A junctional PACSIN2/EHD4/MICAL-L1 complex coordinates VE-cadherin trafficking for endothelial migration and angiogenesis.
Adaptor Proteins, Signal Transducing
/ metabolism
Adherens Junctions
/ genetics
Animals
Antigens, CD
/ metabolism
Cadherins
/ metabolism
Catenins
/ metabolism
Cell Movement
/ genetics
DNA-Binding Proteins
/ metabolism
Human Umbilical Vein Endothelial Cells
/ metabolism
Humans
Mice
Mice, Inbred C57BL
Mice, Knockout
Microfilament Proteins
/ metabolism
Mixed Function Oxygenases
/ metabolism
Neovascularization, Pathologic
/ genetics
Nuclear Proteins
/ metabolism
Signal Transduction
/ genetics
Spheroids, Cellular
/ metabolism
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
10 05 2021
10 05 2021
Historique:
received:
11
03
2020
accepted:
31
03
2021
entrez:
11
5
2021
pubmed:
12
5
2021
medline:
3
6
2021
Statut:
epublish
Résumé
Angiogenic sprouting relies on collective migration and coordinated rearrangements of endothelial leader and follower cells. VE-cadherin-based adherens junctions have emerged as key cell-cell contacts that transmit forces between cells and trigger signals during collective cell migration in angiogenesis. However, the underlying molecular mechanisms that govern these processes and their functional importance for vascular development still remain unknown. We previously showed that the F-BAR protein PACSIN2 is recruited to tensile asymmetric adherens junctions between leader and follower cells. Here we report that PACSIN2 mediates the formation of endothelial sprouts during angiogenesis by coordinating collective migration. We show that PACSIN2 recruits the trafficking regulators EHD4 and MICAL-L1 to the rear end of asymmetric adherens junctions to form a recycling endosome-like tubular structure. The junctional PACSIN2/EHD4/MICAL-L1 complex controls local VE-cadherin trafficking and thereby coordinates polarized endothelial migration and angiogenesis. Our findings reveal a molecular event at force-dependent asymmetric adherens junctions that occurs during the tug-of-war between endothelial leader and follower cells, and allows for junction-based guidance during collective migration in angiogenesis.
Identifiants
pubmed: 33972531
doi: 10.1038/s41467-021-22873-y
pii: 10.1038/s41467-021-22873-y
pmc: PMC8110786
doi:
Substances chimiques
Adaptor Proteins, Signal Transducing
0
Antigens, CD
0
Cadherins
0
Catenins
0
DNA-Binding Proteins
0
EHD4 protein, human
0
Microfilament Proteins
0
Nuclear Proteins
0
PACSIN2 protein, human
0
cadherin 5
0
MICAL1 protein, human
EC 1.-
Mixed Function Oxygenases
EC 1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2610Références
Mol Biol Cell. 2009 Dec;20(24):5181-94
pubmed: 19864458
Curr Biol. 2015 Jan 19;25(2):218-224
pubmed: 25544608
Elife. 2019 Jun 27;8:
pubmed: 31246175
J Cell Sci. 2000 Dec;113 Pt 24:4511-21
pubmed: 11082044
Traffic. 2016 Dec;17(12):1262-1271
pubmed: 27624909
Proc Natl Acad Sci U S A. 2018 Jul 3;115(27):7093-7098
pubmed: 29891700
Proc Natl Acad Sci U S A. 2018 Jul 3;115(27):6885-6887
pubmed: 29925599
J Cell Biol. 2020 May 4;219(5):
pubmed: 32232465
Nat Cell Biol. 2010 Oct;12(10):943-53
pubmed: 20871601
Trends Cell Biol. 2018 Apr;28(4):328-341
pubmed: 29195724
J Cell Sci. 2004 Nov 15;117(Pt 24):5905-12
pubmed: 15522888
J Cell Sci. 2008 Jul 1;121(Pt 13):2115-22
pubmed: 18565824
Mol Biol Cell. 2017 Jan 1;28(1):30-40
pubmed: 27798235
Cold Spring Harb Perspect Biol. 2017 Nov 1;9(11):
pubmed: 28246177
Cold Spring Harb Perspect Biol. 2018 Aug 1;10(8):
pubmed: 28778874
Nat Cell Biol. 2002 Apr;4(4):E97-100
pubmed: 11944043
Cold Spring Harb Perspect Biol. 2018 Aug 1;10(8):
pubmed: 28851748
Cold Spring Harb Perspect Biol. 2017 Mar 1;9(3):
pubmed: 28096264
J Biol Chem. 2016 Jun 24;291(26):13465-78
pubmed: 27189942
Sci Rep. 2015 Nov 27;5:17225
pubmed: 26611125
Proc Natl Acad Sci U S A. 2010 Jun 1;107(22):9944-9
pubmed: 20463286
Tissue Barriers. 2013 Apr 1;1(2):e24180
pubmed: 24665386
Nat Commun. 2018 Nov 16;9(1):4826
pubmed: 30446640
Nat Rev Mol Cell Biol. 2014 Jun;15(6):397-410
pubmed: 24824068
Arterioscler Thromb Vasc Biol. 2008 Feb;28(2):223-32
pubmed: 18162609
Nat Methods. 2006 Sep;3(9):715-9
pubmed: 16929317
Cell Rep. 2014 Oct 23;9(2):504-13
pubmed: 25373898
Dev Cell. 2012 May 15;22(5):952-66
pubmed: 22595670
J Cell Biol. 2012 Mar 5;196(5):641-52
pubmed: 22391038
Trends Cell Biol. 2016 Jun;26(6):420-433
pubmed: 26920934
Nat Rev Mol Cell Biol. 2017 Dec;18(12):743-757
pubmed: 29115298
BMC Biol. 2010 Feb 02;8:11
pubmed: 20122254
Nat Cell Biol. 2014 Apr;16(4):309-21
pubmed: 24658686
Trends Cell Biol. 2011 Feb;21(2):122-31
pubmed: 21067929
Nat Cell Biol. 2014 Jul;16(7):639-51
pubmed: 24929360
Nat Commun. 2016 Jul 15;7:12210
pubmed: 27417273
Mol Biol Cell. 2018 Feb 15;29(4):380-388
pubmed: 29282282
Interface Focus. 2014 Apr 6;4(2):20130060
pubmed: 24748955
Development. 2011 Nov;138(21):4763-76
pubmed: 21965612
Commun Integr Biol. 2010 Mar;3(2):181-3
pubmed: 20585517
Biophys J. 2010 May 19;98(9):1790-800
pubmed: 20441742
J Cell Sci. 2018 Jul 6;131(13):
pubmed: 29980602
EMBO J. 2001 Sep 3;20(17):4973-86
pubmed: 11532961
Proc Natl Acad Sci U S A. 2012 Aug 7;109(32):12974-9
pubmed: 22814373
Nat Commun. 2018 Dec 5;9(1):5187
pubmed: 30518883
Neuron. 2010 Aug 26;67(4):588-602
pubmed: 20797536
Nat Cell Biol. 2015 May;17(5):533-9
pubmed: 25925582
J Cell Biol. 2012 Oct 29;199(3):545-63
pubmed: 23091067
Mol Biol Cell. 2005 Aug;16(8):3642-58
pubmed: 15930129
Biomaterials. 2017 Sep;140:45-57
pubmed: 28624707
J Cell Sci. 2015 Apr 1;128(7):1341-51
pubmed: 25663699
J Biol Chem. 2012 Mar 2;287(10):7556-72
pubmed: 22194609
Traffic. 2008 Jun;9(6):995-1018
pubmed: 18331452
J Cell Biol. 2018 May 7;217(5):1827-1845
pubmed: 29507127
Subcell Biochem. 2012;60:197-222
pubmed: 22674073
Dev Biol. 2008 Apr 15;316(2):312-22
pubmed: 18342303
Trends Cell Biol. 2009 Jan;19(1):8-15
pubmed: 19010680
Cold Spring Harb Perspect Biol. 2018 Oct 1;10(10):
pubmed: 28851747
Nat Commun. 2017 Nov 10;8(1):1402
pubmed: 29123087
PLoS Biol. 2015 Apr 17;13(4):e1002125
pubmed: 25884288
J Cell Biol. 2012 Oct 15;199(2):365-80
pubmed: 23071156
Cold Spring Harb Perspect Biol. 2017 Apr 3;9(4):
pubmed: 28096261
Cell Adh Migr. 2015;9(5):335-9
pubmed: 25482618
Cell Mol Life Sci. 2017 Jan;74(2):279-292
pubmed: 27506620
Mol Biol Cell. 2013 Jun;24(11):1776-90, S1-15
pubmed: 23596323
Nat Struct Biol. 2000 Nov;7(11):1018-22
pubmed: 11062555
Nat Rev Mol Cell Biol. 2018 Nov;19(11):679-696
pubmed: 30194414
Dev Cell. 2017 Mar 13;40(5):467-477.e5
pubmed: 28292425
Nature. 2005 Sep 15;437(7057):426-31
pubmed: 16163360
Nat Cell Biol. 2016 Dec;18(12):1311-1323
pubmed: 27842057
Mol Biol Cell. 2016 Dec 1;27(24):3828-3840
pubmed: 27708138
Pharmacol Res. 2018 Feb;128:200-210
pubmed: 29107716
Nat Commun. 2019 Jan 25;10(1):428
pubmed: 30683896
Appl Environ Microbiol. 2012 Aug;78(15):5440-3
pubmed: 22610439
Nat Commun. 2017 Dec 20;8(1):2210
pubmed: 29263363
FASEB J. 2015 Jul;29(7):3076-84
pubmed: 25857554
Mol Cell Biol. 2011 Jan;31(2):342-50
pubmed: 20974808
Traffic. 2009 Jul;10(7):811-8
pubmed: 19490534
Mol Biol Cell. 2009 Apr;20(7):1970-80
pubmed: 19211843
J R Soc Interface. 2014 Mar 19;11(95):20131072
pubmed: 24647903
Dev Cell. 2017 Nov 20;43(4):463-479.e5
pubmed: 29103954
Dev Cell. 2013 Jul 15;26(1):31-44
pubmed: 23792146