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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...

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Autores principales: Feng, Luyi, Zhao, Tiankai, Xu, Hongmei, Shi, Xuechen, Li, Changhao, Hsia, K Jimmy, Zhang, Sulin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
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.
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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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