Literature DB >> 28289130

Inhibition of ectopic microtubule assembly by the kinesin-13 KLP-7 prevents chromosome segregation and cytokinesis defects in oocytes.

Emmanuelle Gigant1, Marine Stefanutti1, Kimberley Laband1, Agata Gluszek-Kustusz2, Frances Edwards1, Benjamin Lacroix1, Gilliane Maton1, Julie C Canman3, Julie P I Welburn2, Julien Dumont4.   

Abstract

In most species, oocytes lack centrosomes. Accurate meiotic spindle assembly and chromosome segregation - essential to prevent miscarriage or developmental defects - thus occur through atypical mechanisms that are not well characterized. Using quantitative in vitro and in vivo functional assays in the C. elegans oocyte, we provide novel evidence that the kinesin-13 KLP-7 promotes destabilization of the whole cellular microtubule network. By counteracting ectopic microtubule assembly and disorganization of the microtubule network, this function is strictly required for spindle organization, chromosome segregation and cytokinesis in meiotic cells. Strikingly, when centrosome activity was experimentally reduced, the absence of KLP-7 or the mammalian kinesin-13 protein MCAK (KIF2C) also resulted in ectopic microtubule asters during mitosis in C. elegans zygotes or HeLa cells, respectively. Our results highlight the general function of kinesin-13 microtubule depolymerases in preventing ectopic, spontaneous microtubule assembly when centrosome activity is defective or absent, which would otherwise lead to spindle microtubule disorganization and aneuploidy.
© 2017. Published by The Company of Biologists Ltd.

Entities:  

Keywords:  Chromosome segregation; Cytoskeleton; Meiotic spindle; Microtubule depolymerase; Microtubule dynamics; Polar body extrusion

Mesh:

Substances:

Year:  2017        PMID: 28289130      PMCID: PMC5450848          DOI: 10.1242/dev.147504

Source DB:  PubMed          Journal:  Development        ISSN: 0950-1991            Impact factor:   6.868


  61 in total

1.  Two mitotic kinesins cooperate to drive sister chromatid separation during anaphase.

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Journal:  Nature       Date:  2003-12-14       Impact factor: 49.962

2.  MCAK regulates chromosome alignment but is not necessary for preventing aneuploidy in mouse oocyte meiosis I.

Authors:  Crista Illingworth; Negar Pirmadjid; Paul Serhal; Katie Howe; Greg Fitzharris
Journal:  Development       Date:  2010-05-26       Impact factor: 6.868

3.  Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes.

Authors:  Melina Schuh; Jan Ellenberg
Journal:  Cell       Date:  2007-08-10       Impact factor: 41.582

Review 4.  Meiosis: an overview of key differences from mitosis.

Authors:  Hiroyuki Ohkura
Journal:  Cold Spring Harb Perspect Biol       Date:  2015-01-20       Impact factor: 10.005

5.  RNAi analysis of genes expressed in the ovary of Caenorhabditis elegans.

Authors:  F Piano; A J Schetter; M Mangone; L Stein; K J Kemphues
Journal:  Curr Biol       Date:  2000 Dec 14-28       Impact factor: 10.834

6.  SPD-1 is required for the formation of the spindle midzone but is not essential for the completion of cytokinesis in C. elegans embryos.

Authors:  Koen J C Verbrugghe; John G White
Journal:  Curr Biol       Date:  2004-10-05       Impact factor: 10.834

7.  Dual roles of Incenp crucial to the assembly of the acentrosomal metaphase spindle in female meiosis.

Authors:  Nathalie Colombié; C Fiona Cullen; Amy L Brittle; Janet K Jang; William C Earnshaw; Mar Carmena; Kim McKim; Hiroyuki Ohkura
Journal:  Development       Date:  2008-08-28       Impact factor: 6.868

8.  Functional analysis of kinetochore assembly in Caenorhabditis elegans.

Authors:  K Oegema; A Desai; S Rybina; M Kirkham; A A Hyman
Journal:  J Cell Biol       Date:  2001-06-11       Impact factor: 10.539

9.  The KLP-7 Residue S546 Is a Putative Aurora Kinase Site Required for Microtubule Regulation at the Centrosome in C. elegans.

Authors:  Xue Han; Kelly Adames; Ellen M E Sykes; Martin Srayko
Journal:  PLoS One       Date:  2015-07-13       Impact factor: 3.240

10.  Control of microtubule dynamics and length by cyclin A- and cyclin B-dependent kinases in Xenopus egg extracts.

Authors:  F Verde; M Dogterom; E Stelzer; E Karsenti; S Leibler
Journal:  J Cell Biol       Date:  1992-09       Impact factor: 10.539

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  15 in total

Review 1.  Spindle assembly and chromosome dynamics during oocyte meiosis.

Authors:  Timothy J Mullen; Amanda C Davis-Roca; Sarah M Wignall
Journal:  Curr Opin Cell Biol       Date:  2019-05-10       Impact factor: 8.382

2.  Multiple motors cooperate to establish and maintain acentrosomal spindle bipolarity in C. elegans oocyte meiosis.

Authors:  Gabriel Cavin-Meza; Michelle M Kwan; Sarah M Wignall
Journal:  Elife       Date:  2022-02-11       Impact factor: 8.713

3.  The coordination of spindle-positioning forces during the asymmetric division of the Caenorhabditis elegans zygote.

Authors:  Hélène Bouvrais; Laurent Chesneau; Yann Le Cunff; Danielle Fairbrass; Nina Soler; Sylvain Pastezeur; Thierry Pécot; Charles Kervrann; Jacques Pécréaux
Journal:  EMBO Rep       Date:  2021-04-26       Impact factor: 8.807

4.  Translation and codon usage regulate Argonaute slicer activity to trigger small RNA biogenesis.

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Journal:  Nat Commun       Date:  2021-06-09       Impact factor: 14.919

5.  Interplay between microtubule bundling and sorting factors ensures acentriolar spindle stability during C. elegans oocyte meiosis.

Authors:  Timothy J Mullen; Sarah M Wignall
Journal:  PLoS Genet       Date:  2017-09-14       Impact factor: 5.917

6.  Microtubule assembly and pole coalescence: early steps in C aenorhabditis elegans oocyte meiosis I spindle assembly.

Authors:  Chien-Hui Chuang; Aleesa J Schlientz; Jie Yang; Bruce Bowerman
Journal:  Biol Open       Date:  2020-06-25       Impact factor: 2.422

7.  Involvement of Kif4a in Spindle Formation and Chromosome Segregation in Mouse Oocytes.

Authors:  Feng Tang; Meng-Hao Pan; Yujie Lu; Xiang Wan; Yu Zhang; Shao-Chen Sun
Journal:  Aging Dis       Date:  2018-08-01       Impact factor: 6.745

Review 8.  Parts list for a microtubule depolymerising kinesin.

Authors:  Claire T Friel; Julie P Welburn
Journal:  Biochem Soc Trans       Date:  2018-11-22       Impact factor: 5.407

9.  Sumoylation regulates protein dynamics during meiotic chromosome segregation in C. elegans oocytes.

Authors:  Federico Pelisch; Laura Bel Borja; Ellis G Jaffray; Ronald T Hay
Journal:  J Cell Sci       Date:  2019-07-18       Impact factor: 5.285

10.  Cell polarity-dependent centrosome separation in the C. elegans embryo.

Authors:  Alexandra Bondaz; Luca Cirillo; Patrick Meraldi; Monica Gotta
Journal:  J Cell Biol       Date:  2019-10-23       Impact factor: 10.539

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