Polarity-driven three-dimensional spontaneous rotation of a cell doublet

Publikation: Beitrag in FachzeitschriftForschungsartikelBeigetragenBegutachtung

Beitragende

  • Linjie Lu - , Université de Strasbourg, Centre national de la recherche scientifique (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Autor:in)
  • Tristan Guyomar - , Université de Strasbourg, Centre national de la recherche scientifique (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Autor:in)
  • Quentin Vagne - , Universität Genf (Autor:in)
  • Rémi Berthoz - , Université de Strasbourg, Centre national de la recherche scientifique (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Autor:in)
  • Alejandro Torres-Sánchez - , European Molecular Biology Laboratory (EMBL) Barcelona (Autor:in)
  • Michèle Lieb - , Université de Strasbourg, Centre national de la recherche scientifique (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Autor:in)
  • Cecilie Martin-Lemaitre - , Max Planck Institute of Molecular Cell Biology and Genetics, Technische Universität Dresden (Autor:in)
  • Kobus van Unen - , Universität Bern (Autor:in)
  • Alf Honigmann - , Professur für Biophysik, Exzellenzcluster PoL: Physik des Lebens, Biotechnologisches Zentrum (BIOTEC), Max Planck Institute of Molecular Cell Biology and Genetics (Autor:in)
  • Olivier Pertz - , Universität Bern (Autor:in)
  • Daniel Riveline - , Université de Strasbourg, Centre national de la recherche scientifique (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Autor:in)
  • Guillaume Salbreux - , Universität Genf (Autor:in)

Abstract

Mechanical interactions between cells play a fundamental role in the self-organization of organisms. How these interactions drive coordinated cell movement in three dimensions remains unclear. Here we report that cell doublets embedded in a three-dimensional extracellular matrix undergo spontaneous rotations. We investigate the rotation mechanism and find that it is driven by a polarized distribution of myosin within cell cortices. The mismatched orientation of this polarized distribution breaks the doublet mirror symmetry. In addition, cells adhere at their interface through adherens junctions and with the extracellular matrix through focal contacts near myosin clusters. We use a physical theory describing the doublet as two interacting active surfaces to show that rotation is driven by myosin-generated gradients of active tension whose profiles are dictated by interacting cell polarity axes. We also show that three-dimensional shape symmetries are related to broken symmetries of the myosin distribution in cortices. To test for the rotation mechanism, we suppress myosin clusters using laser ablation and generate new myosin clusters by optogenetics. Our work clarifies how polarity-oriented active mechanical forces drive collective cell motion in three dimensions.

Details

OriginalspracheEnglisch
Seitenumfang10
FachzeitschriftNature physics
Jahrgang20
Ausgabenummer7
PublikationsstatusVeröffentlicht - 2024
Peer-Review-StatusJa

Externe IDs

Mendeley 8ef1d3ce-9c1b-3186-954d-662b8c6088eb
ORCID /0000-0003-0475-3790/work/162347134

Schlagworte

ASJC Scopus Sachgebiete