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Fission yeast Dis1 is an unconventional TOG/XMAP215 that induces microtubule catastrophe to drive chromosome pulling

The shortening of microtubules attached to kinetochores is the driving force of chromosome movement during cell division. Specific kinesins are believed to shorten microtubules but are dispensable for viability in yeast, implying the existence of additional factors responsible for microtubule shorte...

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Autores principales: Murase, Yuichi, Yamagishi, Masahiko, Okada, Naoyuki, Toya, Mika, Yajima, Junichiro, Hamada, Takahiro, Sato, Masamitsu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9701203/
https://www.ncbi.nlm.nih.gov/pubmed/36435910
http://dx.doi.org/10.1038/s42003-022-04271-2
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author Murase, Yuichi
Yamagishi, Masahiko
Okada, Naoyuki
Toya, Mika
Yajima, Junichiro
Hamada, Takahiro
Sato, Masamitsu
author_facet Murase, Yuichi
Yamagishi, Masahiko
Okada, Naoyuki
Toya, Mika
Yajima, Junichiro
Hamada, Takahiro
Sato, Masamitsu
author_sort Murase, Yuichi
collection PubMed
description The shortening of microtubules attached to kinetochores is the driving force of chromosome movement during cell division. Specific kinesins are believed to shorten microtubules but are dispensable for viability in yeast, implying the existence of additional factors responsible for microtubule shortening. Here, we demonstrate that Dis1, a TOG/XMAP215 ortholog in fission yeast, promotes microtubule shortening to carry chromosomes. Although TOG/XMAP215 orthologs are generally accepted as microtubule polymerases, Dis1 promoted microtubule catastrophe in vitro and in vivo. Notably, microtubule catastrophe was promoted when the tip was attached to kinetochores, as they steadily anchored Dis1 at the kinetochore-microtubule interface. Engineered Dis1 oligomers artificially tethered at a chromosome arm region induced the shortening of microtubules in contact, frequently pulling the chromosome arm towards spindle poles. This effect was not brought by oligomerised Alp14. Thus, unlike Alp14 and other TOG/XMAP215 orthologs, Dis1 plays an unconventional role in promoting microtubule catastrophe, thereby driving chromosome movement.
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spelling pubmed-97012032022-11-28 Fission yeast Dis1 is an unconventional TOG/XMAP215 that induces microtubule catastrophe to drive chromosome pulling Murase, Yuichi Yamagishi, Masahiko Okada, Naoyuki Toya, Mika Yajima, Junichiro Hamada, Takahiro Sato, Masamitsu Commun Biol Article The shortening of microtubules attached to kinetochores is the driving force of chromosome movement during cell division. Specific kinesins are believed to shorten microtubules but are dispensable for viability in yeast, implying the existence of additional factors responsible for microtubule shortening. Here, we demonstrate that Dis1, a TOG/XMAP215 ortholog in fission yeast, promotes microtubule shortening to carry chromosomes. Although TOG/XMAP215 orthologs are generally accepted as microtubule polymerases, Dis1 promoted microtubule catastrophe in vitro and in vivo. Notably, microtubule catastrophe was promoted when the tip was attached to kinetochores, as they steadily anchored Dis1 at the kinetochore-microtubule interface. Engineered Dis1 oligomers artificially tethered at a chromosome arm region induced the shortening of microtubules in contact, frequently pulling the chromosome arm towards spindle poles. This effect was not brought by oligomerised Alp14. Thus, unlike Alp14 and other TOG/XMAP215 orthologs, Dis1 plays an unconventional role in promoting microtubule catastrophe, thereby driving chromosome movement. Nature Publishing Group UK 2022-11-26 /pmc/articles/PMC9701203/ /pubmed/36435910 http://dx.doi.org/10.1038/s42003-022-04271-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Murase, Yuichi
Yamagishi, Masahiko
Okada, Naoyuki
Toya, Mika
Yajima, Junichiro
Hamada, Takahiro
Sato, Masamitsu
Fission yeast Dis1 is an unconventional TOG/XMAP215 that induces microtubule catastrophe to drive chromosome pulling
title Fission yeast Dis1 is an unconventional TOG/XMAP215 that induces microtubule catastrophe to drive chromosome pulling
title_full Fission yeast Dis1 is an unconventional TOG/XMAP215 that induces microtubule catastrophe to drive chromosome pulling
title_fullStr Fission yeast Dis1 is an unconventional TOG/XMAP215 that induces microtubule catastrophe to drive chromosome pulling
title_full_unstemmed Fission yeast Dis1 is an unconventional TOG/XMAP215 that induces microtubule catastrophe to drive chromosome pulling
title_short Fission yeast Dis1 is an unconventional TOG/XMAP215 that induces microtubule catastrophe to drive chromosome pulling
title_sort fission yeast dis1 is an unconventional tog/xmap215 that induces microtubule catastrophe to drive chromosome pulling
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9701203/
https://www.ncbi.nlm.nih.gov/pubmed/36435910
http://dx.doi.org/10.1038/s42003-022-04271-2
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