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The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure

Dorsal closure is a prominent morphogenetic process during Drosophila embryogenesis, which involves two epithelial tissues, that is, the squamous amnioserosa and the columnar lateral epidermis. Non-muscle myosin II-driven constriction in the amnioserosa leads to a decrease in the apical surface area...

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Autores principales: Lv, Zhiyi, Zhang, Na, Zhang, Xiaozhu, Großhans, Jörg, Kong, Deqing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9148979/
https://www.ncbi.nlm.nih.gov/pubmed/35652100
http://dx.doi.org/10.3389/fcell.2022.865397
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author Lv, Zhiyi
Zhang, Na
Zhang, Xiaozhu
Großhans, Jörg
Kong, Deqing
author_facet Lv, Zhiyi
Zhang, Na
Zhang, Xiaozhu
Großhans, Jörg
Kong, Deqing
author_sort Lv, Zhiyi
collection PubMed
description Dorsal closure is a prominent morphogenetic process during Drosophila embryogenesis, which involves two epithelial tissues, that is, the squamous amnioserosa and the columnar lateral epidermis. Non-muscle myosin II-driven constriction in the amnioserosa leads to a decrease in the apical surface area and pulls on the adjacent lateral epidermis, which subsequently moves dorsally. The pull by the amnioserosa becomes obvious in an elongation of the epidermal cells, especially of those in the first row. The contribution of the epidermal cell elongation has remained unclear to dorsal closure. Cell elongation may be a mere passive consequence or an active response to the pulling by the amnioserosa. Here, we found that the lateral epidermis actively responds. We analyzed tensions within tissues and cell junctions by laser ablation before and during dorsal closure, the elliptical and dorsal closure stages, respectively. Furthermore, we genetically and optochemically induced chronic and acute cell contraction, respectively. In this way, we found that tension in the epidermis increased during dorsal closure. A correspondingly increased tension was not observed at individual junctions, however. Junctional tension even decreased during dorsal closure in the epidermis. We strikingly observed a strong increase of the microtubule amount in the epidermis, while non-muscle myosin II increased in both tissues. Our data suggest that the epidermis actively antagonizes the pull from the amnioserosa during dorsal closure and the increased microtubules might help the epidermis bear part of the mechanical force.
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spelling pubmed-91489792022-05-31 The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure Lv, Zhiyi Zhang, Na Zhang, Xiaozhu Großhans, Jörg Kong, Deqing Front Cell Dev Biol Cell and Developmental Biology Dorsal closure is a prominent morphogenetic process during Drosophila embryogenesis, which involves two epithelial tissues, that is, the squamous amnioserosa and the columnar lateral epidermis. Non-muscle myosin II-driven constriction in the amnioserosa leads to a decrease in the apical surface area and pulls on the adjacent lateral epidermis, which subsequently moves dorsally. The pull by the amnioserosa becomes obvious in an elongation of the epidermal cells, especially of those in the first row. The contribution of the epidermal cell elongation has remained unclear to dorsal closure. Cell elongation may be a mere passive consequence or an active response to the pulling by the amnioserosa. Here, we found that the lateral epidermis actively responds. We analyzed tensions within tissues and cell junctions by laser ablation before and during dorsal closure, the elliptical and dorsal closure stages, respectively. Furthermore, we genetically and optochemically induced chronic and acute cell contraction, respectively. In this way, we found that tension in the epidermis increased during dorsal closure. A correspondingly increased tension was not observed at individual junctions, however. Junctional tension even decreased during dorsal closure in the epidermis. We strikingly observed a strong increase of the microtubule amount in the epidermis, while non-muscle myosin II increased in both tissues. Our data suggest that the epidermis actively antagonizes the pull from the amnioserosa during dorsal closure and the increased microtubules might help the epidermis bear part of the mechanical force. Frontiers Media S.A. 2022-05-16 /pmc/articles/PMC9148979/ /pubmed/35652100 http://dx.doi.org/10.3389/fcell.2022.865397 Text en Copyright © 2022 Lv, Zhang, Zhang, Großhans and Kong. 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
Lv, Zhiyi
Zhang, Na
Zhang, Xiaozhu
Großhans, Jörg
Kong, Deqing
The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure
title The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure
title_full The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure
title_fullStr The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure
title_full_unstemmed The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure
title_short The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure
title_sort lateral epidermis actively counteracts pulling by the amnioserosa during dorsal closure
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9148979/
https://www.ncbi.nlm.nih.gov/pubmed/35652100
http://dx.doi.org/10.3389/fcell.2022.865397
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