Force propagation between epithelial cells depends on active coupling and mechano-structural polarization.

cell biology epithelium force propagation mechanobiology micropattern optogenetics physics of living systems polarity

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
07 08 2023
Historique:
received: 20 09 2022
accepted: 07 08 2023
medline: 21 9 2023
pubmed: 7 8 2023
entrez: 7 8 2023
Statut: epublish

Résumé

Cell-generated forces play a major role in coordinating the large-scale behavior of cell assemblies, in particular during development, wound healing, and cancer. Mechanical signals propagate faster than biochemical signals, but can have similar effects, especially in epithelial tissues with strong cell-cell adhesion. However, a quantitative description of the transmission chain from force generation in a sender cell, force propagation across cell-cell boundaries, and the concomitant response of receiver cells is missing. For a quantitative analysis of this important situation, here we propose a minimal model system of two epithelial cells on an H-pattern ('cell doublet'). After optogenetically activating RhoA, a major regulator of cell contractility, in the sender cell, we measure the mechanical response of the receiver cell by traction force and monolayer stress microscopies. In general, we find that the receiver cells show an active response so that the cell doublet forms a coherent unit. However, force propagation and response of the receiver cell also strongly depend on the mechano-structural polarization in the cell assembly, which is controlled by cell-matrix adhesion to the adhesive micropattern. We find that the response of the receiver cell is stronger when the mechano-structural polarization axis is oriented perpendicular to the direction of force propagation, reminiscent of the Poisson effect in passive materials. We finally show that the same effects are at work in small tissues. Our work demonstrates that cellular organization and active mechanical response of a tissue are key to maintain signal strength and lead to the emergence of elasticity, which means that signals are not dissipated like in a viscous system, but can propagate over large distances.

Identifiants

pubmed: 37548995
doi: 10.7554/eLife.83588
pii: 83588
pmc: PMC10511242
doi:
pii:

Banques de données

Dryad
['10.5061/dryad.sj3tx9683']

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023, Ruppel, Wörthmüller et al.

Déclaration de conflit d'intérêts

AR, DW, VM, MK, IW, PM, AM, JR, GC, GC, TB, US, MB No competing interests declared

Références

Eur Phys J E Soft Matter. 2005 Jan;16(1):5-16
pubmed: 15688136
Physiology (Bethesda). 2013 Nov;28(6):370-9
pubmed: 24186932
Phys Rev Lett. 2010 Sep 17;105(12):128101
pubmed: 20867675
PLoS Comput Biol. 2021 Jun 21;17(6):e1008364
pubmed: 34153027
Elife. 2014 Dec 05;3:e03282
pubmed: 25479385
Phys Rev Lett. 2011 Sep 16;107(12):128101
pubmed: 22026803
Proc Natl Acad Sci U S A. 2010 Mar 16;107(11):4872-7
pubmed: 20194780
Phys Rev Lett. 2019 Apr 26;122(16):168101
pubmed: 31075005
Nat Cell Biol. 2005 Oct;7(10):947-53
pubmed: 16179950
Soft Matter. 2018 Aug 21;14(31):6571-6581
pubmed: 30052252
Science. 2005 Nov 18;310(5751):1139-43
pubmed: 16293750
Phys Rev Lett. 2012 May 11;108(19):198101
pubmed: 23003091
Nat Commun. 2017 Feb 10;8:14396
pubmed: 28186127
Dev Cell. 2004 Apr;6(4):483-95
pubmed: 15068789
Dev Cell. 2015 Jun 8;33(5):611-21
pubmed: 25982674
Methods Cell Biol. 2014;120:93-116
pubmed: 24484659
Biophys J. 2008 Jan 1;94(1):207-20
pubmed: 17827246
Biophys J. 2022 May 3;121(9):1777-1786
pubmed: 35306023
Science. 1997 May 30;276(5317):1425-8
pubmed: 9162012
Proc Natl Acad Sci U S A. 2010 Jun 1;107(22):9944-9
pubmed: 20463286
Biol Cell. 2017 Mar;109(3):127-137
pubmed: 27990663
Dev Cell. 2008 Sep;15(3):470-477
pubmed: 18804441
Nat Rev Mol Cell Biol. 2010 Jun;11(6):414-26
pubmed: 20495582
Biophys J. 2014 Aug 19;107(4):825-33
pubmed: 25140417
Nat Cell Biol. 2018 Jan;20(1):8-20
pubmed: 29269951
Proc Natl Acad Sci U S A. 2012 Jan 31;109(5):1506-11
pubmed: 22307605
Phys Rev Lett. 2018 Oct 26;121(17):178101
pubmed: 30411958
Nat Commun. 2018 Aug 27;9(1):3469
pubmed: 30150695
Curr Protoc Cell Biol. 2010 Jun;Chapter 10:Unit 10.16
pubmed: 20521229
Lab Chip. 2011 Jul 7;11(13):2231-40
pubmed: 21523273
PLoS One. 2013;8(2):e55172
pubmed: 23468843
Phys Rev Lett. 2009 Jul 24;103(4):048101
pubmed: 19659402
Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):10334-9
pubmed: 22689955
Biophys J. 2019 Aug 6;117(3):464-478
pubmed: 31307676
Proc Natl Acad Sci U S A. 2017 Nov 28;114(48):12663-12668
pubmed: 29138312
Nat Cell Biol. 2021 May;23(5):511-525
pubmed: 33972733
Nat Methods. 2020 Mar;17(3):261-272
pubmed: 32015543
Dev Cell. 2020 Jun 22;53(6):646-660.e8
pubmed: 32497487
Nature. 2018 Feb 22;554(7693):523-527
pubmed: 29443958
Nat Commun. 2017 Jun 12;8:15817
pubmed: 28604737
Nat Rev Mol Cell Biol. 2009 Nov;10(11):778-90
pubmed: 19851336
Biophys J. 2023 Feb 21;122(4):684-696
pubmed: 36635962
Proc Natl Acad Sci U S A. 2006 Dec 26;103(52):19771-6
pubmed: 17179050
Biochim Biophys Acta. 2015 Nov;1853(11 Pt B):3095-104
pubmed: 26026889
Biophys J. 2015 Nov 3;109(9):1785-97
pubmed: 26536256
Nat Mater. 2014 Oct;13(10):979-87
pubmed: 25108614
Biophys J. 2008 Oct;95(7):3488-96
pubmed: 18599642
Cell. 2006 Aug 25;126(4):677-89
pubmed: 16923388
Proc Natl Acad Sci U S A. 2010 Dec 21;107(51):22111-6
pubmed: 21127270
Nat Commun. 2021 Jul 9;12(1):4229
pubmed: 34244477
Nat Mater. 2014 Jan;13(1):87-96
pubmed: 24292420
Nat Phys. 2019 Aug;15(8):839-847
pubmed: 33569083
Phys Rev Lett. 2012 Sep 7;109(10):108101
pubmed: 23005331
Science. 2018 Oct 19;362(6412):339-343
pubmed: 30337409
Biophys J. 2015 May 19;108(10):2437-2447
pubmed: 25992722
Proc Natl Acad Sci U S A. 2005 Aug 16;102(33):11594-9
pubmed: 16049098
Phys Rev E Stat Nonlin Soft Matter Phys. 2012 Jan;85(1 Pt 1):011913
pubmed: 22400597
Adv Exp Med Biol. 2019;1146:13-29
pubmed: 31612451
Biophys J. 2016 Mar 29;110(6):1421-9
pubmed: 27028651
PLoS Biol. 2019 Feb 21;17(2):e3000132
pubmed: 30789897
Curr Biol. 2020 May 4;30(9):R383-R387
pubmed: 32369745
Nat Commun. 2023 Feb 9;14(1):717
pubmed: 36759504
Annu Rev Biophys. 2022 May 9;51:327-353
pubmed: 35119944
Nature. 2021 Dec;600(7890):690-694
pubmed: 34880503
Development. 2021 Mar 12;148(18):
pubmed: 33712442
Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10140-5
pubmed: 10468576
Sci Adv. 2020 Sep 23;6(39):
pubmed: 32967835
J Cell Biol. 2017 Sep 4;216(9):2959-2977
pubmed: 28687667
Nature. 2000 May 4;405(6782):81-5
pubmed: 10811222
Science. 2016 Sep 9;353(6304):1157-61
pubmed: 27609894
J Biomech. 2006;39(14):2603-10
pubmed: 16216252
PLoS One. 2009;4(5):e5486
pubmed: 19424501
Nat Mater. 2011 Jun;10(6):469-75
pubmed: 21602808
Nat Commun. 2014 Dec 10;5:5749
pubmed: 25494455

Auteurs

Artur Ruppel (A)

Université Grenoble Alpes, CNRS, LIPhy, Grenoble, France.

Dennis Wörthmüller (D)

Institute for Theoretical Physics, Heidelberg University, Heidelberg, Germany.
BioQuant-Center for Quantitative Biology, Heidelberg University, Heidelberg, Germany.

Vladimir Misiak (V)

Université Grenoble Alpes, CNRS, LIPhy, Grenoble, France.

Manasi Kelkar (M)

London Centre for Nanotechnology, University College London, London, United Kingdom.

Irène Wang (I)

Université Grenoble Alpes, CNRS, LIPhy, Grenoble, France.

Philippe Moreau (P)

Université Grenoble Alpes, CNRS, LIPhy, Grenoble, France.

Adrien Méry (A)

Université Grenoble Alpes, CNRS, LIPhy, Grenoble, France.

Jean Révilloud (J)

Université Grenoble Alpes, CNRS, LIPhy, Grenoble, France.

Guillaume Charras (G)

London Centre for Nanotechnology, University College London, London, United Kingdom.
Department of Cell and Developmental Biology, University College London, London, United Kingdom.
Institute for the Physics of Living Systems, University College London, London, United Kingdom.

Giovanni Cappello (G)

Université Grenoble Alpes, CNRS, LIPhy, Grenoble, France.

Thomas Boudou (T)

Université Grenoble Alpes, CNRS, LIPhy, Grenoble, France.

Ulrich S Schwarz (US)

Institute for Theoretical Physics, Heidelberg University, Heidelberg, Germany.
BioQuant-Center for Quantitative Biology, Heidelberg University, Heidelberg, Germany.

Martial Balland (M)

Université Grenoble Alpes, CNRS, LIPhy, Grenoble, France.

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