Cargando…

A Cdc42-mediated supracellular network drives polarized forces and Drosophila egg chamber extension

Actomyosin supracellular networks emerge during development and tissue repair. These cytoskeletal structures are able to generate large scale forces that can extensively remodel epithelia driving tissue buckling, closure and extension. How supracellular networks emerge, are controlled and mechanical...

Descripción completa

Detalles Bibliográficos
Autores principales: Popkova, Anna, Stone, Orrin J., Chen, Lin, Qin, Xiang, Liu, Chang, Liu, Jiaying, Belguise, Karine, Montell, Denise J., Hahn, Klaus M., Rauzi, Matteo, Wang, Xiaobo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7174421/
https://www.ncbi.nlm.nih.gov/pubmed/32317641
http://dx.doi.org/10.1038/s41467-020-15593-2
_version_ 1783524634556104704
author Popkova, Anna
Stone, Orrin J.
Chen, Lin
Qin, Xiang
Liu, Chang
Liu, Jiaying
Belguise, Karine
Montell, Denise J.
Hahn, Klaus M.
Rauzi, Matteo
Wang, Xiaobo
author_facet Popkova, Anna
Stone, Orrin J.
Chen, Lin
Qin, Xiang
Liu, Chang
Liu, Jiaying
Belguise, Karine
Montell, Denise J.
Hahn, Klaus M.
Rauzi, Matteo
Wang, Xiaobo
author_sort Popkova, Anna
collection PubMed
description Actomyosin supracellular networks emerge during development and tissue repair. These cytoskeletal structures are able to generate large scale forces that can extensively remodel epithelia driving tissue buckling, closure and extension. How supracellular networks emerge, are controlled and mechanically work still remain elusive. During Drosophila oogenesis, the egg chamber elongates along the anterior-posterior axis. Here we show that a dorsal-ventral polarized supracellular F-actin network, running around the egg chamber on the basal side of follicle cells, emerges from polarized intercellular filopodia that radiate from basal stress fibers and extend penetrating neighboring cell cortexes. Filopodia can be mechanosensitive and function as cell-cell anchoring sites. The small GTPase Cdc42 governs the formation and distribution of intercellular filopodia and stress fibers in follicle cells. Finally, our study shows that a Cdc42-dependent supracellular cytoskeletal network provides a scaffold integrating local oscillatory actomyosin contractions at the tissue scale to drive global polarized forces and tissue elongation.
format Online
Article
Text
id pubmed-7174421
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-71744212020-04-28 A Cdc42-mediated supracellular network drives polarized forces and Drosophila egg chamber extension Popkova, Anna Stone, Orrin J. Chen, Lin Qin, Xiang Liu, Chang Liu, Jiaying Belguise, Karine Montell, Denise J. Hahn, Klaus M. Rauzi, Matteo Wang, Xiaobo Nat Commun Article Actomyosin supracellular networks emerge during development and tissue repair. These cytoskeletal structures are able to generate large scale forces that can extensively remodel epithelia driving tissue buckling, closure and extension. How supracellular networks emerge, are controlled and mechanically work still remain elusive. During Drosophila oogenesis, the egg chamber elongates along the anterior-posterior axis. Here we show that a dorsal-ventral polarized supracellular F-actin network, running around the egg chamber on the basal side of follicle cells, emerges from polarized intercellular filopodia that radiate from basal stress fibers and extend penetrating neighboring cell cortexes. Filopodia can be mechanosensitive and function as cell-cell anchoring sites. The small GTPase Cdc42 governs the formation and distribution of intercellular filopodia and stress fibers in follicle cells. Finally, our study shows that a Cdc42-dependent supracellular cytoskeletal network provides a scaffold integrating local oscillatory actomyosin contractions at the tissue scale to drive global polarized forces and tissue elongation. Nature Publishing Group UK 2020-04-21 /pmc/articles/PMC7174421/ /pubmed/32317641 http://dx.doi.org/10.1038/s41467-020-15593-2 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
Popkova, Anna
Stone, Orrin J.
Chen, Lin
Qin, Xiang
Liu, Chang
Liu, Jiaying
Belguise, Karine
Montell, Denise J.
Hahn, Klaus M.
Rauzi, Matteo
Wang, Xiaobo
A Cdc42-mediated supracellular network drives polarized forces and Drosophila egg chamber extension
title A Cdc42-mediated supracellular network drives polarized forces and Drosophila egg chamber extension
title_full A Cdc42-mediated supracellular network drives polarized forces and Drosophila egg chamber extension
title_fullStr A Cdc42-mediated supracellular network drives polarized forces and Drosophila egg chamber extension
title_full_unstemmed A Cdc42-mediated supracellular network drives polarized forces and Drosophila egg chamber extension
title_short A Cdc42-mediated supracellular network drives polarized forces and Drosophila egg chamber extension
title_sort cdc42-mediated supracellular network drives polarized forces and drosophila egg chamber extension
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7174421/
https://www.ncbi.nlm.nih.gov/pubmed/32317641
http://dx.doi.org/10.1038/s41467-020-15593-2
work_keys_str_mv AT popkovaanna acdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT stoneorrinj acdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT chenlin acdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT qinxiang acdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT liuchang acdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT liujiaying acdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT belguisekarine acdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT montelldenisej acdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT hahnklausm acdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT rauzimatteo acdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT wangxiaobo acdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT popkovaanna cdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT stoneorrinj cdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT chenlin cdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT qinxiang cdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT liuchang cdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT liujiaying cdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT belguisekarine cdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT montelldenisej cdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT hahnklausm cdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT rauzimatteo cdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension
AT wangxiaobo cdc42mediatedsupracellularnetworkdrivespolarizedforcesanddrosophilaeggchamberextension