Spindle Fusion Requires Dynein-Mediated Sliding of Oppositely Oriented Microtubules

Jesse C. Gatlin, Alexandre Matov, Aaron C. Groen, Daniel J. Needleman, Thomas J. Maresca, Gaudenz Danuser, Timothy J. Mitchison, E. D. Salmon

Research output: Contribution to journalArticle

49 Scopus citations

Abstract

Background: Bipolar spindle assembly is critical for achieving accurate segregation of chromosomes. In the absence of centrosomes, meiotic spindles achieve bipolarity by a combination of chromosome-initiated microtubule nucleation and stabilization and motor-driven organization of microtubules. Once assembled, the spindle structure is maintained on a relatively long time scale despite the high turnover of the microtubules that comprise it. To study the underlying mechanisms responsible for spindle assembly and steady-state maintenance, we used microneedle manipulation of preassembled spindles in Xenopus egg extracts. Results: When two meiotic spindles were brought close enough together, they interacted, creating an interconnected microtubule structure with supernumerary poles. Without exception, the perturbed system eventually re-established bipolarity, forming a single spindle of normal shape and size. Bipolar spindle fusion was blocked when cytoplasmic dynein function was perturbed, suggesting a critical role for the motor in this process. The fusion of Eg5-inhibited monopoles also required dynein function but only occurred if the initial interpolar separation was less than twice the microtubule radius of a typical monopole. Conclusions: Our experiments uniquely illustrate the architectural plasticity of the spindle and reveal a robust ability of the system to attain a bipolar morphology. We hypothesize that a major mechanism driving spindle fusion is dynein-mediated sliding of oppositely oriented microtubules, a novel function for the motor, and posit that this same mechanism might also be involved in normal spindle assembly and homeostasis.

Original languageEnglish (US)
Pages (from-to)287-296
Number of pages10
JournalCurrent Biology
Volume19
Issue number4
DOIs
StatePublished - Feb 24 2009

Keywords

  • CELLBIO

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

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    Gatlin, J. C., Matov, A., Groen, A. C., Needleman, D. J., Maresca, T. J., Danuser, G., Mitchison, T. J., & Salmon, E. D. (2009). Spindle Fusion Requires Dynein-Mediated Sliding of Oppositely Oriented Microtubules. Current Biology, 19(4), 287-296. https://doi.org/10.1016/j.cub.2009.01.055