Cargando…

Assembly and positioning of actomyosin rings by contractility and planar cell polarity

The actomyosin cytoskeleton is a primary force-generating mechanism in morphogenesis, thus a robust spatial control of cytoskeletal positioning is essential. In this report, we demonstrate that actomyosin contractility and planar cell polarity (PCP) interact in post-mitotic Ciona notochord cells to...

Descripción completa

Detalles Bibliográficos
Autores principales: Sehring, Ivonne M, Recho, Pierre, Denker, Elsa, Kourakis, Matthew, Mathiesen, Birthe, Hannezo, Edouard, Dong, Bo, Jiang, Di
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4612727/
https://www.ncbi.nlm.nih.gov/pubmed/26486861
http://dx.doi.org/10.7554/eLife.09206
_version_ 1782396210226659328
author Sehring, Ivonne M
Recho, Pierre
Denker, Elsa
Kourakis, Matthew
Mathiesen, Birthe
Hannezo, Edouard
Dong, Bo
Jiang, Di
author_facet Sehring, Ivonne M
Recho, Pierre
Denker, Elsa
Kourakis, Matthew
Mathiesen, Birthe
Hannezo, Edouard
Dong, Bo
Jiang, Di
author_sort Sehring, Ivonne M
collection PubMed
description The actomyosin cytoskeleton is a primary force-generating mechanism in morphogenesis, thus a robust spatial control of cytoskeletal positioning is essential. In this report, we demonstrate that actomyosin contractility and planar cell polarity (PCP) interact in post-mitotic Ciona notochord cells to self-assemble and reposition actomyosin rings, which play an essential role for cell elongation. Intriguingly, rings always form at the cells′ anterior edge before migrating towards the center as contractility increases, reflecting a novel dynamical property of the cortex. Our drug and genetic manipulations uncover a tug-of-war between contractility, which localizes cortical flows toward the equator and PCP, which tries to reposition them. We develop a simple model of the physical forces underlying this tug-of-war, which quantitatively reproduces our results. We thus propose a quantitative framework for dissecting the relative contribution of contractility and PCP to the self-assembly and repositioning of cytoskeletal structures, which should be applicable to other morphogenetic events. DOI: http://dx.doi.org/10.7554/eLife.09206.001
format Online
Article
Text
id pubmed-4612727
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-46127272015-10-22 Assembly and positioning of actomyosin rings by contractility and planar cell polarity Sehring, Ivonne M Recho, Pierre Denker, Elsa Kourakis, Matthew Mathiesen, Birthe Hannezo, Edouard Dong, Bo Jiang, Di eLife Biophysics and Structural Biology The actomyosin cytoskeleton is a primary force-generating mechanism in morphogenesis, thus a robust spatial control of cytoskeletal positioning is essential. In this report, we demonstrate that actomyosin contractility and planar cell polarity (PCP) interact in post-mitotic Ciona notochord cells to self-assemble and reposition actomyosin rings, which play an essential role for cell elongation. Intriguingly, rings always form at the cells′ anterior edge before migrating towards the center as contractility increases, reflecting a novel dynamical property of the cortex. Our drug and genetic manipulations uncover a tug-of-war between contractility, which localizes cortical flows toward the equator and PCP, which tries to reposition them. We develop a simple model of the physical forces underlying this tug-of-war, which quantitatively reproduces our results. We thus propose a quantitative framework for dissecting the relative contribution of contractility and PCP to the self-assembly and repositioning of cytoskeletal structures, which should be applicable to other morphogenetic events. DOI: http://dx.doi.org/10.7554/eLife.09206.001 eLife Sciences Publications, Ltd 2015-10-21 /pmc/articles/PMC4612727/ /pubmed/26486861 http://dx.doi.org/10.7554/eLife.09206 Text en © 2015, Sehring et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Biophysics and Structural Biology
Sehring, Ivonne M
Recho, Pierre
Denker, Elsa
Kourakis, Matthew
Mathiesen, Birthe
Hannezo, Edouard
Dong, Bo
Jiang, Di
Assembly and positioning of actomyosin rings by contractility and planar cell polarity
title Assembly and positioning of actomyosin rings by contractility and planar cell polarity
title_full Assembly and positioning of actomyosin rings by contractility and planar cell polarity
title_fullStr Assembly and positioning of actomyosin rings by contractility and planar cell polarity
title_full_unstemmed Assembly and positioning of actomyosin rings by contractility and planar cell polarity
title_short Assembly and positioning of actomyosin rings by contractility and planar cell polarity
title_sort assembly and positioning of actomyosin rings by contractility and planar cell polarity
topic Biophysics and Structural Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4612727/
https://www.ncbi.nlm.nih.gov/pubmed/26486861
http://dx.doi.org/10.7554/eLife.09206
work_keys_str_mv AT sehringivonnem assemblyandpositioningofactomyosinringsbycontractilityandplanarcellpolarity
AT rechopierre assemblyandpositioningofactomyosinringsbycontractilityandplanarcellpolarity
AT denkerelsa assemblyandpositioningofactomyosinringsbycontractilityandplanarcellpolarity
AT kourakismatthew assemblyandpositioningofactomyosinringsbycontractilityandplanarcellpolarity
AT mathiesenbirthe assemblyandpositioningofactomyosinringsbycontractilityandplanarcellpolarity
AT hannezoedouard assemblyandpositioningofactomyosinringsbycontractilityandplanarcellpolarity
AT dongbo assemblyandpositioningofactomyosinringsbycontractilityandplanarcellpolarity
AT jiangdi assemblyandpositioningofactomyosinringsbycontractilityandplanarcellpolarity