Generic comparison of lumen nucleation and fusion in epithelial organoids with and without hydrostatic pressure

Linjie Lu, Kana Fuji, Tristan Guyomar, Michèle Lieb, Marie André, Sakurako Tanida, Makiko Nonomura, Tetsuya Hiraiwa, Yara Alcheikh, Siham Yennek, Heike Petzold, Cecilie Martin-Lemaitre, Anne Grapin-Botton (), Alf Honigmann (), Masaki Sano () and Daniel Riveline ()
Additional contact information
Linjie Lu: Institut de Génétique et de Biologie Moléculaire et Cellulaire
Kana Fuji: The University of Tokyo
Tristan Guyomar: Institut de Génétique et de Biologie Moléculaire et Cellulaire
Michèle Lieb: Institut de Génétique et de Biologie Moléculaire et Cellulaire
Marie André: Institut de Génétique et de Biologie Moléculaire et Cellulaire
Sakurako Tanida: The University of Tokyo
Makiko Nonomura: Nihon University
Tetsuya Hiraiwa: The University of Tokyo
Yara Alcheikh: Max Planck Institute of Molecular Cell Biology and Genetics
Siham Yennek: The Novo Nordisk Foundation Center for Stem Cell Biology
Heike Petzold: Max Planck Institute of Molecular Cell Biology and Genetics
Cecilie Martin-Lemaitre: Center for Molecular and Cellular Bioengineering (CMCB)
Anne Grapin-Botton: Max Planck Institute of Molecular Cell Biology and Genetics
Alf Honigmann: Max Planck Institute of Molecular Cell Biology and Genetics
Masaki Sano: The University of Tokyo
Daniel Riveline: Institut de Génétique et de Biologie Moléculaire et Cellulaire

Nature Communications, 2025, vol. 16, issue 1, 1-16

Abstract: Abstract Many internal organs in the body harbor a fluid-filled lumen. Lumen nucleation and fusion have been reported as dependent on organ-type during organogenesis. In contrast, the physics of lumen suggests that force balance between luminal pressure and cell mechanics leads to generic rules. However, this hypothesis lacks experimental evidence. Here we compare lumen dynamics for three different systems (MDCK cysts, pancreatic spheres, and epiblast model) by using quantitative cell biology, microfabrication, and theory. We report that the initial cell number determines the maximum number of lumens but does not impact the steady state, which is a final single lumen. We show that lumen dynamics is determined by luminal hydrostatic pressure. We also use MDCK cysts to manipulate cell adhesion and lumen volume to successfully reproduce the fusion dynamics of pancreatic spheres and epiblasts. Our results reveal self-organisation rules of lumens with relevance for morphogenesis and tissue engineering.

Date: 2025
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Persistent link: https://EconPapers.repec.org/RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-60780-8

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DOI: 10.1038/s41467-025-60780-8

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