Size-dependent response of cells in epithelial tissue modulated by contractile stress fibers.


Journal

Biophysical journal
ISSN: 1542-0086
Titre abrégé: Biophys J
Pays: United States
ID NLM: 0370626

Informations de publication

Date de publication:
04 04 2023
Historique:
received: 16 10 2022
revised: 07 01 2023
accepted: 18 02 2023
pmc-release: 04 04 2024
medline: 7 4 2023
pubmed: 23 2 2023
entrez: 22 2 2023
Statut: ppublish

Résumé

Although cells with distinct apical areas have been widely observed in epithelial tissues, how the size of cells affects their behavior during tissue deformation and morphogenesis as well as key physical factors modulating such influence remains elusive. Here, we showed that the elongation of cells within the monolayer under anisotropic biaxial stretching increases with their size because the strain released by local cell rearrangement (i.e., T1 transition) is more significant for small cells that possess higher contractility. On the other hand, by incorporating the nucleation, peeling, merging, and breakage dynamics of subcellular stress fibers into classical vertex formulation, we found that stress fibers with orientations predominantly aligned with the main stretching direction will be formed at tricellular junctions, in good agreement with recent experiments. The contractile forces generated by stress fibers help cells to resist imposed stretching, reduce the occurrence of T1 transitions, and, consequently, modulate their size-dependent elongation. Our findings demonstrate that epithelial cells could utilize their size and internal structure to regulate their physical and related biological behaviors. The theoretical framework proposed here can also be extended to investigate the roles of cell geometry and intracellular contraction in processes such as collective cell migration and embryo development.

Identifiants

pubmed: 36809876
pii: S0006-3495(23)00132-7
doi: 10.1016/j.bpj.2023.02.026
pmc: PMC10111366
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1315-1324

Informations de copyright

Copyright © 2023 Biophysical Society. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

Phys Rev E Stat Nonlin Soft Matter Phys. 2009 Feb;79(2 Pt 1):021916
pubmed: 19391787
Dev Cell. 2020 Jun 22;53(6):646-660.e8
pubmed: 32497487
Dev Cell. 2018 Oct 8;47(1):3-19
pubmed: 30300588
Sci Adv. 2021 Jun 30;7(27):
pubmed: 34193426
Nat Phys. 2019 Aug;15(8):839-847
pubmed: 33569083
Soft Matter. 2015 Dec 7;11(45):8782-8
pubmed: 26388023
Biophys J. 2022 Apr 5;121(7):1266-1275
pubmed: 35183521
Nature. 2015 Aug 20;524(7565):351-5
pubmed: 26214737
J Cell Biol. 2016 Apr 25;213(2):243-60
pubmed: 27114502
Biophys J. 2014 Oct 7;107(7):1532-41
pubmed: 25296305
Nat Mater. 2015 Mar;14(3):343-51
pubmed: 25664452
Sci Adv. 2017 Sep 06;3(9):e1700150
pubmed: 28913421
Mol Biol Cell. 2016 Nov 7;27(22):3459-3470
pubmed: 27605707
Biophys J. 2014 Jun 3;106(11):2291-304
pubmed: 24896108
PLoS Comput Biol. 2016 Apr 07;12(4):e1004863
pubmed: 27054883
Biophys J. 2011 Feb 2;100(3):535-543
pubmed: 21281567
Elife. 2017 Feb 15;6:
pubmed: 28181905
Curr Biol. 2021 Sep 27;31(18):R1098-R1110
pubmed: 34582821
Soft Matter. 2014 Mar 28;10(12):1885-90
pubmed: 24652538
Science. 2020 Oct 16;370(6514):
pubmed: 33060329
Biophys J. 2016 Jan 5;110(1):269-77
pubmed: 26745429
Phys Rev X. 2016 Apr-Jun;6(2):
pubmed: 28966874
Phys Rev Lett. 2019 Mar 1;122(8):088104
pubmed: 30932560
Proc Natl Acad Sci U S A. 2010 Dec 7;107(49):20863-8
pubmed: 21078958
Nat Phys. 2014 Sep;10(9):683-690
pubmed: 27340423
Phys Rev Lett. 2022 Jan 7;128(1):018101
pubmed: 35061486
Proc Natl Acad Sci U S A. 2017 Aug 1;114(31):8157-8162
pubmed: 28716911
Dev Cell. 2020 Sep 14;54(5):655-668.e6
pubmed: 32800097
Proc Natl Acad Sci U S A. 2010 Jul 13;107(28):12517-22
pubmed: 20616053
J Biomech Eng. 2017 Feb 1;139(2):
pubmed: 27814431
Phys Biol. 2011 Feb;8(1):015009
pubmed: 21301071
Phys Rev E. 2022 Feb;105(2-1):024404
pubmed: 35291100
Proc Natl Acad Sci U S A. 2012 Oct 9;109(41):16449-54
pubmed: 22991459
Proc Natl Acad Sci U S A. 2020 Dec 29;117(52):33263-33271
pubmed: 33318201
Biophys J. 2008 Mar 1;94(5):1836-53
pubmed: 17921219
Eur Phys J E Soft Matter. 2017 Jan;40(1):2
pubmed: 28083791
Dev Cell. 2021 Dec 6;56(23):3288-3302.e5
pubmed: 34822787
Science. 2020 Nov 27;370(6520):
pubmed: 33243859
Nature. 2019 Sep;573(7773):266-270
pubmed: 31462781
Nat Commun. 2018 Sep 10;9(1):3295
pubmed: 30202062
J Cell Biol. 2004 Dec 20;167(6):1011-7
pubmed: 15596547

Auteurs

Chao Fang (C)

School of Science, Harbin Institute of Technology, Shenzhen, Guangdong, China; Department of Mechanical Engineering, The University of Hong Kong, Pok Fu Lam, Hong Kong; HKU-Shenzhen Institute of Research and Innovation (HKU-SIRI), Shenzhen, Guangdong, China.

Xueying Shao (X)

Department of Mechanical Engineering, The University of Hong Kong, Pok Fu Lam, Hong Kong; HKU-Shenzhen Institute of Research and Innovation (HKU-SIRI), Shenzhen, Guangdong, China; Advanced Biomedical Instrumentation Centre, Hong Kong Science Park, Shatin, New Territories, Hong Kong.

Ye Tian (Y)

Department of Mechanical Engineering, The University of Hong Kong, Pok Fu Lam, Hong Kong; HKU-Shenzhen Institute of Research and Innovation (HKU-SIRI), Shenzhen, Guangdong, China.

Zhiqin Chu (Z)

Department of Electrical and Electronic Engineering, The University of Hong Kong, Pok Fu Lam, Hong Kong; School of Biological Sciences, The University of Hong Kong, Pok Fu Lam, Hong Kong.

Yuan Lin (Y)

Department of Mechanical Engineering, The University of Hong Kong, Pok Fu Lam, Hong Kong; HKU-Shenzhen Institute of Research and Innovation (HKU-SIRI), Shenzhen, Guangdong, China; Advanced Biomedical Instrumentation Centre, Hong Kong Science Park, Shatin, New Territories, Hong Kong. Electronic address: ylin@hku.hk.

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