Ezrin enhances line tension along transcellular tunnel edges via NMIIa driven actomyosin cable formation

Caroline Stefani, David Gonzalez-Rodriguez (), Yosuke Senju, Anne Doye, Nadia Efimova, Sébastien Janel, Justine Lipuma, Meng Chen Tsai, Daniel Hamaoui, Madhavi P. Maddugoda, Olivier Cochet-Escartin, Coline Prévost, Frank Lafont, Tatyana Svitkina, Pekka Lappalainen, Patricia Bassereau () and Emmanuel Lemichez ()
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Caroline Stefani: INSERM, U1065, Université de Nice-Sophia Antipolis, Centre Méditerranéen de Médecine Moléculaire (C3M)
David Gonzalez-Rodriguez: LCP-A2MC, Institut Jean Barriol, Université de Lorraine
Yosuke Senju: Program in Cell and Molecular Biology, Institute of Biotechnology, P.O. Box 56, University of Helsinki
Anne Doye: INSERM, U1065, Université de Nice-Sophia Antipolis, Centre Méditerranéen de Médecine Moléculaire (C3M)
Nadia Efimova: University of Pennsylvania
Sébastien Janel: Multiscale Physics-Biology-Chemistry and Cancer, Cellular Microbiology and Physics of Infection Group, Center for Infection and Immunity of Lille, CNRS UMR8204, INSERM U1019, Institut Pasteur de Lille, Centre Hospitalier Régional de Lille, Université de Lille
Justine Lipuma: INSERM, U1065, Université de Nice-Sophia Antipolis, Centre Méditerranéen de Médecine Moléculaire (C3M)
Meng Chen Tsai: INSERM, U1065, Université de Nice-Sophia Antipolis, Centre Méditerranéen de Médecine Moléculaire (C3M)
Daniel Hamaoui: INSERM, U1065, Université de Nice-Sophia Antipolis, Centre Méditerranéen de Médecine Moléculaire (C3M)
Madhavi P. Maddugoda: INSERM, U1065, Université de Nice-Sophia Antipolis, Centre Méditerranéen de Médecine Moléculaire (C3M)
Olivier Cochet-Escartin: Multiscale Physics-Biology-Chemistry and Cancer, Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, CNRS, UMR168
Coline Prévost: Multiscale Physics-Biology-Chemistry and Cancer, Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, CNRS, UMR168
Frank Lafont: Multiscale Physics-Biology-Chemistry and Cancer, Cellular Microbiology and Physics of Infection Group, Center for Infection and Immunity of Lille, CNRS UMR8204, INSERM U1019, Institut Pasteur de Lille, Centre Hospitalier Régional de Lille, Université de Lille
Tatyana Svitkina: University of Pennsylvania
Pekka Lappalainen: Program in Cell and Molecular Biology, Institute of Biotechnology, P.O. Box 56, University of Helsinki
Patricia Bassereau: Multiscale Physics-Biology-Chemistry and Cancer, Laboratoire Physico Chimie Curie, Institut Curie, PSL Research University, CNRS, UMR168
Emmanuel Lemichez: INSERM, U1065, Université de Nice-Sophia Antipolis, Centre Méditerranéen de Médecine Moléculaire (C3M)

Nature Communications, 2017, vol. 8, issue 1, 1-14

Abstract: Abstract Transendothelial cell macroaperture (TEM) tunnels control endothelium barrier function and are triggered by several toxins from pathogenic bacteria that provoke vascular leakage. Cellular dewetting theory predicted that a line tension of uncharacterized origin works at TEM boundaries to limit their widening. Here, by conducting high-resolution microscopy approaches we unveil the presence of an actomyosin cable encircling TEMs. We develop a theoretical cellular dewetting framework to interpret TEM physical parameters that are quantitatively determined by laser ablation experiments. This establishes the critical role of ezrin and non-muscle myosin II (NMII) in the progressive implementation of line tension. Mechanistically, fluorescence-recovery-after-photobleaching experiments point for the upstream role of ezrin in stabilizing actin filaments at the edges of TEMs, thereby favouring their crosslinking by NMIIa. Collectively, our findings ascribe to ezrin and NMIIa a critical function of enhancing line tension at the cell boundary surrounding the TEMs by promoting the formation of an actomyosin ring.

Date: 2017
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DOI: 10.1038/ncomms15839

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