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Dendritic cells direct circadian anti-tumour immune responses

Author

Listed:
  • Chen Wang

    (University of Geneva)

  • Coline Barnoud

    (University of Geneva)

  • Mara Cenerenti

    (University of Geneva
    Ludwig Institute for Cancer Research)

  • Mengzhu Sun

    (University of Geneva)

  • Irene Caffa

    (University of Genoa)

  • Burak Kizil

    (University of Geneva)

  • Ruben Bill

    (University of Geneva
    AGORA Cancer Research Center
    Massachusetts General Hospital and Harvard Medical School)

  • Yuanlong Liu

    (University of Lausanne
    Swiss Cancer Center Leman
    Swiss Institute of Bioinformatics (SIB))

  • 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
    Geneva Centre for Inflammation Research)

  • Alessio Nencioni

    (University of Genoa
    IRCCS Ospedale Policlinico San Martino)

  • Mikaël J. Pittet

    (University of Geneva
    Ludwig Institute for Cancer Research
    AGORA Cancer Research Center
    Massachusetts General Hospital and Harvard Medical School)

  • Camilla Jandus

    (University of Geneva
    Ludwig Institute for Cancer Research
    Geneva Centre for Inflammation Research)

  • Christoph Scheiermann

    (University of Geneva
    Ludwig-Maximilians-Universität Munich
    Geneva Centre for Inflammation Research)

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.

Suggested Citation

  • 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 , 2023. "Dendritic cells direct circadian anti-tumour immune responses," Nature, Nature, vol. 614(7946), pages 136-143, February.
    • Handle: RePEc:nat:nature:v:614:y:2023:i:7946:d:10.1038_s41586-022-05605-0
    DOI: 10.1038/s41586-022-05605-0
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    Cited by:

    1. Dimitrii Pogorelov & Sebastian Felix Nepomuk Bode & Xin He & Javier Ramiro-Garcia & Fanny Hedin & Wim Ammerlaan & Maria Konstantinou & Christophe M. Capelle & Ni Zeng & Aurélie Poli & Olivia Domingues, 2024. "Multiomics approaches disclose very-early molecular and cellular switches during insect-venom allergen-specific immunotherapy: an observational study," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

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