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

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

Research output: Contribution to journalArticle

23 Citations (Scopus)

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 ≈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.

Original languageEnglish (US)
Pages (from-to)15338-15343
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume106
Issue number36
DOIs
StatePublished - Sep 8 2009

Fingerprint

Spindle Apparatus
Microtubules
Vertebrates
Kinetochores
Metaphase
Kinesin
Chromosome Segregation
Chromosome Positioning
Chromosomes
Stathmin
Spindle Poles
Centromere
Xenopus
Ovum

Keywords

  • Bipolarity
  • Flux
  • Kinesin-5
  • Stathmin

ASJC Scopus subject areas

  • General

Cite this

Op18 reveals the contribution of nonkinetochore microtubules to the dynamic organization of the vertebrate meiotic spindle. / Houghtaling, Benjamin R.; Yang, Ge; Matov, Alexandre; Danuser, Gaudenz; Kapoor, Tarun M.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 106, No. 36, 08.09.2009, p. 15338-15343.

Research output: Contribution to journalArticle

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