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Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation

Many animal embryos pull and close an epithelial sheet around the ellipsoidal egg surface during a gastrulation process known as epiboly. The ovoidal geometry dictates that the epithelial sheet first expands and subsequently compacts. Moreover, the spreading epithelium is mechanically stressed and t...

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Autores principales: Jain, Akanksha, Ulman, Vladimir, Mukherjee, Arghyadip, Prakash, Mangal, Cuenca, Marina B., Pimpale, Lokesh G., Münster, Stefan, Haase, Robert, Panfilio, Kristen A., Jug, Florian, Grill, Stephan W., Tomancak, Pavel, Pavlopoulos, Anastasios
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7645651/
https://www.ncbi.nlm.nih.gov/pubmed/33154375
http://dx.doi.org/10.1038/s41467-020-19356-x
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author Jain, Akanksha
Ulman, Vladimir
Mukherjee, Arghyadip
Prakash, Mangal
Cuenca, Marina B.
Pimpale, Lokesh G.
Münster, Stefan
Haase, Robert
Panfilio, Kristen A.
Jug, Florian
Grill, Stephan W.
Tomancak, Pavel
Pavlopoulos, Anastasios
author_facet Jain, Akanksha
Ulman, Vladimir
Mukherjee, Arghyadip
Prakash, Mangal
Cuenca, Marina B.
Pimpale, Lokesh G.
Münster, Stefan
Haase, Robert
Panfilio, Kristen A.
Jug, Florian
Grill, Stephan W.
Tomancak, Pavel
Pavlopoulos, Anastasios
author_sort Jain, Akanksha
collection PubMed
description Many animal embryos pull and close an epithelial sheet around the ellipsoidal egg surface during a gastrulation process known as epiboly. The ovoidal geometry dictates that the epithelial sheet first expands and subsequently compacts. Moreover, the spreading epithelium is mechanically stressed and this stress needs to be released. Here we show that during extraembryonic tissue (serosa) epiboly in the insect Tribolium castaneum, the non-proliferative serosa becomes regionalized into a solid-like dorsal region with larger non-rearranging cells, and a more fluid-like ventral region surrounding the leading edge with smaller cells undergoing intercalations. Our results suggest that a heterogeneous actomyosin cable contributes to the fluidization of the leading edge by driving sequential eviction and intercalation of individual cells away from the serosa margin. Since this developmental solution utilized during epiboly resembles the mechanism of wound healing, we propose actomyosin cable-driven local tissue fluidization as a conserved morphogenetic module for closure of epithelial gaps.
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spelling pubmed-76456512020-11-10 Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation Jain, Akanksha Ulman, Vladimir Mukherjee, Arghyadip Prakash, Mangal Cuenca, Marina B. Pimpale, Lokesh G. Münster, Stefan Haase, Robert Panfilio, Kristen A. Jug, Florian Grill, Stephan W. Tomancak, Pavel Pavlopoulos, Anastasios Nat Commun Article Many animal embryos pull and close an epithelial sheet around the ellipsoidal egg surface during a gastrulation process known as epiboly. The ovoidal geometry dictates that the epithelial sheet first expands and subsequently compacts. Moreover, the spreading epithelium is mechanically stressed and this stress needs to be released. Here we show that during extraembryonic tissue (serosa) epiboly in the insect Tribolium castaneum, the non-proliferative serosa becomes regionalized into a solid-like dorsal region with larger non-rearranging cells, and a more fluid-like ventral region surrounding the leading edge with smaller cells undergoing intercalations. Our results suggest that a heterogeneous actomyosin cable contributes to the fluidization of the leading edge by driving sequential eviction and intercalation of individual cells away from the serosa margin. Since this developmental solution utilized during epiboly resembles the mechanism of wound healing, we propose actomyosin cable-driven local tissue fluidization as a conserved morphogenetic module for closure of epithelial gaps. Nature Publishing Group UK 2020-11-05 /pmc/articles/PMC7645651/ /pubmed/33154375 http://dx.doi.org/10.1038/s41467-020-19356-x Text en © The Author(s) 2020 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/.
spellingShingle Article
Jain, Akanksha
Ulman, Vladimir
Mukherjee, Arghyadip
Prakash, Mangal
Cuenca, Marina B.
Pimpale, Lokesh G.
Münster, Stefan
Haase, Robert
Panfilio, Kristen A.
Jug, Florian
Grill, Stephan W.
Tomancak, Pavel
Pavlopoulos, Anastasios
Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation
title Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation
title_full Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation
title_fullStr Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation
title_full_unstemmed Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation
title_short Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation
title_sort regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7645651/
https://www.ncbi.nlm.nih.gov/pubmed/33154375
http://dx.doi.org/10.1038/s41467-020-19356-x
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