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Size control of the inner ear via hydraulic feedback

Animals make organs of precise size, shape, and symmetry but how developing embryos do this is largely unknown. Here, we combine quantitative imaging, physical theory, and physiological measurement of hydrostatic pressure and fluid transport in zebrafish to study size control of the developing inner...

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Autores principales: Mosaliganti, Kishore R, Swinburne, Ian A, Chan, Chon U, Obholzer, Nikolaus D, Green, Amelia A, Tanksale, Shreyas, Mahadevan, L, Megason, Sean G
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6773445/
https://www.ncbi.nlm.nih.gov/pubmed/31571582
http://dx.doi.org/10.7554/eLife.39596
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author Mosaliganti, Kishore R
Swinburne, Ian A
Chan, Chon U
Obholzer, Nikolaus D
Green, Amelia A
Tanksale, Shreyas
Mahadevan, L
Megason, Sean G
author_facet Mosaliganti, Kishore R
Swinburne, Ian A
Chan, Chon U
Obholzer, Nikolaus D
Green, Amelia A
Tanksale, Shreyas
Mahadevan, L
Megason, Sean G
author_sort Mosaliganti, Kishore R
collection PubMed
description Animals make organs of precise size, shape, and symmetry but how developing embryos do this is largely unknown. Here, we combine quantitative imaging, physical theory, and physiological measurement of hydrostatic pressure and fluid transport in zebrafish to study size control of the developing inner ear. We find that fluid accumulation creates hydrostatic pressure in the lumen leading to stress in the epithelium and expansion of the otic vesicle. Pressure, in turn, inhibits fluid transport into the lumen. This negative feedback loop between pressure and transport allows the otic vesicle to change growth rate to control natural or experimentally-induced size variation. Spatiotemporal patterning of contractility modulates pressure-driven strain for regional tissue thinning. Our work connects molecular-driven mechanisms, such as osmotic pressure driven strain and actomyosin tension, to the regulation of tissue morphogenesis via hydraulic feedback to ensure robust control of organ size. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).
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spelling pubmed-67734452019-10-02 Size control of the inner ear via hydraulic feedback Mosaliganti, Kishore R Swinburne, Ian A Chan, Chon U Obholzer, Nikolaus D Green, Amelia A Tanksale, Shreyas Mahadevan, L Megason, Sean G eLife Computational and Systems Biology Animals make organs of precise size, shape, and symmetry but how developing embryos do this is largely unknown. Here, we combine quantitative imaging, physical theory, and physiological measurement of hydrostatic pressure and fluid transport in zebrafish to study size control of the developing inner ear. We find that fluid accumulation creates hydrostatic pressure in the lumen leading to stress in the epithelium and expansion of the otic vesicle. Pressure, in turn, inhibits fluid transport into the lumen. This negative feedback loop between pressure and transport allows the otic vesicle to change growth rate to control natural or experimentally-induced size variation. Spatiotemporal patterning of contractility modulates pressure-driven strain for regional tissue thinning. Our work connects molecular-driven mechanisms, such as osmotic pressure driven strain and actomyosin tension, to the regulation of tissue morphogenesis via hydraulic feedback to ensure robust control of organ size. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter). eLife Sciences Publications, Ltd 2019-10-01 /pmc/articles/PMC6773445/ /pubmed/31571582 http://dx.doi.org/10.7554/eLife.39596 Text en © 2019, Mosaliganti et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Computational and Systems Biology
Mosaliganti, Kishore R
Swinburne, Ian A
Chan, Chon U
Obholzer, Nikolaus D
Green, Amelia A
Tanksale, Shreyas
Mahadevan, L
Megason, Sean G
Size control of the inner ear via hydraulic feedback
title Size control of the inner ear via hydraulic feedback
title_full Size control of the inner ear via hydraulic feedback
title_fullStr Size control of the inner ear via hydraulic feedback
title_full_unstemmed Size control of the inner ear via hydraulic feedback
title_short Size control of the inner ear via hydraulic feedback
title_sort size control of the inner ear via hydraulic feedback
topic Computational and Systems Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6773445/
https://www.ncbi.nlm.nih.gov/pubmed/31571582
http://dx.doi.org/10.7554/eLife.39596
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