Literature DB >> 19706424

Op18 reveals the contribution of nonkinetochore microtubules to the dynamic organization of the vertebrate meiotic spindle.

Benjamin R Houghtaling1, Ge Yang, Alexandre Matov, Gaudenz Danuser, Tarun M Kapoor.   

Abstract

Accuracy in chromosome segregation depends on the assembly of a bipolar spindle. Unlike mitotic spindles, which have roughly equal amounts of kinetochore microtubules (kMTs) and nonkinetochore microtubules (non-kMTs), vertebrate meiotic spindles are predominantly comprised of non-kMTs, a large subset of which forms an antiparallel "barrel" array at the spindle equator. Though kMTs are needed to drive chromosome segregation, the contributions of non-kMTs are more mysterious. Here, we show that increasing the concentration of Op18/stathmin, a component of the chromosome-mediated microtubule formation pathway that directly controls microtubule dynamics, can be used to deplete non-kMTs in the vertebrate meiotic spindle assembled in Xenopus egg extracts. Under these conditions, kMTs and the spindle pole-associated non-kMT arrays persist in smaller spindles. In excess Op18, distances between sister kinetochores, an indicator of tension across centromeres, remain unchanged, even though kMTs flux poleward with a approximately 30% slower velocity, and chromosomes oscillate more than in control metaphase spindles. Remarkably, kinesin-5, a conserved motor protein that can push microtubules apart and is required for the assembly and maintenance of bipolar meiotic spindles, is not needed to maintain spindle bipolarity in the presence of excess Op18. Our data suggest that non-kMTs in meiotic spindles contribute to normal kMT dynamics, stable chromosome positioning, and the establishment of proper spindle size. We propose that without non-kMTs, metaphase meiotic spindles are similar to mammalian mitotic spindles, which balance forces to maintain metaphase spindle organization in the absence of extensive antiparallel microtubule overlap at the spindle equator or a key mitotic kinesin.

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Year:  2009        PMID: 19706424      PMCID: PMC2741252          DOI: 10.1073/pnas.0902317106

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  46 in total

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Journal:  Nature       Date:  1996-08-01       Impact factor: 49.962

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Authors:  S S Andersen; A J Ashford; R Tournebize; O Gavet; A Sobel; A A Hyman; E Karsenti
Journal:  Nature       Date:  1997-10-09       Impact factor: 49.962

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Authors:  J C Waters; T J Mitchison; C L Rieder; E D Salmon
Journal:  Mol Biol Cell       Date:  1996-10       Impact factor: 4.138

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Journal:  Biochim Biophys Acta       Date:  1997-07-24

7.  Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo.

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Journal:  Cell       Date:  1995-12-29       Impact factor: 41.582

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Authors:  C L Rieder
Journal:  Chromosoma       Date:  1981       Impact factor: 4.316

9.  The distribution of polar ejection forces determines the amplitude of chromosome directional instability.

Authors:  Kevin Ke; Jun Cheng; Alan J Hunt
Journal:  Curr Biol       Date:  2009-05-14       Impact factor: 10.834

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Authors:  L D Belmont; T J Mitchison
Journal:  Cell       Date:  1996-02-23       Impact factor: 41.582

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  18 in total

1.  Deformations within moving kinetochores reveal different sites of active and passive force generation.

Authors:  Sophie Dumont; E D Salmon; Timothy J Mitchison
Journal:  Science       Date:  2012-06-21       Impact factor: 47.728

2.  Microneedle-based analysis of the micromechanics of the metaphase spindle assembled in Xenopus laevis egg extracts.

Authors:  Yuta Shimamoto; Tarun M Kapoor
Journal:  Nat Protoc       Date:  2012-04-26       Impact factor: 13.491

3.  Using micromanipulation to analyze control of vertebrate meiotic spindle size.

Authors:  Jun Takagi; Takeshi Itabashi; Kazuya Suzuki; Tarun M Kapoor; Yuta Shimamoto; Shin'ichi Ishiwata
Journal:  Cell Rep       Date:  2013-10-10       Impact factor: 9.423

4.  Distinct Roles of the Chromosomal Passenger Complex in the Detection of and Response to Errors in Kinetochore-Microtubule Attachment.

Authors:  Julian Haase; Mary Kate Bonner; Hyunmi Halas; Alexander E Kelly
Journal:  Dev Cell       Date:  2017-09-25       Impact factor: 12.270

5.  Meiosis I in Xenopus oocytes is not error-prone despite lacking spindle assembly checkpoint.

Authors:  Dandan Liu; Hua Shao; Hongmei Wang; X Johné Liu
Journal:  Cell Cycle       Date:  2014-03-19       Impact factor: 4.534

6.  The human T-cell leukemia virus type-1 tax oncoprotein dissociates NF-κB p65RelA-Stathmin complexes and causes catastrophic mitotic spindle damage and genomic instability.

Authors:  Aditi Malu; Tetiana Hutchison; Laçin Yapindi; Katie Smith; Katherine Nelson; Rachel Bergeson; Jordan Pope; Megan Romeo; Carolyn Harrod; Lee Ratner; Carine Van Lint; Robert Harrod
Journal:  Virology       Date:  2019-07-03       Impact factor: 3.616

7.  Insights into the micromechanical properties of the metaphase spindle.

Authors:  Yuta Shimamoto; Yusuke T Maeda; Shin'ichi Ishiwata; Albert J Libchaber; Tarun M Kapoor
Journal:  Cell       Date:  2011-06-24       Impact factor: 41.582

8.  Poly(ADP-ribose) mediates asymmetric division of mouse oocyte.

Authors:  Bingteng Xie; Lu Zhang; Huiling Zhao; Qingyun Bai; Yong Fan; Xiaohui Zhu; Yang Yu; Rong Li; Xin Liang; Qing-Yuan Sun; Mo Li; Jie Qiao
Journal:  Cell Res       Date:  2018-02-20       Impact factor: 25.617

9.  plusTipTracker: Quantitative image analysis software for the measurement of microtubule dynamics.

Authors:  Kathryn T Applegate; Sebastien Besson; Alexandre Matov; Maria H Bagonis; Khuloud Jaqaman; Gaudenz Danuser
Journal:  J Struct Biol       Date:  2011-07-29       Impact factor: 2.867

10.  Interplay of microtubule dynamics and sliding during bipolar spindle formation in mammalian cells.

Authors:  Swapna Kollu; Samuel F Bakhoum; Duane A Compton
Journal:  Curr Biol       Date:  2009-12-29       Impact factor: 10.834

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