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

Linjie Lu, Tristan Guyomar, Quentin Vagne, Rémi Berthoz, Alejandro Torres-Sánchez, Michèle Lieb, Cecilie Martin-Lemaitre, Kobus van Unen, Alf Honigmann, Olivier Pertz, View ORCID ProfileGuillaume Salbreux, View ORCID ProfileDaniel Riveline
doi: https://doi.org/10.1101/2022.12.21.521355
Linjie Lu
1Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
4Institut National de la Santé et de la Recherche Médicale, U964, Illkirch, France
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Tristan Guyomar
1Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
4Institut National de la Santé et de la Recherche Médicale, U964, Illkirch, France
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Quentin Vagne
5University of Geneva, Quai Ernest Ansermet 30, 1205 Genève, Switzerland
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Rémi Berthoz
1Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
4Institut National de la Santé et de la Recherche Médicale, U964, Illkirch, France
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Alejandro Torres-Sánchez
6Tissue Biology and Disease Modelling Unit, European Molecular Biology Laboratory, Doctor Aiguader 88, Barcelona (08003), Spain
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Michèle Lieb
1Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
4Institut National de la Santé et de la Recherche Médicale, U964, Illkirch, France
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Cecilie Martin-Lemaitre
7Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
8Technische Universität Dresden, Biotechnologisches Zentrum, Center for Molecular Cellular Bioengineering (CMCB), Dresden, Germany
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Kobus van Unen
9Institute of Cell Biology, University of Bern, Bern, Switzerland
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Alf Honigmann
7Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
8Technische Universität Dresden, Biotechnologisches Zentrum, Center for Molecular Cellular Bioengineering (CMCB), Dresden, Germany
10Cluster of Excellence Physics of Life, TU Dresden, Dresden, Germany
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Olivier Pertz
9Institute of Cell Biology, University of Bern, Bern, Switzerland
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Guillaume Salbreux
5University of Geneva, Quai Ernest Ansermet 30, 1205 Genève, Switzerland
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  • ORCID record for Guillaume Salbreux
  • For correspondence: Guillaume.Salbreux@unige.ch riveline@unistra.fr
Daniel Riveline
1Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
4Institut National de la Santé et de la Recherche Médicale, U964, Illkirch, France
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  • ORCID record for Daniel Riveline
  • For correspondence: Guillaume.Salbreux@unige.ch riveline@unistra.fr
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Abstract

Cell mechanical interactions play a fundamental role in the self-organisation of organisms. How these interactions drive coordinated cell movement in three-dimensions remains unclear. Here we report that cell doublets embedded in a 3D extracellular matrix undergo spontaneous rotations and we investigate the rotation mechanism using live cell imaging, quantitative measurements, mechanical perturbations, and theory. We find that rotation 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. Using a physical theory describing the doublet as two interacting active surfaces, we find that rotation is driven by myosin-generated gradients of active tension, whose profiles are dictated by interacting cell polarity axes. We show that interface three-dimensional shapes can be understood from the Curie principle: shapes symmetries are related to broken symmetries of myosin distribution in cortices. To test for the rotation mechanism, we suppress myosin clusters using laser ablation and we generate new myosin clusters by optogenetics. Our work clarifies how polarity-oriented active mechanical forces drive collective cell motion in three dimensions.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted December 22, 2022.
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Polarity-driven three-dimensional spontaneous rotation of a cell doublet
Linjie Lu, Tristan Guyomar, Quentin Vagne, Rémi Berthoz, Alejandro Torres-Sánchez, Michèle Lieb, Cecilie Martin-Lemaitre, Kobus van Unen, Alf Honigmann, Olivier Pertz, Guillaume Salbreux, Daniel Riveline
bioRxiv 2022.12.21.521355; doi: https://doi.org/10.1101/2022.12.21.521355
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Polarity-driven three-dimensional spontaneous rotation of a cell doublet
Linjie Lu, Tristan Guyomar, Quentin Vagne, Rémi Berthoz, Alejandro Torres-Sánchez, Michèle Lieb, Cecilie Martin-Lemaitre, Kobus van Unen, Alf Honigmann, Olivier Pertz, Guillaume Salbreux, Daniel Riveline
bioRxiv 2022.12.21.521355; doi: https://doi.org/10.1101/2022.12.21.521355

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