mRNA COVID-19 vaccine elicits potent adaptive immune response without the acute inflammation of SARS-CoV-2 infection

Ellie N. Ivanova; Jasmine Shwetar; Joseph C. Devlin; Terkild B. Buus; Sophie Gray-Gaillard; Akiko Koide; Amber Cornelius; Marie I. Samanovic; Alberto Herrera; Eleni P. Mimitou; Chenzhen Zhang; Trishala Karmacharya; Ludovic Desvignes; Niels Ødum; Peter Smibert; Robert J. Ulrich; Mark J. Mulligan; Shohei Koide; Kelly V. Ruggles; Ramin S. Herati; Sergei B. Koralov

doi:10.1016/j.isci.2023.108572

mRNA COVID-19 vaccine elicits potent adaptive immune response without the acute inflammation of SARS-CoV-2 infection

Ellie N. Ivanova, Jasmine Shwetar, Joseph C. Devlin, Terkild B. Buus, Sophie Gray-Gaillard, Akiko Koide, Amber Cornelius, Marie I. Samanovic, Alberto Herrera, Eleni P. Mimitou, Chenzhen Zhang, Trishala Karmacharya, Ludovic Desvignes, Niels Ødum, Peter Smibert, Robert J. Ulrich, Mark J. Mulligan, Shohei Koide, Kelly V. Ruggles^*, Ramin S. HeratiSergei B. Koralov

^*Corresponding author for this work

Skin Immunology Research Center

Research output: Contribution to journal › Journal article › Research › peer-review

5 Citations (Scopus)

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Abstract

SARS-CoV-2 infection and vaccination elicit potent immune responses. Our study presents a comprehensive multimodal single-cell analysis of blood from COVID-19 patients and healthy volunteers receiving the SARS-CoV-2 vaccine and booster. We profiled immune responses via transcriptional analysis and lymphocyte repertoire reconstruction. COVID-19 patients displayed an enhanced interferon signature and cytotoxic gene upregulation, absent in vaccine recipients. B and T cell repertoire analysis revealed clonal expansion among effector cells in COVID-19 patients and memory cells in vaccine recipients. Furthermore, while clonal αβ T cell responses were observed in both COVID-19 patients and vaccine recipients, expansion of clonal γδ T cells was found only in infected individuals. Our dataset enables side-by-side comparison of immune responses to infection versus vaccination, including clonal B and T cell responses. Our comparative analysis shows that vaccination induces a robust, durable clonal B and T cell responses, without the severe inflammation associated with infection.

Original language	English
Article number	108572
Journal	iScience
Volume	26
Issue number	12
Pages (from-to)	1-19
ISSN	2589-0042
DOIs	https://doi.org/10.1016/j.isci.2023.108572
Publication status	Published - 2023

Bibliographical note

Publisher Copyright:
© 2023 The Authors

Keywords

Immune response
Immunology
Transcriptomics

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Cite this

Ivanova, E. N., Shwetar, J., Devlin, J. C., Buus, T. B., Gray-Gaillard, S., Koide, A., Cornelius, A., Samanovic, M. I., Herrera, A., Mimitou, E. P., Zhang, C., Karmacharya, T., Desvignes, L., Ødum, N., Smibert, P., Ulrich, R. J., Mulligan, M. J., Koide, S., Ruggles, K. V., ... Koralov, S. B. (2023). mRNA COVID-19 vaccine elicits potent adaptive immune response without the acute inflammation of SARS-CoV-2 infection. iScience, 26(12), 1-19. [108572]. https://doi.org/10.1016/j.isci.2023.108572

mRNA COVID-19 vaccine elicits potent adaptive immune response without the acute inflammation of SARS-CoV-2 infection. / Ivanova, Ellie N.; Shwetar, Jasmine; Devlin, Joseph C.; Buus, Terkild B.; Gray-Gaillard, Sophie; Koide, Akiko; Cornelius, Amber; Samanovic, Marie I.; Herrera, Alberto; Mimitou, Eleni P.; Zhang, Chenzhen; Karmacharya, Trishala; Desvignes, Ludovic; Ødum, Niels; Smibert, Peter; Ulrich, Robert J.; Mulligan, Mark J.; Koide, Shohei; Ruggles, Kelly V.; Herati, Ramin S.; Koralov, Sergei B.

In: iScience, Vol. 26, No. 12, 108572, 2023, p. 1-19.

Research output: Contribution to journal › Journal article › Research › peer-review

Ivanova, EN, Shwetar, J, Devlin, JC, Buus, TB, Gray-Gaillard, S, Koide, A, Cornelius, A, Samanovic, MI, Herrera, A, Mimitou, EP, Zhang, C, Karmacharya, T, Desvignes, L, Ødum, N, Smibert, P, Ulrich, RJ, Mulligan, MJ, Koide, S, Ruggles, KV, Herati, RS & Koralov, SB 2023, 'mRNA COVID-19 vaccine elicits potent adaptive immune response without the acute inflammation of SARS-CoV-2 infection', iScience, vol. 26, no. 12, 108572, pp. 1-19. https://doi.org/10.1016/j.isci.2023.108572

Ivanova, Ellie N. ; Shwetar, Jasmine ; Devlin, Joseph C. ; Buus, Terkild B. ; Gray-Gaillard, Sophie ; Koide, Akiko ; Cornelius, Amber ; Samanovic, Marie I. ; Herrera, Alberto ; Mimitou, Eleni P. ; Zhang, Chenzhen ; Karmacharya, Trishala ; Desvignes, Ludovic ; Ødum, Niels ; Smibert, Peter ; Ulrich, Robert J. ; Mulligan, Mark J. ; Koide, Shohei ; Ruggles, Kelly V. ; Herati, Ramin S. ; Koralov, Sergei B. / mRNA COVID-19 vaccine elicits potent adaptive immune response without the acute inflammation of SARS-CoV-2 infection. In: iScience. 2023 ; Vol. 26, No. 12. pp. 1-19.

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abstract = "SARS-CoV-2 infection and vaccination elicit potent immune responses. Our study presents a comprehensive multimodal single-cell analysis of blood from COVID-19 patients and healthy volunteers receiving the SARS-CoV-2 vaccine and booster. We profiled immune responses via transcriptional analysis and lymphocyte repertoire reconstruction. COVID-19 patients displayed an enhanced interferon signature and cytotoxic gene upregulation, absent in vaccine recipients. B and T cell repertoire analysis revealed clonal expansion among effector cells in COVID-19 patients and memory cells in vaccine recipients. Furthermore, while clonal αβ T cell responses were observed in both COVID-19 patients and vaccine recipients, expansion of clonal γδ T cells was found only in infected individuals. Our dataset enables side-by-side comparison of immune responses to infection versus vaccination, including clonal B and T cell responses. Our comparative analysis shows that vaccination induces a robust, durable clonal B and T cell responses, without the severe inflammation associated with infection.",

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AU - Gray-Gaillard, Sophie

AU - Koide, Akiko

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AU - Samanovic, Marie I.

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AU - Mimitou, Eleni P.

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AU - Desvignes, Ludovic

AU - Ødum, Niels

AU - Smibert, Peter

AU - Ulrich, Robert J.

AU - Mulligan, Mark J.

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AU - Herati, Ramin S.

AU - Koralov, Sergei B.

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AB - SARS-CoV-2 infection and vaccination elicit potent immune responses. Our study presents a comprehensive multimodal single-cell analysis of blood from COVID-19 patients and healthy volunteers receiving the SARS-CoV-2 vaccine and booster. We profiled immune responses via transcriptional analysis and lymphocyte repertoire reconstruction. COVID-19 patients displayed an enhanced interferon signature and cytotoxic gene upregulation, absent in vaccine recipients. B and T cell repertoire analysis revealed clonal expansion among effector cells in COVID-19 patients and memory cells in vaccine recipients. Furthermore, while clonal αβ T cell responses were observed in both COVID-19 patients and vaccine recipients, expansion of clonal γδ T cells was found only in infected individuals. Our dataset enables side-by-side comparison of immune responses to infection versus vaccination, including clonal B and T cell responses. Our comparative analysis shows that vaccination induces a robust, durable clonal B and T cell responses, without the severe inflammation associated with infection.

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