Cargando…

Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation

Epithelial folding mediated by apical constriction converts flat epithelial sheets into multilayered, complex tissue structures and is employed throughout the development in most animals(1). Little is known, however, how forces produced near the apical surface of the tissue are transmitted within in...

Descripción completa

Detalles Bibliográficos
Autores principales: He, Bing, Doubrovinski, Konstantin, Polyakov, Oleg, Wieschaus, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4111109/
https://www.ncbi.nlm.nih.gov/pubmed/24590071
http://dx.doi.org/10.1038/nature13070
_version_ 1782328067865182208
author He, Bing
Doubrovinski, Konstantin
Polyakov, Oleg
Wieschaus, Eric
author_facet He, Bing
Doubrovinski, Konstantin
Polyakov, Oleg
Wieschaus, Eric
author_sort He, Bing
collection PubMed
description Epithelial folding mediated by apical constriction converts flat epithelial sheets into multilayered, complex tissue structures and is employed throughout the development in most animals(1). Little is known, however, how forces produced near the apical surface of the tissue are transmitted within individual cells to generate the global changes in cell shape that characterize tissue deformation. Here we apply particle tracking velocimetry in gastrulating Drosophila embryos to measure the movement of cytoplasm and plasma membrane during ventral furrow (VF) formation(2, 3). We find that cytoplasmic redistribution during the lengthening phase of VF formation can be precisely described by viscous flows that quantitatively match the predictions of hydrodynamics. Cell membranes move with the ambient cytoplasm, with little resistance to or driving force on the flow. Strikingly, apical constriction produces similar flow patterns in mutant embryos that fail to form cells prior to gastrulation (“acellular” embryos), such that the global redistribution of cytoplasm mirrors the summed redistribution occurring in individual cells of wild type embryos. Our results suggest that during the lengthening phase of VF formation, hydrodynamic behavior of the cytoplasm provides the predominant mechanism transmitting apically generated forces deep into the tissue and that cell individualization is dispensable.
format Online
Article
Text
id pubmed-4111109
institution National Center for Biotechnology Information
language English
publishDate 2014
record_format MEDLINE/PubMed
spelling pubmed-41111092014-10-17 Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation He, Bing Doubrovinski, Konstantin Polyakov, Oleg Wieschaus, Eric Nature Article Epithelial folding mediated by apical constriction converts flat epithelial sheets into multilayered, complex tissue structures and is employed throughout the development in most animals(1). Little is known, however, how forces produced near the apical surface of the tissue are transmitted within individual cells to generate the global changes in cell shape that characterize tissue deformation. Here we apply particle tracking velocimetry in gastrulating Drosophila embryos to measure the movement of cytoplasm and plasma membrane during ventral furrow (VF) formation(2, 3). We find that cytoplasmic redistribution during the lengthening phase of VF formation can be precisely described by viscous flows that quantitatively match the predictions of hydrodynamics. Cell membranes move with the ambient cytoplasm, with little resistance to or driving force on the flow. Strikingly, apical constriction produces similar flow patterns in mutant embryos that fail to form cells prior to gastrulation (“acellular” embryos), such that the global redistribution of cytoplasm mirrors the summed redistribution occurring in individual cells of wild type embryos. Our results suggest that during the lengthening phase of VF formation, hydrodynamic behavior of the cytoplasm provides the predominant mechanism transmitting apically generated forces deep into the tissue and that cell individualization is dispensable. 2014-03-02 2014-04-17 /pmc/articles/PMC4111109/ /pubmed/24590071 http://dx.doi.org/10.1038/nature13070 Text en Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
He, Bing
Doubrovinski, Konstantin
Polyakov, Oleg
Wieschaus, Eric
Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation
title Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation
title_full Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation
title_fullStr Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation
title_full_unstemmed Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation
title_short Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation
title_sort apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4111109/
https://www.ncbi.nlm.nih.gov/pubmed/24590071
http://dx.doi.org/10.1038/nature13070
work_keys_str_mv AT hebing apicalconstrictiondrivestissuescalehydrodynamicflowtomediatecellelongation
AT doubrovinskikonstantin apicalconstrictiondrivestissuescalehydrodynamicflowtomediatecellelongation
AT polyakovoleg apicalconstrictiondrivestissuescalehydrodynamicflowtomediatecellelongation
AT wieschauseric apicalconstrictiondrivestissuescalehydrodynamicflowtomediatecellelongation