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Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis
Morphogenetic epithelial movement occurs during embryogenesis and drives complex tissue formation. However, how epithelial cells coordinate their unidirectional movement while maintaining epithelial integrity is unclear. Here we propose a novel mechanism for collective epithelial cell movement based...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4682055/ https://www.ncbi.nlm.nih.gov/pubmed/26656655 http://dx.doi.org/10.1038/ncomms10074 |
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author | Sato, Katsuhiko Hiraiwa, Tetsuya Maekawa, Emi Isomura, Ayako Shibata, Tatsuo Kuranaga, Erina |
author_facet | Sato, Katsuhiko Hiraiwa, Tetsuya Maekawa, Emi Isomura, Ayako Shibata, Tatsuo Kuranaga, Erina |
author_sort | Sato, Katsuhiko |
collection | PubMed |
description | Morphogenetic epithelial movement occurs during embryogenesis and drives complex tissue formation. However, how epithelial cells coordinate their unidirectional movement while maintaining epithelial integrity is unclear. Here we propose a novel mechanism for collective epithelial cell movement based on Drosophila genitalia rotation, in which epithelial tissue rotates clockwise around the genitalia. We found that this cell movement occurs autonomously and requires myosin II. The moving cells exhibit repeated left–right-biased junction remodelling, while maintaining adhesion with their neighbours, in association with a polarized myosin II distribution. Reducing myosinID, known to cause counter-clockwise epithelial-tissue movement, reverses the myosin II distribution. Numerical simulations revealed that a left–right asymmetry in cell intercalation is sufficient to induce unidirectional cellular movement. The cellular movement direction is also associated with planar cell-shape chirality. These findings support a model in which left–right asymmetric cell intercalation within an epithelial sheet drives collective cellular movement in the same direction. |
format | Online Article Text |
id | pubmed-4682055 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | Nature Publishing Group |
record_format | MEDLINE/PubMed |
spelling | pubmed-46820552015-12-29 Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis Sato, Katsuhiko Hiraiwa, Tetsuya Maekawa, Emi Isomura, Ayako Shibata, Tatsuo Kuranaga, Erina Nat Commun Article Morphogenetic epithelial movement occurs during embryogenesis and drives complex tissue formation. However, how epithelial cells coordinate their unidirectional movement while maintaining epithelial integrity is unclear. Here we propose a novel mechanism for collective epithelial cell movement based on Drosophila genitalia rotation, in which epithelial tissue rotates clockwise around the genitalia. We found that this cell movement occurs autonomously and requires myosin II. The moving cells exhibit repeated left–right-biased junction remodelling, while maintaining adhesion with their neighbours, in association with a polarized myosin II distribution. Reducing myosinID, known to cause counter-clockwise epithelial-tissue movement, reverses the myosin II distribution. Numerical simulations revealed that a left–right asymmetry in cell intercalation is sufficient to induce unidirectional cellular movement. The cellular movement direction is also associated with planar cell-shape chirality. These findings support a model in which left–right asymmetric cell intercalation within an epithelial sheet drives collective cellular movement in the same direction. Nature Publishing Group 2015-12-10 /pmc/articles/PMC4682055/ /pubmed/26656655 http://dx.doi.org/10.1038/ncomms10074 Text en Copyright © 2015, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved. http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ |
spellingShingle | Article Sato, Katsuhiko Hiraiwa, Tetsuya Maekawa, Emi Isomura, Ayako Shibata, Tatsuo Kuranaga, Erina Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis |
title | Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis |
title_full | Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis |
title_fullStr | Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis |
title_full_unstemmed | Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis |
title_short | Left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis |
title_sort | left–right asymmetric cell intercalation drives directional collective cell movement in epithelial morphogenesis |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4682055/ https://www.ncbi.nlm.nih.gov/pubmed/26656655 http://dx.doi.org/10.1038/ncomms10074 |
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