Generic comparison of lumen nucleation and fusion in epithelial organoids with and without hydrostatic pressure
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. How...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2025-07-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-60780-8 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849331628195708928 |
|---|---|
| author | 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 Daniel Riveline |
| author_facet | 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 Daniel Riveline |
| author_sort | Linjie Lu |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-165efd3eb53744c49f96d6e62590560f |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-165efd3eb53744c49f96d6e62590560f2025-08-20T03:46:28ZengNature PortfolioNature Communications2041-17232025-07-0116111610.1038/s41467-025-60780-8Generic comparison of lumen nucleation and fusion in epithelial organoids with and without hydrostatic pressureLinjie Lu0Kana Fuji1Tristan Guyomar2Michèle Lieb3Marie André4Sakurako Tanida5Makiko Nonomura6Tetsuya Hiraiwa7Yara Alcheikh8Siham Yennek9Heike Petzold10Cecilie Martin-Lemaitre11Anne Grapin-Botton12Alf Honigmann13Masaki Sano14Daniel Riveline15Institut de Génétique et de Biologie Moléculaire et CellulaireUniversal Biology Institute, Graduate School of Science, The University of TokyoInstitut de Génétique et de Biologie Moléculaire et CellulaireInstitut de Génétique et de Biologie Moléculaire et CellulaireInstitut de Génétique et de Biologie Moléculaire et CellulaireUniversal Biology Institute, Graduate School of Science, The University of TokyoDepartment of Mathematical Information Engineering, College of Industrial Technology, Nihon UniversityUniversal Biology Institute, Graduate School of Science, The University of TokyoMax Planck Institute of Molecular Cell Biology and GeneticsThe Novo Nordisk Foundation Center for Stem Cell BiologyMax Planck Institute of Molecular Cell Biology and GeneticsTechnische Universität Dresden, Biotechnologisches Zentrum, Center for Molecular and Cellular Bioengineering (CMCB)Max Planck Institute of Molecular Cell Biology and GeneticsMax Planck Institute of Molecular Cell Biology and GeneticsUniversal Biology Institute, Graduate School of Science, The University of TokyoInstitut de Génétique et de Biologie Moléculaire et CellulaireAbstract 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.https://doi.org/10.1038/s41467-025-60780-8 |
| spellingShingle | 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 Daniel Riveline Generic comparison of lumen nucleation and fusion in epithelial organoids with and without hydrostatic pressure Nature Communications |
| title | Generic comparison of lumen nucleation and fusion in epithelial organoids with and without hydrostatic pressure |
| title_full | Generic comparison of lumen nucleation and fusion in epithelial organoids with and without hydrostatic pressure |
| title_fullStr | Generic comparison of lumen nucleation and fusion in epithelial organoids with and without hydrostatic pressure |
| title_full_unstemmed | Generic comparison of lumen nucleation and fusion in epithelial organoids with and without hydrostatic pressure |
| title_short | Generic comparison of lumen nucleation and fusion in epithelial organoids with and without hydrostatic pressure |
| title_sort | generic comparison of lumen nucleation and fusion in epithelial organoids with and without hydrostatic pressure |
| url | https://doi.org/10.1038/s41467-025-60780-8 |
| work_keys_str_mv | AT linjielu genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT kanafuji genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT tristanguyomar genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT michelelieb genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT marieandre genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT sakurakotanida genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT makikononomura genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT tetsuyahiraiwa genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT yaraalcheikh genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT sihamyennek genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT heikepetzold genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT ceciliemartinlemaitre genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT annegrapinbotton genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT alfhonigmann genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT masakisano genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure AT danielriveline genericcomparisonoflumennucleationandfusioninepithelialorganoidswithandwithouthydrostaticpressure |