Extrafollicular B cell responses correlate with neutralizing antibodies and morbidity in COVID-19
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Abstract
A wide spectrum of clinical manifestations has become a hallmark of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) COVID-19 pandemic, although the immunological underpinnings of diverse disease outcomes remain to be defined. We performed detailed characterization of B cell responses through high-dimensional flow cytometry to reveal substantial heterogeneity in both effector and immature populations. More notably, critically ill patients displayed hallmarks of extrafollicular B cell activation and shared B cell repertoire features previously described in autoimmune settings. Extrafollicular activation correlated strongly with large antibody-secreting cell expansion and early production of high concentrations of SARS-CoV-2-specific neutralizing antibodies. Yet, these patients had severe disease with elevated inflammatory biomarkers, multiorgan failure and death. Overall, these findings strongly suggest a pathogenic role for immune activation in subsets of patients with COVID-19. Our study provides further evidence that targeted immunomodulatory therapy may be beneficial in specific patient subpopulations and can be informed by careful immune profiling.
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High neutralizing antibody titers are associated with severe disease and potentially extrafollicular B cell responses.
“High neutralizing antibody titers are associated with severe disease and potentially extrafollicular B cell responses (Piccoli et al., 2020; Woodruff et al., 2020), while SARS-CoV-2-specific Tfh cells have different associations depending on the study (Juno et al., 2020; Meckiff et al., 2020; Rydyznski Moderbacher et al., 2020; Oja et al., 2020).”
From Adaptive immunity to SARS-CoV-2 and COVID-19 (2021) · cites this paper as Woodruff et al., 2020
In humans, age-associated B cells are found within the late memory fraction (IgD-CD27-, also called double negative B cells).
“In humans, these cells are found within the late memory fraction (IgD-CD27-, also called double negative B cells), secrete inflammatory mediators like TNFα, IL-6, IL-8, and have been implicated in autoimmune disease, chronic viral infections, and more recently in COVID-19156-158.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [158]
Human age-associated B cells secrete inflammatory mediators such as TNFα, IL-6, and IL-8.
“In humans, these cells are found within the late memory fraction (IgD-CD27-, also called double negative B cells), secrete inflammatory mediators like TNFα, IL-6, IL-8, and have been implicated in autoimmune disease, chronic viral infections, and more recently in COVID-19156-158.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [158]
These expanded cells express CD11c and T-bet in a skewed extrafollicular B cell response with lupus-like autoimmune signatures.
“During COVID-19, critically ill patients show expansion of such cells, which also expressed CD11c and T-bet, in a skewed extrafollicular B cell response, with signatures of lupus-like autoimmune disease158.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [158]
Human age-associated B cells have been implicated in autoimmune disease, chronic viral infections, and COVID-19.
“In humans, these cells are found within the late memory fraction (IgD-CD27-, also called double negative B cells), secrete inflammatory mediators like TNFα, IL-6, IL-8, and have been implicated in autoimmune disease, chronic viral infections, and more recently in COVID-19156-158.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [158]
Critically ill COVID-19 patients show expansion of age-associated B cell-like cells.
“During COVID-19, critically ill patients show expansion of such cells, which also expressed CD11c and T-bet, in a skewed extrafollicular B cell response, with signatures of lupus-like autoimmune disease158.”
From SARS-CoV-2, COVID-19 and the aging immune system (2021) · cites this paper as [158]
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SARS-CoV-2, COVID-19 and the aging immune system
Bartleson, J. M., Radenkovic, D., Covarrubias, A. J., Furman, D., Winer, D. A., & Verdin, E. (2021) · Nature Aging · doi:10.1038/s43587-021-00114-7 · Cited by 359 · see citing works
Highly functional virus-specific cellular immune response in asymptomatic SARS-CoV-2 infection
Le Bert, N., Clapham, H. E., Tan, A. T., Chia, W. N., Tham, C. Y. L., Lim, J. M., Kunasegaran, K., Tan, L. W. L., Dutertre, C.-A., Shankar, N., et al. (2021) · Journal of Experimental Medicine · doi:10.1084/jem.20202617 · Cited by 330 · see citing works
Maturation and persistence of the anti-SARS-CoV-2 memory B cell response
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- Authors
- Woodruff, M. C., Ramonell, R. P., Nguyen, D. C., Cashman, K. S., Saini, A. S., Haddad, N. S., Ley, A. M., Kyu, S., Howell, J. C., Ozturk, T., Lee, S., Suryadevara, N., Case, J. B., Bugrovsky, R., Chen, W., Estrada, J., Morrison-Porter, A., Derrico, A., Anam, F. A., Sharma, M., Wu, H. M., Le, S. N., Jenks, S. A., Tipton, C. M., Staitieh, B., Daiss, J. L., Ghosn, E., Diamond, M. S., Carnahan, R. H., Crowe, J. E., Hu, W. T., Lee, F. E.-H., & Sanz, I.
- Affiliations
- Emory University (US)
- Vanderbilt University Medical Center (US)
- Washington University in St. Louis (US)
- Corresponding author
- Lee, F. Eun-Hyung
- ORCID
- Woodruff, Matthew C.
- Ramonell, Richard P.
- Nguyen, Doan C.
- Cashman, Kevin S.
- Saini, Ankur Singh
- Haddad, Natalie S.
- Kyu, Shuya
- Howell, J. Christina
- Ozturk, Tugba
- Suryadevara, Naveenchandra
- Case, James Brett
- Bugrovsky, Regina
- Anam, Fabliha A.
- Sharma, Monika
- Wu, Henry M.
- Le, Sang N.
- Jenks, Scott A.
- Tipton, Christopher M.
- Staitieh, Bashar
- Daiss, John L.
- Ghosn, Eliver
- Diamond, Michael S.
- Carnahan, Robert H.
- Crowe, James E.
- Hu, William T.
- Lee, F. Eun-Hyung
- Sanz, Ignacio
- Venue
- Nature Immunology
- Published
- 2020-10-07
- Volume
- 21
- Issue
- 12
- Pages
- 1506-1516
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- PMC
- PMC7739702
- OpenAlex
- W3091861357
- Cited by
- 791
- References
- 67
- Citations by year
- 2026: 54 · 2025: 81 · 2024: 107 · 2023: 123 · 2022: 169 · 2021: 208 · 2020: 46 · 2014: 1 · 2013: 1
- FWCI
- 17.91
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Nature Immunology (publishedVersion)
- medRxiv (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- PubMed Central (submittedVersion)
- Funders
- Division of Intramural Research, National Institute of Allergy and Infectious Diseases (R01 AI127828, 75N93019C00074, U19-AI110483, P01-AI125180-01, R37-AI049660, 1R01AI121252, 1U01AI141993)
- U.S. Department of Health & Human Services | NIH | National Heart, Lung, and Blood Institute (T32-HL116271-07)
- U.S. Department of Health & Human Services | NIH | National Institute on Aging (R01-AG054991)
- United States Department of Defense | Defense Advanced Research Projects Agency (HR001117S0019)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- COVID-19 pandemic, SARS-CoV-2, neutralizing antibodies, antibody-secreting cells, B cell heterogeneity, critically ill patients, immune activation, multiple organ failure, immunomodulatory therapy, systemic lupus erythematosus
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