The bidirectional depolymerizer MCAK generates force by disassembling both microtubule ends

Yusuke Oguchi, Seiichi Uchimura, Takashi Ohki, Sergey Mikhailenko, Shin'Ichi Ishiwata

Research output: Contribution to journalArticle

42 Citations (Scopus)

Abstract

During cell division the replicated chromosomes are segregated precisely towards the spindle poles. Although many cellular processes involving motility require ATP-fuelled force generation by motor proteins, most models of the chromosome movement invoke the release of energy stored at strained (owing to GTP hydrolysis) plus ends of microtubules. This energy is converted into chromosome movement through passive couplers, whereas the role of molecular motors is limited to the regulation of microtubule dynamics. Here we report, that the microtubule-depolymerizing activity of MCAK (mitotic centromere-associated kinesin), the founding member of the kinesin-13 family, is accompanied by the generation of significant tensiongremarkably, at both microtubule ends. An MCAK-decorated bead strongly attaches to the microtubule side, but readily slides along it in either direction under weak external loads and tightly captures and disassembles both microtubule ends. We show that the depolymerization force increases with the number of interacting MCAK molecules and is ∼1-pN per motor. These results provide a simple model for the generation of driving force and the regulation of chromosome segregation by the activity of MCAK at both kinetochores and spindle poles through aside-sliding, end-catchinmechanism.

Original languageEnglish
Pages (from-to)846-852
Number of pages7
JournalNature Cell Biology
Volume13
Issue number7
DOIs
Publication statusPublished - 2011 Jul

Fingerprint

Kinesin
Centromere
Microtubules
Spindle Poles
Chromosomes
Kinetochores
Chromosome Segregation
Guanosine Triphosphate
Cell Division
Hydrolysis
Adenosine Triphosphate
Proteins

ASJC Scopus subject areas

  • Cell Biology

Cite this

The bidirectional depolymerizer MCAK generates force by disassembling both microtubule ends. / Oguchi, Yusuke; Uchimura, Seiichi; Ohki, Takashi; Mikhailenko, Sergey; Ishiwata, Shin'Ichi.

In: Nature Cell Biology, Vol. 13, No. 7, 07.2011, p. 846-852.

Research output: Contribution to journalArticle

Oguchi, Yusuke ; Uchimura, Seiichi ; Ohki, Takashi ; Mikhailenko, Sergey ; Ishiwata, Shin'Ichi. / The bidirectional depolymerizer MCAK generates force by disassembling both microtubule ends. In: Nature Cell Biology. 2011 ; Vol. 13, No. 7. pp. 846-852.
@article{9fbec5703ba9449483d17aea686951bb,
title = "The bidirectional depolymerizer MCAK generates force by disassembling both microtubule ends",
abstract = "During cell division the replicated chromosomes are segregated precisely towards the spindle poles. Although many cellular processes involving motility require ATP-fuelled force generation by motor proteins, most models of the chromosome movement invoke the release of energy stored at strained (owing to GTP hydrolysis) plus ends of microtubules. This energy is converted into chromosome movement through passive couplers, whereas the role of molecular motors is limited to the regulation of microtubule dynamics. Here we report, that the microtubule-depolymerizing activity of MCAK (mitotic centromere-associated kinesin), the founding member of the kinesin-13 family, is accompanied by the generation of significant tensiongremarkably, at both microtubule ends. An MCAK-decorated bead strongly attaches to the microtubule side, but readily slides along it in either direction under weak external loads and tightly captures and disassembles both microtubule ends. We show that the depolymerization force increases with the number of interacting MCAK molecules and is ∼1-pN per motor. These results provide a simple model for the generation of driving force and the regulation of chromosome segregation by the activity of MCAK at both kinetochores and spindle poles through aside-sliding, end-catchinmechanism.",
author = "Yusuke Oguchi and Seiichi Uchimura and Takashi Ohki and Sergey Mikhailenko and Shin'Ichi Ishiwata",
year = "2011",
month = "7",
doi = "10.1038/ncb2256",
language = "English",
volume = "13",
pages = "846--852",
journal = "Nature Cell Biology",
issn = "1465-7392",
publisher = "Nature Publishing Group",
number = "7",

}

TY - JOUR

T1 - The bidirectional depolymerizer MCAK generates force by disassembling both microtubule ends

AU - Oguchi, Yusuke

AU - Uchimura, Seiichi

AU - Ohki, Takashi

AU - Mikhailenko, Sergey

AU - Ishiwata, Shin'Ichi

PY - 2011/7

Y1 - 2011/7

N2 - During cell division the replicated chromosomes are segregated precisely towards the spindle poles. Although many cellular processes involving motility require ATP-fuelled force generation by motor proteins, most models of the chromosome movement invoke the release of energy stored at strained (owing to GTP hydrolysis) plus ends of microtubules. This energy is converted into chromosome movement through passive couplers, whereas the role of molecular motors is limited to the regulation of microtubule dynamics. Here we report, that the microtubule-depolymerizing activity of MCAK (mitotic centromere-associated kinesin), the founding member of the kinesin-13 family, is accompanied by the generation of significant tensiongremarkably, at both microtubule ends. An MCAK-decorated bead strongly attaches to the microtubule side, but readily slides along it in either direction under weak external loads and tightly captures and disassembles both microtubule ends. We show that the depolymerization force increases with the number of interacting MCAK molecules and is ∼1-pN per motor. These results provide a simple model for the generation of driving force and the regulation of chromosome segregation by the activity of MCAK at both kinetochores and spindle poles through aside-sliding, end-catchinmechanism.

AB - During cell division the replicated chromosomes are segregated precisely towards the spindle poles. Although many cellular processes involving motility require ATP-fuelled force generation by motor proteins, most models of the chromosome movement invoke the release of energy stored at strained (owing to GTP hydrolysis) plus ends of microtubules. This energy is converted into chromosome movement through passive couplers, whereas the role of molecular motors is limited to the regulation of microtubule dynamics. Here we report, that the microtubule-depolymerizing activity of MCAK (mitotic centromere-associated kinesin), the founding member of the kinesin-13 family, is accompanied by the generation of significant tensiongremarkably, at both microtubule ends. An MCAK-decorated bead strongly attaches to the microtubule side, but readily slides along it in either direction under weak external loads and tightly captures and disassembles both microtubule ends. We show that the depolymerization force increases with the number of interacting MCAK molecules and is ∼1-pN per motor. These results provide a simple model for the generation of driving force and the regulation of chromosome segregation by the activity of MCAK at both kinetochores and spindle poles through aside-sliding, end-catchinmechanism.

UR - http://www.scopus.com/inward/record.url?scp=79960004101&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79960004101&partnerID=8YFLogxK

U2 - 10.1038/ncb2256

DO - 10.1038/ncb2256

M3 - Article

C2 - 21602793

AN - SCOPUS:79960004101

VL - 13

SP - 846

EP - 852

JO - Nature Cell Biology

JF - Nature Cell Biology

SN - 1465-7392

IS - 7

ER -