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

Rémy Char, Zhuangzhuang Liu, Cédric Jacqueline, Marion Davieau, Maria-Graciela Delgado, Clara Soufflet, Mathieu Fallet, Lionel Chasson, Raphael Chapuy, Voahirana Camosseto, Eva Strock, Rejane Rua, Catarina R. Almeida, Bing Su, Ana-Maria Lennon-Duménil, Beatrice Nal, Antoine Roquilly, Yinming Liang, Stéphane Méresse, Evelina Gatti () and Philippe Pierre ()
Additional contact information
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
Philippe Pierre: Aix Marseille Université, CNRS, INSERM, CIML

Nature Communications, 2023, vol. 14, issue 1, 1-20

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-40062-x

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