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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...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2022
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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. |
format | Online Article Text |
id | pubmed-9395190 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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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