Robust gap repair in the contractile ring ensures timely completion of cytokinesis
Autor(a) principal: | |
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Data de Publicação: | 2016 |
Outros Autores: | , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
Texto Completo: | http://hdl.handle.net/10400.7/727 |
Resumo: | 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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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.European Research Council grant: (640553); Fundo Europeu de Desenvolvimento Regional (FEDER) funds: (Operational Competitiveness Program - COMPETE); Fundação para a Ciência e a Tecnologia grant:(NORTE-07-0124-FEDER-000003); Fundação Luso-Americana para o Desenvolvimento (Life Science 2020); Louis-Jeantet Young Investigator Award; European Social Fund (Programa Operacional Temático Potencial Type 4.2); Programa Operacional Regional do Norte (Quadro de Referência Estratégico Nacional - FEDER).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/10400.7/727engRobust gap repair in the contractile ring ensures timely completion of cytokinesis Ana M. Silva, Daniel S. Osório, Antonio J. Pereira, Helder Maiato, Inês Mendes Pinto, Boris Rubinstein, Reto Gassmann, Ivo Andreas Telley, Ana Xavier Carvalho J Cell Biol Dec 2016, 215 (6) 789-799; DOI: 10.1083/jcb.20160508010.1083/jcb.201605080info:eu-repo/semantics/embargoedAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2022-11-29T14:35:07Zoai:arca.igc.gulbenkian.pt:10400.7/727Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T16:11:57.474973Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse |
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 |
format |
article |
status_str |
publishedVersion |
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 |
Robust gap repair in the contractile ring ensures timely completion of cytokinesis Ana M. Silva, Daniel S. Osório, Antonio J. Pereira, Helder Maiato, Inês Mendes Pinto, Boris Rubinstein, Reto Gassmann, Ivo Andreas Telley, Ana Xavier Carvalho J Cell Biol Dec 2016, 215 (6) 789-799; DOI: 10.1083/jcb.201605080 10.1083/jcb.201605080 |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/embargoedAccess |
eu_rights_str_mv |
embargoedAccess |
dc.format.none.fl_str_mv |
application/pdf |
dc.publisher.none.fl_str_mv |
Rockefeller University Press |
publisher.none.fl_str_mv |
Rockefeller University Press |
dc.source.none.fl_str_mv |
reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação instacron:RCAAP |
instname_str |
Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
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RCAAP |
institution |
RCAAP |
reponame_str |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
collection |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
repository.name.fl_str_mv |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
repository.mail.fl_str_mv |
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1799130574748647424 |