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

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  • Linjie Lu

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire
    Université de Strasbourg
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale)

  • Kana Fuji

    (The University of Tokyo)

  • Tristan Guyomar

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire
    Université de Strasbourg
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale)

  • Michèle Lieb

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire
    Université de Strasbourg
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale)

  • Marie André

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire
    Université de Strasbourg
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale)

  • Sakurako Tanida

    (The University of Tokyo
    The University of Tokyo
    The University of Tokyo)

  • Makiko Nonomura

    (Nihon University)

  • Tetsuya Hiraiwa

    (The University of Tokyo
    National University of Singapore
    Academia Sinica)

  • 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)
    TU Dresden)

  • Anne Grapin-Botton

    (Max Planck Institute of Molecular Cell Biology and Genetics
    The Novo Nordisk Foundation Center for Stem Cell Biology)

  • Alf Honigmann

    (Max Planck Institute of Molecular Cell Biology and Genetics
    Center for Molecular and Cellular Bioengineering (CMCB)
    TU Dresden)

  • Masaki Sano

    (The University of Tokyo
    Shanghai Jiao Tong University)

  • Daniel Riveline

    (Institut de Génétique et de Biologie Moléculaire et Cellulaire
    Université de Strasbourg
    Centre National de la Recherche Scientifique
    Institut National de la Santé et de la Recherche Médicale)

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.

Suggested Citation

  • 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 & An, 2025. "Generic comparison of lumen nucleation and fusion in epithelial organoids with and without hydrostatic pressure," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-60780-8
    DOI: 10.1038/s41467-025-60780-8
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