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

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Linjie Lu - , University of Strasbourg, French National Centre for Scientific Research (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Author)
  • Tristan Guyomar - , University of Strasbourg, French National Centre for Scientific Research (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Author)
  • Quentin Vagne - , University of Geneva (Author)
  • Rémi Berthoz - , University of Strasbourg, French National Centre for Scientific Research (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Author)
  • Alejandro Torres-Sánchez - , European Molecular Biology Laboratory (EMBL) Barcelona (Author)
  • Michèle Lieb - , University of Strasbourg, French National Centre for Scientific Research (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Author)
  • Cecilie Martin-Lemaitre - , Max Planck Institute of Molecular Cell Biology and Genetics, TUD Dresden University of Technology (Author)
  • Kobus van Unen - , University of Bern (Author)
  • Alf Honigmann - , Chair of Biophysics, Clusters of Excellence PoL: Physics of Life, Biotechnology Center, Max Planck Institute of Molecular Cell Biology and Genetics (Author)
  • Olivier Pertz - , University of Bern (Author)
  • Daniel Riveline - , University of Strasbourg, French National Centre for Scientific Research (CNRS), INSERM - Institut national de la santé et de la recherche médicale (Author)
  • Guillaume Salbreux - , University of Geneva (Author)

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

Original languageEnglish
JournalNature physics
Publication statusPublished - 2024
Peer-reviewedYes

External IDs

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

Keywords

ASJC Scopus subject areas