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Physical forces guide curvature sensing and cell migration mode bifurcating
The ability of cells to sense and adapt to curvy topographical features has been implicated in organ morphogenesis, tissue repair, and tumor metastasis. However, how individual cells or multicellular assemblies sense and differentiate curvatures remains elusive. Here, we reveal a curvature sensing m...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10482382/ https://www.ncbi.nlm.nih.gov/pubmed/37680491 http://dx.doi.org/10.1093/pnasnexus/pgad237 |
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author | Feng, Luyi Zhao, Tiankai Xu, Hongmei Shi, Xuechen Li, Changhao Hsia, K Jimmy Zhang, Sulin |
author_facet | Feng, Luyi Zhao, Tiankai Xu, Hongmei Shi, Xuechen Li, Changhao Hsia, K Jimmy Zhang, Sulin |
author_sort | Feng, Luyi |
collection | PubMed |
description | The ability of cells to sense and adapt to curvy topographical features has been implicated in organ morphogenesis, tissue repair, and tumor metastasis. However, how individual cells or multicellular assemblies sense and differentiate curvatures remains elusive. Here, we reveal a curvature sensing mechanism in which surface tension can selectively activate either actin or integrin flows, leading to bifurcating cell migration modes: focal adhesion formation that enables cell crawling at convex front edges and actin cable assembly that pulls cells forward at concave front edges. The molecular flows and curved front morphogenesis are sustained by coordinated cellular tension generation and transmission. We track the molecular flows and mechanical force transduction pathways by a phase-field model, which predicts that multicellular curvature sensing is more efficient than individual cells, suggesting collective intelligence of cells. The unique ability of cells in curvature sensing and migration mode bifurcating may offer insights into emergent collective patterns and functions of living active systems at different length scales. |
format | Online Article Text |
id | pubmed-10482382 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-104823822023-09-07 Physical forces guide curvature sensing and cell migration mode bifurcating Feng, Luyi Zhao, Tiankai Xu, Hongmei Shi, Xuechen Li, Changhao Hsia, K Jimmy Zhang, Sulin PNAS Nexus Physical Sciences and Engineering The ability of cells to sense and adapt to curvy topographical features has been implicated in organ morphogenesis, tissue repair, and tumor metastasis. However, how individual cells or multicellular assemblies sense and differentiate curvatures remains elusive. Here, we reveal a curvature sensing mechanism in which surface tension can selectively activate either actin or integrin flows, leading to bifurcating cell migration modes: focal adhesion formation that enables cell crawling at convex front edges and actin cable assembly that pulls cells forward at concave front edges. The molecular flows and curved front morphogenesis are sustained by coordinated cellular tension generation and transmission. We track the molecular flows and mechanical force transduction pathways by a phase-field model, which predicts that multicellular curvature sensing is more efficient than individual cells, suggesting collective intelligence of cells. The unique ability of cells in curvature sensing and migration mode bifurcating may offer insights into emergent collective patterns and functions of living active systems at different length scales. Oxford University Press 2023-08-01 /pmc/articles/PMC10482382/ /pubmed/37680491 http://dx.doi.org/10.1093/pnasnexus/pgad237 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of National Academy of Sciences. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Physical Sciences and Engineering Feng, Luyi Zhao, Tiankai Xu, Hongmei Shi, Xuechen Li, Changhao Hsia, K Jimmy Zhang, Sulin Physical forces guide curvature sensing and cell migration mode bifurcating |
title | Physical forces guide curvature sensing and cell migration mode bifurcating |
title_full | Physical forces guide curvature sensing and cell migration mode bifurcating |
title_fullStr | Physical forces guide curvature sensing and cell migration mode bifurcating |
title_full_unstemmed | Physical forces guide curvature sensing and cell migration mode bifurcating |
title_short | Physical forces guide curvature sensing and cell migration mode bifurcating |
title_sort | physical forces guide curvature sensing and cell migration mode bifurcating |
topic | Physical Sciences and Engineering |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10482382/ https://www.ncbi.nlm.nih.gov/pubmed/37680491 http://dx.doi.org/10.1093/pnasnexus/pgad237 |
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