Dendritic cells direct circadian anti-tumour immune responses

Chen Wang, Coline Barnoud, Mara Cenerenti, Mengzhu Sun, Irene Caffa, Burak Kizil, Ruben Bill, Yuanlong Liu, Robert Pick, Laure Garnier, Olga A. Gkountidi, Louise M. Ince, Stephan Holtkamp, Nadine Fournier, Olivier Michielin, Daniel E. Speiser, Stéphanie Hugues, Alessio Nencioni, Mikaël J. Pittet, Camilla Jandus and Christoph Scheiermann ()
Additional contact information
Chen Wang: University of Geneva
Coline Barnoud: University of Geneva
Mara Cenerenti: University of Geneva
Mengzhu Sun: University of Geneva
Irene Caffa: University of Genoa
Burak Kizil: University of Geneva
Ruben Bill: University of Geneva
Yuanlong Liu: University of Lausanne
Robert Pick: University of Geneva
Laure Garnier: University of Geneva
Olga A. Gkountidi: University of Geneva
Louise M. Ince: University of Geneva
Stephan Holtkamp: Ludwig-Maximilians-Universität Munich
Nadine Fournier: Swiss Institute of Bioinformatics (SIB)
Olivier Michielin: AGORA Cancer Research Center
Daniel E. Speiser: University of Lausanne
Stéphanie Hugues: University of Geneva
Alessio Nencioni: University of Genoa
Mikaël J. Pittet: University of Geneva
Camilla Jandus: University of Geneva
Christoph Scheiermann: University of Geneva

Nature, 2023, vol. 614, issue 7946, 136-143

Abstract: Abstract The process of cancer immunosurveillance is a mechanism of tumour suppression that can protect the host from cancer development throughout its lifetime1,2. However, it is unknown whether the effectiveness of cancer immunosurveillance fluctuates over a single day. Here we demonstrate that the initial time of day of tumour engraftment dictates the ensuing tumour size across mouse cancer models. Using immunodeficient mice as well as mice lacking lineage-specific circadian functions, we show that dendritic cells (DCs) and CD8+ T cells exert circadian anti-tumour functions that control melanoma volume. Specifically, we find that rhythmic trafficking of DCs to the tumour draining lymph node governs a circadian response of tumour-antigen-specific CD8+ T cells that is dependent on the circadian expression of the co-stimulatory molecule CD80. As a consequence, cancer immunotherapy is more effective when synchronized with DC functions, shows circadian outcomes in mice and suggests similar effects in humans. These data demonstrate that the circadian rhythms of anti-tumour immune components are not only critical for controlling tumour size but can also be of therapeutic relevance.

Date: 2023
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DOI: 10.1038/s41586-022-05605-0

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