Interaction dynamics between innate and adaptive immune cells responding to SARS-CoV-2 vaccination in non-human primates

Chaim A. Schramm, Damee Moon, Lowrey Peyton, Noemia S. Lima, Christian Wake, Kristin L. Boswell, Amy R. Henry, Farida Laboune, David Ambrozak, Samuel W. Darko, I-Ting Teng, Kathryn E. Foulds, Andrea Carfi, Darin K. Edwards, Peter D. Kwong, Richard A. Koup, Robert A. Seder () and Daniel C. Douek ()
Additional contact information
Chaim A. Schramm: National Institutes of Health
Damee Moon: National Institutes of Health
Lowrey Peyton: National Institutes of Health
Noemia S. Lima: National Institutes of Health
Christian Wake: National Institutes of Health
Kristin L. Boswell: National Institutes of Health
Amy R. Henry: National Institutes of Health
Farida Laboune: National Institutes of Health
David Ambrozak: National Institutes of Health
Samuel W. Darko: National Institutes of Health
I-Ting Teng: National Institutes of Health
Kathryn E. Foulds: National Institutes of Health
Andrea Carfi: Moderna Inc.
Darin K. Edwards: Moderna Inc.
Peter D. Kwong: National Institutes of Health
Richard A. Koup: National Institutes of Health
Robert A. Seder: National Institutes of Health
Daniel C. Douek: National Institutes of Health

Nature Communications, 2023, vol. 14, issue 1, 1-17

Abstract: Abstract As SARS-CoV-2 variants continue evolving, testing updated vaccines in non-human primates remains important for guiding human clinical practice. To date, such studies have focused on antibody titers and antigen-specific B and T cell frequencies. Here, we extend our understanding by integrating innate and adaptive immune responses to mRNA-1273 vaccination in rhesus macaques. We sorted innate immune cells from a pre-vaccine time point, as well as innate immune cells and antigen-specific peripheral B and T cells two weeks after each of two vaccine doses and used single-cell sequencing to assess the transcriptomes and adaptive immune receptors of each cell. We show that a subset of S-specific T cells expresses cytokines critical for activating innate responses, with a concomitant increase in CCR5-expressing intermediate monocytes and a shift of natural killer cells to a more cytotoxic phenotype. The second vaccine dose, administered 4 weeks after the first, elicits an increase in circulating germinal center-like B cells 2 weeks later, which are more clonally expanded and enriched for epitopes in the receptor binding domain. Both doses stimulate inflammatory response genes associated with elevated antibody production. Overall, we provide a comprehensive picture of bidirectional signaling between innate and adaptive components of the immune system and suggest potential mechanisms for the enhanced response to secondary exposure.

Date: 2023
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DOI: 10.1038/s41467-023-43420-x

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