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Journal of Cell BiologyVolume 215, Issue 6, 2016, Pages 789-799

Robust gap repair in the contractile ring ensures timely completion of cytokinesis(Article)(Open Access)

  • Silva, A.M.,
  • Osório, D.S.,
  • Pereira, A.J.,
  • Maiato, H.,
  • Pinto, I.M.,
  • Rubinstein, B.,
  • Gassmann, R.,
  • Telley, I.A.,
  • Carvalho, A.X.
  • View Correspondence (jump link)
  • aInstituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, 4200-135, Portugal
  • bInstituto de Biologia Molecular e Celular, Porto, 4200-135, Portugal
  • cInternational Iberian Nanotechnology Laboratory, Braga, 4715-330, Portugal
  • dStowers Institute for Medical Research, Kansas City, MO 64110, United States
  • eInstituto Gulbenkian de Ciência, Fundação Calouste Gulbenkian, Oeiras, 2780-156, Portugal

Abstract

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. © 2016 Silva et al.

Indexed keywords

EMTREE drug terms:contractile proteincontractile ringmyosin adenosine triphosphataseunclassified drugfused heterocyclic ringslatrunculin Amyosin adenosine triphosphatasethiazolidine derivative
EMTREE medical terms:actin polymerizationamnion bandArticleCaenorhabditis eleganscontrolled studycytokinesisembryolaser surgerymicrosurgerynonhumanpriority journaltensionanimalcytologydrug effectsembryologylasermetabolismnonmammalian embryo
MeSH:ActomyosinAnimalsBridged Bicyclo Compounds, HeterocyclicCaenorhabditis elegansCytokinesisEmbryo, NonmammalianLasersMicrosurgeryThiazolidines

Chemicals and CAS Registry Numbers:

myosin adenosine triphosphatase; latrunculin A, 76343-93-6;

Actomyosin; Bridged Bicyclo Compounds, Heterocyclic; latrunculin A; Thiazolidines

  • ISSN: 00219525
  • CODEN: JCLBA
  • Source Type: Journal
  • Original language: English
  • DOI: 10.1083/jcb.201605080
  • PubMed ID: 27974482
  • Document Type: Article
  • Publisher: Rockefeller University Press

  Carvalho, A.X.; Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal;
© Copyright 2017 Elsevier B.V., All rights reserved.

Cited by 8 documents

Mangione, M.C. , Gould, K.L.
Molecular form and function of the cytokinetic ring
(2019) Journal of Cell Science
Leite, J. , Osorio, D.S. , Sobral, A.F.
Network contractility during cytokinesis—from molecular to global views
(2019) Biomolecules
Chan, F.-Y. , Silva, A.M. , Saramago, J.
The ARP2/3 complex prevents excessive formin activity during cytokinesis
(2019) Molecular Biology of the Cell
View details of all 8 citations
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