Structural Model for Tubulin Recognition and Deformation by Kinesin-13 Microtubule Depolymerases

被引:59
作者
Asenjo, Ana B. [1 ]
Chatterjee, Chandrima [1 ]
Tan, Dongyan [1 ]
DePaoli, Vania [1 ]
Rice, William J. [2 ]
Diaz-Avalos, Ruben [2 ]
Silvestry, Mariena [2 ]
Sosa, Hernando [1 ]
机构
[1] Yeshiva Univ Albert Einstein Coll Med, Dept Physiol & Biophys, Bronx, NY 10461 USA
[2] New York Struct Biol Ctr, New York, NY 10027 USA
基金
美国国家卫生研究院;
关键词
FLUORESCENCE POLARIZATION MICROSCOPY; CENTROMERE-ASSOCIATED KINESIN; ALPHA-BETA-TUBULIN; MCAK; MOTOR; DEPOLYMERIZATION; PROTEIN; MECHANISM; DOMAIN; VISUALIZATION;
D O I
10.1016/j.celrep.2013.01.030
中图分类号
Q2 [细胞生物学];
学科分类号
071013 [干细胞生物学];
摘要
To elucidate the structural basis of the mechanism of microtubule depolymerization by kinesin-13s, we analyzed complexes of tubulin and the Drosophila melanogaster kinesin-13 KLP10A by electron microscopy (EM) and fluorescence polarization microscopy. We report a nanometer-resolution (1.1 nm) cryo-EM three-dimensional structure of the KLP10A head domain (KLP10AHD) bound to curved tubulin. We found that binding of KLP10AHD induces a distinct tubulin configuration with displacement (shear) between tubulin subunits in addition to curvature. In this configuration, the kinesin-binding site differs from that in straight tubulin, providing an explanation for the distinct interaction modes of kinesin-13s with the microtubule lattice or its ends. The KLP10AHD-tubulin interface comprises three areas of interaction, suggesting a crossbow-type tubulin-bending mechanism. These areas include the kinesin-13 family conserved KVD residues, and as predicted from the crossbow model, mutating these residues changes the orientation and mobility of KLP10AHDs interacting with the microtubule.
引用
收藏
页码:759 / 768
页数:10
相关论文
共 42 条
[1]
Configuration of the two kinesin motor domains during ATP hydrolysis [J].
Asenjo, AB ;
Krohn, N ;
Sosa, H .
NATURE STRUCTURAL BIOLOGY, 2003, 10 (10) :836-842
[2]
A mobile kinesin-head intermediate during the ATP-waiting state [J].
Asenjo, Ana B. ;
Sosa, Hernando .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2009, 106 (14) :5657-5662
[3]
Changeux Jean-Pierre, 2011, F1000 Biol Rep, V3, P19, DOI 10.3410/B3-19
[4]
Catalysis of the microtubule on-rate is the major parameter regulating the depolymerase activity of MCAK [J].
Cooper, Jeremy R. ;
Wagenbach, Michael ;
Asbury, Charles L. ;
Wordeman, Linda .
NATURE STRUCTURAL & MOLECULAR BIOLOGY, 2010, 17 (01) :77-U98
[5]
Kin I kinesins are microtubule-destabilizing enzymes [J].
Desai, A ;
Verma, S ;
Mitchison, TJ ;
Walczak, CE .
CELL, 1999, 96 (01) :69-78
[6]
The kinesin-13 MCAK has an unconventional ATPase cycle adapted for microtubule depolymerization [J].
Friel, Claire T. ;
Howard, Jonathon .
EMBO JOURNAL, 2011, 30 (19) :3928-3939
[7]
Depolymerizing Kinesins Kip3 and MCAK Shape Cellular Microtubule Architecture by Differential Control of Catastrophe [J].
Gardner, Melissa K. ;
Zanic, Marija ;
Gell, Christopher ;
Bormuth, Volker ;
Howard, Jonathon .
CELL, 2011, 147 (05) :1092-1103
[8]
The road less traveled: Emerging principles of kinesin motor utilization [J].
Goldstein, LSB ;
Philp, AV .
ANNUAL REVIEW OF CELL AND DEVELOPMENTAL BIOLOGY, 1999, 15 :141-183
[9]
The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends [J].
Helenius, J ;
Brouhard, G ;
Kalaidzidis, Y ;
Diez, S ;
Howard, J .
NATURE, 2006, 441 (7089) :115-119
[10]
Full-length dimeric MCAK is a more efficient microtubule depolymerase than minimal domain monomeric MCAK [J].
Hertzer, KM ;
Ems-McClung, SC ;
Kline-Smith, SL ;
Lipkin, TG ;
Gilbert, SP ;
Walczak, CE .
MOLECULAR BIOLOGY OF THE CELL, 2006, 17 (02) :700-710