Prevalent, protective, and convergent IgG recognition of SARS-CoV-2 non-RBD spike epitopes

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Abstract

The molecular composition and binding epitopes of the immunoglobulin G (IgG) antibodies that circulate in blood plasma following SARS-CoV-2 infection are unknown. Proteomic deconvolution of the IgG repertoire to the spike glycoprotein in convalescent subjects revealed that the response is directed predominantly (>80%) against epitopes residing outside the receptor-binding domain (RBD). In one subject, just four IgG lineages accounted for 93.5% of the response, including an N-terminal domain (NTD)-directed antibody that was protective against lethal viral challenge. Genetic, structural, and functional characterization of a multi-donor class of “public” antibodies revealed an NTD epitope that is recurrently mutated among emerging SARS-CoV-2 variants of concern. These data show that “public” NTD-directed and other non-RBD plasma antibodies are prevalent and have implications for SARS-CoV-2 protection and antibody escape.

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Author and article information

Journal

Journal ID (nlm-ta): Science

Journal ID (iso-abbrev): Science

Journal ID (publisher-id): SCIENCE

Title: Science (New York, N.y.)

Publisher: American Association for the Advancement of Science

ISSN (Print): 0036-8075

ISSN (Electronic): 1095-9203

Publication date (Electronic): 04 May 2021

Electronic Location Identifier: eabg5268

Affiliations

[1 ]Department of Molecular Biosciences, The University of Texas at Austin, Austin, TX, USA.

[2 ]Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.

[3 ]Department of Chemical Engineering, The University of Texas at Austin, Austin, TX, USA.

[4 ]Department of Biomedical Engineering, The University of Texas at Austin, Austin, TX, USA.

[5 ]Department of Chemistry, The University of Texas at Austin, Austin, TX, USA.

[6 ]U.S. Army Medical Research Institute of Infectious Diseases, Frederick, MD, USA.

[7 ]CCDC Army Research Laboratory-South, The University of Texas at Austin, Austin, TX, USA.

[8 ]Biomedicine Design, Pfizer, Cambridge, MA, USA.

[9 ]Biotechnology Core Facility Branch, Division of Scientific Resources, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA.

[10 ]Tulane National Primate Research Center Department of Microbiology 18703 Three Rivers Road Covington, LA, USA.

[11 ]Immunology and Pathogenesis Branch, Influenza Division, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA.

[12 ]Center for Biomedical Research Support, The University of Texas at Austin, Austin, TX, USA.

[13 ]Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, TX, USA.

[14 ]Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.

[15 ]Department of Oncology, Dell Medical School, The University of Texas at Austin, Austin, TX, USA.

Author notes

[#]

These authors contributed equally to this work.

[* ]Corresponding author. Email: jlavinder@ 123456utexas.edu (J.J.L.); gci@ 123456utexas.edu (G.C.I.)

Author information

William N. Voss https://orcid.org/0000-0002-4403-1939

Yixuan J. Hou https://orcid.org/0000-0002-8323-7243

Nicole V. Johnson https://orcid.org/0000-0003-4351-125X

George Delidakis https://orcid.org/0000-0002-4330-9476

Jin Eyun Kim https://orcid.org/0000-0002-6297-3292

Kamyab Javanmardi https://orcid.org/0000-0002-6449-6709

Andrew P. Horton https://orcid.org/0000-0002-0272-4411

Chelsea J. Paresi https://orcid.org/0000-0002-2405-8085

Yuri Tanno https://orcid.org/0000-0002-1868-7168

Chia-Wei Chou https://orcid.org/0000-0001-9618-338X

Shawn A. Abbasi https://orcid.org/0000-0002-7516-5876

Katia George https://orcid.org/0000-0001-8511-7918

Daniel R. Boutz https://orcid.org/0000-0001-7462-4105

Jonathan R. McDaniel https://orcid.org/0000-0001-8575-3535

Daniel Billick https://orcid.org/0000-0001-5002-7699

Lori Rowe https://orcid.org/0000-0003-3744-496X

Justin Lee https://orcid.org/0000-0002-6539-2637

Suryaprakash Sambhara https://orcid.org/0000-0002-4715-5793

Michelle Gadush https://orcid.org/0000-0002-1705-7076

Nianshuang Wang https://orcid.org/0000-0002-7569-011X

Maria D. Person https://orcid.org/0000-0001-8161-9339

Brent L. Iverson https://orcid.org/0000-0001-7974-3605

John Dye https://orcid.org/0000-0002-0883-5016

Andrew Herbert https://orcid.org/0000-0003-4697-7928

Ilya J. Finkelstein https://orcid.org/0000-0002-9371-2431

Ralph S. Baric https://orcid.org/0000-0001-6827-8701

Jason S. McLellan https://orcid.org/0000-0003-3991-542X

George Georgiou https://orcid.org/0000-0002-8823-3073

Jason J. Lavinder https://orcid.org/0000-0001-6044-1332

Gregory C. Ippolito https://orcid.org/0000-0002-7565-7002

Article

Publisher ID: abg5268

DOI: 10.1126/science.abg5268

PMC ID: 8224265

PubMed ID: 33947773

SO-VID: d6b351bf-fb2a-4f53-967c-c8f7f5700f93

Copyright © Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution license, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date received : 12 January 2021

Date accepted : 29 April 2021

Funding

Funded by: doi http://dx.doi.org/10.13039/100000054, National Cancer Institute;

Award ID: U54-CA260543

Funded by: doi http://dx.doi.org/10.13039/100000054, National Cancer Institute;

Award ID: U54-CA260543