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The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces

Three-dimensional collective epithelial rotation around a given axis represents a coordinated cellular movement driving tissue morphogenesis and transformation. Questions regarding these behaviors and their relationship with substrate curvatures are intimately linked to spontaneous active matter pro...

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Autores principales: Glentis, Alexandros, Blanch-Mercader, Carles, Balasubramaniam, Lakshmi, Saw, Thuan Beng, d’Alessandro, Joseph, Janel, Sebastien, Douanier, Audrey, Delaval, Benedicte, Lafont, Frank, Lim, Chwee Teck, Delacour, Delphine, Prost, Jacques, Xi, Wang, Ladoux, Benoit
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9473582/
https://www.ncbi.nlm.nih.gov/pubmed/36103541
http://dx.doi.org/10.1126/sciadv.abn5406
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author Glentis, Alexandros
Blanch-Mercader, Carles
Balasubramaniam, Lakshmi
Saw, Thuan Beng
d’Alessandro, Joseph
Janel, Sebastien
Douanier, Audrey
Delaval, Benedicte
Lafont, Frank
Lim, Chwee Teck
Delacour, Delphine
Prost, Jacques
Xi, Wang
Ladoux, Benoit
author_facet Glentis, Alexandros
Blanch-Mercader, Carles
Balasubramaniam, Lakshmi
Saw, Thuan Beng
d’Alessandro, Joseph
Janel, Sebastien
Douanier, Audrey
Delaval, Benedicte
Lafont, Frank
Lim, Chwee Teck
Delacour, Delphine
Prost, Jacques
Xi, Wang
Ladoux, Benoit
author_sort Glentis, Alexandros
collection PubMed
description Three-dimensional collective epithelial rotation around a given axis represents a coordinated cellular movement driving tissue morphogenesis and transformation. Questions regarding these behaviors and their relationship with substrate curvatures are intimately linked to spontaneous active matter processes and to vital morphogenetic and embryonic processes. Here, using interdisciplinary approaches, we study the dynamics of epithelial layers lining different cylindrical surfaces. We observe large-scale, persistent, and circumferential rotation in both concavely and convexly curved cylindrical tissues. While epithelia of inverse curvature show an orthogonal switch in actomyosin network orientation and opposite apicobasal polarities, their rotational movements emerge and vary similarly within a common curvature window. We further reveal that this persisting rotation requires stable cell-cell adhesion and Rac-1–dependent cell polarity. Using an active polar gel model, we unveil the different relationships of collective cell polarity and actin alignment with curvatures, which lead to coordinated rotational behavior despite the inverted curvature and cytoskeleton order.
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spelling pubmed-94735822022-09-29 The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces Glentis, Alexandros Blanch-Mercader, Carles Balasubramaniam, Lakshmi Saw, Thuan Beng d’Alessandro, Joseph Janel, Sebastien Douanier, Audrey Delaval, Benedicte Lafont, Frank Lim, Chwee Teck Delacour, Delphine Prost, Jacques Xi, Wang Ladoux, Benoit Sci Adv Biomedicine and Life Sciences Three-dimensional collective epithelial rotation around a given axis represents a coordinated cellular movement driving tissue morphogenesis and transformation. Questions regarding these behaviors and their relationship with substrate curvatures are intimately linked to spontaneous active matter processes and to vital morphogenetic and embryonic processes. Here, using interdisciplinary approaches, we study the dynamics of epithelial layers lining different cylindrical surfaces. We observe large-scale, persistent, and circumferential rotation in both concavely and convexly curved cylindrical tissues. While epithelia of inverse curvature show an orthogonal switch in actomyosin network orientation and opposite apicobasal polarities, their rotational movements emerge and vary similarly within a common curvature window. We further reveal that this persisting rotation requires stable cell-cell adhesion and Rac-1–dependent cell polarity. Using an active polar gel model, we unveil the different relationships of collective cell polarity and actin alignment with curvatures, which lead to coordinated rotational behavior despite the inverted curvature and cytoskeleton order. American Association for the Advancement of Science 2022-09-14 /pmc/articles/PMC9473582/ /pubmed/36103541 http://dx.doi.org/10.1126/sciadv.abn5406 Text en Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Biomedicine and Life Sciences
Glentis, Alexandros
Blanch-Mercader, Carles
Balasubramaniam, Lakshmi
Saw, Thuan Beng
d’Alessandro, Joseph
Janel, Sebastien
Douanier, Audrey
Delaval, Benedicte
Lafont, Frank
Lim, Chwee Teck
Delacour, Delphine
Prost, Jacques
Xi, Wang
Ladoux, Benoit
The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces
title The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces
title_full The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces
title_fullStr The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces
title_full_unstemmed The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces
title_short The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces
title_sort emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces
topic Biomedicine and Life Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9473582/
https://www.ncbi.nlm.nih.gov/pubmed/36103541
http://dx.doi.org/10.1126/sciadv.abn5406
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