A release-and-capture mechanism generates an essential non-centrosomal microtubule array during tube budding.
Actins
Actomyosin
/ metabolism
Animals
Cell Division
/ physiology
Centrosome
/ metabolism
Cytoskeletal Proteins
/ metabolism
Drosophila
Katanin
Male
Microfilament Proteins
/ metabolism
Microtubule-Associated Proteins
/ metabolism
Microtubules
/ metabolism
Morphogenesis
Salivary Glands
Tubulin
/ metabolism
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
02 07 2021
02 07 2021
Historique:
received:
01
05
2020
accepted:
27
05
2021
entrez:
3
7
2021
pubmed:
4
7
2021
medline:
23
7
2021
Statut:
epublish
Résumé
Non-centrosomal microtubule arrays serve crucial functions in cells, yet the mechanisms of their generation are poorly understood. During budding of the epithelial tubes of the salivary glands in the Drosophila embryo, we previously demonstrated that the activity of pulsatile apical-medial actomyosin depends on a longitudinal non-centrosomal microtubule array. Here we uncover that the exit from the last embryonic division cycle of the epidermal cells of the salivary gland placode leads to one centrosome in the cells losing all microtubule-nucleation capacity. This restriction of nucleation activity to the second, Centrobin-enriched, centrosome is key for proper morphogenesis. Furthermore, the microtubule-severing protein Katanin and the minus-end-binding protein Patronin accumulate in an apical-medial position only in placodal cells. Loss of either in the placode prevents formation of the longitudinal microtubule array and leads to loss of apical-medial actomyosin and impaired apical constriction. We thus propose a mechanism whereby Katanin-severing at the single active centrosome releases microtubule minus-ends that are then anchored by apical-medial Patronin to promote formation of the longitudinal microtubule array crucial for apical constriction and tube formation.
Identifiants
pubmed: 34215746
doi: 10.1038/s41467-021-24332-0
pii: 10.1038/s41467-021-24332-0
pmc: PMC8253823
doi:
Substances chimiques
Actins
0
Cytoskeletal Proteins
0
Microfilament Proteins
0
Microtubule-Associated Proteins
0
Tubulin
0
Actomyosin
9013-26-7
Katanin
EC 5.6.1.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4096Subventions
Organisme : Medical Research Council
ID : MC_UP_1201/11
Pays : United Kingdom
Organisme : Medical Research Council
ID : U105178780
Pays : United Kingdom
Références
PLoS Biol. 2004 Dec;2(12):e429
pubmed: 15562320
Dev Cell. 2010 May 18;18(5):790-801
pubmed: 20493812
Development. 2005 Aug;132(15):3515-24
pubmed: 16000381
J Cell Biol. 2019 Aug 5;218(8):2726-2742
pubmed: 31227595
PLoS Biol. 2008 Sep 16;6(9):e224
pubmed: 18798690
Nat Cell Biol. 2015 Sep;17(9):1089-93
pubmed: 26316453
J Cell Biol. 2009 Nov 2;187(3):355-63
pubmed: 19948479
Curr Biol. 2010 Dec 21;20(24):2178-86
pubmed: 21145741
Development. 2008 Jul;135(13):2227-38
pubmed: 18508861
J Cell Biol. 2003 Sep 29;162(7):1305-15
pubmed: 14517208
J Cell Biol. 2015 Jul 6;210(1):79-97
pubmed: 26150390
Cold Spring Harb Perspect Biol. 2015 Feb 02;7(2):a015800
pubmed: 25646378
Development. 2019 Sep 6;146(17):
pubmed: 31399470
Elife. 2014 Aug 22;3:e03399
pubmed: 25149451
Dev Cell. 2014 Feb 10;28(3):295-309
pubmed: 24486153
J Cell Sci. 2003 Apr 1;116(Pt 7):1157-73
pubmed: 12615960
Cell. 2010 Oct 15;143(2):263-74
pubmed: 20946984
Mol Biol Cell. 2021 May 1;32(10):1033-1047
pubmed: 33788621
Dev Cell. 2016 Jul 11;38(1):61-72
pubmed: 27404359
J Cell Biol. 1999 Apr 19;145(2):305-15
pubmed: 10209026
Nat Struct Mol Biol. 2011 Dec 11;19(1):117-21
pubmed: 22157958
Dev Cell. 2014 Jun 9;29(5):562-576
pubmed: 24914560
J Cell Sci. 1983 May;61:31-70
pubmed: 6411748
Nat Cell Biol. 2013 Mar;15(3):241-8
pubmed: 23354166
J Cell Sci. 1997 Oct;110 ( Pt 19):2391-401
pubmed: 9410878
Cell. 1989 Apr 7;57(1):177-87
pubmed: 2702688
Curr Biol. 2012 Apr 10;22(7):575-82
pubmed: 22425160
Mol Biol Cell. 2007 Oct;18(10):4037-49
pubmed: 17671162
Curr Biol. 2007 Oct 23;17(20):1759-64
pubmed: 17919907
Science. 2017 Sep 1;357(6354):925-928
pubmed: 28860385
Proc Natl Acad Sci U S A. 2016 Jan 12;113(2):332-7
pubmed: 26715742
Neuron. 2017 Dec 20;96(6):1264-1271.e5
pubmed: 29198755
Nat Cell Biol. 2009 Jul;11(7):859-64
pubmed: 19503074
Curr Biol. 2007 Sep 4;17(17):1498-503
pubmed: 17716897
Curr Biol. 2014 Jun 2;24(11):1276-82
pubmed: 24835456
Nat Commun. 2011;2:243
pubmed: 21407209
Development. 2017 Sep 1;144(17):3012-3021
pubmed: 28851722
Elife. 2018 Jul 17;7:
pubmed: 30015616
Nat Rev Mol Cell Biol. 2011 Oct 12;12(11):709-21
pubmed: 21993292
Dev Cell. 2018 Nov 19;47(4):453-463.e3
pubmed: 30458138
Elife. 2018 Mar 16;7:
pubmed: 29547120
Dev Cell. 2012 Nov 13;23(5):939-53
pubmed: 23153493
Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):15050-5
pubmed: 11742088
Nat Methods. 2009 Jun;6(6):458-64
pubmed: 19412170
Proc Natl Acad Sci U S A. 2014 Apr 22;111(16):5860-5
pubmed: 24706919
Exp Cell Res. 1997 Jul 10;234(1):183-90
pubmed: 9223385
Biol Cell. 1999 Nov;91(8):585-96
pubmed: 10629938
Genetics. 2009 Feb;181(2):543-65
pubmed: 19064711
J Cell Biol. 1982 Jun;93(3):576-82
pubmed: 6811596
Open Biol. 2012 Aug;2(8):120104
pubmed: 22977736
Nat Cell Biol. 2018 Jan;20(1):36-45
pubmed: 29203884
Nat Cell Biol. 2018 Oct;20(10):1126-1133
pubmed: 30202051
Cell Rep. 2018 Dec 26;25(13):3618-3630.e6
pubmed: 30590037
J Cell Sci. 2016 Jul 1;129(13):2651-9
pubmed: 27231092
Cell. 2006 Jun 30;125(7):1375-86
pubmed: 16814722
Cell. 2008 Nov 28;135(5):948-59
pubmed: 19041755
J Cell Sci. 2016 Nov 15;129(22):4278-4288
pubmed: 27802168
Dev Biol. 2001 Sep 1;237(1):54-67
pubmed: 11518505
Dev Cell. 2014 Mar 31;28(6):659-69
pubmed: 24656740
J Cell Biol. 2014 Mar 31;204(7):1111-21
pubmed: 24687279
Development. 1993 Jun;118(2):401-15
pubmed: 8223268
Cell. 1993 Nov 5;75(3):419-29
pubmed: 8221885
Dev Cell. 2019 Jul 22;50(2):197-211.e5
pubmed: 31204174
Curr Biol. 2015 Feb 16;25(4):R162-71
pubmed: 25689915
Dev Biol. 2000 Jan 15;217(2):362-74
pubmed: 10625560
J Cell Sci. 2017 May 15;130(10):1709-1715
pubmed: 28386021
Curr Opin Cell Biol. 2017 Feb;44:93-101
pubmed: 27666167
Curr Biol. 2017 Jul 10;27(13):1928-1940.e6
pubmed: 28669756
Curr Biol. 2019 Oct 21;29(20):3370-3385.e7
pubmed: 31522942
Development. 2010 Aug;137(16):2743-52
pubmed: 20663818
Genetics. 2007 Mar;175(3):1505-31
pubmed: 17194782