TY - JOUR
T1 - Fission yeast Dis1 is an unconventional TOG/XMAP215 that induces microtubule catastrophe to drive chromosome pulling
AU - Murase, Yuichi
AU - Yamagishi, Masahiko
AU - Okada, Naoyuki
AU - Toya, Mika
AU - Yajima, Junichiro
AU - Hamada, Takahiro
AU - Sato, Masamitsu
N1 - Funding Information:
We thank Ayumu Yamamoto, Yasushi Hiraoka, Takashi Toda and Masayuki Yamamoto for the yeast strains. We are grateful to Yuichiro Watanabe for microscopy support and to Yasutaka Kakui for valuable discussions. Y.M. was supported by JST SPRING, Grant no. JPMJSP2128. This study was supported by JSPS KAKENHI JP25291041, JP15H01359, JP16H04787, JP16H01317, JP18K19347, and JP21H00261 to M.S., and JP17K07397 and JP20K06645 to M.T. This study was also supported by the Ohsumi Frontier Science Foundation (OFSF), the Institute for Fermentation, Osaka (IFO) and Waseda University grants for Special Research Projects 2017B-242, 2017B-243, 2018B-222, 2019C-570, 2020R-038, and 2022C-164 to M.S and 2018S-139, 2019C-571, 2021C-584 and 2022C-170 to M.T.
Publisher Copyright:
© 2022, The Author(s).
PY - 2022/12
Y1 - 2022/12
N2 - 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.
AB - 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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U2 - 10.1038/s42003-022-04271-2
DO - 10.1038/s42003-022-04271-2
M3 - Article
C2 - 36435910
AN - SCOPUS:85142602738
SN - 2399-3642
VL - 5
JO - Communications Biology
JF - Communications Biology
IS - 1
M1 - 1298
ER -