Tight junctions control lumen morphology via hydrostatic pressure and junctional tension,Developmental Cell

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Tight junctions control lumen morphology via hydrostatic pressure and junctional tension
Developmental Cell ( IF 10.7 ) Pub Date : 2024-08-12 , DOI: 10.1016/j.devcel.2024.07.016
Markus Mukenhirn ₁ , Chen-Ho Wang ₂ , Tristan Guyomar ₃ , Matthew J Bovyn ₄ , Michael F Staddon ₄ , Rozemarijn E van der Veen ₅ , Riccardo Maraspini ₂ , Linjie Lu ₃ , Cecilie Martin-Lemaitre ₆ , Masaki Sano ₇ , Martin Lehmann ₅ , Tetsuya Hiraiwa ₈ , Daniel Riveline ₃ , Alf Honigmann ₉

Affiliation

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.
Max Planck Institute of Molecular Cell Biology and Genetics, 01309 Dresden, Germany.
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.
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.
Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP), 13125 Berlin, Germany.
Biotechnology Center, Center for Molecular and Cellular Bioengineering, Technische Universität Dresden, 01069 Dresden, Germany.
Institute of Natural Sciences, School of Physics and Astronomy, Shanghai Jiao Tong University, Shanghai 200240, China.
Mechanobiology Institute, National University of Singapore, Singapore 117411, Singapore; Universal Biology Institute, The University of Tokyo, Hongo, Tokyo 113-0033, Japan.
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.

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.

中文翻译：

紧密连接通过静水压力和连接张力控制管腔形态

上皮组织形成充满液体的管腔对于器官发育至关重要。细胞如何控制液压力和皮质力以控制管腔形态尚不清楚。在这里，我们使用 MDCK-II 囊肿量化了紧密连接在管腔形成中的机械作用。我们发现，由密蛋白受体形成的细胞旁离子屏障不是管腔液压充气所必需的。然而，小带闭塞支架的耗竭导致管腔塌陷和顶膜折叠。将静水管腔压力和连接张力的定量测量与建模相结合，使我们能够从压力-张力力平衡中解释管腔形态。紧密连接通过抑制肌球蛋白降低皮质张力来促进管腔充气。此外，我们的结果表明，根尖面积过大有助于管腔张开。总体而言，我们提供了上皮细胞如何使用紧密连接来调节组织和管腔形状的机械理解。

更新日期：2024-08-12

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