A hydro-osmotic coarsening theory of biological cavity formation.

Fluid-filled biological cavities are ubiquitous, but their collective dynamics has remained largely unexplored from a physical perspective. Based on experimental observations in early embryos, we propose a model where a cavity forms through the coarsening of myriad of pressurized micrometric lumens,...

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Auteurs principaux:	Mathieu Le Verge-Serandour, Hervé Turlier
Format:	article
Langue:	EN
Publié:	Public Library of Science (PLoS) 2021
Sujets:	Biology (General) QH301-705.5
Accès en ligne:	https://doaj.org/article/010d3aec8647496c98023cdba3d27f37
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spelling	oai:doaj.org-article:010d3aec8647496c98023cdba3d27f372021-12-02T19:57:51ZA hydro-osmotic coarsening theory of biological cavity formation.1553-734X1553-735810.1371/journal.pcbi.1009333https://doaj.org/article/010d3aec8647496c98023cdba3d27f372021-09-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.1009333https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Fluid-filled biological cavities are ubiquitous, but their collective dynamics has remained largely unexplored from a physical perspective. Based on experimental observations in early embryos, we propose a model where a cavity forms through the coarsening of myriad of pressurized micrometric lumens, that interact by ion and fluid exchanges through the intercellular space. Performing extensive numerical simulations, we find that hydraulic fluxes lead to a self-similar coarsening of lumens in time, characterized by a robust dynamic scaling exponent. The collective dynamics is primarily controlled by hydraulic fluxes, which stem from lumen pressures differences and are dampened by water permeation through the membrane. Passive osmotic heterogeneities play, on the contrary, a minor role on cavity formation but active ion pumping can largely modify the coarsening dynamics: it prevents the lumen network from a collective collapse and gives rise to a novel coalescence-dominated regime exhibiting a distinct scaling law. Interestingly, we prove numerically that spatially biasing ion pumping may be sufficient to position the cavity, suggesting a novel mode of symmetry breaking to control tissue patterning. Providing generic testable predictions, our model forms a comprehensive theoretical basis for hydro-osmotic interaction between biological cavities, that shall find wide applications in embryo and tissue morphogenesis.Mathieu Le Verge-SerandourHervé TurlierPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 17, Iss 9, p e1009333 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Mathieu Le Verge-Serandour Hervé Turlier A hydro-osmotic coarsening theory of biological cavity formation.
description	Fluid-filled biological cavities are ubiquitous, but their collective dynamics has remained largely unexplored from a physical perspective. Based on experimental observations in early embryos, we propose a model where a cavity forms through the coarsening of myriad of pressurized micrometric lumens, that interact by ion and fluid exchanges through the intercellular space. Performing extensive numerical simulations, we find that hydraulic fluxes lead to a self-similar coarsening of lumens in time, characterized by a robust dynamic scaling exponent. The collective dynamics is primarily controlled by hydraulic fluxes, which stem from lumen pressures differences and are dampened by water permeation through the membrane. Passive osmotic heterogeneities play, on the contrary, a minor role on cavity formation but active ion pumping can largely modify the coarsening dynamics: it prevents the lumen network from a collective collapse and gives rise to a novel coalescence-dominated regime exhibiting a distinct scaling law. Interestingly, we prove numerically that spatially biasing ion pumping may be sufficient to position the cavity, suggesting a novel mode of symmetry breaking to control tissue patterning. Providing generic testable predictions, our model forms a comprehensive theoretical basis for hydro-osmotic interaction between biological cavities, that shall find wide applications in embryo and tissue morphogenesis.
format	article
author	Mathieu Le Verge-Serandour Hervé Turlier
author_facet	Mathieu Le Verge-Serandour Hervé Turlier
author_sort	Mathieu Le Verge-Serandour
title	A hydro-osmotic coarsening theory of biological cavity formation.
title_short	A hydro-osmotic coarsening theory of biological cavity formation.
title_full	A hydro-osmotic coarsening theory of biological cavity formation.
title_fullStr	A hydro-osmotic coarsening theory of biological cavity formation.
title_full_unstemmed	A hydro-osmotic coarsening theory of biological cavity formation.
title_sort	hydro-osmotic coarsening theory of biological cavity formation.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/010d3aec8647496c98023cdba3d27f37
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A hydro-osmotic coarsening theory of biological cavity formation.

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