The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces.
Journal
Science advances
ISSN: 2375-2548
Titre abrégé: Sci Adv
Pays: United States
ID NLM: 101653440
Informations de publication
Date de publication:
16 Sep 2022
16 Sep 2022
Historique:
entrez:
14
9
2022
pubmed:
15
9
2022
medline:
15
9
2022
Statut:
ppublish
Résumé
Three-dimensional collective epithelial rotation around a given axis represents a coordinated cellular movement driving tissue morphogenesis and transformation. Questions regarding these behaviors and their relationship with substrate curvatures are intimately linked to spontaneous active matter processes and to vital morphogenetic and embryonic processes. Here, using interdisciplinary approaches, we study the dynamics of epithelial layers lining different cylindrical surfaces. We observe large-scale, persistent, and circumferential rotation in both concavely and convexly curved cylindrical tissues. While epithelia of inverse curvature show an orthogonal switch in actomyosin network orientation and opposite apicobasal polarities, their rotational movements emerge and vary similarly within a common curvature window. We further reveal that this persisting rotation requires stable cell-cell adhesion and Rac-1-dependent cell polarity. Using an active polar gel model, we unveil the different relationships of collective cell polarity and actin alignment with curvatures, which lead to coordinated rotational behavior despite the inverted curvature and cytoskeleton order.
Identifiants
pubmed: 36103541
doi: 10.1126/sciadv.abn5406
pmc: PMC9473582
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
eabn5406Références
Soft Matter. 2017 Feb 8;13(6):1235-1243
pubmed: 28098306
Nat Phys. 2021 Oct;17:1130-1136
pubmed: 35721781
Nat Commun. 2018 Sep 28;9(1):3995
pubmed: 30266986
Science. 2011 Feb 25;331(6020):1071-4
pubmed: 21212324
Nat Commun. 2021 Jul 5;12(1):4118
pubmed: 34226542
Curr Biol. 2005 Jan 26;15(2):R64-7
pubmed: 15668160
Nat Commun. 2019 Mar 12;10(1):1186
pubmed: 30862791
Proc Natl Acad Sci U S A. 2019 Apr 16;116(16):7867-7872
pubmed: 30923113
Sci Rep. 2020 Sep 8;10(1):14784
pubmed: 32901063
J Cell Biol. 1995 Jul;130(1):67-77
pubmed: 7790378
Proc Natl Acad Sci U S A. 2012 Feb 7;109(6):1973-8
pubmed: 22308439
Phys Rev E Stat Nonlin Soft Matter Phys. 2012 Jun;85(6 Pt 1):061701
pubmed: 23005108
Elife. 2023 Jan 17;12:
pubmed: 36649186
Dev Cell. 2006 May;10(5):673-80
pubmed: 16678780
Nat Commun. 2015 Jul 09;6:7683
pubmed: 26158873
Eur Phys J E Soft Matter. 2005 Jan;16(1):5-16
pubmed: 15688136
Dev Dyn. 2005 Mar;232(3):559-74
pubmed: 15704134
Soft Matter. 2020 Apr 29;16(16):4032-4042
pubmed: 32270809
Proc Natl Acad Sci U S A. 2007 Oct 9;104(41):15988-93
pubmed: 17905871
Phys Rev Lett. 2019 Apr 26;122(16):168002
pubmed: 31075037
Proc Natl Acad Sci U S A. 2012 Jan 31;109(5):1506-11
pubmed: 22307605
Nat Commun. 2014 Nov 21;5:5511
pubmed: 25413675
Nat Commun. 2015 Jun 25;6:7525
pubmed: 26109233
Science. 2020 Oct 16;370(6514):
pubmed: 33060329
Curr Opin Cell Biol. 2021 Oct;72:54-62
pubmed: 34134013
J Theor Biol. 2017 Dec 21;435:110-115
pubmed: 28923372
Proc Math Phys Eng Sci. 2020 Sep;476(2241):20200313
pubmed: 33071582
Nat Commun. 2020 Apr 21;11(1):1921
pubmed: 32317641
Adv Anat Embryol Cell Biol. 2016;219:69-93
pubmed: 27207363
Nat Rev Mol Cell Biol. 2016 Feb;17(2):97-109
pubmed: 26726037
Nat Rev Mol Cell Biol. 2017 Dec;18(12):743-757
pubmed: 29115298
J Cell Sci. 2005 Jan 1;118(Pt 1):51-63
pubmed: 15585576
Elife. 2021 Nov 23;10:
pubmed: 34812144
Nat Cell Biol. 2008 Dec;10(12):1401-10
pubmed: 18978783
Phys Rev Lett. 2012 May 18;108(20):207803
pubmed: 23003189
Phys Biol. 2009 Oct 20;6(4):046010
pubmed: 19843983
Acta Biomater. 2018 Sep 1;77:311-321
pubmed: 30006316
Soft Matter. 2015 Mar 28;11(12):2434-44
pubmed: 25662487
Nat Cell Biol. 2014 Jul;16(7):639-51
pubmed: 24929360
Proc Math Phys Eng Sci. 2018 Jun;474(2214):20170686
pubmed: 29977124
Biophys J. 2011 Jun 8;100(11):2566-75
pubmed: 21641301
EMBO Rep. 2012 Nov 6;13(11):984-91
pubmed: 23059978
Proc Natl Acad Sci U S A. 2015 May 12;112(19):5944-9
pubmed: 25922533
Cell Rep. 2018 Jun 19;23(12):3447-3456
pubmed: 29924989
Biophys J. 2010 May 19;98(9):1790-800
pubmed: 20441742
Soft Matter. 2015 Oct 7;11(37):7328-36
pubmed: 26265162
Nat Mater. 2021 Aug;20(8):1156-1166
pubmed: 33603188
Phys Rev Lett. 2022 Sep 9;129(11):118001
pubmed: 36154433
Phys Rev E Stat Nonlin Soft Matter Phys. 2014 Jul;90(1):012501
pubmed: 25122318
Nat Phys. 2019 Apr;15:393-402
pubmed: 30984281
Proc Natl Acad Sci U S A. 2012 Aug 7;109(32):12974-9
pubmed: 22814373
Proc Natl Acad Sci U S A. 2011 Mar 22;108(12):4714-9
pubmed: 21321233
Nat Cell Biol. 2010 Jun;12(6):533-42
pubmed: 20453849
Nat Commun. 2017 Nov 15;8(1):1517
pubmed: 29142242
Annu Rev Biomed Eng. 2004;6:275-302
pubmed: 15255771
Proc Natl Acad Sci U S A. 2013 Jan 2;110(1):163-8
pubmed: 23248267
Mol Biol Cell. 2007 May;18(5):1943-52
pubmed: 17344479
Methods Cell Biol. 2018;146:3-21
pubmed: 30037465
Sci Adv. 2022 Apr 15;8(15):eabk2712
pubmed: 35427161
Biophys J. 2008 Dec 15;95(12):6060-71
pubmed: 18820238
Elife. 2018 Nov 05;7:
pubmed: 30394875
Eur J Cell Biol. 2008 Apr;87(4):251-66
pubmed: 18191498
Science. 2008 Dec 5;322(5907):1502-5
pubmed: 19056976
Science. 2016 Sep 9;353(6304):1157-61
pubmed: 27609894
Nat Commun. 2015 Dec 10;6:10074
pubmed: 26656655
Curr Opin Cell Biol. 2008 Apr;20(2):227-34
pubmed: 18282696
Nat Mater. 2011 Jun;10(6):469-75
pubmed: 21602808
Proc Natl Acad Sci U S A. 2018 Nov 27;115(48):12188-12193
pubmed: 30429314
Nat Phys. 2020 Jul;16(7):802-809
pubmed: 32641972