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A cell membrane model that reproduces cortical flow-driven cell migration and collective movement

Many fundamental biological processes are dependent on cellular migration. Although the mechanical mechanisms of single-cell migration are relatively well understood, those underlying migration of multiple cells adhered to each other in a cluster, referred to as cluster migration, are poorly underst...

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Autor principal: Sato, Katsuhiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10328438/
https://www.ncbi.nlm.nih.gov/pubmed/37427380
http://dx.doi.org/10.3389/fcell.2023.1126819
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author Sato, Katsuhiko
author_facet Sato, Katsuhiko
author_sort Sato, Katsuhiko
collection PubMed
description Many fundamental biological processes are dependent on cellular migration. Although the mechanical mechanisms of single-cell migration are relatively well understood, those underlying migration of multiple cells adhered to each other in a cluster, referred to as cluster migration, are poorly understood. A key reason for this knowledge gap is that many forces—including contraction forces from actomyosin networks, hydrostatic pressure from the cytosol, frictional forces from the substrate, and forces from adjacent cells—contribute to cell cluster movement, making it challenging to model, and ultimately elucidate, the final result of these forces. This paper describes a two-dimensional cell membrane model that represents cells on a substrate with polygons and expresses various mechanical forces on the cell surface, keeping these forces balanced at all times by neglecting cell inertia. The model is discrete but equivalent to a continuous model if appropriate replacement rules for cell surface segments are chosen. When cells are given a polarity, expressed by a direction-dependent surface tension reflecting the location dependence of contraction and adhesion on a cell boundary, the cell surface begins to flow from front to rear as a result of force balance. This flow produces unidirectional cell movement, not only for a single cell but also for multiple cells in a cluster, with migration speeds that coincide with analytical results from a continuous model. Further, if the direction of cell polarity is tilted with respect to the cluster center, surface flow induces cell cluster rotation. The reason why this model moves while keeping force balance on cell surface (i.e., under no net forces from outside) is because of the implicit inflow and outflow of cell surface components through the inside of the cell. An analytical formula connecting cell migration speed and turnover rate of cell surface components is presented.
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spelling pubmed-103284382023-07-08 A cell membrane model that reproduces cortical flow-driven cell migration and collective movement Sato, Katsuhiko Front Cell Dev Biol Cell and Developmental Biology Many fundamental biological processes are dependent on cellular migration. Although the mechanical mechanisms of single-cell migration are relatively well understood, those underlying migration of multiple cells adhered to each other in a cluster, referred to as cluster migration, are poorly understood. A key reason for this knowledge gap is that many forces—including contraction forces from actomyosin networks, hydrostatic pressure from the cytosol, frictional forces from the substrate, and forces from adjacent cells—contribute to cell cluster movement, making it challenging to model, and ultimately elucidate, the final result of these forces. This paper describes a two-dimensional cell membrane model that represents cells on a substrate with polygons and expresses various mechanical forces on the cell surface, keeping these forces balanced at all times by neglecting cell inertia. The model is discrete but equivalent to a continuous model if appropriate replacement rules for cell surface segments are chosen. When cells are given a polarity, expressed by a direction-dependent surface tension reflecting the location dependence of contraction and adhesion on a cell boundary, the cell surface begins to flow from front to rear as a result of force balance. This flow produces unidirectional cell movement, not only for a single cell but also for multiple cells in a cluster, with migration speeds that coincide with analytical results from a continuous model. Further, if the direction of cell polarity is tilted with respect to the cluster center, surface flow induces cell cluster rotation. The reason why this model moves while keeping force balance on cell surface (i.e., under no net forces from outside) is because of the implicit inflow and outflow of cell surface components through the inside of the cell. An analytical formula connecting cell migration speed and turnover rate of cell surface components is presented. Frontiers Media S.A. 2023-06-23 /pmc/articles/PMC10328438/ /pubmed/37427380 http://dx.doi.org/10.3389/fcell.2023.1126819 Text en Copyright © 2023 Sato. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Sato, Katsuhiko
A cell membrane model that reproduces cortical flow-driven cell migration and collective movement
title A cell membrane model that reproduces cortical flow-driven cell migration and collective movement
title_full A cell membrane model that reproduces cortical flow-driven cell migration and collective movement
title_fullStr A cell membrane model that reproduces cortical flow-driven cell migration and collective movement
title_full_unstemmed A cell membrane model that reproduces cortical flow-driven cell migration and collective movement
title_short A cell membrane model that reproduces cortical flow-driven cell migration and collective movement
title_sort cell membrane model that reproduces cortical flow-driven cell migration and collective movement
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10328438/
https://www.ncbi.nlm.nih.gov/pubmed/37427380
http://dx.doi.org/10.3389/fcell.2023.1126819
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