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RUFY3 regulates endolysosomes perinuclear positioning, antigen presentation and migration in activated phagocytes

Author

Listed:
  • Rémy Char

    (Aix Marseille Université, CNRS, INSERM, CIML)

  • Zhuangzhuang Liu

    (Xinxiang Medical University)

  • Cédric Jacqueline

    (Nantes Université, CHU Nantes, INSERM, Center for Research in Transplantation and Translational Immunology)

  • Marion Davieau

    (Nantes Université, CHU Nantes, INSERM, Center for Research in Transplantation and Translational Immunology)

  • Maria-Graciela Delgado

    (INSERM U932, Institut Curie)

  • Clara Soufflet

    (Aix Marseille Université, CNRS, INSERM, CIML)

  • Mathieu Fallet

    (Aix Marseille Université, CNRS, INSERM, CIML)

  • Lionel Chasson

    (Aix Marseille Université, CNRS, INSERM, CIML)

  • Raphael Chapuy

    (Aix Marseille Université, CNRS, INSERM, CIML)

  • Voahirana Camosseto

    (Aix Marseille Université, CNRS, INSERM, CIML)

  • Eva Strock

    (Aix Marseille Université, CNRS, INSERM, CIML)

  • Rejane Rua

    (Aix Marseille Université, CNRS, INSERM, CIML)

  • Catarina R. Almeida

    (University of Aveiro)

  • Bing Su

    (Shanghai Jiao Tong University School of Medicine)

  • Ana-Maria Lennon-Duménil

    (INSERM U932, Institut Curie)

  • Beatrice Nal

    (Aix Marseille Université, CNRS, INSERM, CIML)

  • Antoine Roquilly

    (Nantes Université, CHU Nantes, INSERM, Center for Research in Transplantation and Translational Immunology)

  • Yinming Liang

    (Xinxiang Medical University)

  • Stéphane Méresse

    (Aix Marseille Université, CNRS, INSERM, CIML)

  • Evelina Gatti

    (Aix Marseille Université, CNRS, INSERM, CIML
    University of Aveiro)

  • Philippe Pierre

    (Aix Marseille Université, CNRS, INSERM, CIML
    University of Aveiro
    Shanghai Jiao Tong University School of Medicine)

Abstract

Endo-lysosomes transport along microtubules and clustering in the perinuclear area are two necessary steps for microbes to activate specialized phagocyte functions. We report that RUN and FYVE domain-containing protein 3 (RUFY3) exists as two alternative isoforms distinguishable by the presence of a C-terminal FYVE domain and by their affinity for phosphatidylinositol 3-phosphate on endosomal membranes. The FYVE domain-bearing isoform (iRUFY3) is preferentially expressed in primary immune cells and up-regulated upon activation by microbes and Interferons. iRUFY3 is necessary for ARL8b + /LAMP1+ endo-lysosomes positioning in the pericentriolar organelles cloud of LPS-activated macrophages. We show that iRUFY3 controls macrophages migration, MHC II presentation and responses to Interferon-γ, while being important for intracellular Salmonella replication. Specific inactivation of rufy3 in phagocytes leads to aggravated pathologies in mouse upon LPS injection or bacterial pneumonia. This study highlights the role of iRUFY3 in controlling endo-lysosomal dynamics, which contributes to phagocyte activation and immune response regulation.

Suggested Citation

  • Rémy Char & Zhuangzhuang Liu & Cédric Jacqueline & Marion Davieau & Maria-Graciela Delgado & Clara Soufflet & Mathieu Fallet & Lionel Chasson & Raphael Chapuy & Voahirana Camosseto & Eva Strock & Reja, 2023. "RUFY3 regulates endolysosomes perinuclear positioning, antigen presentation and migration in activated phagocytes," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40062-x
    DOI: 10.1038/s41467-023-40062-x
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    References listed on IDEAS

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    1. Camilla Raiborg & Eva M. Wenzel & Nina M. Pedersen & Hallvard Olsvik & Kay O. Schink & Sebastian W. Schultz & Marina Vietri & Veronica Nisi & Cecilia Bucci & Andreas Brech & Terje Johansen & Harald St, 2015. "Repeated ER–endosome contacts promote endosome translocation and neurite outgrowth," Nature, Nature, vol. 520(7546), pages 234-238, April.
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