Cargando…
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...
Autores principales: | , , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1784789533051584512 |
---|---|
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. |
format | Online Article Text |
id | pubmed-9473582 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | American Association for the Advancement of Science |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT glentisalexandros theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT blanchmercadercarles theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT balasubramaniamlakshmi theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT sawthuanbeng theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT dalessandrojoseph theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT janelsebastien theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT douanieraudrey theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT delavalbenedicte theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT lafontfrank theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT limchweeteck theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT delacourdelphine theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT prostjacques theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT xiwang theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT ladouxbenoit theemergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT glentisalexandros emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT blanchmercadercarles emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT balasubramaniamlakshmi emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT sawthuanbeng emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT dalessandrojoseph emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT janelsebastien emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT douanieraudrey emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT delavalbenedicte emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT lafontfrank emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT limchweeteck emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT delacourdelphine emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT prostjacques emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT xiwang emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces AT ladouxbenoit emergenceofspontaneouscoordinatedepithelialrotationoncylindricalcurvedsurfaces |