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Gap geometry dictates epithelial closure efficiency

Author

Listed:
  • Andrea Ravasio

    (Mechanobiology Institute, National University of Singapore)

  • Ibrahim Cheddadi

    (Sorbonne Universités, UPMC University Paris 06, CNRS UMR 7598, Laboratoire Jacques-Louis Lions
    Present address: INRIA Virtual Plants, Campus St Priest - BAT 5, CC 05018, 860 rue de St Priest, 34095 Montpellier Cedex 5, France)

  • Tianchi Chen

    (Mechanobiology Institute, National University of Singapore)

  • Telmo Pereira

    (CEDOC - Chronic Diseases Research Center, NOVA Medical School, Rua Camara Pestana, 6, Lisbon)

  • Hui Ting Ong

    (Mechanobiology Institute, National University of Singapore)

  • Cristina Bertocchi

    (Mechanobiology Institute, National University of Singapore)

  • Agusti Brugues

    (ICREA at Institute for Bioengineering of Catalonia and Universitat de Barcelona)

  • Antonio Jacinto

    (CEDOC - Chronic Diseases Research Center, NOVA Medical School, Rua Camara Pestana, 6, Lisbon)

  • Alexandre J. Kabla

    (University of Cambridge)

  • Yusuke Toyama

    (Mechanobiology Institute, National University of Singapore
    Department of Biological Sciences National University of Singapore
    Temasek Life Sciences Laboratory)

  • Xavier Trepat

    (ICREA at Institute for Bioengineering of Catalonia and Universitat de Barcelona)

  • Nir Gov

    (Weizmann Institute of Science)

  • Luís Neves de Almeida

    (Sorbonne Universités, UPMC University Paris 06, CNRS UMR 7598, Laboratoire Jacques-Louis Lions
    INRIA-Paris-Rocquencourt, MAMBA Team)

  • Benoit Ladoux

    (Mechanobiology Institute, National University of Singapore
    Institut Jacques Monod (IJM), CNRS UMR 7592 and Université Paris Diderot)

Abstract

Closure of wounds and gaps in tissues is fundamental for the correct development and physiology of multicellular organisms and, when misregulated, may lead to inflammation and tumorigenesis. To re-establish tissue integrity, epithelial cells exhibit coordinated motion into the void by active crawling on the substrate and by constricting a supracellular actomyosin cable. Coexistence of these two mechanisms strongly depends on the environment. However, the nature of their coupling remains elusive because of the complexity of the overall process. Here we demonstrate that epithelial gap geometry in both in vitro and in vivo regulates these collective mechanisms. In addition, the mechanical coupling between actomyosin cable contraction and cell crawling acts as a large-scale regulator to control the dynamics of gap closure. Finally, our computational modelling clarifies the respective roles of the two mechanisms during this process, providing a robust and universal mechanism to explain how epithelial tissues restore their integrity.

Suggested Citation

  • Andrea Ravasio & Ibrahim Cheddadi & Tianchi Chen & Telmo Pereira & Hui Ting Ong & Cristina Bertocchi & Agusti Brugues & Antonio Jacinto & Alexandre J. Kabla & Yusuke Toyama & Xavier Trepat & Nir Gov &, 2015. "Gap geometry dictates epithelial closure efficiency," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms8683
    DOI: 10.1038/ncomms8683
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    Cited by:

    1. Nicole Morales-Camilo & Jingzhun Liu & Manuel J. Ramírez & Patricio Canales-Salgado & Juan José Alegría & Xuyao Liu & Hui Ting Ong & Nelson P. Barrera & Angélica Fierro & Yusuke Toyama & Benjamin T. G, 2024. "Alternative molecular mechanisms for force transmission at adherens junctions via β-catenin-vinculin interaction," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Aurélien Villedieu & Lale Alpar & Isabelle Gaugué & Amina Joudat & François Graner & Floris Bosveld & Yohanns Bellaïche, 2023. "Homeotic compartment curvature and tension control spatiotemporal folding dynamics," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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