Force-induced changes of α-catenin conformation stabilize vascular junctions independently of vinculin.


Journal

Journal of cell science
ISSN: 1477-9137
Titre abrégé: J Cell Sci
Pays: England
ID NLM: 0052457

Informations de publication

Date de publication:
15 12 2021
Historique:
received: 08 06 2021
accepted: 18 11 2021
pubmed: 2 12 2021
medline: 3 2 2022
entrez: 1 12 2021
Statut: ppublish

Résumé

Cadherin-mediated cell adhesion requires anchoring via the β-catenin-α-catenin complex to the actin cytoskeleton, yet, α-catenin only binds F-actin weakly. A covalent fusion of VE-cadherin to α-catenin enhances actin anchorage in endothelial cells and strongly stabilizes endothelial junctions in vivo, blocking inflammatory responses. Here, we have analyzed the underlying mechanism. We found that VE-cadherin-α-catenin constitutively recruits the actin adaptor vinculin. However, removal of the vinculin-binding region of α-catenin did not impair the ability of VE-cadherin-α-catenin to enhance junction integrity. Searching for an alternative explanation for the junction-stabilizing mechanism, we found that an antibody-defined epitope, normally buried in a short α1-helix of the actin-binding domain (ABD) of α-catenin, is openly displayed in junctional VE-cadherin-α-catenin chimera. We found that this epitope became exposed in normal α-catenin upon triggering thrombin-induced tension across the VE-cadherin complex. These results suggest that the VE-cadherin-α-catenin chimera stabilizes endothelial junctions due to conformational changes in the ABD of α-catenin that support constitutive strong binding to actin.

Identifiants

pubmed: 34851405
pii: 273834
doi: 10.1242/jcs.259012
pmc: PMC8729784
pii:
doi:

Substances chimiques

Actins 0
Cadherins 0
alpha Catenin 0
Vinculin 125361-02-6

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2021. Published by The Company of Biologists Ltd.

Déclaration de conflit d'intérêts

Competing interests The authors declare no competing or financial interests.

Références

Curr Biol. 2013 Feb 18;23(4):R159-61
pubmed: 23428328
Elife. 2020 Sep 24;9:
pubmed: 32969337
J Cell Biol. 1999 Mar 22;144(6):1311-22
pubmed: 10087272
Proc Natl Acad Sci U S A. 1990 Jun;87(11):4246-50
pubmed: 2349235
Science. 2014 Oct 31;346(6209):1254211
pubmed: 25359979
J Exp Med. 2015 Dec 14;212(13):2267-87
pubmed: 26642851
J Cell Biol. 2005 Aug 29;170(5):803-12
pubmed: 16129787
J Biol Chem. 2013 May 31;288(22):15913-25
pubmed: 23589308
Proc Natl Acad Sci U S A. 2008 Jan 8;105(1):13-9
pubmed: 18093941
Curr Biol. 2013 Feb 18;23(4):271-81
pubmed: 23375895
Nat Cell Biol. 2013 Mar;15(3):261-73
pubmed: 23417122
J Cell Biol. 2010 Jun 28;189(7):1107-15
pubmed: 20584916
EMBO J. 1989 Jun;8(6):1711-7
pubmed: 2788574
J Cell Sci. 2012 Jan 1;125(Pt 1):233-45
pubmed: 22266901
J Cell Biol. 1998 Aug 10;142(3):847-57
pubmed: 9700171
Nat Commun. 2014 Jul 31;5:4525
pubmed: 25077739
EMBO J. 2011 Aug 19;30(20):4157-70
pubmed: 21857650
Curr Protoc Cell Biol. 2010 Jun;Chapter 10:Unit 10.16
pubmed: 20521229
Mol Cell Biol. 2014 May;34(9):1634-48
pubmed: 24567373
Elife. 2020 Sep 11;9:
pubmed: 32915141
J Cell Biol. 2012 Mar 5;196(5):641-52
pubmed: 22391038
EMBO J. 2021 May 3;40(9):e106113
pubmed: 33604918
J Cell Sci. 1997 Apr;110 ( Pt 8):1013-22
pubmed: 9152027
Proc Natl Acad Sci U S A. 2012 May 29;109(22):8576-81
pubmed: 22586082
J Exp Med. 2011 Nov 21;208(12):2393-401
pubmed: 22025303
J Cell Biol. 2015 Sep 28;210(7):1065-74
pubmed: 26416960
J Cell Biol. 2008 Dec 15;183(6):989-97
pubmed: 19075109
J Biol Chem. 2002 May 24;277(21):18868-74
pubmed: 11907041
J Cell Biol. 1997 Jul 14;138(1):181-92
pubmed: 9214391
Nat Commun. 2018 Nov 30;9(1):5121
pubmed: 30504777
Cell. 2005 Dec 2;123(5):903-15
pubmed: 16325583
J Biol Chem. 2000 Sep 8;275(36):27979-88
pubmed: 10856295
J Cell Biol. 1994 Oct;127(1):235-45
pubmed: 7929566
Nat Cell Biol. 2010 Jun;12(6):533-42
pubmed: 20453849
Integr Biol (Camb). 2015 Oct;7(10):1109-19
pubmed: 25968913
Cell Regul. 1989 Nov;1(1):37-44
pubmed: 2519616
EMBO J. 1988 Dec 1;7(12):3679-84
pubmed: 3061804
Nat Cell Biol. 2004 Jan;6(1):21-30
pubmed: 14647292
J Biol Chem. 1998 Mar 13;273(11):6166-70
pubmed: 9497337
J Biol Chem. 2013 Feb 15;288(7):4957-69
pubmed: 23266828
Angiogenesis. 2005;8(3):217-27
pubmed: 16328161
Biol Open. 2012 Nov 15;1(11):1128-40
pubmed: 23213393

Auteurs

Cao Nguyen Duong (CN)

Department of Vascular Cell Biology, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Randy Brückner (R)

Department of Vascular Cell Biology, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Martina Schmitt (M)

Department of Vascular Cell Biology, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Astrid F Nottebaum (AF)

Department of Vascular Cell Biology, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Laura J Braun (LJ)

Department of Vascular Cell Biology, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Marika Meyer Zu Brickwedde (M)

Department of Vascular Cell Biology, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Ute Ipe (U)

Department of Vascular Cell Biology, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Hermann Vom Bruch (H)

Department of Cell and Developmental Biology, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Hans R Schöler (HR)

Department of Cell and Developmental Biology, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Giuseppe Trapani (G)

Bioactive Materials Laboratory, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Britta Trappmann (B)

Bioactive Materials Laboratory, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Mirsana P Ebrahimkutty (MP)

Institute of Medical Physics and Biophysics, University of Muenster, Muenster 48149, Germany.

Stephan Huveneers (S)

Amsterdam University Medical Center, Location AMC, University of Amsterdam, Amsterdam, The Netherlands.

Johan de Rooij (J)

Center for Molecular Medicine, University Medical Center Utrecht, 3584 CG Utrecht, The Netherlands.

Noboru Ishiyama (N)

Princess Margaret Cancer Centre, University Health Network, Toronto, ON M5G 1L7, Canada.

Mitsuhiko Ikura (M)

Princess Margaret Cancer Centre, University Health Network, Toronto, ON M5G 1L7, Canada.

Dietmar Vestweber (D)

Department of Vascular Cell Biology, Max Planck Institute for Molecular Biomedicine, D-48149 Münster, Germany.

Articles similaires

Cerebrospinal Fluid Animals Liver Glymphatic System Spinal Cord
Animals Humans Mice Neoplasms Tumor Microenvironment
Humans Animals Adherens Junctions Intercellular Junctions Tight Junctions
Exosomes Humans Endothelial Cells Animals Epithelial-Mesenchymal Transition

Classifications MeSH