Cited by 107SARS-CoV-2 and COVID-19 ResearchImmune responses and vaccinationsT-cell and B-cell Immunology

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Prior vaccination promotes early activation of memory T cells and enhances immune responses during SARS-CoV-2 breakthrough infection

Painter, Mark M., Johnston, Timothy S., Lundgreen, Kendall A., Santos, Jefferson J. S., Qin, Juliana S., Goel, Rishi R., Apostolidis, Sokratis A., Mathew, Divij, Fulmer, Bria, Williams, Justine C., McKeague, Michelle L., Pattekar, Ajinkya, Goode, Ahmad, Nasta, Sean, Baxter, Amy E., Giles, Josephine R., Skelly, Ashwin N., Felley, Laura E., McLaughlin, Maura, Weaver, Joellen, Penn Medicine BioBank, Ritchie, Marylyn D., Feldman, Michael D., Weaver, JoEllen, Naseer, Nawar, Poindexter, Afiya, Brock, Ashlei, Hu-Sain, Khadijah, Ko, Yi-An, Livingstone, Meghan, Vadivieso, Fred, Kloter, Ashley, DerOhannessian, Stephanie, Tran, Teo, Morrel, Linda, Haubein, Ned, Dunn, Joseph, Verma, Anurag, Morse, Colleen, Risman, Marjorie, Judy, Renae, Verma, Shefali S., Bradford, Yuki, Dudek, Scott, Drivas, Theodore, Kuthuru, Oliva, Dougherty, Jeanette, Adamski, Sharon, Long, Sherea, Kee, Macy, Clendenin, Cynthia, da Silva Antunes, Ricardo, Grifoni, Alba, Weiskopf, Daniela, Sette, Alessandro, Huang, Alexander C., Rader, Daniel J., Hensley, Scott E., Bates, Paul, Greenplate, Allison R., Wherry, E. John·2023·Nature Immunology

DOI 10.1038/s41590-023-01613-y

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Abstract

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection of vaccinated individuals is increasingly common but rarely results in severe disease, likely due to the enhanced potency and accelerated kinetics of memory immune responses. However, there have been few opportunities to rigorously study early recall responses during human viral infection. To better understand human immune memory and identify potential mediators of lasting vaccine efficacy, we used high-dimensional flow cytometry and SARS-CoV-2 antigen probes to examine immune responses in longitudinal samples from vaccinated individuals infected during the Omicron wave. These studies revealed heightened spike-specific responses during infection of vaccinated compared to unvaccinated individuals. Spike-specific cluster of differentiation (CD)4 T cells and plasmablasts expanded and CD8 T cells were robustly activated during the first week. In contrast, memory B cell activation, neutralizing antibody production and primary responses to nonspike antigens occurred during the second week. Collectively, these data demonstrate the functionality of vaccine-primed immune memory and highlight memory T cells as rapid responders during SARS-CoV-2 infection.

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Authors: Painter, M. M., Johnston, T. S., Lundgreen, K. A., Santos, J. J. S., Qin, J. S., Goel, R. R., Apostolidis, S. A., Mathew, D., Fulmer, B., Williams, J. C., McKeague, M. L., Pattekar, A., Goode, A., Nasta, S., Baxter, A. E., Giles, J. R., Skelly, A. N., Felley, L. E., McLaughlin, M., Weaver, J., BioBank, P. M., Ritchie, M. D., Feldman, M. D., Weaver, J., Naseer, N., Poindexter, A., Brock, A., Hu-Sain, K., Ko, Y.-A., Livingstone, M., Vadivieso, F., Kloter, A., DerOhannessian, S., Tran, T., Morrel, L., Haubein, N., Dunn, J., Verma, A., Morse, C., Risman, M., Judy, R., Verma, S. S., Bradford, Y., Dudek, S., Drivas, T., Kuthuru, O., Dougherty, J., Adamski, S., Long, S., Kee, M., Clendenin, C., da Silva Antunes, R., Grifoni, A., Weiskopf, D., Sette, A., Huang, A. C., Rader, D. J., Hensley, S. E., Bates, P., Greenplate, A. R., & Wherry, E. J.
Affiliations: University of Pennsylvania (US)
National Institutes of Health (US)
Parker Institute for Cancer Immunotherapy (US)
University of Michigan (US)
University of Pennsylvania Health System (US)
La Jolla Institute for Immunology (US)
Corresponding author: Wherry, E. John
ORCID: Painter, Mark M.
Johnston, Timothy S.
Lundgreen, Kendall A.
Santos, Jefferson J. S.
Qin, Juliana S.
Goel, Rishi R.
Apostolidis, Sokratis A.
Mathew, Divij
Fulmer, Bria
Williams, Justine C.
McKeague, Michelle L.
Pattekar, Ajinkya
Baxter, Amy E.
Giles, Josephine R.
Skelly, Ashwin N.
Ritchie, Marylyn D.
Feldman, Michael D.
Kuthuru, Oliva
Dougherty, Jeanette
Adamski, Sharon
Long, Sherea
Clendenin, Cynthia
da Silva Antunes, Ricardo
Grifoni, Alba
Weiskopf, Daniela
Sette, Alessandro
Huang, Alexander C.
Rader, Daniel J.
Hensley, Scott E.
Bates, Paul
Greenplate, Allison R.
Wherry, E. John
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2023-09-21
Volume: 24
Issue: 10
Pages: 1711-1724
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/s41590-023-01613-y
OpenAlex: W4386923860
Cited by: 106
References: 70
Citations by year: 2026: 22 · 2025: 32 · 2024: 40 · 2023: 10
FWCI: 21.73
Type: journal article
Language: en
Open access: closed
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. Department of Health & Human Services | National Institutes of Health (AI082630, AI108545, AI155577, AI149680, U19AI082630, 75N9301900065, AI152236)
Parker Foundation
U.S. Department of Health & Human Services | NIH | National Center for Advancing Translational Sciences (UL1TR001878)
Topics: Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: SARS-CoV-2, breakthrough infection, COVID-19 vaccination, memory T cells, CD4+ T cells, CD8+ T cells, plasmablasts, memory B cells, Omicron variant, recall immune response, neutralizing antibodies
MeSH terms: COVID-19, SARS-CoV-2, COVID-19 Vaccines, Memory B Cells, Memory T Cells, Breakthrough Infections, Adult, Antibodies, Viral, Female, Humans, Immunologic Memory, Lymphocyte Activation, Male, Middle Aged, Vaccination, CD8-Positive T-Lymphocytes, Antibodies, Neutralizing, Spike Glycoprotein, Coronavirus

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Prior vaccination promotes early activation of memory T cells and enhances immune responses during SARS-CoV-2 breakthrough infection

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