Influence of circadian clocks on adaptive immunity and vaccination responses

Louise Madeleine Ince, Coline Barnoud, Lydia Kay Lutes, Robert Pick, Chen Wang, Flore Sinturel, Chien-Sin Chen, Alba Juan, Jasmin Weber, Stephan J. Holtkamp, Sophia Martina Hergenhan, Jennifer Geddes-McAlister, Stefan Ebner, Paola Fontannaz, Benjamin Meyer, Maria Vono, Stéphane Jemelin, Charna Dibner, Claire-Anne Siegrist, Felix Meissner, Frederik Graw and Christoph Scheiermann ()
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Louise Madeleine Ince: University of Geneva
Coline Barnoud: University of Geneva
Lydia Kay Lutes: University of Geneva
Robert Pick: University of Geneva
Chen Wang: University of Geneva
Flore Sinturel: University of Geneva
Chien-Sin Chen: Walter-Brendel-Centre of Experimental Medicine, Ludwig-Maximilians-University Munich, BioMedical Centre
Alba Juan: Walter-Brendel-Centre of Experimental Medicine, Ludwig-Maximilians-University Munich, BioMedical Centre
Jasmin Weber: Walter-Brendel-Centre of Experimental Medicine, Ludwig-Maximilians-University Munich, BioMedical Centre
Stephan J. Holtkamp: Walter-Brendel-Centre of Experimental Medicine, Ludwig-Maximilians-University Munich, BioMedical Centre
Sophia Martina Hergenhan: Walter-Brendel-Centre of Experimental Medicine, Ludwig-Maximilians-University Munich, BioMedical Centre
Jennifer Geddes-McAlister: Experimental Systems Immunology, Max Planck Institute of Biochemistry
Stefan Ebner: Experimental Systems Immunology, Max Planck Institute of Biochemistry
Paola Fontannaz: University of Geneva
Benjamin Meyer: University of Geneva
Maria Vono: University of Geneva
Stéphane Jemelin: University of Geneva
Charna Dibner: University of Geneva
Claire-Anne Siegrist: University of Geneva
Felix Meissner: Experimental Systems Immunology, Max Planck Institute of Biochemistry
Frederik Graw: Heidelberg University
Christoph Scheiermann: University of Geneva

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract The adaptive immune response is under circadian control, yet, why adaptive immune reactions continue to exhibit circadian changes over long periods of time is unknown. Using a combination of experimental and mathematical modeling approaches, we show here that dendritic cells migrate from the skin to the draining lymph node in a time-of-day-dependent manner, which provides an enhanced likelihood for functional interactions with T cells. Rhythmic expression of TNF in the draining lymph node enhances BMAL1-controlled ICAM-1 expression in high endothelial venules, resulting in lymphocyte infiltration and lymph node expansion. Lymph node cellularity continues to be different for weeks after the initial time-of-day-dependent challenge, which governs the immune response to vaccinations directed against Hepatitis A virus as well as SARS-CoV-2. In this work, we present a mechanistic understanding of the time-of-day dependent development and maintenance of an adaptive immune response, providing a strategy for using time-of-day to optimize vaccination regimes.

Date: 2023
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DOI: 10.1038/s41467-023-35979-2

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