Evolution of antibody immunity to SARS-CoV-2

Christian Gaebler, Zijun Wang, Julio C. C. Lorenzi, Frauke Muecksch, Shlomo Finkin, Minami Tokuyama, Alice Cho, Mila Jankovic, Dennis Schaefer-Babajew, Thiago Y. Oliveira, Melissa Cipolla, Charlotte Viant, Christopher O. Barnes, Yaron Bram, Gaëlle Breton, Thomas Hägglöf, Pilar Mendoza, Arlene Hurley, Martina Turroja, Kristie Gordon, Katrina G. Millard, Victor Ramos, Fabian Schmidt, Yiska Weisblum, Divya Jha, Michael Tankelevich, Gustavo Martinez-Delgado, Jim Yee, Roshni Patel, Juan Dizon, Cecille Unson-O’Brien, Irina Shimeliovich, Davide F. Robbiani, Zhen Zhao, Anna Gazumyan, Robert E. Schwartz, Theodora Hatziioannou, Pamela J. Bjorkman, Saurabh Mehandru (), Paul D. Bieniasz (), Marina Caskey () and Michel C. Nussenzweig ()
Additional contact information
Christian Gaebler: The Rockefeller University
Zijun Wang: The Rockefeller University
Julio C. C. Lorenzi: The Rockefeller University
Frauke Muecksch: The Rockefeller University
Shlomo Finkin: The Rockefeller University
Minami Tokuyama: Icahn School of Medicine at Mount Sinai
Alice Cho: The Rockefeller University
Mila Jankovic: The Rockefeller University
Dennis Schaefer-Babajew: The Rockefeller University
Thiago Y. Oliveira: The Rockefeller University
Melissa Cipolla: The Rockefeller University
Charlotte Viant: The Rockefeller University
Christopher O. Barnes: California Institute of Technology
Yaron Bram: Weill Cornell Medicine
Gaëlle Breton: The Rockefeller University
Thomas Hägglöf: The Rockefeller University
Pilar Mendoza: The Rockefeller University
Arlene Hurley: The Rockefeller University
Martina Turroja: The Rockefeller University
Kristie Gordon: The Rockefeller University
Katrina G. Millard: The Rockefeller University
Victor Ramos: The Rockefeller University
Fabian Schmidt: The Rockefeller University
Yiska Weisblum: The Rockefeller University
Divya Jha: Icahn School of Medicine at Mount Sinai
Michael Tankelevich: Icahn School of Medicine at Mount Sinai
Gustavo Martinez-Delgado: Icahn School of Medicine at Mount Sinai
Jim Yee: Weill Cornell Medicine
Roshni Patel: The Rockefeller University
Juan Dizon: The Rockefeller University
Cecille Unson-O’Brien: The Rockefeller University
Irina Shimeliovich: The Rockefeller University
Davide F. Robbiani: Università della Svizzera Italiana
Zhen Zhao: Weill Cornell Medicine
Anna Gazumyan: The Rockefeller University
Robert E. Schwartz: Weill Cornell Medicine
Theodora Hatziioannou: The Rockefeller University
Pamela J. Bjorkman: California Institute of Technology
Saurabh Mehandru: Icahn School of Medicine at Mount Sinai
Paul D. Bieniasz: The Rockefeller University
Marina Caskey: The Rockefeller University
Michel C. Nussenzweig: The Rockefeller University

Nature, 2021, vol. 591, issue 7851, 639-644

Abstract: Abstract Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has infected 78 million individuals and is responsible for over 1.7 million deaths to date. Infection is associated with the development of variable levels of antibodies with neutralizing activity, which can protect against infection in animal models1,2. Antibody levels decrease with time, but, to our knowledge, the nature and quality of the memory B cells that would be required to produce antibodies upon reinfection has not been examined. Here we report on the humoral memory response in a cohort of 87 individuals assessed at 1.3 and 6.2 months after infection with SARS-CoV-2. We find that titres of IgM and IgG antibodies against the receptor-binding domain (RBD) of the spike protein of SARS-CoV-2 decrease significantly over this time period, with IgA being less affected. Concurrently, neutralizing activity in plasma decreases by fivefold in pseudotype virus assays. By contrast, the number of RBD-specific memory B cells remains unchanged at 6.2 months after infection. Memory B cells display clonal turnover after 6.2 months, and the antibodies that they express have greater somatic hypermutation, resistance to RBD mutations and increased potency, indicative of continued evolution of the humoral response. Immunofluorescence and PCR analyses of intestinal biopsies obtained from asymptomatic individuals at 4 months after the onset of coronavirus disease 2019 (COVID-19) revealed the persistence of SARS-CoV-2 nucleic acids and immunoreactivity in the small bowel of 7 out of 14 individuals. We conclude that the memory B cell response to SARS-CoV-2 evolves between 1.3 and 6.2 months after infection in a manner that is consistent with antigen persistence.

Date: 2021
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DOI: 10.1038/s41586-021-03207-w

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