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Memory B cell repertoire for recognition of evolving SARS-CoV-2 spike

Pei Tong, Avneesh Gautam, Ian Windsor, Meghan Travers, Yuezhou Chen, Nicholas Garcia, Noah B. Whiteman, Lindsay G.A. McKay, Felipe J.N. Lelis, Shaghayegh Habibi, Yongfei Cai, Linda J. Rennick, W. Paul Duprex, Kevin R. McCarthy, Christy L. Lavine, Teng Zuo, Junrui Lin, Adam Zuiani, Jared Feldman, Elizabeth A. MacDonald, Blake M. Hauser, Anthony Griffths, Michael S. Seaman, Aaron G. Schmidt, Bing Chen, Donna Neuberg, Goran Bajic, Stephen C. Harrison, View ORCID ProfileDuane R. Wesemann
doi: https://doi.org/10.1101/2021.03.10.434840
Pei Tong
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Avneesh Gautam
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Ian Windsor
2Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA
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Meghan Travers
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Yuezhou Chen
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Nicholas Garcia
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Noah B. Whiteman
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Lindsay G.A. McKay
3Department of Microbiology, Boston University School of Medicine, Boston, MA 02115, USA
4National Emerging Infectious Diseases Laboratories, Boston University, Boston, MA 02115, USA
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Felipe J.N. Lelis
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Shaghayegh Habibi
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Yongfei Cai
5Laboratory of Molecular Medicine, Boston Children’s Hospital, Boston, MA 02115, USA
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Linda J. Rennick
6The Center for Vaccine Research, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261
7The Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh PA
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W. Paul Duprex
6The Center for Vaccine Research, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261
7The Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh PA
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Kevin R. McCarthy
6The Center for Vaccine Research, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261
7The Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh PA
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Christy L. Lavine
8Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA 02115, USA
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Teng Zuo
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Junrui Lin
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Adam Zuiani
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Jared Feldman
9Ragon Institute of MGH, MIT, and Harvard, Cambridge, MA 02139, USA
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Elizabeth A. MacDonald
2Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA
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Blake M. Hauser
9Ragon Institute of MGH, MIT, and Harvard, Cambridge, MA 02139, USA
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Anthony Griffths
3Department of Microbiology, Boston University School of Medicine, Boston, MA 02115, USA
4National Emerging Infectious Diseases Laboratories, Boston University, Boston, MA 02115, USA
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Michael S. Seaman
8Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA 02115, USA
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Aaron G. Schmidt
9Ragon Institute of MGH, MIT, and Harvard, Cambridge, MA 02139, USA
10Department of Microbiology, Harvard Medical School, Boston MA 02115
11Massachusetts Consortium on Pathogen Readiness, Boston, MA 02115, USA
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Bing Chen
5Laboratory of Molecular Medicine, Boston Children’s Hospital, Boston, MA 02115, USA
11Massachusetts Consortium on Pathogen Readiness, Boston, MA 02115, USA
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Donna Neuberg
12Department of Data Science, Dana-Farber Cancer Institute, Boston, MA 02215, USA
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Goran Bajic
2Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA
5Laboratory of Molecular Medicine, Boston Children’s Hospital, Boston, MA 02115, USA
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Stephen C. Harrison
2Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA
5Laboratory of Molecular Medicine, Boston Children’s Hospital, Boston, MA 02115, USA
11Massachusetts Consortium on Pathogen Readiness, Boston, MA 02115, USA
13Howard Hughes Medical Institute, Boston, MA 02115, USA
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Duane R. Wesemann
1Department of Medicine, Division of Allergy and Immunology, Division of Genetics, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
11Massachusetts Consortium on Pathogen Readiness, Boston, MA 02115, USA
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  • ORCID record for Duane R. Wesemann
  • For correspondence: dwesemann@bwh.harvard.edu
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ABSTRACT

Memory B cell reserves can generate protective antibodies against repeated SARS-CoV-2 infections, but with an unknown reach from original infection to antigenically drifted variants. We charted memory B cell receptor-encoded monoclonal antibodies (mAbs) from 19 COVID-19 convalescent subjects against SARS-CoV-2 spike (S) and found 7 major mAb competition groups against epitopes recurrently targeted across individuals. Inclusion of published and newly determined structures of mAb-S complexes identified corresponding epitopic regions. Group assignment correlated with cross-CoV-reactivity breadth, neutralization potency, and convergent antibody signatures. mAbs that competed for binding the original S isolate bound differentially to S variants, suggesting the protective importance of otherwise-redundant recognition. The results furnish a global atlas of the S-specific memory B cell repertoire and illustrate properties conferring robustness against emerging SARS-CoV-2 variants.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 10, 2021.
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Memory B cell repertoire for recognition of evolving SARS-CoV-2 spike
Pei Tong, Avneesh Gautam, Ian Windsor, Meghan Travers, Yuezhou Chen, Nicholas Garcia, Noah B. Whiteman, Lindsay G.A. McKay, Felipe J.N. Lelis, Shaghayegh Habibi, Yongfei Cai, Linda J. Rennick, W. Paul Duprex, Kevin R. McCarthy, Christy L. Lavine, Teng Zuo, Junrui Lin, Adam Zuiani, Jared Feldman, Elizabeth A. MacDonald, Blake M. Hauser, Anthony Griffths, Michael S. Seaman, Aaron G. Schmidt, Bing Chen, Donna Neuberg, Goran Bajic, Stephen C. Harrison, Duane R. Wesemann
bioRxiv 2021.03.10.434840; doi: https://doi.org/10.1101/2021.03.10.434840
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Memory B cell repertoire for recognition of evolving SARS-CoV-2 spike
Pei Tong, Avneesh Gautam, Ian Windsor, Meghan Travers, Yuezhou Chen, Nicholas Garcia, Noah B. Whiteman, Lindsay G.A. McKay, Felipe J.N. Lelis, Shaghayegh Habibi, Yongfei Cai, Linda J. Rennick, W. Paul Duprex, Kevin R. McCarthy, Christy L. Lavine, Teng Zuo, Junrui Lin, Adam Zuiani, Jared Feldman, Elizabeth A. MacDonald, Blake M. Hauser, Anthony Griffths, Michael S. Seaman, Aaron G. Schmidt, Bing Chen, Donna Neuberg, Goran Bajic, Stephen C. Harrison, Duane R. Wesemann
bioRxiv 2021.03.10.434840; doi: https://doi.org/10.1101/2021.03.10.434840

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