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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...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The Rockefeller University Press
2016
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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. |
format | Online Article Text |
id | pubmed-5166501 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2016 |
publisher | The Rockefeller University Press |
record_format | MEDLINE/PubMed |
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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