Evolution of antibody immunity to SARS-CoV-2
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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 models 1,2. 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.
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Increasing levels of antibody somatic mutations suggest that ongoing germinal centre activity drives further affinity maturation of antibody responses over time.
“increasing levels of antibody somatic mutations suggest that ongoing germinal centre activity drives the further affinity maturation of antibody responses over time2.”
From Prospects for durable immune control of SARS-CoV-2 and prevention of reinfection (2021) · cites this paper as [2]
SARS-CoV-2-specific memory B cells accumulate over the first few months after initial infection.
“We and others have shown that SARS-CoV-2-specific memory B cells accumulate over the first few months after initial infection2,3,8,9,28 (Fig. 1a)”
From Prospects for durable immune control of SARS-CoV-2 and prevention of reinfection (2021) · cites this paper as [2]
Frequencies of circulating memory B cells continue to increase for several months after recovery from COVID-19 when most other responses decline, suggesting recall of B cell memory may extend antibody-dependent protection despite waning serological titres.
“The observations that frequencies of circulating memory B cells continue to increase for several months after recovery from COVID-19 (refs2,3,8,9,28), when most other responses are declining (Fig. 1a), suggest that recall of B cell memory may provide a mechanism to extend the duration of antibody-dependent protection in the face of waning serological titres.”
From Prospects for durable immune control of SARS-CoV-2 and prevention of reinfection (2021) · cites this paper as [2]
Eight weeks after the second mRNA vaccine dose, volunteers had high IgM and IgG binding titers to SARS-CoV-2 S and RBD.
“8 weeks after the second vaccine injection volunteers showed high levels of IgM, and IgG anti-SARS-CoV-2 spike protein (S) and receptor binding domain (RBD) binding titers3,5,6.”
From mRNA vaccine-elicited antibodies to SARS-CoV-2 and circulating variants (2021) · cites this paper as [5]
These findings are consistent with earlier work that has suggested that SHM and affinity maturation are important for the acquisition of broader neutralization activity of RBD-binding antibodies that are formed in response to SARS-CoV-2 infection.
“These findings are consistent with earlier work that has suggested that SHM and affinity maturation are important for the acquisition of broader neutralization activity of RBD-binding antibodies that are formed in response to SARS-CoV-2 infection (48, 49).”
From mRNA vaccines induce durable immune memory to SARS-CoV-2 and variants of concern (2021) · cites this paper as [48]
There was an overall increase in the apparent avidity of plasma antibodies between 1.3 and 12 months (P < 0.0001).
“Consistent with this observation, there was an overall increase in the apparent avidity of plasma antibodies between 1.3 and 12 months3,4 (P < 0.0001) (Extended Data Fig. 7c).”
From Naturally enhanced neutralizing breadth against SARS-CoV-2 one year after infection (2021) · cites this paper as [4]
All participants tested negative for active infection at the 12-month time point as measured by a saliva-based PCR assay.
“All participants tested negative for active infection at the 12-month time point as measured by a saliva-based PCR assay4.”
From Naturally enhanced neutralizing breadth against SARS-CoV-2 one year after infection (2021) · cites this paper as [4]
The memory B cell compartment accumulates mutations and undergoes clonal evolution over the initial six months after infection.
“The memory B cell compartment accumulates mutations and undergoes clonal evolution over the initial six months after infection4,9,21,22.”
From Naturally enhanced neutralizing breadth against SARS-CoV-2 one year after infection (2021) · cites this paper as [4]
SARS-CoV-2 protein and nucleic acids have been reported to remain in the gut for at least two months after infection.
“In addition, SARS-CoV-2 protein and nucleic acids have been reported to remain in the gut for at least two months after infection4.”
From Naturally enhanced neutralizing breadth against SARS-CoV-2 one year after infection (2021) · cites this paper as [4]
SARS-CoV-2 infection rapidly elicits nAbs that decline, but remain detectable, over several months.
“SARS-CoV-2 infection rapidly elicits nAbs (16, 21–24) that decline, but remain detectable, over several months (25–29).”
From mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection (2021) · cites this paper as [27]
Mutations found in emergent S variants decrease sensitivity to neutralization by mAbs, convalescent plasma, and sera from vaccinated individuals.
“Mutations found in emergent S variants decrease sensitivity to neutralization by mAbs, convalescent plasma, and sera from vaccinated individuals (27, 37, 58, 61–70).”
From mRNA vaccination boosts cross-variant neutralizing antibodies elicited by SARS-CoV-2 infection (2021) · cites this paper as [27]
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Research works printed but not linked: 1
- [50]Weisblum Y Escape from neutralizing antibodies by SARS-CoV-2 spike protein variants. eLife 9, e61312 (2020). 33112236 PMC7723407
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- Authors
- Gaebler, C., Wang, Z., Lorenzi, J. C. C., Muecksch, F., Finkin, S., Tokuyama, M., Cho, A., Jankovic, M., Schaefer-Babajew, D., Oliveira, T. Y., Cipolla, M., Viant, C., Barnes, C. O., Bram, Y., Breton, G., Hägglöf, T., Mendoza, P., Hurley, A., Turroja, M., Gordon, K., Millard, K. G., Ramos, V., Schmidt, F., Weisblum, Y., Jha, D., Tankelevich, M., Martinez-Delgado, G., Yee, J., Patel, R., Dizon, J., Unson-O’Brien, C., Shimeliovich, I., Robbiani, D. F., Zhao, Z., Gazumyan, A., Schwartz, R. E., Hatziioannou, T., Bjorkman, P. J., Mehandru, S., Bieniasz, P. D., Caskey, M., & Nussenzweig, M. C.
- Affiliations
- Rockefeller University (US)
- Icahn School of Medicine at Mount Sinai (US)
- California Institute of Technology (US)
- Weill Cornell Medicine (US)
- Institute for Research in Biomedicine (CH)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Mehandru, Saurabh
- Bieniasz, Paul D.
- Caskey, Marina
- Nussenzweig, Michel C.
- ORCID
- Gaebler, Christian
- Wang, Zijun
- Lorenzi, Julio C. C.
- Muecksch, Frauke
- Finkin, Shlomo
- Tokuyama, Minami
- Cho, Alice
- Schaefer-Babajew, Dennis
- Oliveira, Thiago Y.
- Cipolla, Melissa
- Viant, Charlotte
- Barnes, Christopher O.
- Bram, Yaron
- Breton, Gaëlle
- Mendoza, Pilar
- Hurley, Arlene
- Turroja, Martina
- Millard, Katrina G.
- Ramos, Victor
- Schmidt, Fabian
- Weisblum, Yiska
- Jha, Divya
- Yee, Jim
- Dizon, Juan
- Shimeliovich, Irina
- Robbiani, Davide F.
- Zhao, Zhen
- Gazumyan, Anna
- Schwartz, Robert E.
- Bjorkman, Pamela J.
- Mehandru, Saurabh
- Bieniasz, Paul D.
- Caskey, Marina
- Nussenzweig, Michel C.
- Venue
- Nature
- Published
- 2021-01-18
- Volume
- 591
- Issue
- 7851
- Pages
- 639-644
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC8221082
- OpenAlex
- W3121906900
- Cited by
- 1,674
- References
- 70
- Citations by year
- 2026: 60 · 2025: 116 · 2024: 170 · 2023: 283 · 2022: 510 · 2021: 519 · 2020: 15
- FWCI
- 117.16
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- PubMed Central (submittedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Howard Hughes Medical Institute (UL1TR001866)
- George Mason University
- California Institute of Technology
- Wellcome Trust
- European Commission (101003650)
- National Institutes of Health (/ NIDDK R01, P01-AI138398-S1, AI150464, TR001866, UL1TR001866)
- Beckman Institute, California Institute of Technology
- National Cancer Institute (R01CA234614)
- National Institute of Allergy and Infectious Diseases (P01 AI138398-S1, R01AI078788, P50AI150464, AI150464, U19AI111825, P01AI138938, R37AI064003, R01AI107301)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK123749, R01DK120035, 1RO3DK117252, R01DK121072, DK123749, R03DK117252)
- National Center for Advancing Translational Sciences (TR001866)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Keywords
- SARS-CoV-2, COVID-19 pandemic, antibody immunity, memory B cells, humoral immune response, neutralizing antibodies, receptor binding domain, spike protein, somatic hypermutation, antibody waning, IgA, IgG, IgM, reinfection
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