How dynamic prestress governs the shape of living systems, from the subcellular to tissue scale.

actomyosin anelasticity contractility growth living tissues prestress

Journal

Interface focus
ISSN: 2042-8898
Titre abrégé: Interface Focus
Pays: England
ID NLM: 101531990

Informations de publication

Date de publication:
06 Dec 2022
Historique:
received: 15 06 2022
accepted: 08 09 2022
entrez: 4 11 2022
pubmed: 5 11 2022
medline: 5 11 2022
Statut: epublish

Résumé

Cells and tissues change shape both to carry out their function and during pathology. In most cases, these deformations are driven from within the systems themselves. This is permitted by a range of molecular actors, such as active crosslinkers and ion pumps, whose activity is biologically controlled in space and time. The resulting stresses are propagated within complex and dynamical architectures like networks or cell aggregates. From a mechanical point of view, these effects can be seen as the generation of prestress or prestrain, resulting from either a contractile or growth activity. In this review, we present this concept of prestress and the theoretical tools available to conceptualize the statics and dynamics of living systems. We then describe a range of phenomena where prestress controls shape changes in biopolymer networks (especially the actomyosin cytoskeleton and fibrous tissues) and cellularized tissues. Despite the diversity of scale and organization, we demonstrate that these phenomena stem from a limited number of spatial distributions of prestress, which can be categorized as heterogeneous, anisotropic or differential. We suggest that in addition to growth and contraction, a third type of prestress-topological prestress-can result from active processes altering the microstructure of tissue.

Identifiants

pubmed: 36330322
doi: 10.1098/rsfs.2022.0038
pii: rsfs20220038
pmc: PMC9560792
doi:

Types de publication

Journal Article Review

Langues

eng

Pagination

20220038

Informations de copyright

© 2022 The Author(s).

Références

PLoS Comput Biol. 2022 Jan 28;18(1):e1009812
pubmed: 35089922
Nat Commun. 2014 Nov 11;5:5343
pubmed: 25385672
EMBO J. 2013 Oct 30;32(21):2790-803
pubmed: 24022370
Dev Cell. 2018 Dec 17;47(6):727-740.e6
pubmed: 30503752
J Biomech. 1991;24(5):307-15
pubmed: 2050707
PLoS Biol. 2015 Nov 06;13(11):e1002292
pubmed: 26544693
Phys Rev E. 2019 May;99(5-1):053001
pubmed: 31212512
Science. 2005 Nov 18;310(5751):1139-43
pubmed: 16293750
Biomech Model Mechanobiol. 2016 Dec;15(6):1405-1421
pubmed: 26984743
PLoS One. 2014 Feb 04;9(2):e86725
pubmed: 24504016
Nature. 2018 Sep;561(7723):401-405
pubmed: 30185907
Science. 2007 Jan 19;315(5810):370-3
pubmed: 17234946
Nat Cell Biol. 2015 Oct;17(10):1247-58
pubmed: 26389664
J R Soc Interface. 2012 Oct 7;9(75):2614-23
pubmed: 22628216
Dev Cell. 2019 Nov 4;51(3):299-312.e4
pubmed: 31607650
Science. 1980 Apr 11;208(4440):177-9
pubmed: 6987736
Trends Cell Biol. 2022 Jun;32(6):537-551
pubmed: 35190218
Nat Commun. 2022 Jun 10;13(1):3348
pubmed: 35688832
J Math Biol. 2004 May;48(5):477-99
pubmed: 15133619
Physiol Rev. 2014 Jan;94(1):235-63
pubmed: 24382887
Elife. 2015 Jun 23;4:e07090
pubmed: 26102528
Proc Natl Acad Sci U S A. 2012 Sep 18;109(38):15101-8
pubmed: 22932871
Nat Mater. 2013 Mar;12(3):253-61
pubmed: 23291707
Nat Cell Biol. 2021 Jul;23(7):745-757
pubmed: 34155382
Nat Commun. 2015 Jan 22;6:5942
pubmed: 25608644
J Cell Sci. 2011 Dec 15;124(Pt 24):4233-40
pubmed: 22193960
J Cell Biol. 2012 Mar 19;196(6):757-74
pubmed: 22412019
Mol Biol Cell. 2013 Mar;24(6):757-67
pubmed: 23345594
Nat Cell Biol. 2013 Dec;15(12):1405-14
pubmed: 24212092
Phys Rev Lett. 2020 Aug 21;125(8):088102
pubmed: 32909763
PLoS Comput Biol. 2019 Oct 28;15(10):e1007251
pubmed: 31658254
Dev Cell. 2019 Dec 2;51(5):564-574.e6
pubmed: 31735668
Philos Trans R Soc Lond B Biol Sci. 2017 May 19;372(1720):
pubmed: 28348256
Nat Mater. 2020 Jan;19(1):109-117
pubmed: 31451778
J Cell Sci. 2019 Dec 13;132(24):
pubmed: 31836688
Nature. 2014 Oct 23;514(7523):498-502
pubmed: 25341788
J Cell Biol. 2018 Dec 3;217(12):4230-4252
pubmed: 30275107
Development. 2017 May 15;144(10):1876-1886
pubmed: 28432215
Nat Phys. 2016 Aug;12(8):762-766
pubmed: 27642362
Curr Biol. 2014 Jul 7;24(13):1492-9
pubmed: 24930964
Nat Cell Biol. 2018 Jan;20(1):8-20
pubmed: 29269951
Proc Natl Acad Sci U S A. 2015 May 5;112(18):5726-31
pubmed: 25908119
Nat Commun. 2017 May 15;8:15014
pubmed: 28504247
Cell. 2017 Sep 21;171(1):188-200.e16
pubmed: 28867286
Nat Commun. 2019 Jul 4;10(1):2951
pubmed: 31273212
Phys Rev E. 2020 Jul;102(1-1):012401
pubmed: 32795061
J Mech Phys Solids. 2021 Jan;146:
pubmed: 34054143
Curr Opin Cell Biol. 2018 Feb;50:79-85
pubmed: 29482169
Curr Biol. 2017 Oct 23;27(20):3132-3142.e4
pubmed: 28988857
J Cell Biol. 2014 Apr 14;205(1):83-96
pubmed: 24711500
Rep Prog Phys. 2018 Mar;81(3):036602
pubmed: 28649969
Nature. 2004 Aug 5;430(7000):689-93
pubmed: 15254551
Science. 2017 Aug 25;357(6353):811-815
pubmed: 28705989
Exp Cell Res. 2016 Apr 10;343(1):14-20
pubmed: 26519907
Circ Res. 1990 Jan;66(1):37-45
pubmed: 2295143
Proc Math Phys Eng Sci. 2020 May;476(2237):20190716
pubmed: 32518502
Nature. 2005 Jan 27;433(7024):421-5
pubmed: 15674293
J Cell Sci. 2012 Apr 1;125(Pt 7):1666-72
pubmed: 22328507
Phys Rev E. 2018 May;97(5-1):052409
pubmed: 29906905
Dev Cell. 2017 Nov 20;43(4):480-492.e6
pubmed: 29107560
Mol Syst Biol. 2017 Sep 27;13(9):941
pubmed: 28954810
Cell. 2021 Dec 22;184(26):6313-6325.e18
pubmed: 34942099
Cell. 2016 Jan 14;164(1-2):115-127
pubmed: 26771487
Proc Natl Acad Sci U S A. 2009 Oct 27;106(43):18243-8
pubmed: 19805036
Prog Biophys Biophys Chem. 1957;7:255-318
pubmed: 13485191
Cell Adh Migr. 2011 Jan-Feb;5(1):16-9
pubmed: 20818154
Nature. 1998 May 14;393(6681):178-81
pubmed: 9603522
Nat Commun. 2017 Oct 17;8(1):1002
pubmed: 29042539
J Cell Sci. 2014 Jun 1;127(Pt 11):2507-17
pubmed: 24659804
Nat Cell Biol. 2017 Jun;19(6):689-697
pubmed: 28530659
J Biomech. 2011 Apr 29;44(7):1285-90
pubmed: 21396648
Phys Rev E Stat Nonlin Soft Matter Phys. 2009 Jan;79(1 Pt 1):011917
pubmed: 19257079
Trends Cell Biol. 1999 May;9(5):187-92
pubmed: 10322453
J Cell Biol. 1986 Mar;102(3):1074-84
pubmed: 3949874
Phys Rev E. 2018 Jan;97(1-1):012410
pubmed: 29448458
Biophys J. 2016 Oct 4;111(7):1519-1527
pubmed: 27705774
Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1484-9
pubmed: 12552122
Cell. 1996 Feb 9;84(3):371-9
pubmed: 8608590
Phys Biol. 2006 Jun 21;3(2):130-7
pubmed: 16829699
Biophys J. 2015 Jul 7;109(1):154-63
pubmed: 26153712
Nat Mater. 2011 Jan;10(1):61-6
pubmed: 21131961
Elife. 2017 Apr 04;6:
pubmed: 28372636
J Elast. 2017 Dec;129(1-2):107-124
pubmed: 28894347
Philos Trans A Math Phys Eng Sci. 2009 Sep 13;367(1902):3555-83
pubmed: 19657011
Nat Cell Biol. 2009 Jul;11(7):859-64
pubmed: 19503074
Nat Cell Biol. 2013 Jun;15(6):637-46
pubmed: 23708000
Curr Biol. 2007 Dec 18;17(24):2095-104
pubmed: 18082406
Sci Rep. 2014 Jul 10;4:5644
pubmed: 25008163
Bull Math Biol. 2019 Aug;81(8):3219-3244
pubmed: 30242633
Nature. 2009 Jan 22;457(7228):495-9
pubmed: 19029882
HFSP J. 2009 Aug;3(4):265-72
pubmed: 20119483
Proc Natl Acad Sci U S A. 2013 Sep 10;110(37):14843-8
pubmed: 23980147
Science. 2013 Oct 11;342(6155):212-8
pubmed: 23989955
Cancer Cell. 2012 Mar 20;21(3):418-29
pubmed: 22439937
Nat Cell Biol. 2016 Nov;18(11):1161-1172
pubmed: 27749821
Proc Natl Acad Sci U S A. 2010 Dec 21;107(51):22111-6
pubmed: 21127270
Phys Rev E Stat Nonlin Soft Matter Phys. 2013 Feb;87(2):022720
pubmed: 23496561
Am J Physiol Cell Physiol. 2002 Mar;282(3):C617-24
pubmed: 11832347
J Invest Dermatol. 1991 Nov;97(5):898-902
pubmed: 1919053
Nat Phys. 2019 Aug;15(8):839-847
pubmed: 33569083
Biochim Biophys Acta. 1958 Feb;27(2):229-46
pubmed: 13522722
Cold Spring Harb Perspect Biol. 2016 Aug 01;8(8):
pubmed: 26988969
Biophys J. 2006 May 15;90(10):3762-73
pubmed: 16500961
Curr Opin Genet Dev. 2018 Aug;51:78-87
pubmed: 30077073
Nat Methods. 2009 Jun;6(6):458-64
pubmed: 19412170
Cell. 2014 Oct 9;159(2):415-27
pubmed: 25303534
Nature. 2018 Nov;563(7730):203-208
pubmed: 30401836
Nat Rev Cancer. 2020 Mar;20(3):174-186
pubmed: 31980749
PLoS One. 2009;4(2):e4632
pubmed: 19247489
Proc Natl Acad Sci U S A. 2015 Mar 3;112(9):2740-5
pubmed: 25730854
Nature. 2016 Feb 25;530(7591):495-8
pubmed: 26886796
Biophys J. 2015 May 19;108(10):2437-2447
pubmed: 25992722
Philos Trans R Soc Lond B Biol Sci. 2017 May 19;372(1720):
pubmed: 28348254
Proc Natl Acad Sci U S A. 2016 Mar 15;113(11):2827-32
pubmed: 26921325
Soft Matter. 2007 Feb 14;3(3):299-306
pubmed: 32900146
Elife. 2017 Jan 28;6:
pubmed: 28117665
Proc Math Phys Eng Sci. 2020 Jan;476(2233):20190523
pubmed: 32082058
Curr Opin Cell Biol. 2016 Oct;42:113-120
pubmed: 27371889
Biophys J. 2008 Mar 1;94(5):1836-53
pubmed: 17921219
Phys Rev Lett. 2013 Sep 6;111(10):108102
pubmed: 25166712
Development. 2007 Sep;134(17):3049-54
pubmed: 17652351
Biophys J. 2016 Mar 29;110(6):1421-9
pubmed: 27028651
Phys Rev Lett. 2018 Dec 28;121(26):268102
pubmed: 30636158
Trends Cell Biol. 2012 Oct;22(10):536-45
pubmed: 22871642
Nature. 2004 Jun 10;429(6992):667-71
pubmed: 15190355
J Biomech. 1994 Apr;27(4):455-67
pubmed: 8188726
Nature. 2011 Aug 03;476(7358):57-62
pubmed: 21814276
J Biomech Eng. 1991 Feb;113(1):36-41
pubmed: 2020174
Nat Commun. 2018 Jul 27;9(1):2960
pubmed: 30054479
J R Soc Interface. 2013 Sep 25;10(89):20130726
pubmed: 24068179
Nat Cell Biol. 2021 Jul;23(7):733-744
pubmed: 34155381
J Cell Sci. 2012 Apr 15;125(Pt 8):1855-64
pubmed: 22544950
Ann Biomed Eng. 1991;19(3):237-49
pubmed: 1928868
Philos Trans R Soc Lond B Biol Sci. 2017 May 19;372(1720):
pubmed: 28348250
Biomech Model Mechanobiol. 2016 Jun;15(3):663-81
pubmed: 26264498
Elife. 2016 May 16;5:
pubmed: 27183005
Int J Dev Biol. 2006;50(2-3):81-92
pubmed: 16479477
Dev Cell. 2016 May 9;37(3):213-25
pubmed: 27165554
Proc Natl Acad Sci U S A. 2009 Nov 3;106(44):18581-6
pubmed: 19846787
Biophys J. 2012 Feb 8;102(3):443-51
pubmed: 22325266
Curr Opin Cell Biol. 2021 Oct;72:146-155
pubmed: 34461581
J Cell Sci. 1993 Mar;104 ( Pt 3):613-27
pubmed: 8314865
Phys Rev E. 2022 Sep;106(3-1):034403
pubmed: 36266852
Nat Cell Biol. 2011 Jun 12;13(7):771-8
pubmed: 21666685
Dev Cell. 2009 Nov;17(5):736-43
pubmed: 19879198
Proc Natl Acad Sci U S A. 2010 Sep 21;107(38):16518-23
pubmed: 20823257
J Math Biol. 1997 Sep;35(8):869-907
pubmed: 9314193
Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13661-5
pubmed: 9391082
J Embryol Exp Morphol. 1984 Apr;80:1-20
pubmed: 6747520
Rep Prog Phys. 2014 Apr;77(4):046603
pubmed: 24695087
Nat Methods. 2016 Apr 28;13(5):415-23
pubmed: 27123817
J Mech Behav Biomed Mater. 2015 Dec;52:14-21
pubmed: 25862347
PLoS Comput Biol. 2019 Jun 20;15(6):e1007121
pubmed: 31220080
Nat Mater. 2021 Mar;20(3):410-420
pubmed: 33077951
Biophys J. 2018 Feb 6;114(3):675-687
pubmed: 29414713
Biophys J. 1999 Apr;76(4):2307-16
pubmed: 10096925
Phys Rev Lett. 2016 Sep 16;117(12):124101
pubmed: 27689279
Proc Natl Acad Sci U S A. 2012 Jul 31;109(31):12568-73
pubmed: 22802638
PLoS One. 2010 Apr 06;5(4):e10046
pubmed: 20386607
J Biomech. 1987;20(3):235-9
pubmed: 3584149
EMBO J. 2018 Dec 3;37(23):
pubmed: 30442834
Philos Trans R Soc Lond B Biol Sci. 2020 Oct 12;375(1809):20190564
pubmed: 32829686
Dev Cell. 2004 Mar;6(3):343-55
pubmed: 15030758
Proc Natl Acad Sci U S A. 2018 Apr 17;115(16):4075-4080
pubmed: 29618614
Nature. 1992 May 21;357(6375):257-60
pubmed: 1589024
Proc Natl Acad Sci U S A. 2009 Jun 23;106(25):10097-102
pubmed: 19541627
Phys Rev Lett. 2008 Feb 15;100(6):068101
pubmed: 18352520
Phys Rev Lett. 2011 Oct 28;107(18):188102
pubmed: 22107677
Proc Natl Acad Sci U S A. 2020 Apr 28;117(17):9377-9383
pubmed: 32284424
Nat Commun. 2023 Mar 3;14(1):1220
pubmed: 36869053
Biomech Model Mechanobiol. 2021 Apr;20(2):585-608
pubmed: 33219879
Sci Adv. 2021 Jul 2;7(27):
pubmed: 34215576
Sci Rep. 2017 Nov 16;7(1):15688
pubmed: 29146997
Nat Commun. 2014 Dec 10;5:5749
pubmed: 25494455
Nat Commun. 2018 Jun 18;9(1):2366
pubmed: 29915285
Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):5992-7
pubmed: 15079054

Auteurs

Alexander Erlich (A)

Université Grenoble Alpes, CNRS, LIPHY, 38000 Grenoble, France.

Jocelyn Étienne (J)

Université Grenoble Alpes, CNRS, LIPHY, 38000 Grenoble, France.

Jonathan Fouchard (J)

Laboratoire de Biologie du Développement, Institut de Biologie Paris Seine (IBPS), Sorbonne Université, CNRS (UMR 7622), INSERM (URL 1156), 7 quai Saint Bernard, 75005 Paris, France.

Tom Wyatt (T)

Wellcome Trust-Medical Research Council Cambridge Stem Cell Institute, University of Cambridge, Cambridge, UK.

Classifications MeSH