Influenza vaccination reveals sex dimorphic imprints of prior mild COVID-19

Rachel Sparks, William W. Lau, Can Liu, Kyu Lee Han, Kiera L. Vrindten, Guangping Sun, Milann Cox, Sarah F. Andrews, Neha Bansal, Laura E. Failla, Jody Manischewitz, Gabrielle Grubbs, Lisa R. King, Galina Koroleva, Stephanie Leimenstoll, LaQuita Snow, Jinguo Chen, Juanjie Tang, Amrita Mukherjee, Brian A. Sellers, Richard Apps, Adrian B. McDermott, Andrew J. Martins, Evan M. Bloch, Hana Golding, Surender Khurana and John S. Tsang ()
Additional contact information
Rachel Sparks: NIAID, NIH
William W. Lau: NIAID, NIH
Can Liu: NIAID, NIH
Kyu Lee Han: NIAID, NIH
Kiera L. Vrindten: NIAID, NIH
Guangping Sun: NIAID, NIH
Milann Cox: NIAID, NIH
Sarah F. Andrews: NIAID, NIH
Neha Bansal: NIAID, NIH
Laura E. Failla: NIAID, NIH
Jody Manischewitz: FDA
Gabrielle Grubbs: FDA
Lisa R. King: FDA
Galina Koroleva: NIAID, NIH
Stephanie Leimenstoll: NIAID, NIH
LaQuita Snow: NIAID, NIH
Jinguo Chen: NIAID, NIH
Juanjie Tang: FDA
Amrita Mukherjee: NIAID, NIH
Brian A. Sellers: NIAID, NIH
Richard Apps: NIAID, NIH
Adrian B. McDermott: NIAID, NIH
Andrew J. Martins: NIAID, NIH
Evan M. Bloch: Johns Hopkins University School of Medicine
Hana Golding: FDA
Surender Khurana: FDA
John S. Tsang: NIAID, NIH

Nature, 2023, vol. 614, issue 7949, 752-761

Abstract: Abstract Acute viral infections can have durable functional impacts on the immune system long after recovery, but how they affect homeostatic immune states and responses to future perturbations remain poorly understood1–4. Here we use systems immunology approaches, including longitudinal multimodal single-cell analysis (surface proteins, transcriptome and V(D)J sequences) to comparatively assess baseline immune statuses and responses to influenza vaccination in 33 healthy individuals after recovery from mild, non-hospitalized COVID-19 (mean, 151 days after diagnosis) and 40 age- and sex-matched control individuals who had never had COVID-19. At the baseline and independent of time after COVID-19, recoverees had elevated T cell activation signatures and lower expression of innate immune genes including Toll-like receptors in monocytes. Male individuals who had recovered from COVID-19 had coordinately higher innate, influenza-specific plasmablast, and antibody responses after vaccination compared with healthy male individuals and female individuals who had recovered from COVID-19, in part because male recoverees had monocytes with higher IL-15 responses early after vaccination coupled with elevated prevaccination frequencies of ‘virtual memory’-like CD8+ T cells poised to produce more IFNγ after IL-15 stimulation. Moreover, the expression of the repressed innate immune genes in monocytes increased by day 1 to day 28 after vaccination in recoverees, therefore moving towards the prevaccination baseline of the healthy control individuals. By contrast, these genes decreased on day 1 and returned to the baseline by day 28 in the control individuals. Our study reveals sex-dimorphic effects of previous mild COVID-19 and suggests that viral infections in humans can establish new immunological set-points that affect future immune responses in an antigen-agnostic manner.

Date: 2023
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DOI: 10.1038/s41586-022-05670-5

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