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Patterning and dynamics of membrane adhesion under hydraulic stress

Hydraulic fracturing plays a major role in cavity formation during embryonic development, when pressurized fluid opens microlumens at cell-cell contacts, which evolve to form a single large lumen. However, the fundamental physical mechanisms behind these processes remain masked by the complexity and...

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Autores principales: Dinet, Céline, Torres-Sánchez, Alejandro, Lanfranco, Roberta, Di Michele, Lorenzo, Arroyo, Marino, Staykova, Margarita
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10656516/
https://www.ncbi.nlm.nih.gov/pubmed/37978292
http://dx.doi.org/10.1038/s41467-023-43246-7
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author Dinet, Céline
Torres-Sánchez, Alejandro
Lanfranco, Roberta
Di Michele, Lorenzo
Arroyo, Marino
Staykova, Margarita
author_facet Dinet, Céline
Torres-Sánchez, Alejandro
Lanfranco, Roberta
Di Michele, Lorenzo
Arroyo, Marino
Staykova, Margarita
author_sort Dinet, Céline
collection PubMed
description Hydraulic fracturing plays a major role in cavity formation during embryonic development, when pressurized fluid opens microlumens at cell-cell contacts, which evolve to form a single large lumen. However, the fundamental physical mechanisms behind these processes remain masked by the complexity and specificity of biological systems. Here, we show that adhered lipid vesicles subjected to osmotic stress form hydraulic microlumens similar to those in cells. Combining vesicle experiments with theoretical modelling and numerical simulations, we provide a physical framework for the hydraulic reconfiguration of cell-cell adhesions. We map the conditions for microlumen formation from a pristine adhesion, the emerging dynamical patterns and their subsequent maturation. We demonstrate control of the fracturing process depending on the applied pressure gradients and the type and density of membrane bonds. Our experiments further reveal an unexpected, passive transition of microlumens to closed buds that suggests a physical route to adhesion remodeling by endocytosis.
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spelling pubmed-106565162023-11-17 Patterning and dynamics of membrane adhesion under hydraulic stress Dinet, Céline Torres-Sánchez, Alejandro Lanfranco, Roberta Di Michele, Lorenzo Arroyo, Marino Staykova, Margarita Nat Commun Article Hydraulic fracturing plays a major role in cavity formation during embryonic development, when pressurized fluid opens microlumens at cell-cell contacts, which evolve to form a single large lumen. However, the fundamental physical mechanisms behind these processes remain masked by the complexity and specificity of biological systems. Here, we show that adhered lipid vesicles subjected to osmotic stress form hydraulic microlumens similar to those in cells. Combining vesicle experiments with theoretical modelling and numerical simulations, we provide a physical framework for the hydraulic reconfiguration of cell-cell adhesions. We map the conditions for microlumen formation from a pristine adhesion, the emerging dynamical patterns and their subsequent maturation. We demonstrate control of the fracturing process depending on the applied pressure gradients and the type and density of membrane bonds. Our experiments further reveal an unexpected, passive transition of microlumens to closed buds that suggests a physical route to adhesion remodeling by endocytosis. Nature Publishing Group UK 2023-11-17 /pmc/articles/PMC10656516/ /pubmed/37978292 http://dx.doi.org/10.1038/s41467-023-43246-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Dinet, Céline
Torres-Sánchez, Alejandro
Lanfranco, Roberta
Di Michele, Lorenzo
Arroyo, Marino
Staykova, Margarita
Patterning and dynamics of membrane adhesion under hydraulic stress
title Patterning and dynamics of membrane adhesion under hydraulic stress
title_full Patterning and dynamics of membrane adhesion under hydraulic stress
title_fullStr Patterning and dynamics of membrane adhesion under hydraulic stress
title_full_unstemmed Patterning and dynamics of membrane adhesion under hydraulic stress
title_short Patterning and dynamics of membrane adhesion under hydraulic stress
title_sort patterning and dynamics of membrane adhesion under hydraulic stress
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10656516/
https://www.ncbi.nlm.nih.gov/pubmed/37978292
http://dx.doi.org/10.1038/s41467-023-43246-7
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