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Metaphase kinetochore movements are regulated by kinesin-8 motors and microtubule dynamic instability

During metaphase, sister chromatids are connected to microtubules extending from the opposite spindle poles via kinetochores to protein complexes on the chromosome. Kinetochores congress to the equatorial plane of the spindle and oscillate around it, with kinesin-8 motors restricting these movements...

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Autores principales: Klemm, Anna H., Bosilj, Agneza, Gluncˇic´, Matko, Pavin, Nenad, Tolic´, Iva M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5994901/
https://www.ncbi.nlm.nih.gov/pubmed/29851559
http://dx.doi.org/10.1091/mbc.E17-11-0667
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author Klemm, Anna H.
Bosilj, Agneza
Gluncˇic´, Matko
Pavin, Nenad
Tolic´, Iva M.
author_facet Klemm, Anna H.
Bosilj, Agneza
Gluncˇic´, Matko
Pavin, Nenad
Tolic´, Iva M.
author_sort Klemm, Anna H.
collection PubMed
description During metaphase, sister chromatids are connected to microtubules extending from the opposite spindle poles via kinetochores to protein complexes on the chromosome. Kinetochores congress to the equatorial plane of the spindle and oscillate around it, with kinesin-8 motors restricting these movements. Yet, the physical mechanism underlying kinetochore movements is unclear. We show that kinetochore movements in the fission yeast Schizosaccharomyces pombe are regulated by kinesin-8-promoted microtubule catastrophe, force-induced rescue, and microtubule dynamic instability. A candidate screen showed that among the selected motors only kinesin-8 motors Klp5/Klp6 are required for kinetochore centering. Kinesin-8 accumulates at the end of microtubules, where it promotes catastrophe. Laser ablation of the spindle resulted in kinetochore movement toward the intact spindle pole in wild-type and klp5Δ cells, suggesting that kinetochore movement is driven by pulling forces. Our theoretical model with Langevin description of microtubule dynamic instability shows that kinesin-8 motors are required for kinetochore centering, whereas sensitivity of rescue to force is necessary for the generation of oscillations. We found that irregular kinetochore movements occur for a broader range of parameters than regular oscillations. Thus, our work provides an explanation for how regulation of microtubule dynamic instability contributes to kinetochore congression and the accompanying movements around the spindle center.
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spelling pubmed-59949012018-08-16 Metaphase kinetochore movements are regulated by kinesin-8 motors and microtubule dynamic instability Klemm, Anna H. Bosilj, Agneza Gluncˇic´, Matko Pavin, Nenad Tolic´, Iva M. Mol Biol Cell Articles During metaphase, sister chromatids are connected to microtubules extending from the opposite spindle poles via kinetochores to protein complexes on the chromosome. Kinetochores congress to the equatorial plane of the spindle and oscillate around it, with kinesin-8 motors restricting these movements. Yet, the physical mechanism underlying kinetochore movements is unclear. We show that kinetochore movements in the fission yeast Schizosaccharomyces pombe are regulated by kinesin-8-promoted microtubule catastrophe, force-induced rescue, and microtubule dynamic instability. A candidate screen showed that among the selected motors only kinesin-8 motors Klp5/Klp6 are required for kinetochore centering. Kinesin-8 accumulates at the end of microtubules, where it promotes catastrophe. Laser ablation of the spindle resulted in kinetochore movement toward the intact spindle pole in wild-type and klp5Δ cells, suggesting that kinetochore movement is driven by pulling forces. Our theoretical model with Langevin description of microtubule dynamic instability shows that kinesin-8 motors are required for kinetochore centering, whereas sensitivity of rescue to force is necessary for the generation of oscillations. We found that irregular kinetochore movements occur for a broader range of parameters than regular oscillations. Thus, our work provides an explanation for how regulation of microtubule dynamic instability contributes to kinetochore congression and the accompanying movements around the spindle center. The American Society for Cell Biology 2018-06-01 /pmc/articles/PMC5994901/ /pubmed/29851559 http://dx.doi.org/10.1091/mbc.E17-11-0667 Text en © 2018 Klemm, Bosilj, et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0/ This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Articles
Klemm, Anna H.
Bosilj, Agneza
Gluncˇic´, Matko
Pavin, Nenad
Tolic´, Iva M.
Metaphase kinetochore movements are regulated by kinesin-8 motors and microtubule dynamic instability
title Metaphase kinetochore movements are regulated by kinesin-8 motors and microtubule dynamic instability
title_full Metaphase kinetochore movements are regulated by kinesin-8 motors and microtubule dynamic instability
title_fullStr Metaphase kinetochore movements are regulated by kinesin-8 motors and microtubule dynamic instability
title_full_unstemmed Metaphase kinetochore movements are regulated by kinesin-8 motors and microtubule dynamic instability
title_short Metaphase kinetochore movements are regulated by kinesin-8 motors and microtubule dynamic instability
title_sort metaphase kinetochore movements are regulated by kinesin-8 motors and microtubule dynamic instability
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5994901/
https://www.ncbi.nlm.nih.gov/pubmed/29851559
http://dx.doi.org/10.1091/mbc.E17-11-0667
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