Tight junctions control lumen morphology via hydrostatic pressure and junctional tension.

biological physics lumen morphogenesis lumen pressure mechano-biology myosin contractility tight junction tissue hydraulics

Journal

Developmental cell
ISSN: 1878-1551
Titre abrégé: Dev Cell
Pays: United States
ID NLM: 101120028

Informations de publication

Date de publication:
08 Aug 2024
Historique:
received: 11 05 2023
revised: 24 02 2024
accepted: 16 07 2024
medline: 14 8 2024
pubmed: 14 8 2024
entrez: 13 8 2024
Statut: aheadofprint

Résumé

Formation of fluid-filled lumina by epithelial tissues is essential for organ development. How cells control the hydraulic and cortical forces to control lumen morphology is not well understood. Here, we quantified the mechanical role of tight junctions in lumen formation using MDCK-II cysts. We found that the paracellular ion barrier formed by claudin receptors is not required for the hydraulic inflation of a lumen. However, the depletion of the zonula occludens scaffold resulted in lumen collapse and folding of apical membranes. Combining quantitative measurements of hydrostatic lumen pressure and junctional tension with modeling enabled us to explain lumen morphologies from the pressure-tension force balance. Tight junctions promote lumen inflation by decreasing cortical tension via the inhibition of myosin. In addition, our results suggest that excess apical area contributes to lumen opening. Overall, we provide a mechanical understanding of how epithelial cells use tight junctions to modulate tissue and lumen shape.

Identifiants

pubmed: 39137775
pii: S1534-5807(24)00456-8
doi: 10.1016/j.devcel.2024.07.016
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests

Auteurs

Markus Mukenhirn (M)

Biotechnology Center, Center for Molecular and Cellular Bioengineering, Technische Universität Dresden, 01069 Dresden, Germany; Max Planck Institute of Molecular Cell Biology and Genetics, 01309 Dresden, Germany.

Chen-Ho Wang (CH)

Max Planck Institute of Molecular Cell Biology and Genetics, 01309 Dresden, Germany.

Tristan Guyomar (T)

Université de Strasbourg, IGBMC UMR 7104 - UMR-S 1258, 67400 Illkirch, France; CNRS, UMR 7104, 67400 Illkirch, France; Inserm, UMR-S 1258, 67400 Illkirch, France; IGBMC, Institut de Génétique et de Biologie Moléculaire et Cellulaire, 67400 Illkirch, France.

Matthew J Bovyn (MJ)

Max Planck Institute of Molecular Cell Biology and Genetics, 01309 Dresden, Germany; Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany; Center for Systems Biology Dresden, 01307 Dresden, Germany.

Michael F Staddon (MF)

Max Planck Institute of Molecular Cell Biology and Genetics, 01309 Dresden, Germany; Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany; Center for Systems Biology Dresden, 01307 Dresden, Germany.

Rozemarijn E van der Veen (RE)

Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP), 13125 Berlin, Germany.

Riccardo Maraspini (R)

Max Planck Institute of Molecular Cell Biology and Genetics, 01309 Dresden, Germany.

Linjie Lu (L)

Université de Strasbourg, IGBMC UMR 7104 - UMR-S 1258, 67400 Illkirch, France; CNRS, UMR 7104, 67400 Illkirch, France; Inserm, UMR-S 1258, 67400 Illkirch, France; IGBMC, Institut de Génétique et de Biologie Moléculaire et Cellulaire, 67400 Illkirch, France.

Cecilie Martin-Lemaitre (C)

Biotechnology Center, Center for Molecular and Cellular Bioengineering, Technische Universität Dresden, 01069 Dresden, Germany.

Masaki Sano (M)

Institute of Natural Sciences, School of Physics and Astronomy, Shanghai Jiao Tong University, Shanghai 200240, China.

Martin Lehmann (M)

Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP), 13125 Berlin, Germany.

Tetsuya Hiraiwa (T)

Mechanobiology Institute, National University of Singapore, Singapore 117411, Singapore; Universal Biology Institute, The University of Tokyo, Hongo, Tokyo 113-0033, Japan.

Daniel Riveline (D)

Université de Strasbourg, IGBMC UMR 7104 - UMR-S 1258, 67400 Illkirch, France; CNRS, UMR 7104, 67400 Illkirch, France; Inserm, UMR-S 1258, 67400 Illkirch, France; IGBMC, Institut de Génétique et de Biologie Moléculaire et Cellulaire, 67400 Illkirch, France. Electronic address: riveline@unistra.fr.

Alf Honigmann (A)

Biotechnology Center, Center for Molecular and Cellular Bioengineering, Technische Universität Dresden, 01069 Dresden, Germany; Max Planck Institute of Molecular Cell Biology and Genetics, 01309 Dresden, Germany; Cluster of Excellence Physics of Life, TU Dresden, 01062 Dresden, Germany. Electronic address: alf.honigmann@tu-dresden.de.

Classifications MeSH