3D single cell migration driven by temporal correlation between oscillating force dipoles
- University of Strasbourg, CNRS, IGBMC, France
- Institute Curie, France
- Univ. Lyon, Université Claude Bernard Lyon 1, CNRS UMR 5306, France
- Universität des Saarlandes, Germany
- INSERM UMR S1109, Institut d'Hématologie et d'Immunologie, France
- Institut Curie, CNRS UMR168, France
Abstract
Directional cell locomotion requires symmetry breaking between the front and rear of the cell. In some cells, symmetry breaking manifests itself in a directional flow of actin from the front to the rear of the cell. Many cells, especially in physiological 3D matrices do not show such coherent actin dynamics and present seemingly competing protrusion/retraction dynamics at their front and back. How symmetry breaking manifests itself for such cells is therefore elusive. We take inspiration from the scallop theorem proposed by Purcell for micro-swimmers in Newtonian fluids: self-propelled objects undergoing persistent motion at low Reynolds number must follow a cycle of shape changes that breaks temporal symmetry. We report similar observations for cells crawling in 3D. We quantified cell motion using a combination of 3D live cell imaging, visualization of the matrix displacement and a minimal model with multipolar expansion. We show that our cells embedded in a 3D matrix form myosin-driven force dipoles at both sides of the nucleus, that locally and periodically pinch the matrix. The existence of a phase shift between the two dipoles is required for directed cell motion which manifests itself as cycles with finite area in the dipole-quadrupole diagram, a formal equivalence to the Purcell cycle. We confirm this mechanism by triggering local dipolar contractions with a laser. This leads to directed motion. Our study reveals that these cells control their motility by synchronizing dipolar forces distributed at front and back. This result opens new strategies to externally control cell motion as well as for the design of micro-crawlers.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 1, 2, 3, 4 and 5.
Article and author information
Author details
Hélène Delanoë-Ayari
Funding
Deutsch-Französische Hochschule (CDFA-01-13)
- Albrecht Ott
- Daniel Riveline
Agence Nationale de la Recherche (ANR-10-IDEX-0002-02)
- Daniel Riveline
ICAM Branch Contributions
- Marco Leoni
- Pierre Sens
Agence Nationale de la Recherche (ANR-10-LBX-0038)
- Marco Leoni
- Pierre Sens
Agence Nationale de la Recherche (ANR-10-IDEX-0001-02)
- Marco Leoni
- Pierre Sens
Deutsche Forschungsgemeinschaft (SFB 1027)
- Albrecht Ott
Centre National de la Recherche Scientifique
- Daniel Riveline
ciFRC Strasbourg
- Daniel Riveline
University of 'Strasbourg
- Daniel Riveline
Labex IGBMC
- Daniel Riveline
Foundation Cino del Duca
- Daniel Riveline
Region Alsace
- Daniel Riveline
Saarland University
- Daniel Riveline
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Raymond E Goldstein, University of Cambridge, United Kingdom
Version history
- Preprint posted: May 8, 2020 (view preprint)
- Received: June 6, 2021
- Accepted: July 28, 2022
- Accepted Manuscript published: July 28, 2022 (version 1)
- Version of Record published: August 18, 2022 (version 2)
Copyright
© 2022, Godeau et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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3D single cell migration driven by temporal correlation between oscillating force dipoles
eLife 11:e71032.
https://doi.org/10.7554/eLife.71032
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