Genetic induction and mechanochemical propagation of a morphogenetic wave.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
08 2019
Historique:
received: 28 09 2018
accepted: 10 07 2019
pubmed: 16 8 2019
medline: 27 3 2020
entrez: 16 8 2019
Statut: ppublish

Résumé

Tissue morphogenesis arises from coordinated changes in cell shape driven by actomyosin contractions. Patterns of gene expression regionalize cell behaviours by controlling actomyosin contractility. Here we report two modes of control over Rho1 and myosin II (MyoII) activation in the Drosophila endoderm. First, Rho1-MyoII are induced in a spatially restricted primordium via localized transcription of the G-protein-coupled receptor ligand Fog. Second, a tissue-scale wave of Rho1-MyoII activation and cell invagination progresses anteriorly away from the primordium. The wave does not require sustained gene transcription, and is not governed by regulated Fog delivery. Instead, MyoII inhibition blocks Rho1 activation and propagation, revealing a mechanical feedback driven by MyoII. We find that MyoII activation and invagination in each row of cells drives adhesion to the vitelline membrane mediated by integrins, apical spreading, MyoII activation and invagination in the next row. Endoderm morphogenesis thus emerges from local transcriptional initiation and a mechanically driven cycle of cell deformation.

Identifiants

pubmed: 31413363
doi: 10.1038/s41586-019-1492-9
pii: 10.1038/s41586-019-1492-9
pmc: PMC8985608
mid: NIHMS1620917
doi:

Substances chimiques

Drosophila Proteins 0
Integrins 0
Myosin Type II EC 3.6.1.-
Rho1 protein, Drosophila EC 3.6.5.2
rho GTP-Binding Proteins EC 3.6.5.2

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

467-473

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM098441
Pays : United States
Organisme : NIGMS NIH HHS
ID : 1R01 GM098441-06
Pays : United States

Commentaires et corrections

Type : CommentIn

Références

Nat Rev Mol Cell Biol. 2014 Dec;15(12):825-33
pubmed: 25355507
J Theor Biol. 1998 Mar 7;191(1):103-14
pubmed: 9593661
Cell. 2013 May 23;153(5):948-62
pubmed: 23706734
Sci Signal. 2013 Nov 12;6(301):ra98
pubmed: 24222713
Cell. 1994 Mar 25;76(6):1075-89
pubmed: 8137424
Mol Biol Cell. 2014 Nov 5;25(22):3486-93
pubmed: 25368427
Dev Cell. 2009 Nov;17(5):736-43
pubmed: 19879198
Mech Dev. 2007 Mar;124(3):167-79
pubmed: 17267182
Dev Genes Evol. 1998 Jul;208(5):290-4
pubmed: 9683745
Dev Biol. 1981 Jul 30;85(2):446-62
pubmed: 7196351
Proc Natl Acad Sci U S A. 2009 May 19;106(20):8284-9
pubmed: 19429710
Cell. 2009 Jun 26;137(7):1331-42
pubmed: 19563762
Nature. 2014 Apr 17;508(7496):392-6
pubmed: 24590071
PLoS Biol. 2015 Nov 06;13(11):e1002292
pubmed: 26544693
Nat Cell Biol. 2015 Oct;17(10):1247-58
pubmed: 26389664
Development. 2014 May;141(10):1987-98
pubmed: 24803648
Science. 1990 Apr 27;248(4954):495-8
pubmed: 2158673
Genes Dev. 1989 Dec;3(12B):2025-38
pubmed: 2560750
Science. 2012 Mar 9;335(6073):1232-5
pubmed: 22323741
Cell. 2010 Sep 3;142(5):773-86
pubmed: 20813263
Curr Opin Cell Biol. 2013 Feb;25(1):107-15
pubmed: 22985541
Dev Cell. 2002 Jun;2(6):785-96
pubmed: 12062090
Nat Commun. 2017 Jan 23;8:13883
pubmed: 28112149
Development. 1994 Nov;120(11):3131-43
pubmed: 7720557
Nat Rev Mol Cell Biol. 2007 Aug;8(8):633-44
pubmed: 17643125
J Cell Biol. 2018 Dec 3;217(12):4230-4252
pubmed: 30275107
Nature. 2010 Sep 30;467(7315):617-21
pubmed: 20852613
Nat Cell Biol. 2015 Jul;17(7):849-55
pubmed: 26075357
Nat Commun. 2017 May 15;8:15014
pubmed: 28504247
Nature. 2014 Nov 27;515(7528):523-7
pubmed: 25363762
Methods Mol Biol. 2008;420:207-18
pubmed: 18641949
Nat Commun. 2015 Oct 26;6:8677
pubmed: 26497898
EMBO J. 1999 Jun 15;18(12):3187-92
pubmed: 10369659
Nature. 2010 Dec 23;468(7327):1110-4
pubmed: 21068726
Nat Cell Biol. 2015 Nov;17(11):1471-83
pubmed: 26479320
Methods Mol Biol. 2008;420:219-38
pubmed: 18641950
Development. 2013 Oct;140(20):4246-55
pubmed: 24026125
Dev Cell. 2004 Sep;7(3):413-24
pubmed: 15363415
Nat Cell Biol. 2009 Jul;11(7):859-64
pubmed: 19503074
Nat Methods. 2009 Jun;6(6):431-4
pubmed: 19465919
Nature. 2009 Jan 22;457(7228):495-9
pubmed: 19029882
Nat Rev Mol Cell Biol. 2009 Jan;10(1):21-33
pubmed: 19197329
Nature. 2019 Apr;568(7752):395-399
pubmed: 30918398
Nat Cell Biol. 2016 Mar;18(3):261-70
pubmed: 26780298
Traffic. 2016 Aug;17(8):839-59
pubmed: 26929436
Development. 1997 Nov;124(22):4583-94
pubmed: 9409675
Curr Biol. 2015 Jan 19;25(2):141-151
pubmed: 25532891
J Cell Sci. 2011 Feb 15;124(Pt 4):635-46
pubmed: 21266466
Elife. 2017 Jan 28;6:
pubmed: 28117665
Nature. 2017 Jan 18;541(7637):311-320
pubmed: 28102269
Development. 2005 Sep;132(18):4165-78
pubmed: 16123312
Development. 1991 Jan;111(1):1-14
pubmed: 1901784
Nature. 2004 Jun 10;429(6992):667-71
pubmed: 15190355
Trends Cell Biol. 2013 Feb;23(2):47-53
pubmed: 23122885
Curr Biol. 2013 Nov 4;23(21):2140-5
pubmed: 24139738
Development. 1991 Jul;112(3):775-89
pubmed: 1935689
Dev Cell. 2015 Jan 26;32(2):241-55
pubmed: 25625209
Science. 2012 Oct 12;338(6104):257-60
pubmed: 23066079
Nature. 2015 Aug 20;524(7565):351-5
pubmed: 26214737
Curr Biol. 2016 Aug 22;26(16):2079-89
pubmed: 27451898
Development. 1998 Feb;125(4):589-97
pubmed: 9435280
Nat Cell Biol. 2013 Aug;15(8):926-36
pubmed: 23831726

Auteurs

Anaïs Bailles (A)

IBDM-UMR7288, Aix Marseille Université and CNRS, Marseille, France.
Turing Centre for Living Systems, Marseille, France.

Claudio Collinet (C)

IBDM-UMR7288, Aix Marseille Université and CNRS, Marseille, France. claudio.collinet@univ-amu.fr.
Turing Centre for Living Systems, Marseille, France. claudio.collinet@univ-amu.fr.

Jean-Marc Philippe (JM)

IBDM-UMR7288, Aix Marseille Université and CNRS, Marseille, France.
Turing Centre for Living Systems, Marseille, France.

Pierre-François Lenne (PF)

IBDM-UMR7288, Aix Marseille Université and CNRS, Marseille, France.
Turing Centre for Living Systems, Marseille, France.

Edwin Munro (E)

Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, IL, USA.

Thomas Lecuit (T)

IBDM-UMR7288, Aix Marseille Université and CNRS, Marseille, France. thomas.lecuit@univ-amu.fr.
Turing Centre for Living Systems, Marseille, France. thomas.lecuit@univ-amu.fr.
Collège de France, Paris, France. thomas.lecuit@univ-amu.fr.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH