Literature DB >> 35652100

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

Zhiyi Lv1, Na Zhang2, Xiaozhu Zhang3,4,5, Jörg Großhans2, Deqing Kong2.   

Abstract

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.
Copyright © 2022 Lv, Zhang, Zhang, Großhans and Kong.

Entities:  

Keywords:  cell shape change; dorsal closure; microtubules; morphogenesis; optochemistry; tissue mechanics

Year:  2022        PMID: 35652100      PMCID: PMC9148979          DOI: 10.3389/fcell.2022.865397

Source DB:  PubMed          Journal:  Front Cell Dev Biol        ISSN: 2296-634X


  58 in total

1.  Forces for morphogenesis investigated with laser microsurgery and quantitative modeling.

Authors:  M Shane Hutson; Yoichiro Tokutake; Ming-Shien Chang; James W Bloor; Stephanos Venakides; Daniel P Kiehart; Glenn S Edwards
Journal:  Science       Date:  2003-02-06       Impact factor: 47.728

2.  The cytoskeletal protein α-catenin unfurls upon binding to vinculin.

Authors:  Erumbi S Rangarajan; Tina Izard
Journal:  J Biol Chem       Date:  2012-04-06       Impact factor: 5.157

3.  From the Cover: Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering.

Authors:  Juan Huang; Wenke Zhou; Wei Dong; Annie M Watson; Yang Hong
Journal:  Proc Natl Acad Sci U S A       Date:  2009-05-08       Impact factor: 11.205

Review 4.  Programmed and self-organized flow of information during morphogenesis.

Authors:  Claudio Collinet; Thomas Lecuit
Journal:  Nat Rev Mol Cell Biol       Date:  2021-01-22       Impact factor: 94.444

5.  Amnioserosa cell constriction but not epidermal actin cable tension autonomously drives dorsal closure.

Authors:  Laurynas Pasakarnis; Erich Frei; Emmanuel Caussinus; Markus Affolter; Damian Brunner
Journal:  Nat Cell Biol       Date:  2016-10-17       Impact factor: 28.824

6.  Force-dependent conformational switch of α-catenin controls vinculin binding.

Authors:  Mingxi Yao; Wu Qiu; Ruchuan Liu; Artem K Efremov; Peiwen Cong; Rima Seddiki; Manon Payre; Chwee Teck Lim; Benoit Ladoux; René-Marc Mège; Jie Yan
Journal:  Nat Commun       Date:  2014-07-31       Impact factor: 14.919

Review 7.  Biodiversity-based development and evolution: the emerging research systems in model and non-model organisms.

Authors:  Long Zhao; Feng Gao; Shan Gao; Yujun Liang; Hongan Long; Zhiyi Lv; Ying Su; Naihao Ye; Liusuo Zhang; Chengtian Zhao; Xiaoyu Wang; Weibo Song; Shicui Zhang; Bo Dong
Journal:  Sci China Life Sci       Date:  2021-04-22       Impact factor: 6.038

8.  The spectraplakin Short stop is an essential microtubule regulator involved in epithelial closure in Drosophila.

Authors:  Zsanett Takács; Ferenc Jankovics; Péter Vilmos; Péter Lénárt; Katja Röper; Miklós Erdélyi
Journal:  J Cell Sci       Date:  2017-01-06       Impact factor: 5.285

Review 9.  Planar Cell Polarity and E-Cadherin in Tissue-Scale Shape Changes in Drosophila Embryos.

Authors:  Deqing Kong; Jörg Großhans
Journal:  Front Cell Dev Biol       Date:  2020-12-23
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