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

Detalhes bibliográficos
Autor(a) principal: Silva, Ana M
Data de Publicação: 2016
Outros Autores: Osório, Daniel S, Pereira, Antonio J, Maiato, Helder, Pinto, Inês Mendes, Rubinstein, Boris, Gassmann, Reto, Telley, Ivo Andreas, Carvalho, Ana Xavier
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.
id RCAP_4851675fa9dc6cc4bb1009a8b5ffca91
oai_identifier_str oai:arca.igc.gulbenkian.pt:10400.7/727
network_acronym_str RCAP
network_name_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository_id_str 7160
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.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
instacron_str 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
_version_ 1799130574748647424