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Robust gap repair in the contractile ring ensures timely completion of cytokinesis

Cytokinesis in animal cells requires the constriction of an actomyosin contractile ring, whose architecture and mechanism remain poorly understood. We use laser microsurgery to explore the biophysical properties of constricting rings in Caenorhabditis elegans embryos. Laser cutting causes rings to s...

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Autores principales: Silva, Ana M., Osório, Daniel S., Pereira, Antonio J., Maiato, Helder, Pinto, Inês Mendes, Rubinstein, Boris, Gassmann, Reto, Telley, Ivo Andreas, Carvalho, Ana Xavier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5166501/
https://www.ncbi.nlm.nih.gov/pubmed/27974482
http://dx.doi.org/10.1083/jcb.201605080
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author Silva, Ana M.
Osório, Daniel S.
Pereira, Antonio J.
Maiato, Helder
Pinto, Inês Mendes
Rubinstein, Boris
Gassmann, Reto
Telley, Ivo Andreas
Carvalho, Ana Xavier
author_facet Silva, Ana M.
Osório, Daniel S.
Pereira, Antonio J.
Maiato, Helder
Pinto, Inês Mendes
Rubinstein, Boris
Gassmann, Reto
Telley, Ivo Andreas
Carvalho, Ana Xavier
author_sort Silva, Ana M.
collection PubMed
description Cytokinesis in animal cells requires the constriction of an actomyosin contractile ring, whose architecture and mechanism remain poorly understood. We use laser microsurgery to explore the biophysical properties of constricting rings in Caenorhabditis elegans embryos. Laser cutting causes rings to snap open. However, instead of disintegrating, ring topology recovers and constriction proceeds. In response to severing, a finite gap forms and is repaired by recruitment of new material in an actin polymerization–dependent manner. An open ring is able to constrict, and rings repair from successive cuts. After gap repair, an increase in constriction velocity allows cytokinesis to complete at the same time as controls. Our analysis demonstrates that tension in the ring increases while net cortical tension at the site of ingression decreases throughout constriction and suggests that cytokinesis is accomplished by contractile modules that assemble and contract autonomously, enabling local repair of the actomyosin network. Consequently, cytokinesis is a highly robust process impervious to discontinuities in contractile ring structure.
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spelling pubmed-51665012017-06-19 Robust gap repair in the contractile ring ensures timely completion of cytokinesis Silva, Ana M. Osório, Daniel S. Pereira, Antonio J. Maiato, Helder Pinto, Inês Mendes Rubinstein, Boris Gassmann, Reto Telley, Ivo Andreas Carvalho, Ana Xavier J Cell Biol Research Articles Cytokinesis in animal cells requires the constriction of an actomyosin contractile ring, whose architecture and mechanism remain poorly understood. We use laser microsurgery to explore the biophysical properties of constricting rings in Caenorhabditis elegans embryos. Laser cutting causes rings to snap open. However, instead of disintegrating, ring topology recovers and constriction proceeds. In response to severing, a finite gap forms and is repaired by recruitment of new material in an actin polymerization–dependent manner. An open ring is able to constrict, and rings repair from successive cuts. After gap repair, an increase in constriction velocity allows cytokinesis to complete at the same time as controls. Our analysis demonstrates that tension in the ring increases while net cortical tension at the site of ingression decreases throughout constriction and suggests that cytokinesis is accomplished by contractile modules that assemble and contract autonomously, enabling local repair of the actomyosin network. Consequently, cytokinesis is a highly robust process impervious to discontinuities in contractile ring structure. The Rockefeller University Press 2016-12-19 /pmc/articles/PMC5166501/ /pubmed/27974482 http://dx.doi.org/10.1083/jcb.201605080 Text en © 2016 Silva et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Research Articles
Silva, Ana M.
Osório, Daniel S.
Pereira, Antonio J.
Maiato, Helder
Pinto, Inês Mendes
Rubinstein, Boris
Gassmann, Reto
Telley, Ivo Andreas
Carvalho, Ana Xavier
Robust gap repair in the contractile ring ensures timely completion of cytokinesis
title Robust gap repair in the contractile ring ensures timely completion of cytokinesis
title_full Robust gap repair in the contractile ring ensures timely completion of cytokinesis
title_fullStr Robust gap repair in the contractile ring ensures timely completion of cytokinesis
title_full_unstemmed Robust gap repair in the contractile ring ensures timely completion of cytokinesis
title_short Robust gap repair in the contractile ring ensures timely completion of cytokinesis
title_sort robust gap repair in the contractile ring ensures timely completion of cytokinesis
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5166501/
https://www.ncbi.nlm.nih.gov/pubmed/27974482
http://dx.doi.org/10.1083/jcb.201605080
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