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Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms

Epithelial folding transforms simple sheets of cells into complex three-dimensional tissues and organs during animal development. Epithelial folding has mainly been attributed to mechanical forces generated by an apically localized actomyosin network, however, contributions of forces generated at ba...

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Autores principales: Sui, Liyuan, Alt, Silvanus, Weigert, Martin, Dye, Natalie, Eaton, Suzanne, Jug, Florian, Myers, Eugene W., Jülicher, Frank, Salbreux, Guillaume, Dahmann, Christian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6218478/
https://www.ncbi.nlm.nih.gov/pubmed/30397306
http://dx.doi.org/10.1038/s41467-018-06497-3
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author Sui, Liyuan
Alt, Silvanus
Weigert, Martin
Dye, Natalie
Eaton, Suzanne
Jug, Florian
Myers, Eugene W.
Jülicher, Frank
Salbreux, Guillaume
Dahmann, Christian
author_facet Sui, Liyuan
Alt, Silvanus
Weigert, Martin
Dye, Natalie
Eaton, Suzanne
Jug, Florian
Myers, Eugene W.
Jülicher, Frank
Salbreux, Guillaume
Dahmann, Christian
author_sort Sui, Liyuan
collection PubMed
description Epithelial folding transforms simple sheets of cells into complex three-dimensional tissues and organs during animal development. Epithelial folding has mainly been attributed to mechanical forces generated by an apically localized actomyosin network, however, contributions of forces generated at basal and lateral cell surfaces remain largely unknown. Here we show that a local decrease of basal tension and an increased lateral tension, but not apical constriction, drive the formation of two neighboring folds in developing Drosophila wing imaginal discs. Spatially defined reduction of extracellular matrix density results in local decrease of basal tension in the first fold; fluctuations in F-actin lead to increased lateral tension in the second fold. Simulations using a 3D vertex model show that the two distinct mechanisms can drive epithelial folding. Our combination of lateral and basal tension measurements with a mechanical tissue model reveals how simple modulations of surface and edge tension drive complex three-dimensional morphological changes.
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spelling pubmed-62184782018-11-07 Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms Sui, Liyuan Alt, Silvanus Weigert, Martin Dye, Natalie Eaton, Suzanne Jug, Florian Myers, Eugene W. Jülicher, Frank Salbreux, Guillaume Dahmann, Christian Nat Commun Article Epithelial folding transforms simple sheets of cells into complex three-dimensional tissues and organs during animal development. Epithelial folding has mainly been attributed to mechanical forces generated by an apically localized actomyosin network, however, contributions of forces generated at basal and lateral cell surfaces remain largely unknown. Here we show that a local decrease of basal tension and an increased lateral tension, but not apical constriction, drive the formation of two neighboring folds in developing Drosophila wing imaginal discs. Spatially defined reduction of extracellular matrix density results in local decrease of basal tension in the first fold; fluctuations in F-actin lead to increased lateral tension in the second fold. Simulations using a 3D vertex model show that the two distinct mechanisms can drive epithelial folding. Our combination of lateral and basal tension measurements with a mechanical tissue model reveals how simple modulations of surface and edge tension drive complex three-dimensional morphological changes. Nature Publishing Group UK 2018-11-05 /pmc/articles/PMC6218478/ /pubmed/30397306 http://dx.doi.org/10.1038/s41467-018-06497-3 Text en © The Author(s) 2018 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
Sui, Liyuan
Alt, Silvanus
Weigert, Martin
Dye, Natalie
Eaton, Suzanne
Jug, Florian
Myers, Eugene W.
Jülicher, Frank
Salbreux, Guillaume
Dahmann, Christian
Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms
title Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms
title_full Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms
title_fullStr Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms
title_full_unstemmed Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms
title_short Differential lateral and basal tension drive folding of Drosophila wing discs through two distinct mechanisms
title_sort differential lateral and basal tension drive folding of drosophila wing discs through two distinct mechanisms
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6218478/
https://www.ncbi.nlm.nih.gov/pubmed/30397306
http://dx.doi.org/10.1038/s41467-018-06497-3
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