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3D single cell migration driven by temporal correlation between oscillating force dipoles

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...

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Autores principales: Godeau, Amélie Luise, Leoni, Marco, Comelles, Jordi, Guyomar, Tristan, Lieb, Michele, Delanoë-Ayari, Hélène, Ott, Albrecht, Harlepp, Sebastien, Sens, Pierre, Riveline, Daniel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9395190/
https://www.ncbi.nlm.nih.gov/pubmed/35899947
http://dx.doi.org/10.7554/eLife.71032
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author Godeau, Amélie Luise
Leoni, Marco
Comelles, Jordi
Guyomar, Tristan
Lieb, Michele
Delanoë-Ayari, Hélène
Ott, Albrecht
Harlepp, Sebastien
Sens, Pierre
Riveline, Daniel
author_facet Godeau, Amélie Luise
Leoni, Marco
Comelles, Jordi
Guyomar, Tristan
Lieb, Michele
Delanoë-Ayari, Hélène
Ott, Albrecht
Harlepp, Sebastien
Sens, Pierre
Riveline, Daniel
author_sort Godeau, Amélie Luise
collection PubMed
description 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.
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spelling pubmed-93951902022-08-23 3D single cell migration driven by temporal correlation between oscillating force dipoles Godeau, Amélie Luise Leoni, Marco Comelles, Jordi Guyomar, Tristan Lieb, Michele Delanoë-Ayari, Hélène Ott, Albrecht Harlepp, Sebastien Sens, Pierre Riveline, Daniel eLife Physics of Living Systems 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. eLife Sciences Publications, Ltd 2022-07-28 /pmc/articles/PMC9395190/ /pubmed/35899947 http://dx.doi.org/10.7554/eLife.71032 Text en © 2022, Godeau, Leoni et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Physics of Living Systems
Godeau, Amélie Luise
Leoni, Marco
Comelles, Jordi
Guyomar, Tristan
Lieb, Michele
Delanoë-Ayari, Hélène
Ott, Albrecht
Harlepp, Sebastien
Sens, Pierre
Riveline, Daniel
3D single cell migration driven by temporal correlation between oscillating force dipoles
title 3D single cell migration driven by temporal correlation between oscillating force dipoles
title_full 3D single cell migration driven by temporal correlation between oscillating force dipoles
title_fullStr 3D single cell migration driven by temporal correlation between oscillating force dipoles
title_full_unstemmed 3D single cell migration driven by temporal correlation between oscillating force dipoles
title_short 3D single cell migration driven by temporal correlation between oscillating force dipoles
title_sort 3d single cell migration driven by temporal correlation between oscillating force dipoles
topic Physics of Living Systems
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9395190/
https://www.ncbi.nlm.nih.gov/pubmed/35899947
http://dx.doi.org/10.7554/eLife.71032
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