Minus-end-directed kinesin-14 motors align antiparallel microtubules to control metaphase spindle length

Austin J. Hepperla, Patrick T. Willey, Courtney E Coombes, Breanna M. Schuster, Maryam Gerami-Nejad, Mark McClellan, Soumya R Mukherjee, Janet Fox, Mark Winey, David J Odde, Eileen O'Toole, Melissa K Gardner

Research output: Contribution to journalArticle

32 Citations (Scopus)

Abstract

During cell division, a microtubule-based mitotic spindle mediates the faithful segregation of duplicated chromosomes into daughter cells. Proper length control of the metaphase mitotic spindle is critical to this process and is thought to be achieved through a mechanism in which spindle pole separation forces from plus-end-directed motors are balanced by forces from minus-end-directed motors that pull spindle poles together. However, in contrast to this model, metaphase mitotic spindles with inactive kinesin-14minus-end-directed motors often have shorter spindle lengths, along with poorly aligned spindle microtubules. A mechanistic explanation for this paradox is unknown. Using computational modeling, invitro reconstitution, live-cell fluorescence microscopy, and electron microscopy, we now find that the budding yeast kinesin-14 molecular motor Kar3-Cik1 can efficiently align spindle microtubules along the spindle axis. This then allows plus-end-directed kinesin-5 motors to efficiently exert the outward microtubule sliding forces needed for proper spindle bipolarity.

Original languageEnglish (US)
Pages (from-to)61-72
Number of pages12
JournalDevelopmental Cell
Volume31
Issue number1
DOIs
StatePublished - Oct 13 2014

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Kinesin
Metaphase
Microtubules
Spindle Apparatus
Spindle Poles
Poles
Chromosome Segregation
Saccharomycetales
Fluorescence Microscopy
Cell Division
Fluorescence microscopy
Electron Microscopy
Chromosomes
Yeast
Electron microscopy
Cells

Cite this

Minus-end-directed kinesin-14 motors align antiparallel microtubules to control metaphase spindle length. / Hepperla, Austin J.; Willey, Patrick T.; Coombes, Courtney E; Schuster, Breanna M.; Gerami-Nejad, Maryam; McClellan, Mark; Mukherjee, Soumya R; Fox, Janet; Winey, Mark; Odde, David J; O'Toole, Eileen; Gardner, Melissa K.

In: Developmental Cell, Vol. 31, No. 1, 13.10.2014, p. 61-72.

Research output: Contribution to journalArticle

Hepperla, AJ, Willey, PT, Coombes, CE, Schuster, BM, Gerami-Nejad, M, McClellan, M, Mukherjee, SR, Fox, J, Winey, M, Odde, DJ, O'Toole, E & Gardner, MK 2014, 'Minus-end-directed kinesin-14 motors align antiparallel microtubules to control metaphase spindle length', Developmental Cell, vol. 31, no. 1, pp. 61-72. https://doi.org/10.1016/j.devcel.2014.07.023
Hepperla AJ, Willey PT, Coombes CE, Schuster BM, Gerami-Nejad M, McClellan M et al. Minus-end-directed kinesin-14 motors align antiparallel microtubules to control metaphase spindle length. Developmental Cell. 2014 Oct 13;31(1):61-72. https://doi.org/10.1016/j.devcel.2014.07.023
Hepperla, Austin J. ; Willey, Patrick T. ; Coombes, Courtney E ; Schuster, Breanna M. ; Gerami-Nejad, Maryam ; McClellan, Mark ; Mukherjee, Soumya R ; Fox, Janet ; Winey, Mark ; Odde, David J ; O'Toole, Eileen ; Gardner, Melissa K. / Minus-end-directed kinesin-14 motors align antiparallel microtubules to control metaphase spindle length. In: Developmental Cell. 2014 ; Vol. 31, No. 1. pp. 61-72.
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