 2020, Integrated pipeline for the accelerated discovery of antiviral antibody therapeutics, Nat. Biomed. Eng., 4, 1030, 10.1038/s41551-020-0594-x Grant, 2006, Bio3d: an R package for the comparative analysis of protein structures, Bioinformatics, 22, 2695, 10.1093/bioinformatics/btl461 Hamilton, 2003, Production of complex human glycoproteins in yeast, Science, 301, 1244, 10.1126/science.1088166 Hassan, 2020, A SARS-CoV-2 Infection Model in Mice Demonstrates Protection by Neutralizing Antibodies, Cell, 182, 744, 10.1016/j.cell.2020.06.011 He, 2014, Identification of diverse alphacoronaviruses and genomic characterization of a novel severe acute respiratory syndrome-like coronavirus from bats in China, J. Virol., 88, 7070, 10.1128/JVI.00631-14 Hilton, 2020, dms-view: Interactive visualization tool for deep mutational scanning data, JOSS, 5, 2353, 10.21105/joss.02353 Hsieh, 2020, Structure-based design of prefusion-stabilized SARS-CoV-2 spikes, Science, 369, 1501, 10.1126/science.abd0826 Huang, 2020, Plasmablast-derived antibody response to acute SARS-CoV-2 infection in humans, bioRxiv Huo, 2020, Neutralization of SARS-CoV-2 by Destruction of the Prefusion Spike, Cell Host Microbe, 28, 445, 10.1016/j.chom.2020.06.010 Jin, 1992, High resolution functional analysis of antibody-antigen interactions, J. Mol. Biol., 226, 851, 10.1016/0022-2836(92)90636-X Ju, 2020, Human neutralizing antibodies elicited by SARS-CoV-2 infection, Nature, 584, 115, 10.1038/s41586-020-2380-z Julg, 2017, Protection against a mixed SHIV challenge by a broadly neutralizing antibody cocktail, Sci. Transl. Med., 9, 9 Katoh, 2013, MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Mol. Biol. Evol., 30, 772, 10.1093/molbev/mst010 Korber, 2020, Tracking Changes in SARS-CoV-2 Spike: Evidence that D614G Increases Infectivity of the COVID-19 Virus, Cell, 182, 812, 10.1016/j.cell.2020.06.043 Lam, 2020, Identifying SARS-CoV-2-related coronaviruses in Malayan pangolins, Nature, 583, 282, 10.1038/s41586-020-2169-0 Lan, 2020, Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor, Nature, 581, 215, 10.1038/s41586-020-2180-5 Lee, 2019, Mapping person-to-person variation in viral mutations that escape polyclonal serum targeting influenza hemagglutinin, eLife, 8, 8, 10.7554/eLife.49324 Letko, 2020, Functional assessment of cell entry and receptor usage for SARS-CoV-2 and other lineage B betacoronaviruses, Nat. Microbiol., 5, 562, 10.1038/s41564-020-0688-y Li, 2005, Structure of SARS coronavirus spike receptor-binding domain complexed with receptor, Science, 309, 1864, 10.1126/science.1116480 Li, 2020, The Impact of Mutations in SARS-CoV-2 Spike on Viral Infectivity and Antigenicity, Cell, 182, 1284, 10.1016/j.cell.2020.07.012 Linnemann, 1973, Measles vaccine: immunity, reinfection and revaccination, Am. J. Epidemiol., 97, 365, 10.1093/oxfordjournals.aje.a121517 Liu, 2020, Potent neutralizing antibodies against multiple epitopes on SARS-CoV-2 spike, Nature, 584, 450, 10.1038/s41586-020-2571-7 Loes, 2020, Attenuated Influenza Virions Expressing the SARS-CoV-2 Receptor-Binding Domain Induce Neutralizing Antibodies in Mice, Viruses, 12, 987, 10.3390/v12090987 Mastronarde, 2005, Automated electron microscope tomography using robust prediction of specimen movements, J. Struct. Biol., 152, 36, 10.1016/j.jsb.2005.07.007 Ohi, 2004, Negative Staining and Image Classification - Powerful Tools in Modern Electron Microscopy, Biol. Proced. Online, 6, 23, 10.1251/bpo70 Otwinowski, 2018, Inferring the shape of global epistasis, Proc. Natl. Acad. Sci. USA, 115, E7550, 10.1073/pnas.1804015115 Panum, 1939, Observation made during the epidemic of measles on the Faroe Islands in the year 1846, Med Classics, 3, 839 Pettersen, 2004, UCSF Chimera—a visualization system for exploratory research and analysis, Journal of Computational Chemistry, 25, 1605, 10.1002/jcc.20084 Piccoli, 2020, Mapping Neutralizing and Immunodominant Sites on the SARS-CoV-2 Spike Receptor-Binding Domain by Structure-Guided High-Resolution Serology, Cell, 183, 1024, 10.1016/j.cell.2020.09.037 Punjani, 2017, cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination, Nat. Methods, 14, 290, 10.1038/nmeth.4169 Rogers, 2020, Isolation of potent SARS-CoV-2 neutralizing antibodies and protection from disease in a small animal model, Science, 369, 956, 10.1126/science.abc7520 Schmidt, 2015, Viral receptor-binding site antibodies with diverse germline origins, Cell, 161, 1026, 10.1016/j.cell.2015.04.028 Schommers, 2020, Restriction of HIV-1 Escape by a Highly Broad and Potent Neutralizing Antibody, Cell, 180, 471, 10.1016/j.cell.2020.01.010 Seydoux, 2020, Analysis of a SARS-CoV-2-Infected Individual Reveals Development of Potent Neutralizing Antibodies with Limited Somatic Mutation, Immunity, 53, 98, 10.1016/j.immuni.2020.06.001 Shang, 2020, Structural basis of receptor recognition by SARS-CoV-2, Nature, 581, 221, 10.1038/s41586-020-2179-y Smith, 1970, Natural selection and the concept of a protein space, Nature, 225, 563, 10.1038/225563a0 Smith, 2004, Mapping the antigenic and genetic evolution of influenza virus, Science, 305, 371, 10.1126/science.1097211 Starr, 2020, Deep Mutational Scanning of SARS-CoV-2 Receptor Binding Domain Reveals Constraints on Folding and ACE2 Binding, Cell, 182, 1295, 10.1016/j.cell.2020.08.012 Steffen, 2020, The receptor binding domain of SARS-CoV-2 spike is the key target of neutralizing antibody in human polyclonal sera, bioRxiv ter Meulen, 2006, Human monoclonal antibody combination against SARS coronavirus: synergy and coverage of escape mutants, PLoS Med., 3, e237, 10.1371/journal.pmed.0030237 Tian, 2020, Potent binding of 2019 novel coronavirus spike protein by a SARS coronavirus-specific human monoclonal antibody, Emerg. Microbes Infect., 9, 382, 10.1080/22221751.2020.1729069 Tong, 2009, Detection of novel SARS-like and other coronaviruses in bats from Kenya, Emerg. Infect. Dis., 15, 482, 10.3201/eid1503.081013 Tortorici, 2020, Ultrapotent human antibodies protect against SARS-CoV-2 challenge via multiple mechanisms, Science, eabe3354 Walls, 2020, Elicitation of potent neutralizing antibody responses by designed protein nanoparticle vaccines for SARS-CoV-2, Cell, 183, 10.1016/j.cell.2020.10.043 Walls, 2020, Structure, Function, and Antigenicity of the SARS-CoV-2 Spike Glycoprotein, Cell, 181, 281, 10.1016/j.cell.2020.02.058 Wec, 2019, Development of a Human Antibody Cocktail that Deploys Multiple Functions to Confer Pan-Ebolavirus Protection, Cell Host Microbe, 25, 39, 10.1016/j.chom.2018.12.004 Wec, 2020, Broad neutralization of SARS-related viruses by human monoclonal antibodies, Science, 369, 731, 10.1126/science.abc7424 Weisblum, 2020, Escape from neutralizing antibodies by SARS-CoV-2 spike protein variants, eLife, 9, e61312, 10.7554/eLife.61312 Weissman, 2020, D614G Spike Mutation Increases SARS CoV-2 Susceptibility to Neutralization, medRxiv Wentz, 2007, A novel high-throughput screen reveals yeast genes that increase secretion of heterologous proteins, Appl. Environ. Microbiol., 73, 1189, 10.1128/AEM.02427-06 Wong, 2017, Receptor-binding loops in alphacoronavirus adaptation and evolution, Nat. Commun., 8, 1735, 10.1038/s41467-017-01706-x Wrapp, 2020, Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation, Science, 367, 1260, 10.1126/science.abb2507 Wu, 2020, A noncompeting pair of human neutralizing antibodies block COVID-19 virus binding to its receptor ACE2, Science, 368, 1274, 10.1126/science.abc2241 Yang, 2015, Isolation and Characterization of a Novel Bat Coronavirus Closely Related to the Direct Progenitor of Severe Acute Respiratory Syndrome Coronavirus, J. Virol., 90, 3253, 10.1128/JVI.02582-15 Yuan, 2020, A highly conserved cryptic epitope in the receptor binding domains of SARS-CoV-2 and SARS-CoV, Science, 368, 630, 10.1126/science.abb7269 Zhou, 2020, A Novel Bat Coronavirus Closely Related to SARS-CoV-2 Contains Natural Insertions at the S1/S2 Cleavage Site of the Spike Protein, Curr. Biol., 30, 2196, 10.1016/j.cub.2020.05.023 Zhou, 2020, A pneumonia outbreak associated with a new coronavirus of probable bat origin, Nature, 579, 270, 10.1038/s41586-020-2012-7 Zhou, 2020, A pH-dependent switch mediates conformational masking of SARS-CoV-2 spike, bioRxiv Zost, 2020, Potently neutralizing and protective human antibodies against SARS-CoV-2, Nature, 584, 443, 10.1038/s41586-020-2548-6 Zost, 2020, Rapid isolation and profiling of a diverse panel of human monoclonal antibodies targeting the SARS-CoV-2 spike protein, Nat. Med., 26, 1422, 10.1038/s41591-020-0998-x