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

Bibliographic Details
Main Author: Silva, Ana M
Publication Date: 2016
Other Authors: Osório, Daniel S, Pereira, Antonio J, Maiato, Helder, Pinto, Inês Mendes, Rubinstein, Boris, Gassmann, Reto, Telley, Ivo Andreas, Carvalho, Ana Xavier
Format: Article
Language: eng
Source: Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)
Download full: http://hdl.handle.net/10400.7/727
Summary: 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 Robust gap repair in the contractile ring ensures timely completion of cytokinesiscytokinesisCaenorhabditis elegans embryosring constrictionCytokinesis 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.Rockefeller University PressARCASilva, Ana MOsório, Daniel SPereira, Antonio JMaiato, HelderPinto, Inês MendesRubinstein, BorisGassmann, RetoTelley, Ivo AndreasCarvalho, Ana Xavier2017-06-06T00:30:09Z2016-12-192016-12-19T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.7/727eng10.1083/jcb.201605080info:eu-repo/semantics/openAccessreponame:Repositórios Científicos de Acesso Aberto de Portugal (RCAAP)instname:FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiainstacron:RCAAP2024-11-21T14:21:47Zoai:arca.igc.gulbenkian.pt:10400.7/727Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireinfo@rcaap.ptopendoar:https://opendoar.ac.uk/repository/71602025-05-28T19:15:26.504336Repositórios Científicos de Acesso Aberto de Portugal (RCAAP) - FCCN, serviços digitais da FCT – Fundação para a Ciência e a Tecnologiafalse
dc.title.none.fl_str_mv 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
spellingShingle Robust gap repair in the contractile ring ensures timely completion of cytokinesis
Silva, Ana M
cytokinesis
Caenorhabditis elegans embryos
ring constriction
title_short 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_sort Robust gap repair in the contractile ring ensures timely completion of cytokinesis
author Silva, Ana M
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_role author
author2 Osório, Daniel S
Pereira, Antonio J
Maiato, Helder
Pinto, Inês Mendes
Rubinstein, Boris
Gassmann, Reto
Telley, Ivo Andreas
Carvalho, Ana Xavier
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv ARCA
dc.contributor.author.fl_str_mv Silva, Ana M
Osório, Daniel S
Pereira, Antonio J
Maiato, Helder
Pinto, Inês Mendes
Rubinstein, Boris
Gassmann, Reto
Telley, Ivo Andreas
Carvalho, Ana Xavier
dc.subject.por.fl_str_mv cytokinesis
Caenorhabditis elegans embryos
ring constriction
topic cytokinesis
Caenorhabditis elegans embryos
ring constriction
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.
publishDate 2016
dc.date.none.fl_str_mv 2016-12-19
2016-12-19T00:00:00Z
2017-06-06T00:30:09Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
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dc.identifier.uri.fl_str_mv http://hdl.handle.net/10400.7/727
url http://hdl.handle.net/10400.7/727
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv 10.1083/jcb.201605080
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dc.publisher.none.fl_str_mv Rockefeller University Press
publisher.none.fl_str_mv Rockefeller University Press
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