Cited by 310Influenza Virus Research StudiesT-cell and B-cell ImmunologyImmune responses and vaccinations

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Human germinal centres engage memory and naive B cells after influenza vaccination

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Turner, Jackson S., Zhou, Julian Q., Han, Julianna, Schmitz, Aaron J., Rizk, Amena A., Alsoussi, Wafaa B., Lei, Tingting, Amor, Mostafa, McIntire, Katherine M., Meade, Philip, Strohmeier, Shirin, Brent, Rafael I., Richey, Sara T., Haile, Alem, Yang, Yuhe R., Klebert, Michael K., Suessen, Teresa, Teefey, Sharlene, Presti, Rachel M., Krammer, Florian, Kleinstein, Steven H., Ward, Andrew B., Ellebedy, Ali H.·2020·Nature

DOI 10.1038/s41586-020-2711-0PMC PMC7566073

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Abstract

Influenza viruses remain a major public health threat. Seasonal influenza vaccination in humans primarily stimulates pre-existing memory B cells, which differentiate into a transient wave of circulating antibody-secreting plasmablasts 1-3. This recall response contributes to 'original antigenic sin'-the selective increase of antibody species elicited by previous exposures to influenza virus antigens 4. It remains unclear whether such vaccination can also induce germinal centre reactions in the draining lymph nodes, where diversification and maturation of recruited B cells can occur 5. Here we used ultrasound-guided fine needle aspiration to serially sample the draining lymph nodes and investigate the dynamics and specificity of germinal centre B cell responses after influenza vaccination in humans. Germinal centre B cells that bind to influenza vaccine could be detected as early as one week after vaccination. In three out of eight participants, we detected vaccine-binding germinal centre B cells up to nine weeks after vaccination. Between 12% and 88% of the responding germinal centre B cell clones overlapped with B cells detected among early circulating plasmablasts. These shared B cell clones had high frequencies of somatic hypermutation and encoded broadly cross-reactive monoclonal antibodies. By contrast, vaccine-induced B cell clones detected only in the germinal centre compartment exhibited significantly lower frequencies of somatic hypermutation and predominantly encoded strain-specific monoclonal antibodies, which suggests a naive B cell origin. Some of these strain-specific monoclonal antibodies recognized epitopes that were not targeted by the early plasmablast response. Thus, influenza virus vaccination in humans can elicit a germinal centre reaction that recruits B cell clones that can target new epitopes, thereby broadening the spectrum of vaccine-induced protective antibodies.

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Authors: Turner, J. S., Zhou, J. Q., Han, J., Schmitz, A. J., Rizk, A. A., Alsoussi, W. B., Lei, T., Amor, M., McIntire, K. M., Meade, P., Strohmeier, S., Brent, R. I., Richey, S. T., Haile, A., Yang, Y. R., Klebert, M. K., Suessen, T., Teefey, S., Presti, R. M., Krammer, F., Kleinstein, S. H., Ward, A. B., & Ellebedy, A. H.
Affiliations: Washington University in St. Louis (US)
Yale University (US)
Scripps Research Institute (US)
Icahn School of Medicine at Mount Sinai (US)
Corresponding author: Ellebedy, Ali H.
ORCID: Turner, Jackson S.
Zhou, Julian Q.
Han, Julianna
Schmitz, Aaron J.
Alsoussi, Wafaa B.
Lei, Tingting
McIntire, Katherine M.
Meade, Philip
Strohmeier, Shirin
Brent, Rafael I.
Richey, Sara T.
Yang, Yuhe R.
Klebert, Michael K.
Teefey, Sharlene
Presti, Rachel M.
Krammer, Florian
Kleinstein, Steven H.
Ward, Andrew B.
Ellebedy, Ali H.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2020-08-31
Volume: 586
Issue: 7827
Pages: 127-132
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-020-2711-0
PMC: PMC7566073
OpenAlex: W3082694457
Cited by: 304
References: 54
Citations by year: 2026: 46 · 2025: 40 · 2024: 53 · 2023: 58 · 2022: 51 · 2021: 50 · 2020: 5
FWCI: 29.37
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Institutes of Health (UL1TR000448, UL1TR002345)
National Cancer Institute (T32CA009547, P30CA091842)
National Institute of Allergy and Infectious Diseases (HHSN272201400008C), AI117287, R01AI128821, R01AI117287, R01AI104739, AI128821, R01AI104732, R56AI117287, 75N93019C00051, T32AI007244, R21AI139813, U01AI141990, U19AI089992, HHSN 272201400006C)
National Center for Advancing Translational Sciences
Topics: Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
Keywords: influenza vaccination, germinal center, memory B cells, naive B cells, somatic hypermutation, original antigenic sin, plasmablasts, monoclonal antibodies, cross-reactive antibodies, strain-specific antibodies, draining lymph nodes, vaccine-induced antibody response
MeSH terms: Adult, Animals, B-Lymphocytes, Clone Cells, Female, Humans, Immunologic Memory, Influenza, Human, Influenza Vaccines, Male, Epitope Mapping, Germinal Center, Mice

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Human germinal centres engage memory and naive B cells after influenza vaccination

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