Chromosome Congression by Kinesin-5 Motor-Mediated Disassembly of Longer Kinetochore Microtubules

Melissa K. Gardner; David C. Bouck; Leocadia V. Paliulis; Janet B. Meehl; Eileen T. O'Toole; Julian Haase; Adelheid Soubry; Ajit P. Joglekar; Mark Winey; Edward D. Salmon; Kerry Bloom; David J. Odde

doi:10.1016/j.cell.2008.09.046

Chromosome Congression by Kinesin-5 Motor-Mediated Disassembly of Longer Kinetochore Microtubules

Melissa K. Gardner, David C. Bouck, Leocadia V. Paliulis, Janet B. Meehl, Eileen T. O'Toole, Julian Haase, Adelheid Soubry, Ajit P. Joglekar, Mark Winey, Edward D. Salmon, Kerry Bloom, David J. Odde

Research output: Contribution to journal › Article › peer-review

135 Scopus citations

Abstract

During mitosis, sister chromatids congress to the spindle equator and are subsequently segregated via attachment to dynamic kinetochore microtubule (kMT) plus ends. A major question is how kMT plus-end assembly is spatially regulated to achieve chromosome congression. Here we find in budding yeast that the widely conserved kinesin-5 sliding motor proteins, Cin8p and Kip1p, mediate chromosome congression by suppressing kMT plus-end assembly of longer kMTs. Of the two, Cin8p is the major effector and its activity requires a functional motor domain. In contrast, the depolymerizing kinesin-8 motor Kip3p plays a minor role in spatial regulation of yeast kMT assembly. Our analysis identified a model where kinesin-5 motors bind to kMTs, move to kMT plus ends, and upon arrival at a growing plus end promote net kMT plus-end disassembly. In conclusion, we find that length-dependent control of net kMT assembly by kinesin-5 motors yields a simple and stable self-organizing mechanism for chromosome congression.

Original language	English (US)
Pages (from-to)	894-906
Number of pages	13
Journal	Cell
Volume	135
Issue number	5
DOIs	https://doi.org/10.1016/j.cell.2008.09.046
State	Published - Nov 28 2008

Bibliographical note

Funding Information:
The authors thank Dominique Seetapun for providing matlab kymograph code, Drs. Tom Hays and Leah Gheber for helpful discussions, Dr. Jeff Molk for comments on the manuscript, and Marybeth Anderson for assistance with bim1Δ images. Plasmids and strains were kindly provided by Drs. S. Reed, B. Errede, M.A. Hoyt, L. Gheber, and D. Pellman. This work was supported by NIH grant GM071522 to D.J.O. K.B. is supported by NIH grant GM32238 and M.K.G. is supported by NIH NRSA grant EB005568. E.T.O. is supported in part by grant RR-00592 from the National Center for Research Resources of the NIH to A. Hoenger. L.V.P. is supported by a SPIRE fellowship (GM00678).

Keywords

MOLIMMUNO
SIGNALING

Access

10.1016/j.cell.2008.09.046

OpenUrl availability

Full text

Cite this

@article{d5a5ddf1c0a345de9b3aa0c756c54f83,

title = "Chromosome Congression by Kinesin-5 Motor-Mediated Disassembly of Longer Kinetochore Microtubules",

abstract = "During mitosis, sister chromatids congress to the spindle equator and are subsequently segregated via attachment to dynamic kinetochore microtubule (kMT) plus ends. A major question is how kMT plus-end assembly is spatially regulated to achieve chromosome congression. Here we find in budding yeast that the widely conserved kinesin-5 sliding motor proteins, Cin8p and Kip1p, mediate chromosome congression by suppressing kMT plus-end assembly of longer kMTs. Of the two, Cin8p is the major effector and its activity requires a functional motor domain. In contrast, the depolymerizing kinesin-8 motor Kip3p plays a minor role in spatial regulation of yeast kMT assembly. Our analysis identified a model where kinesin-5 motors bind to kMTs, move to kMT plus ends, and upon arrival at a growing plus end promote net kMT plus-end disassembly. In conclusion, we find that length-dependent control of net kMT assembly by kinesin-5 motors yields a simple and stable self-organizing mechanism for chromosome congression.",

keywords = "MOLIMMUNO, SIGNALING",

author = "Gardner, {Melissa K.} and Bouck, {David C.} and Paliulis, {Leocadia V.} and Meehl, {Janet B.} and O'Toole, {Eileen T.} and Julian Haase and Adelheid Soubry and Joglekar, {Ajit P.} and Mark Winey and Salmon, {Edward D.} and Kerry Bloom and Odde, {David J.}",

note = "Funding Information: The authors thank Dominique Seetapun for providing matlab kymograph code, Drs. Tom Hays and Leah Gheber for helpful discussions, Dr. Jeff Molk for comments on the manuscript, and Marybeth Anderson for assistance with bim1Δ images. Plasmids and strains were kindly provided by Drs. S. Reed, B. Errede, M.A. Hoyt, L. Gheber, and D. Pellman. This work was supported by NIH grant GM071522 to D.J.O. K.B. is supported by NIH grant GM32238 and M.K.G. is supported by NIH NRSA grant EB005568. E.T.O. is supported in part by grant RR-00592 from the National Center for Research Resources of the NIH to A. Hoenger. L.V.P. is supported by a SPIRE fellowship (GM00678). ",

year = "2008",

month = nov,

day = "28",

doi = "10.1016/j.cell.2008.09.046",

language = "English (US)",

volume = "135",

pages = "894--906",

journal = "Cell",

issn = "0092-8674",

publisher = "Cell Press",

number = "5",

}

TY - JOUR

T1 - Chromosome Congression by Kinesin-5 Motor-Mediated Disassembly of Longer Kinetochore Microtubules

AU - Gardner, Melissa K.

AU - Bouck, David C.

AU - Paliulis, Leocadia V.

AU - Meehl, Janet B.

AU - O'Toole, Eileen T.

AU - Haase, Julian

AU - Soubry, Adelheid

AU - Joglekar, Ajit P.

AU - Winey, Mark

AU - Salmon, Edward D.

AU - Bloom, Kerry

AU - Odde, David J.

N1 - Funding Information: The authors thank Dominique Seetapun for providing matlab kymograph code, Drs. Tom Hays and Leah Gheber for helpful discussions, Dr. Jeff Molk for comments on the manuscript, and Marybeth Anderson for assistance with bim1Δ images. Plasmids and strains were kindly provided by Drs. S. Reed, B. Errede, M.A. Hoyt, L. Gheber, and D. Pellman. This work was supported by NIH grant GM071522 to D.J.O. K.B. is supported by NIH grant GM32238 and M.K.G. is supported by NIH NRSA grant EB005568. E.T.O. is supported in part by grant RR-00592 from the National Center for Research Resources of the NIH to A. Hoenger. L.V.P. is supported by a SPIRE fellowship (GM00678).

PY - 2008/11/28

Y1 - 2008/11/28

N2 - During mitosis, sister chromatids congress to the spindle equator and are subsequently segregated via attachment to dynamic kinetochore microtubule (kMT) plus ends. A major question is how kMT plus-end assembly is spatially regulated to achieve chromosome congression. Here we find in budding yeast that the widely conserved kinesin-5 sliding motor proteins, Cin8p and Kip1p, mediate chromosome congression by suppressing kMT plus-end assembly of longer kMTs. Of the two, Cin8p is the major effector and its activity requires a functional motor domain. In contrast, the depolymerizing kinesin-8 motor Kip3p plays a minor role in spatial regulation of yeast kMT assembly. Our analysis identified a model where kinesin-5 motors bind to kMTs, move to kMT plus ends, and upon arrival at a growing plus end promote net kMT plus-end disassembly. In conclusion, we find that length-dependent control of net kMT assembly by kinesin-5 motors yields a simple and stable self-organizing mechanism for chromosome congression.

AB - During mitosis, sister chromatids congress to the spindle equator and are subsequently segregated via attachment to dynamic kinetochore microtubule (kMT) plus ends. A major question is how kMT plus-end assembly is spatially regulated to achieve chromosome congression. Here we find in budding yeast that the widely conserved kinesin-5 sliding motor proteins, Cin8p and Kip1p, mediate chromosome congression by suppressing kMT plus-end assembly of longer kMTs. Of the two, Cin8p is the major effector and its activity requires a functional motor domain. In contrast, the depolymerizing kinesin-8 motor Kip3p plays a minor role in spatial regulation of yeast kMT assembly. Our analysis identified a model where kinesin-5 motors bind to kMTs, move to kMT plus ends, and upon arrival at a growing plus end promote net kMT plus-end disassembly. In conclusion, we find that length-dependent control of net kMT assembly by kinesin-5 motors yields a simple and stable self-organizing mechanism for chromosome congression.

KW - MOLIMMUNO

KW - SIGNALING

UR - http://www.scopus.com/inward/record.url?scp=56349157171&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=56349157171&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2008.09.046

DO - 10.1016/j.cell.2008.09.046

M3 - Article

C2 - 19041752

AN - SCOPUS:56349157171

SN - 0092-8674

VL - 135

SP - 894

EP - 906

JO - Cell

JF - Cell

IS - 5

ER -

Chromosome Congression by Kinesin-5 Motor-Mediated Disassembly of Longer Kinetochore Microtubules

Abstract

Bibliographical note

Keywords

Access

OpenUrl availability

Other files and links

Fingerprint

Cite this