Mechanisms mitigating problems with multiple kinetochores on one microtubule in early mitosis

Zuojun Yue, Shinya Komoto, Marek Gierlinski, Debora Pasquali, Etsushi Kitamura, Tomoyuki U. Tanaka (Lead / Corresponding author)

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Abstract

Proper chromosome segregation in mitosis relies on correct kinetochore interaction with spindle microtubules. In early mitosis, each kinetochore usually interacts with the lateral
side of each microtubule and is subsequently tethered at the microtubule end. However, since eukaryotic cells carry multiple chromosomes, multiple kinetochores could occasionally interact with a single microtubule. The consequence of this is unknown. Here we find that, although two kinetochores (two pairs of sister kinetochores) can interact with the lateral side of one microtubule, only one kinetochore can form sustained attachment to the microtubule end in budding yeast. This leads to detachment of the other kinetochore from the microtubule end or its proximity. Intriguingly, in this context, kinetochore sliding along a microtubule towards a spindle pole delays and diminishes discernible kinetochore detachment. This effect expedites collection of the entire set of kinetochores to a spindle pole. We propose that cells are equipped with the kinetochore sliding mechanism to mitigate the problem with multiple kinetochores on one microtubule in early mitosis.
Original languageEnglish
Pages (from-to)2266-2276
Number of pages11
JournalJournal of Cell Science
Volume130
Issue number14
Early online date25 May 2017
DOIs
Publication statusPublished - 15 Jul 2017

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Kinetochores
Mitosis
Microtubules
Spindle Poles
Chromosome Segregation
Saccharomycetales
Eukaryotic Cells

Keywords

  • Kinetochore
  • Microtubule
  • Kinetochore sliding
  • End-on-attachment
  • Early mitosis
  • Budding yeast

Cite this

@article{722f00340e0f4ffda444089200f58671,
title = "Mechanisms mitigating problems with multiple kinetochores on one microtubule in early mitosis",
abstract = "Proper chromosome segregation in mitosis relies on correct kinetochore interaction with spindle microtubules. In early mitosis, each kinetochore usually interacts with the lateralside of each microtubule and is subsequently tethered at the microtubule end. However, since eukaryotic cells carry multiple chromosomes, multiple kinetochores could occasionally interact with a single microtubule. The consequence of this is unknown. Here we find that, although two kinetochores (two pairs of sister kinetochores) can interact with the lateral side of one microtubule, only one kinetochore can form sustained attachment to the microtubule end in budding yeast. This leads to detachment of the other kinetochore from the microtubule end or its proximity. Intriguingly, in this context, kinetochore sliding along a microtubule towards a spindle pole delays and diminishes discernible kinetochore detachment. This effect expedites collection of the entire set of kinetochores to a spindle pole. We propose that cells are equipped with the kinetochore sliding mechanism to mitigate the problem with multiple kinetochores on one microtubule in early mitosis.",
keywords = "Kinetochore, Microtubule, Kinetochore sliding, End-on-attachment, Early mitosis, Budding yeast",
author = "Zuojun Yue and Shinya Komoto and Marek Gierlinski and Debora Pasquali and Etsushi Kitamura and Tanaka, {Tomoyuki U.}",
note = "This work was supported by the Wellcome Trust (096535, 083524, 097945), the Medical Research Council (84678, K015869) and ERC advanced grant (322682). T.U.T. is a Wellcome Trust Principal Research Fellow.",
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Mechanisms mitigating problems with multiple kinetochores on one microtubule in early mitosis. / Yue, Zuojun; Komoto, Shinya; Gierlinski, Marek; Pasquali, Debora; Kitamura, Etsushi; Tanaka, Tomoyuki U. (Lead / Corresponding author).

In: Journal of Cell Science, Vol. 130, No. 14, 15.07.2017, p. 2266-2276.

Research output: Contribution to journalArticle

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T1 - Mechanisms mitigating problems with multiple kinetochores on one microtubule in early mitosis

AU - Yue, Zuojun

AU - Komoto, Shinya

AU - Gierlinski, Marek

AU - Pasquali, Debora

AU - Kitamura, Etsushi

AU - Tanaka, Tomoyuki U.

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N2 - Proper chromosome segregation in mitosis relies on correct kinetochore interaction with spindle microtubules. In early mitosis, each kinetochore usually interacts with the lateralside of each microtubule and is subsequently tethered at the microtubule end. However, since eukaryotic cells carry multiple chromosomes, multiple kinetochores could occasionally interact with a single microtubule. The consequence of this is unknown. Here we find that, although two kinetochores (two pairs of sister kinetochores) can interact with the lateral side of one microtubule, only one kinetochore can form sustained attachment to the microtubule end in budding yeast. This leads to detachment of the other kinetochore from the microtubule end or its proximity. Intriguingly, in this context, kinetochore sliding along a microtubule towards a spindle pole delays and diminishes discernible kinetochore detachment. This effect expedites collection of the entire set of kinetochores to a spindle pole. We propose that cells are equipped with the kinetochore sliding mechanism to mitigate the problem with multiple kinetochores on one microtubule in early mitosis.

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KW - Kinetochore

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