Spatiotemporal oscillation in confined epithelial motion upon fluid-to-solid transition

Fluid-to-solid phase transition in multicellular assembly is crucial in many developmental biological processes, such as embryogenesis and morphogenesis. However, biomechanical studies in this area are limited, and little is known about factors governing the transition and how cell behaviors are reg...

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Main Authors: Yu, Jing, Cai, Pingqiang, Zhang, Xiaoqian, Zhao, Tiankai, Liang, Linlin, Zhang, Sulin, Liu, Hong, Chen, Xiaodong
Other Authors: School of Materials Science and Engineering
Format: Article
Language:English
Published: 2022
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Online Access:https://hdl.handle.net/10356/156386
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Institution: Nanyang Technological University
Language: English
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spelling sg-ntu-dr.10356-1563862023-07-14T16:05:40Z Spatiotemporal oscillation in confined epithelial motion upon fluid-to-solid transition Yu, Jing Cai, Pingqiang Zhang, Xiaoqian Zhao, Tiankai Liang, Linlin Zhang, Sulin Liu, Hong Chen, Xiaodong School of Materials Science and Engineering Innovative Centre for Flexible Devices Max Planck-NTU Joint Lab for Artificial Senses Engineering::Materials Collective Cell Migration Fluid-to-Solid Transition Fluid-to-solid phase transition in multicellular assembly is crucial in many developmental biological processes, such as embryogenesis and morphogenesis. However, biomechanical studies in this area are limited, and little is known about factors governing the transition and how cell behaviors are regulated. Due to different stresses present, cells could behave distinctively depending on the nature of tissue. Here we report a fluid-to-solid transition in geometrically confined multicellular assemblies. Under circular confinement, Madin-Darby canine kidney (MDCK) monolayers undergo spatiotemporally oscillatory motions that are strongly dependent on the confinement size and distance from the periphery of the monolayers. Nanomechanical mapping reveals that epithelial tensional stress and traction forces on the substrate are both dependent on confinement size. The oscillation pattern and cellular nanomechanics profile appear well correlated with stress fiber assembly and cell polarization. These experimental observations imply that the confinement size-dependent surface tension regulates actin fiber assembly, cellular force generation, and cell polarization. Our analyses further suggest a characteristic confinement size (approximates to MDCK's natural correlation length) below which surface tension is sufficiently high and triggers a fluid-to-solid transition of the monolayers. Our findings may shed light on the geometrical and nanomechanical control of tissue morphogenesis and growth. National Research Foundation (NRF) Submitted/Accepted version This work was financially supported by the NTU-Northwestern Institute for Nanomedicine and the National Research Foundation, Prime Minister’s Office, Singapore, under the NRF Investigatorship (NRF-NRFI2017-07). 2022-04-19T05:05:57Z 2022-04-19T05:05:57Z 2021 Journal Article Yu, J., Cai, P., Zhang, X., Zhao, T., Liang, L., Zhang, S., Liu, H. & Chen, X. (2021). Spatiotemporal oscillation in confined epithelial motion upon fluid-to-solid transition. ACS Nano, 15(4), 7618-7627. https://dx.doi.org/10.1021/acsnano.1c01165 1936-086X https://hdl.handle.net/10356/156386 10.1021/acsnano.1c01165 33844497 2-s2.0-85105040815 4 15 7618 7627 en NRF-NRFI2017-07 ACS Nano This document is the Accepted Manuscript version of a Published Work that appeared in final form in ACS Nano, copyright © American Chemical Society after peer review and technical editing by the publisher. To access the final edited and published work see https://doi.org/10.1021/acsnano.1c01165. 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::Materials
Collective Cell Migration
Fluid-to-Solid Transition
spellingShingle Engineering::Materials
Collective Cell Migration
Fluid-to-Solid Transition
Yu, Jing
Cai, Pingqiang
Zhang, Xiaoqian
Zhao, Tiankai
Liang, Linlin
Zhang, Sulin
Liu, Hong
Chen, Xiaodong
Spatiotemporal oscillation in confined epithelial motion upon fluid-to-solid transition
description Fluid-to-solid phase transition in multicellular assembly is crucial in many developmental biological processes, such as embryogenesis and morphogenesis. However, biomechanical studies in this area are limited, and little is known about factors governing the transition and how cell behaviors are regulated. Due to different stresses present, cells could behave distinctively depending on the nature of tissue. Here we report a fluid-to-solid transition in geometrically confined multicellular assemblies. Under circular confinement, Madin-Darby canine kidney (MDCK) monolayers undergo spatiotemporally oscillatory motions that are strongly dependent on the confinement size and distance from the periphery of the monolayers. Nanomechanical mapping reveals that epithelial tensional stress and traction forces on the substrate are both dependent on confinement size. The oscillation pattern and cellular nanomechanics profile appear well correlated with stress fiber assembly and cell polarization. These experimental observations imply that the confinement size-dependent surface tension regulates actin fiber assembly, cellular force generation, and cell polarization. Our analyses further suggest a characteristic confinement size (approximates to MDCK's natural correlation length) below which surface tension is sufficiently high and triggers a fluid-to-solid transition of the monolayers. Our findings may shed light on the geometrical and nanomechanical control of tissue morphogenesis and growth.
author2 School of Materials Science and Engineering
author_facet School of Materials Science and Engineering
Yu, Jing
Cai, Pingqiang
Zhang, Xiaoqian
Zhao, Tiankai
Liang, Linlin
Zhang, Sulin
Liu, Hong
Chen, Xiaodong
format Article
author Yu, Jing
Cai, Pingqiang
Zhang, Xiaoqian
Zhao, Tiankai
Liang, Linlin
Zhang, Sulin
Liu, Hong
Chen, Xiaodong
author_sort Yu, Jing
title Spatiotemporal oscillation in confined epithelial motion upon fluid-to-solid transition
title_short Spatiotemporal oscillation in confined epithelial motion upon fluid-to-solid transition
title_full Spatiotemporal oscillation in confined epithelial motion upon fluid-to-solid transition
title_fullStr Spatiotemporal oscillation in confined epithelial motion upon fluid-to-solid transition
title_full_unstemmed Spatiotemporal oscillation in confined epithelial motion upon fluid-to-solid transition
title_sort spatiotemporal oscillation in confined epithelial motion upon fluid-to-solid transition
publishDate 2022
url https://hdl.handle.net/10356/156386
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