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Optineurin links Hace1-dependent Rac ubiquitylation to integrin-mediated mechanotransduction to control bacterial invasion and cell division

Author

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  • Serena Petracchini

    (Université Paris Cité, CNRS UMR6047, INSERM U1306, Unité des Toxines Bactériennes)

  • Daniel Hamaoui

    (Université Côte d’Azur, INSERM, C3M, Team Microbial Toxins in Host-Pathogen Interactions
    Equipe Labellisée Ligue Contre le Cancer)

  • Anne Doye

    (Université Côte d’Azur, INSERM, C3M, Team Microbial Toxins in Host-Pathogen Interactions
    Equipe Labellisée Ligue Contre le Cancer)

  • Atef Asnacios

    (Université Paris Cité, CNRS, Laboratoire Matière et Systèmes Complexes, UMR7057)

  • Florian Fage

    (Université Paris Cité, CNRS, Laboratoire Matière et Systèmes Complexes, UMR7057)

  • Elisa Vitiello

    (Université Grenoble Alpes, CNRS, LiPhy)

  • Martial Balland

    (Université Grenoble Alpes, CNRS, LiPhy)

  • Sebastien Janel

    (Université de Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019-UMR9017, CIIL—Center for Infection and Immunity of Lille)

  • Frank Lafont

    (Université de Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019-UMR9017, CIIL—Center for Infection and Immunity of Lille)

  • Mukund Gupta

    (Université Paris Cité, CNRS, Institut Jacques Monod)

  • Benoit Ladoux

    (Université Paris Cité, CNRS, Institut Jacques Monod)

  • Jerôme Gilleron

    (Université Côte d’Azur, INSERM, C3M, Team Cellular and Molecular Pathophysiology of Obesity and Diabetes)

  • Teresa M. Maia

    (VIB-UGent Center for Medical Biotechnology, VIB
    Ghent University
    VIB Proteomics Core, VIB)

  • Francis Impens

    (VIB-UGent Center for Medical Biotechnology, VIB
    Ghent University
    VIB Proteomics Core, VIB)

  • Laurent Gagnoux-Palacios

    (Université Côte d’Azur, CNRS, INSERM, Institut de Biologie Valrose (iBV))

  • Mads Daugaard

    (Vancouver Prostate Centre
    Department of Urologic Sciences, University of British Columbia)

  • Poul H. Sorensen

    (University of British Columbia)

  • Emmanuel Lemichez

    (Université Paris Cité, CNRS UMR6047, INSERM U1306, Unité des Toxines Bactériennes
    Université Côte d’Azur, INSERM, C3M, Team Microbial Toxins in Host-Pathogen Interactions
    Equipe Labellisée Ligue Contre le Cancer)

  • Amel Mettouchi

    (Université Paris Cité, CNRS UMR6047, INSERM U1306, Unité des Toxines Bactériennes
    Université Côte d’Azur, INSERM, C3M, Team Microbial Toxins in Host-Pathogen Interactions
    Equipe Labellisée Ligue Contre le Cancer)

Abstract

Extracellular matrix (ECM) elasticity is perceived by cells via focal adhesion structures, which transduce mechanical cues into chemical signalling to conform cell behavior. Although the contribution of ECM compliance to the control of cell migration or division is extensively studied, little is reported regarding infectious processes. We study this phenomenon with the extraintestinal Escherichia coli pathogen UTI89. We show that UTI89 takes advantage, via its CNF1 toxin, of integrin mechanoactivation to trigger its invasion into cells. We identify the HACE1 E3 ligase-interacting protein Optineurin (OPTN) as a protein regulated by ECM stiffness. Functional analysis establishes a role of OPTN in bacterial invasion and integrin mechanical coupling and for stimulation of HACE1 E3 ligase activity towards the Rac1 GTPase. Consistent with a role of OPTN in cell mechanics, OPTN knockdown cells display defective integrin-mediated traction force buildup, associated with limited cellular invasion by UTI89. Nevertheless, OPTN knockdown cells display strong mechanochemical adhesion signalling, enhanced Rac1 activation and increased cyclin D1 translation, together with enhanced cell proliferation independent of ECM stiffness. Together, our data ascribe a new function to OPTN in mechanobiology.

Suggested Citation

  • Serena Petracchini & Daniel Hamaoui & Anne Doye & Atef Asnacios & Florian Fage & Elisa Vitiello & Martial Balland & Sebastien Janel & Frank Lafont & Mukund Gupta & Benoit Ladoux & Jerôme Gilleron & Te, 2022. "Optineurin links Hace1-dependent Rac ubiquitylation to integrin-mediated mechanotransduction to control bacterial invasion and cell division," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33803-x
    DOI: 10.1038/s41467-022-33803-x
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    References listed on IDEAS

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    1. Yuting Feng & Shuyi Wang & Xiaoye Liu & Yiming Han & Hongwei Xu & Xiaocen Duan & Wenyue Xie & Zhuoling Tian & Zuoying Yuan & Zhuo Wan & Liang Xu & Siying Qin & Kangmin He & Jianyong Huang, 2023. "Geometric constraint-triggered collagen expression mediates bacterial-host adhesion," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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