Interplay between Extracellular Matrix Stiffness and JAM-A Regulates Mechanical Load on ZO-1 and Tight Junction Assembly.

Actomyosin / metabolism Animals Dogs Extracellular Matrix / metabolism Madin Darby Canine Kidney Cells Receptors, Cell Surface / metabolism Rho Guanine Nucleotide Exchange Factors / metabolism Signal Transduction Tensile Strength Tight Junctions / metabolism Zonula Occludens-1 Protein / metabolism
ECM FRET tension-sensor JAM-A ZO-1 actomyosin hydrogel mechanotransduction p114RhoGEF stiffness tight junction

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
21 07 2020
Historique:
received: 20 11 2019
revised: 08 05 2020
accepted: 26 06 2020
entrez: 23 7 2020
pubmed: 23 7 2020
medline: 29 4 2021
Statut: ppublish

Résumé

Tight-junction-regulated actomyosin activity determines epithelial and endothelial tension on adherens junctions and drives morphogenetic processes; however, whether or not tight junctions themselves are under tensile stress is not clear. Here, we use a tension sensor based on ZO-1, a scaffolding protein that links the junctional membrane to the cytoskeleton, to determine if tight junctions carry a mechanical load. Our data indicate that ZO-1 is under mechanical tension and that forces acting on ZO-1 are regulated by extracellular matrix (ECM) stiffness and the junctional adhesion molecule JAM-A. JAM-A depletion stimulates junctional recruitment of p114RhoGEF/ARHGEF18, mechanical tension on ZO-1, and traction forces at focal adhesions. p114RhoGEF is required for activation of junctional actomyosin activity and tight junction integrity on stiff but not soft ECM. Thus, junctional ZO-1 bears a mechanical load, and junction assembly is regulated by interplay between the physical properties of the ECM and adhesion-regulated signaling at tight junctions.

Identifiants

DOI: 10.1016/j.celrep.2020.107924 PMID: 32697990 PMC: PMC7383227
pubmed: 32697990
pii: S2211-1247(20)30905-0
doi: 10.1016/j.celrep.2020.107924
pmc: PMC7383227
pii:
doi:

Substances chimiques

Receptors, Cell Surface 0
Rho Guanine Nucleotide Exchange Factors 0
Zonula Occludens-1 Protein 0
Actomyosin 9013-26-7

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

107924

Subventions

Organisme : Medical Research Council
ID : G0400678
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0900098
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/N014855/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/N001133/1
Pays : United Kingdom

Informations de copyright

Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interests The authors declare no competing interests.

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Auteurs

Alexis J Haas (AJ)

UCL Institute of Ophthalmology, University College London, London EC1V 9EL, UK.

Ceniz Zihni (C)

UCL Institute of Ophthalmology, University College London, London EC1V 9EL, UK.

Artur Ruppel (A)

LiPhy, CNRS, Université Grenoble Alpes, Grenoble 38000, France.

Christian Hartmann (C)

Institute-associated Research Group "Cell adhesion and cell polarity," Institute of Medical Biochemistry, ZMBE, University of Münster, Münster 48149, Germany.

Klaus Ebnet (K)

Institute-associated Research Group "Cell adhesion and cell polarity," Institute of Medical Biochemistry, ZMBE, University of Münster, Münster 48149, Germany.

Masazumi Tada (M)

Department of Cell and Developmental Biology, University College London, London WC1E 6BT, UK.

Maria S Balda (MS)

UCL Institute of Ophthalmology, University College London, London EC1V 9EL, UK. Electronic address: m.balda@ucl.ac.uk.

Karl Matter (K)

UCL Institute of Ophthalmology, University College London, London EC1V 9EL, UK. Electronic address: k.matter@ucl.ac.uk.

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Classifications MeSH

questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines contractiles › Protéines du muscle › Actomyosine › Interplay between Extracellular Matrix...
questionsmedicales.fr › Eucaryotes › Animaux › Interplay between Extracellular Matrix...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Carnivora › Pinnipedia › Canidae › Chiens › Interplay between Extracellular Matrix...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace extracellulaire › Matrice extracellulaire › Interplay between Extracellular Matrix...
questionsmedicales.fr › Cellules › Cellules épithéliales › Cellules rénales canines Madin-Darby › Interplay between Extracellular Matrix...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Récepteurs de surface cellulaire › Interplay between Extracellular Matrix...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Régulateurs des protéines G › Facteurs d'échange de nucléotides guanyliques › Rho guanine nucleotide exchange factors › Interplay between Extracellular Matrix...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Transduction du signal › Interplay between Extracellular Matrix...
questionsmedicales.fr › Phénomènes physiques › Phénomènes mécaniques › Résistance à la traction › Interplay between Extracellular Matrix...
questionsmedicales.fr › Cellules › Structures cellulaires › Membrane cellulaire › Structures de la membrane cellulaire › Jonctions intercellulaires › Jonctions serrées › Interplay between Extracellular Matrix...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Protéines de la jonction serrée › Protéines de la zonula occludens › Protéine-1 de la zonula occludens › Interplay between Extracellular Matrix...