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Rab5ab-Mediated Yolk Cell Membrane Endocytosis Is Essential for Zebrafish Epiboly and Mechanical Equilibrium During Gastrulation

Morphogenesis in early embryos demands the coordinated distribution of cells and tissues to their final destination in a spatio-temporal controlled way. Spatial and scalar differences in adhesion and contractility are essential for these morphogenetic movements, while the role that membrane remodeli...

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Autores principales: Marsal, Maria, Hernández-Vega, Amayra, Pouille, Philippe-Alexandre, Martin-Blanco, Enrique
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8585776/
https://www.ncbi.nlm.nih.gov/pubmed/34778246
http://dx.doi.org/10.3389/fcell.2021.697097
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author Marsal, Maria
Hernández-Vega, Amayra
Pouille, Philippe-Alexandre
Martin-Blanco, Enrique
author_facet Marsal, Maria
Hernández-Vega, Amayra
Pouille, Philippe-Alexandre
Martin-Blanco, Enrique
author_sort Marsal, Maria
collection PubMed
description Morphogenesis in early embryos demands the coordinated distribution of cells and tissues to their final destination in a spatio-temporal controlled way. Spatial and scalar differences in adhesion and contractility are essential for these morphogenetic movements, while the role that membrane remodeling may play remains less clear. To evaluate how membrane turnover modulates tissue arrangements we studied the role of endocytosis in zebrafish epiboly. Experimental analyses and modeling have shown that the expansion of the blastoderm relies on an asymmetry of mechanical tension in the yolk cell generated as a result of actomyosin-dependent contraction and membrane removal. Here we show that the GTPase Rab5ab is essential for the endocytosis and the removal of the external yolk cell syncytial layer (E-YSL) membrane. Interfering in its expression exclusively in the yolk resulted in the reduction of yolk cell actomyosin contractility, the disruption of cortical and internal flows, a disequilibrium in force balance and epiboly impairment. We conclude that regulated membrane remodeling is crucial for directing cell and tissue mechanics, preserving embryo geometry and coordinating morphogenetic movements during epiboly.
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spelling pubmed-85857762021-11-13 Rab5ab-Mediated Yolk Cell Membrane Endocytosis Is Essential for Zebrafish Epiboly and Mechanical Equilibrium During Gastrulation Marsal, Maria Hernández-Vega, Amayra Pouille, Philippe-Alexandre Martin-Blanco, Enrique Front Cell Dev Biol Cell and Developmental Biology Morphogenesis in early embryos demands the coordinated distribution of cells and tissues to their final destination in a spatio-temporal controlled way. Spatial and scalar differences in adhesion and contractility are essential for these morphogenetic movements, while the role that membrane remodeling may play remains less clear. To evaluate how membrane turnover modulates tissue arrangements we studied the role of endocytosis in zebrafish epiboly. Experimental analyses and modeling have shown that the expansion of the blastoderm relies on an asymmetry of mechanical tension in the yolk cell generated as a result of actomyosin-dependent contraction and membrane removal. Here we show that the GTPase Rab5ab is essential for the endocytosis and the removal of the external yolk cell syncytial layer (E-YSL) membrane. Interfering in its expression exclusively in the yolk resulted in the reduction of yolk cell actomyosin contractility, the disruption of cortical and internal flows, a disequilibrium in force balance and epiboly impairment. We conclude that regulated membrane remodeling is crucial for directing cell and tissue mechanics, preserving embryo geometry and coordinating morphogenetic movements during epiboly. Frontiers Media S.A. 2021-10-29 /pmc/articles/PMC8585776/ /pubmed/34778246 http://dx.doi.org/10.3389/fcell.2021.697097 Text en Copyright © 2021 Marsal, Hernández-Vega, Pouille and Martin-Blanco. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Marsal, Maria
Hernández-Vega, Amayra
Pouille, Philippe-Alexandre
Martin-Blanco, Enrique
Rab5ab-Mediated Yolk Cell Membrane Endocytosis Is Essential for Zebrafish Epiboly and Mechanical Equilibrium During Gastrulation
title Rab5ab-Mediated Yolk Cell Membrane Endocytosis Is Essential for Zebrafish Epiboly and Mechanical Equilibrium During Gastrulation
title_full Rab5ab-Mediated Yolk Cell Membrane Endocytosis Is Essential for Zebrafish Epiboly and Mechanical Equilibrium During Gastrulation
title_fullStr Rab5ab-Mediated Yolk Cell Membrane Endocytosis Is Essential for Zebrafish Epiboly and Mechanical Equilibrium During Gastrulation
title_full_unstemmed Rab5ab-Mediated Yolk Cell Membrane Endocytosis Is Essential for Zebrafish Epiboly and Mechanical Equilibrium During Gastrulation
title_short Rab5ab-Mediated Yolk Cell Membrane Endocytosis Is Essential for Zebrafish Epiboly and Mechanical Equilibrium During Gastrulation
title_sort rab5ab-mediated yolk cell membrane endocytosis is essential for zebrafish epiboly and mechanical equilibrium during gastrulation
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8585776/
https://www.ncbi.nlm.nih.gov/pubmed/34778246
http://dx.doi.org/10.3389/fcell.2021.697097
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