A human antibody reveals a conserved site on beta-coronavirus spike proteins and confers protection against SARS-CoV-2 infection

Zhou, Panpan; Yuan, Meng; Song, Ge; Beutler, Nathan; Shaabani, Namir; Huang, Deli; He, Wan-ting; Zhu, Xueyong; Callaghan, Sean; Yong, Peter; Anzanello, Fabio; Peng, Linghang; Ricketts, James; Parren, Mara; Garcia, Elijah; Rawlings, Stephen A.; Smith, Davey M.; Nemazee, David; Teijaro, John R.; Rogers, Thomas F.; Wilson, Ian A.; Burton, Dennis R.; Andrabi, Raiees

doi:10.1126/scitranslmed.abi9215

Title: A human antibody reveals a conserved site on beta-coronavirus spike proteins and confers protection against SARS-CoV-2 infection

Journal Article · 07 February 2022 · Science Translational Medicine

DOI: https://doi.org/10.1126/scitranslmed.abi9215 · OSTI ID:1982965

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^[1]; Parren, Mara ^[1]; Garcia, Elijah ^[1];

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The Scripps Research Inst., La Jolla, CA (United States)
Univ. of California, San Diego, CA (United States)
The Scripps Research Inst., La Jolla, CA (United States); Univ. of California, San Diego, CA (United States)
The Scripps Research Inst., La Jolla, CA (United States); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Harvard Univ., Cambridge, MA (United States); Ragon Institute of Massachusetts General Hospital, Cambridge, MA (United States)

Broadly neutralizing antibodies (bnAbs) to coronaviruses (CoVs) are valuable in their own right as prophylactic and therapeutic reagents to treat diverse CoVs and as templates for rational pan-CoV vaccine design. We recently described a bnAb, CC40.8, from a CoV disease 2019 (COVID-19) convalescent donor that exhibits broad reactivity with human β-CoVs. Here, we showed that CC40.8 targets the conserved S2 stem helix region of the CoV spike fusion machinery. We determined a crystal structure of CC40.8 Fab with a SARS-CoV-2 S2 stem peptide at 1.6-Å resolution and found that the peptide adopted a mainly helical structure. Conserved residues in β-CoVs interacted with CC40.8 antibody, thereby providing a molecular basis for its broad reactivity. CC40.8 exhibited in vivo protective efficacy against SARS-CoV-2 challenge in two animal models. In both models, CC40.8-treated animals exhibited less weight loss and reduced lung viral titers compared to controls. Furthermore, we noted that CC40.8-like bnAbs are relatively rare in human COVID-19 infection, and therefore, their elicitation may require rational structure-based vaccine design strategies. Overall, our study describes a target on β-CoV spike proteins for protective antibodies that may facilitate the development of pan–β-CoV vaccines.

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Research Organization:: SLAC National Accelerator Laboratory, Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1982965

Journal Information:: Science Translational Medicine, Journal Name: Science Translational Medicine Journal Issue: 637 Vol. 14; ISSN 1946-6234

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

References (96)

Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention Wu, Zunyou; McGoogan, Jennifer M. JAMA, Vol. 323, Issue 13 https://doi.org/10.1001/jama.2020.2648	journal	April 2020
SARS-CoV-2 Viral Variants—Tackling a Moving Target Mascola, John R.; Graham, Barney S.; Fauci, Anthony S. JAMA, Vol. 325, Issue 13 https://doi.org/10.1001/jama.2021.2088	journal	April 2021
Improvements to the APBS biomolecular solvation software suite: Improvements to the APBS Software Suite Jurrus, Elizabeth; Engel, Dave; Star, Keith Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3280	journal	October 2017
Serological Evidence of Bat SARS-Related Coronavirus Infection in Humans, China Wang, Ning; Li, Shi-Yue; Yang, Xing-Lou Virologica Sinica, Vol. 33, Issue 1 https://doi.org/10.1007/s12250-018-0012-7	journal	February 2018
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China Huang, Chaolin; Wang, Yeming; Li, Xingwang The Lancet, Vol. 395, Issue 10223 https://doi.org/10.1016/S0140-6736(20)30183-5	journal	February 2020
Comparing SARS-CoV-2 with SARS-CoV and influenza pandemics Petersen, Eskild; Koopmans, Marion; Go, Unyeong The Lancet Infectious Diseases, Vol. 20, Issue 9 https://doi.org/10.1016/S1473-3099(20)30484-9	journal	September 2020
Structure, Function, and Antigenicity of the SARS-CoV-2 Spike Glycoprotein Walls, Alexandra C.; Park, Young-Jun; Tortorici, M. Alejandra Cell, Vol. 181, Issue 2 https://doi.org/10.1016/j.cell.2020.02.058	journal	April 2020
Potent Neutralizing Antibodies against SARS-CoV-2 Identified by High-Throughput Single-Cell Sequencing of Convalescent Patients’ B Cells Cao, Yunlong; Su, Bin; Guo, Xianghua Cell, Vol. 182, Issue 1 https://doi.org/10.1016/j.cell.2020.05.025	journal	July 2020
Structures of Human Antibodies Bound to SARS-CoV-2 Spike Reveal Common Epitopes and Recurrent Features of Antibodies Barnes, Christopher O.; West, Anthony P.; Huey-Tubman, Kathryn E. Cell, Vol. 182, Issue 4 https://doi.org/10.1016/j.cell.2020.06.025	journal	August 2020
Structurally Resolved SARS-CoV-2 Antibody Shows High Efficacy in Severely Infected Hamsters and Provides a Potent Cocktail Pairing Strategy Du, Shuo; Cao, Yunlong; Zhu, Qinyu Cell, Vol. 183, Issue 4 https://doi.org/10.1016/j.cell.2020.09.035	journal	November 2020
Compromised Humoral Functional Evolution Tracks with SARS-CoV-2 Mortality Zohar, Tomer; Loos, Carolin; Fischinger, Stephanie Cell, Vol. 183, Issue 6 https://doi.org/10.1016/j.cell.2020.10.052	journal	December 2020
Site-Specific Glycosylation of Virion-Derived HIV-1 Env Is Mimicked by a Soluble Trimeric Immunogen Struwe, Weston B.; Chertova, Elena; Allen, Joel D. Cell Reports, Vol. 24, Issue 8 https://doi.org/10.1016/j.celrep.2018.07.080	journal	August 2018
Linear epitope landscape of the SARS-CoV-2 Spike protein constructed from 1,051 COVID-19 patients Li, Yang; Ma, Ming-liang; Lei, Qing Cell Reports, Vol. 34, Issue 13 https://doi.org/10.1016/j.celrep.2021.108915	journal	March 2021
Functional Relevance of Improbable Antibody Mutations for HIV Broadly Neutralizing Antibody Development Wiehe, Kevin; Bradley, Todd; Meyerhoff, R. Ryan Cell Host & Microbe, Vol. 23, Issue 6 https://doi.org/10.1016/j.chom.2018.04.018	journal	June 2018
Rational Vaccine Design in the Time of COVID-19 Burton, Dennis R.; Walker, Laura M. Cell Host & Microbe, Vol. 27, Issue 5 https://doi.org/10.1016/j.chom.2020.04.022	journal	May 2020
Shaping a universally broad antibody response to influenza amidst a variable immunoglobulin landscape Andrews, Sarah F.; McDermott, Adrian B. Current Opinion in Immunology, Vol. 53 https://doi.org/10.1016/j.coi.2018.04.009	journal	August 2018
Strategies for a multi-stage neutralizing antibody-based HIV vaccine Andrabi, Raiees; Bhiman, Jinal N.; Burton, Dennis R. Current Opinion in Immunology, Vol. 53 https://doi.org/10.1016/j.coi.2018.04.025	journal	August 2018
A systematic review and meta-analysis of published research data on COVID-19 infection fatality rates Meyerowitz-Katz, Gideon; Merone, Lea International Journal of Infectious Diseases, Vol. 101 https://doi.org/10.1016/j.ijid.2020.09.1464	journal	December 2020
Identification of Common Features in Prototype Broadly Neutralizing Antibodies to HIV Envelope V2 Apex to Facilitate Vaccine Design Andrabi, Raiees; Voss, James E.; Liang, Chi-Hui Immunity, Vol. 43, Issue 5 https://doi.org/10.1016/j.immuni.2015.10.014	journal	November 2015
SARS-CoV-2 Vaccines: Status Report Amanat, Fatima; Krammer, Florian Immunity, Vol. 52, Issue 4 https://doi.org/10.1016/j.immuni.2020.03.007	journal	April 2020
Optimization and validation of the TZM-bl assay for standardized assessments of neutralizing antibodies against HIV-1 Sarzotti-Kelsoe, Marcella; Bailer, Robert T.; Turk, Ellen Journal of Immunological Methods, Vol. 409 https://doi.org/10.1016/j.jim.2013.11.022	journal	July 2014
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Epitope-resolved profiling of the SARS-CoV-2 antibody response identifies cross-reactivity with endemic human coronaviruses Ladner, Jason T.; Henson, Sierra N.; Boyle, Annalee S. Cell Reports Medicine, Vol. 2, Issue 1 https://doi.org/10.1016/j.xcrm.2020.100189	journal	January 2021
Variant-proof vaccines — invest now for the next pandemic Burton, Dennis R.; Topol, Eric J. Nature, Vol. 590, Issue 7846 https://doi.org/10.1038/d41586-021-00340-4	journal	February 2021
Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor Ge, Xing-Yi; Li, Jia-Lu; Yang, Xing-Lou Nature, Vol. 503, Issue 7477 https://doi.org/10.1038/nature12711	journal	October 2013
Structural basis of potent Zika–dengue virus antibody cross-neutralization Barba-Spaeth, Giovanna; Dejnirattisai, Wanwisa; Rouvinski, Alexander Nature, Vol. 536, Issue 7614 https://doi.org/10.1038/nature18938	journal	June 2016
A SARS-like cluster of circulating bat coronaviruses shows potential for human emergence Menachery, Vineet D.; Yount, Boyd L.; Debbink, Kari Nature Medicine, Vol. 21, Issue 12 https://doi.org/10.1038/nm.3985	journal	November 2015
Antibodies, viruses and vaccines Burton, Dennis R. Nature Reviews Immunology, Vol. 2, Issue 9 https://doi.org/10.1038/nri891	journal	September 2002
Broad-spectrum antivirals against viral fusion Vigant, Frederic; Santos, Nuno C.; Lee, Benhur Nature Reviews Microbiology, Vol. 13, Issue 7 https://doi.org/10.1038/nrmicro3475	journal	June 2015
Linear epitopes of SARS-CoV-2 spike protein elicit neutralizing antibodies in COVID-19 patients Li, Yang; Lai, Dan-yun; Zhang, Hai-nan Cellular & Molecular Immunology, Vol. 17, Issue 10 https://doi.org/10.1038/s41423-020-00523-5	journal	September 2020
Differential processing of HIV envelope glycans on the virus and soluble recombinant trimer Cao, Liwei; Pauthner, Matthias; Andrabi, Raiees Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-06121-4	journal	September 2018
A conserved immunogenic and vulnerable site on the coronavirus spike protein delineated by cross-reactive monoclonal antibodies Wang, Chunyan; van Haperen, Rien; Gutiérrez-Álvarez, Javier Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21968-w	journal	March 2021
Cross-reactive serum and memory B-cell responses to spike protein in SARS-CoV-2 and endemic coronavirus infection Song, Ge; He, Wan-ting; Callaghan, Sean Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-23074-3	journal	May 2021
Broadly neutralizing antibodies from human survivors target a conserved site in the Ebola virus glycoprotein HR2–MPER region Flyak, Andrew I.; Kuzmina, Natalia; Murin, Charles D. Nature Microbiology, Vol. 3, Issue 6 https://doi.org/10.1038/s41564-018-0157-z	journal	May 2018
Functional assessment of cell entry and receptor usage for SARS-CoV-2 and other lineage B betacoronaviruses Letko, Michael; Marzi, Andrea; Munster, Vincent Nature Microbiology, Vol. 5, Issue 4 https://doi.org/10.1038/s41564-020-0688-y	journal	February 2020
Viral targets for vaccines against COVID-19 Dai, Lianpan; Gao, George F. Nature Reviews Immunology, Vol. 21, Issue 2 https://doi.org/10.1038/s41577-020-00480-0	journal	December 2020
Origin and evolution of pathogenic coronaviruses Cui, Jie; Li, Fang; Shi, Zheng-Li Nature Reviews Microbiology, Vol. 17, Issue 3 https://doi.org/10.1038/s41579-018-0118-9	journal	December 2018
SARS-CoV-2 variants, spike mutations and immune escape Harvey, William T.; Carabelli, Alessandro M.; Jackson, Ben Nature Reviews Microbiology, Vol. 19, Issue 7 https://doi.org/10.1038/s41579-021-00573-0	journal	June 2021
Commonality despite exceptional diversity in the baseline human antibody repertoire Briney, Bryan; Inderbitzin, Anne; Joyce, Collin Nature, Vol. 566, Issue 7744 https://doi.org/10.1038/s41586-019-0879-y	journal	January 2019
A pneumonia outbreak associated with a new coronavirus of probable bat origin Zhou, Peng; Yang, Xing-Lou; Wang, Xian-Guang Nature, Vol. 579, Issue 7798 https://doi.org/10.1038/s41586-020-2012-7	journal	February 2020
The pathogenicity of SARS-CoV-2 in hACE2 transgenic mice Bao, Linlin; Deng, Wei; Huang, Baoying Nature, Vol. 583, Issue 7818 https://doi.org/10.1038/s41586-020-2312-y	journal	May 2020
Cross-neutralization of SARS-CoV-2 by a human monoclonal SARS-CoV antibody Pinto, Dora; Park, Young-Jun; Beltramello, Martina Nature, Vol. 583, Issue 7815 https://doi.org/10.1038/s41586-020-2349-y	journal	May 2020
Human neutralizing antibodies elicited by SARS-CoV-2 infection Ju, Bin; Zhang, Qi; Ge, Jiwan Nature, Vol. 584, Issue 7819 https://doi.org/10.1038/s41586-020-2380-z	journal	May 2020
A human neutralizing antibody targets the receptor-binding site of SARS-CoV-2 Shi, Rui; Shan, Chao; Duan, Xiaomin Nature, Vol. 584, Issue 7819 https://doi.org/10.1038/s41586-020-2381-y	journal	May 2020
Convergent antibody responses to SARS-CoV-2 in convalescent individuals Robbiani, Davide F.; Gaebler, Christian; Muecksch, Frauke Nature, Vol. 584, Issue 7821 https://doi.org/10.1038/s41586-020-2456-9	journal	June 2020
Potently neutralizing and protective human antibodies against SARS-CoV-2 Zost, Seth J.; Gilchuk, Pavlo; Case, James Brett Nature, Vol. 584, Issue 7821 https://doi.org/10.1038/s41586-020-2548-6	journal	July 2020
SARS-CoV-2 vaccines in development Krammer, Florian Nature, Vol. 586, Issue 7830 https://doi.org/10.1038/s41586-020-2798-3	journal	September 2020
mRNA vaccine-elicited antibodies to SARS-CoV-2 and circulating variants Wang, Zijun; Schmidt, Fabian; Weisblum, Yiska Nature, Vol. 592, Issue 7855 https://doi.org/10.1038/s41586-021-03324-6	journal	February 2021
Antibody resistance of SARS-CoV-2 variants B.1.351 and B.1.1.7 Wang, Pengfei; Nair, Manoj S.; Liu, Lihong Nature, Vol. 593, Issue 7857 https://doi.org/10.1038/s41586-021-03398-2	journal	March 2021
SARS-CoV-2 501Y.V2 escapes neutralization by South African COVID-19 donor plasma Wibmer, Constantinos Kurt; Ayres, Frances; Hermanus, Tandile Nature Medicine, Vol. 27, Issue 4 https://doi.org/10.1038/s41591-021-01285-x	journal	March 2021
Structural basis for broad coronavirus neutralization Sauer, Maximilian M.; Tortorici, M. Alejandra; Park, Young-Jun Nature Structural & Molecular Biology, Vol. 28, Issue 6 https://doi.org/10.1038/s41594-021-00596-4	journal	May 2021
Repertoire Builder: high-throughput structural modeling of B and T cell receptors Schritt, Dimitri; Li, Songling; Rozewicki, John Molecular Systems Design & Engineering, Vol. 4, Issue 4 https://doi.org/10.1039/C9ME00020H	journal	January 2019
Identification of a Novel Coronavirus in Patients with Severe Acute Respiratory Syndrome Drosten, Christian; Günther, Stephan; Preiser, Wolfgang New England Journal of Medicine, Vol. 348, Issue 20 https://doi.org/10.1056/NEJMoa030747	journal	May 2003
Isolation of a Novel Coronavirus from a Man with Pneumonia in Saudi Arabia Zaki, Ali M.; van Boheemen, Sander; Bestebroer, Theo M. New England Journal of Medicine, Vol. 367, Issue 19 https://doi.org/10.1056/NEJMoa1211721	journal	November 2012
Human coronavirus NL63 employs the severe acute respiratory syndrome coronavirus receptor for cellular entry Hofmann, H.; Pyrc, K.; van der Hoek, L. Proceedings of the National Academy of Sciences, Vol. 102, Issue 22 https://doi.org/10.1073/pnas.0409465102	journal	May 2005
Crystal structure of NL63 respiratory coronavirus receptor-binding domain complexed with its human receptor Wu, K.; Li, W.; Peng, G. Proceedings of the National Academy of Sciences, Vol. 106, Issue 47 https://doi.org/10.1073/pnas.0908837106	journal	November 2009
SARS-like WIV1-CoV poised for human emergence Menachery, Vineet D.; Yount, Boyd L.; Sims, Amy C. Proceedings of the National Academy of Sciences, Vol. 113, Issue 11 https://doi.org/10.1073/pnas.1517719113	journal	March 2016
Structural basis of influenza virus fusion inhibition by the antiviral drug Arbidol Kadam, Rameshwar U.; Wilson, Ian A. Proceedings of the National Academy of Sciences, Vol. 114, Issue 2 https://doi.org/10.1073/pnas.1617020114	journal	December 2016
Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen Pallesen, Jesper; Wang, Nianshuang; Corbett, Kizzmekia S. Proceedings of the National Academy of Sciences, Vol. 114, Issue 35 https://doi.org/10.1073/pnas.1707304114	journal	August 2017
A new lease on life for an HIV-neutralizing antibody class and vaccine target Burton, Dennis R. Proceedings of the National Academy of Sciences, Vol. 118, Issue 7 https://doi.org/10.1073/pnas.2026390118	journal	January 2021
SARS-CoV-2 escape from a highly neutralizing COVID-19 convalescent plasma Andreano, Emanuele; Piccini, Giulia; Licastro, Danilo Proceedings of the National Academy of Sciences, Vol. 118, Issue 36 https://doi.org/10.1073/pnas.2103154118	journal	August 2021
Amino acid substitution matrices from protein blocks. Henikoff, S.; Henikoff, J. G. Proceedings of the National Academy of Sciences, Vol. 89, Issue 22, p. 10915-10919 https://doi.org/10.1073/pnas.89.22.10915	journal	November 1992
PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Dolinsky, T. J.; Nielsen, J. E.; McCammon, J. A. Nucleic Acids Research, Vol. 32, Issue Web Server, p. W665-W667 https://doi.org/10.1093/nar/gkh381	journal	July 2004
IgBLAST: an immunoglobulin variable domain sequence analysis tool Ye, Jian; Ma, Ning; Madden, Thomas L. Nucleic Acids Research, Vol. 41, Issue W1 https://doi.org/10.1093/nar/gkt382	journal	May 2013
What Are the Most Powerful Immunogen Design Vaccine Strategies?: Reverse Vaccinology 2.0 Shows Great Promise Burton, Dennis R. Cold Spring Harbor Perspectives in Biology, Vol. 9, Issue 11 https://doi.org/10.1101/cshperspect.a030262	journal	February 2017
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Structure of SARS Coronavirus Spike Receptor-Binding Domain Complexed with Receptor Li, F. Science, Vol. 309, Issue 5742 https://doi.org/10.1126/science.1116480	journal	September 2005
Broad and Potent Neutralizing Antibodies from an African Donor Reveal a New HIV-1 Vaccine Target Walker, L. M.; Phogat, S. K.; Chan-Hui, P. -Y. Science, Vol. 326, Issue 5950 https://doi.org/10.1126/science.1178746	journal	September 2009
Highly Conserved Protective Epitopes on Influenza B Viruses Dreyfus, C.; Laursen, N. S.; Kwaks, T. Science, Vol. 337, Issue 6100 https://doi.org/10.1126/science.1222908	journal	August 2012
Rational HIV Immunogen Design to Target Specific Germline B Cell Receptors Jardine, J.; Julien, J. -P.; Menis, S. Science, Vol. 340, Issue 6133 https://doi.org/10.1126/science.1234150	journal	March 2013
Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation Wrapp, Daniel; Wang, Nianshuang; Corbett, Kizzmekia S. Science, Vol. 367, Issue 6483 https://doi.org/10.1126/science.abb2507	journal	February 2020
A noncompeting pair of human neutralizing antibodies block COVID-19 virus binding to its receptor ACE2 Wu, Yan; Wang, Feiran; Shen, Chenguang Science, Vol. 368, Issue 6496 https://doi.org/10.1126/science.abc2241	journal	May 2020
Potent neutralizing antibodies from COVID-19 patients define multiple targets of vulnerability Brouwer, Philip J. M.; Caniels, Tom G.; van der Straten, Karlijn Science, Vol. 369, Issue 6504 https://doi.org/10.1126/science.abc5902	journal	June 2020
Broad neutralization of SARS-related viruses by human monoclonal antibodies Wec, Anna Z.; Wrapp, Daniel; Herbert, Andrew S. Science, Vol. 369, Issue 6504 https://doi.org/10.1126/science.abc7424	journal	June 2020
Isolation of potent SARS-CoV-2 neutralizing antibodies and protection from disease in a small animal model Rogers, Thomas F.; Zhao, Fangzhu; Huang, Deli Science, Vol. 369, Issue 6506 https://doi.org/10.1126/science.abc7520	journal	June 2020
Structure-based design of prefusion-stabilized SARS-CoV-2 spikes Hsieh, Ching-Lin; Goldsmith, Jory A.; Schaub, Jeffrey M. Science, Vol. 369, Issue 6510 https://doi.org/10.1126/science.abd0826	journal	July 2020
Studies in humanized mice and convalescent humans yield a SARS-CoV-2 antibody cocktail Hansen, Johanna; Baum, Alina; Pascal, Kristen E. Science https://doi.org/10.1126/science.abd0827	journal	June 2020
Structural basis of a shared antibody response to SARS-CoV-2 Yuan, Meng; Liu, Hejun; Wu, Nicholas C. Science, Vol. 369, Issue 6507 https://doi.org/10.1126/science.abd2321	journal	July 2020
Distinct conformational states of SARS-CoV-2 spike protein Cai, Yongfei; Zhang, Jun; Xiao, Tianshu Science https://doi.org/10.1126/science.abd4251	journal	July 2020
A universal coronavirus vaccine Koff, Wayne C.; Berkley, Seth F. Science, Vol. 371, Issue 6531 https://doi.org/10.1126/science.abh0447	journal	February 2021
Structural and functional ramifications of antigenic drift in recent SARS-CoV-2 variants Yuan, Meng; Huang, Deli; Lee, Chang-Chun D. Science, Vol. 373, Issue 6556 https://doi.org/10.1126/science.abh1139	journal	August 2021
Broad betacoronavirus neutralization by a stem helix–specific human antibody Pinto, Dora; Sauer, Maximilian M.; Czudnochowski, Nadine Science, Vol. 373, Issue 6559 https://doi.org/10.1126/science.abj3321	journal	September 2021
The receptor binding domain of the viral spike protein is an immunodominant and highly specific target of antibodies in SARS-CoV-2 patients Premkumar, Lakshmanane; Segovia-Chumbez, Bruno; Jadi, Ramesh Science Immunology, Vol. 5, Issue 48 https://doi.org/10.1126/sciimmunol.abc8413	journal	June 2020
Early cross-coronavirus reactive signatures of humoral immunity against COVID-19 Kaplonek, Paulina; Wang, Chuangqi; Bartsch, Yannic Science Immunology, Vol. 6, Issue 64 https://doi.org/10.1126/sciimmunol.abj2901	journal	October 2021
Further Evidence for Bats as the Evolutionary Source of Middle East Respiratory Syndrome Coronavirus Anthony, S. J.; Gilardi, K.; Menachery, V. D. mBio, Vol. 8, Issue 2 https://doi.org/10.1128/mBio.00373-17	journal	April 2017
Broadly Neutralizing Antiviral Antibodies Corti, Davide; Lanzavecchia, Antonio Annual Review of Immunology, Vol. 31, Issue 1 https://doi.org/10.1146/annurev-immunol-032712-095916	journal	March 2013
Structure-Based Vaccine Antigen Design Graham, Barney S.; Gilman, Morgan S. A.; McLellan, Jason S. Annual Review of Medicine, Vol. 70, Issue 1 https://doi.org/10.1146/annurev-med-121217-094234	journal	January 2019
Human Coronavirus: Host-Pathogen Interaction Fung, To Sing; Liu, Ding Xiang Annual Review of Microbiology, Vol. 73, Issue 1 https://doi.org/10.1146/annurev-micro-020518-115759	journal	September 2019
Structure, Function, and Evolution of Coronavirus Spike Proteins Li, Fang Annual Review of Virology, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-virology-110615-042301	journal	September 2016
Inhibition of HIV-1 by Fusion Inhibitors Eggink, Dirk; Berkhout, Ben; W. Sanders, Rogier Current Pharmaceutical Design, Vol. 16, Issue 33 https://doi.org/10.2174/138161210794079218	journal	November 2010
High Levels of Common Cold Coronavirus Antibodies in Convalescent Plasma Are Associated With Improved Survival in COVID-19 Patients Greenbaum, Uri; Klein, Kimberly; Martinez, Fernando Frontiers in Immunology, Vol. 12 https://doi.org/10.3389/fimmu.2021.675679	journal	April 2021
Preliminary Identification of Potential Vaccine Targets for the COVID-19 Coronavirus (SARS-CoV-2) Based on SARS-CoV Immunological Studies Ahmed, Syed Faraz; Quadeer, Ahmed A.; McKay, Matthew R. Viruses, Vol. 12, Issue 3 https://doi.org/10.3390/v12030254	journal	February 2020
Escape from neutralizing antibodies by SARS-CoV-2 spike protein variants Weisblum, Yiska; Schmidt, Fabian; Zhang, Fengwen eLife, Vol. 9 https://doi.org/10.7554/eLife.61312	journal	October 2020