Tight junctions control lumen morphology via hydrostatic pressure and junctional tension
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.
Authors
- Tristan Guyomar (ORCID: https://orcid.org/0009-0000-2079-4475)
- Daniel Riveline (ORCID: https://orcid.org/0000-0002-4632-011X)
- Cécilie Martin-Lemaitre
- Tetsuya Hiraiwa (ORCID: https://orcid.org/0000-0003-3221-345X)
- Michael F. Staddon (ORCID: https://orcid.org/0000-0002-8240-7554)
- Chen-Ho Wang
- Matthew J. Bovyn (ORCID: https://orcid.org/0000-0001-9331-4583)
- Linjie Lu (ORCID: https://orcid.org/0000-0003-1445-5201)
- Alf Honigmann (ORCID: https://orcid.org/0000-0003-0475-3790)
- Rozemarijn E. van der Veen (ORCID: https://orcid.org/0000-0003-0017-9373)
- Martin Lehmann (ORCID: https://orcid.org/0000-0002-8370-6353)
- Riccardo Maraspini (ORCID: https://orcid.org/0000-0002-0985-3902)
- Markus Mukenhirn (ORCID: https://orcid.org/0000-0002-7240-3816)
- Masaki Sano
Institutions
- Centre National de la Recherche Scientifique (FR)
- Inserm (FR)
- National University of Singapore (SG)
- Shanghai Jiao Tong University (CN)
- Institut de génétique et de biologie moléculaire et cellulaire (FR)
- Leibniz-Forschungsinstitut für Molekulare Pharmakologie (DE)
- Max Planck Institute for the Physics of Complex Systems (DE)
- Center for Systems Biology Dresden (DE)
- Max Planck Institute of Molecular Cell Biology and Genetics (DE)
- Université de Strasbourg (FR)
- The University of Tokyo (JP)
- Technische Universität Dresden (DE)
Publication Details
- Journal
- Developmental Cell
- Published
- 2024-08-12
- DOI
- https://doi.org/10.1016/j.devcel.2024.07.016
- Citations
- 27
- Primary Topic
- Barrier Structure and Function Studies
- Type
- article
- Field-Weighted Citation Impact
- 6.68
Funders
- Volkswagen Foundation
- Agence Nationale de la Recherche
- Institut National de la Santé et de la Recherche Médicale
- Université de Strasbourg
- Max-Planck-Gesellschaft
- Centre National de la Recherche Scientifique
- Mechanobiology Institute, Singapore
- National Institute for Physiological Sciences