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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Main Authors: Feng, Luyi, Zhao, Tiankai, Xu, Hongmei, Shi, Xuechen, Li, Changhao, Hsia, K. Jimmy, Zhang, Sulin
Other Authors: School of Chemistry, Chemical Engineering and Biotechnology
Format: Article
Language:English
Published: 2024
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Online Access:https://hdl.handle.net/10356/173169
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Institution: Nanyang Technological University
Language: English
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spelling sg-ntu-dr.10356-1731692024-01-19T15:31:51Z 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 School of Chemistry, Chemical Engineering and Biotechnology School of Mechanical and Aerospace Engineering Engineering::Bioengineering Engineering::Mechanical engineering Surface Tension Molecular Flow 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. Nanyang Technological University Published version S.Z. would like to acknowledge the support from the National Institutes of Health (NIH-NHLBIR21 HL122902 and NIHNIDIS R01NS123433). K.J.H. and H.X. would like to acknowledge the financial support from Nanyang Technological University (Grant M4082428.050). H.X. would like to acknowledge the Research Scholarship awarded by NTU. 2024-01-16T02:38:25Z 2024-01-16T02:38:25Z 2023 Journal Article Feng, L., Zhao, T., Xu, H., Shi, X., Li, C., Hsia, K. J. & Zhang, S. (2023). Physical forces guide curvature sensing and cell migration mode bifurcating. PNAS Nexus, 2(8), 1-9. https://dx.doi.org/10.1093/pnasnexus/pgad237 2752-6542 https://hdl.handle.net/10356/173169 10.1093/pnasnexus/pgad237 37680491 2-s2.0-85179402119 8 2 1 9 en M4082428.050 PNAS Nexus © The Author(s) 2023. Published by Oxford University Press on behalf of National Academy of Sciences. 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. application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Engineering::Bioengineering
Engineering::Mechanical engineering
Surface Tension
Molecular Flow
spellingShingle Engineering::Bioengineering
Engineering::Mechanical engineering
Surface Tension
Molecular Flow
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
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.
author2 School of Chemistry, Chemical Engineering and Biotechnology
author_facet School of Chemistry, Chemical Engineering and Biotechnology
Feng, Luyi
Zhao, Tiankai
Xu, Hongmei
Shi, Xuechen
Li, Changhao
Hsia, K. Jimmy
Zhang, Sulin
format Article
author Feng, Luyi
Zhao, Tiankai
Xu, Hongmei
Shi, Xuechen
Li, Changhao
Hsia, K. Jimmy
Zhang, Sulin
author_sort Feng, Luyi
title Physical forces guide curvature sensing and cell migration mode bifurcating
title_short 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_sort physical forces guide curvature sensing and cell migration mode bifurcating
publishDate 2024
url https://hdl.handle.net/10356/173169
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