The circadian clock influences T cell responses to vaccination by regulating dendritic cell antigen processing

Mariana P. Cervantes-Silva, Richard G. Carroll, Mieszko M. Wilk, Diana Moreira, Cloe A. Payet, James R. O’Siorain, Shannon L. Cox, Lauren E. Fagan, Paula A. Klavina, Yan He, Tabea Drewinski, Alan McGinley, Sharleen M. Buel, George A. Timmons, James O. Early, Roger J. S. Preston, Jennifer M. Hurley, David K. Finlay, Ingmar Schoen, F. Javier Sánchez-García, Kingston H. G. Mills and Annie M. Curtis ()
Additional contact information
Mariana P. Cervantes-Silva: Royal College of Surgeons in Ireland RCSI
Richard G. Carroll: Royal College of Surgeons in Ireland RCSI
Mieszko M. Wilk: Trinity College Dublin
Diana Moreira: Trinity College Dublin
Cloe A. Payet: Royal College of Surgeons in Ireland RCSI
James R. O’Siorain: Royal College of Surgeons in Ireland RCSI
Shannon L. Cox: Royal College of Surgeons in Ireland RCSI
Lauren E. Fagan: Royal College of Surgeons in Ireland RCSI
Paula A. Klavina: Royal College of Surgeons in Ireland RCSI
Yan He: Royal College of Surgeons in Ireland RCSI
Tabea Drewinski: Royal College of Surgeons in Ireland RCSI
Alan McGinley: Royal College of Surgeons in Ireland RCSI
Sharleen M. Buel: Rensselaer Polytechnic Institute
George A. Timmons: Royal College of Surgeons in Ireland RCSI
James O. Early: Royal College of Surgeons in Ireland RCSI
Roger J. S. Preston: Royal College of Surgeons in Ireland RCSI
Jennifer M. Hurley: Rensselaer Polytechnic Institute
David K. Finlay: Trinity College Dublin
Ingmar Schoen: Royal College of Surgeons in Ireland RCSI
F. Javier Sánchez-García: Instituto Politécnico Nacional
Kingston H. G. Mills: Trinity College Dublin
Annie M. Curtis: Royal College of Surgeons in Ireland RCSI

Nature Communications, 2022, vol. 13, issue 1, 1-18

Abstract: Abstract Dendritic cells play a key role in processing and presenting antigens to naïve T cells to prime adaptive immunity. Circadian rhythms are known to regulate many aspects of immunity; however, the role of circadian rhythms in dendritic cell function is still unclear. Here, we show greater T cell responses when mice are immunised in the middle of their rest versus their active phase. We find a circadian rhythm in antigen processing that correlates with rhythms in both mitochondrial morphology and metabolism, dependent on the molecular clock gene, Bmal1. Using Mdivi-1, a compound that promotes mitochondrial fusion, we are able to rescue the circadian deficit in antigen processing and mechanistically link mitochondrial morphology and antigen processing. Furthermore, we find that circadian changes in mitochondrial Ca2+ are central to the circadian regulation of antigen processing. Our results indicate that rhythmic changes in mitochondrial calcium, which are associated with changes in mitochondrial morphology, regulate antigen processing.

Date: 2022
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DOI: 10.1038/s41467-022-34897-z

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