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

47 Citations (Scopus)

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

Fingerprint

Dyneins
Microtubules
microtubules
Fusion reactions
Chromosomes
Cytoplasmic Dyneins
Spindle Apparatus
Plasticity
Poles
Nucleation
Stabilization
centrosomes
Centrosome
Chromosome Segregation
chromosome segregation
Xenopus
Ovum
homeostasis
Homeostasis
Experiments

Keywords

  • CELLBIO

ASJC Scopus subject areas

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

Cite this

Gatlin, J. C., Matov, A., Groen, A. C., Needleman, D. J., Maresca, T. J., Danuser, G., ... 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

Spindle Fusion Requires Dynein-Mediated Sliding of Oppositely Oriented Microtubules. / Gatlin, Jesse C.; Matov, Alexandre; Groen, Aaron C.; Needleman, Daniel J.; Maresca, Thomas J.; Danuser, Gaudenz; Mitchison, Timothy J.; Salmon, E. D.

In: Current Biology, Vol. 19, No. 4, 24.02.2009, p. 287-296.

Research output: Contribution to journalArticle

Gatlin, JC, Matov, A, Groen, AC, Needleman, DJ, Maresca, TJ, Danuser, G, Mitchison, TJ & Salmon, ED 2009, 'Spindle Fusion Requires Dynein-Mediated Sliding of Oppositely Oriented Microtubules', Current Biology, vol. 19, no. 4, pp. 287-296. https://doi.org/10.1016/j.cub.2009.01.055
Gatlin, Jesse C. ; Matov, Alexandre ; Groen, Aaron C. ; Needleman, Daniel J. ; Maresca, Thomas J. ; Danuser, Gaudenz ; Mitchison, Timothy J. ; Salmon, E. D. / Spindle Fusion Requires Dynein-Mediated Sliding of Oppositely Oriented Microtubules. In: Current Biology. 2009 ; Vol. 19, No. 4. pp. 287-296.
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