9-Ångström Structure of a Microtubule-Bound Mitotic Motor

Journal of Molecular Biology

Volumn 388, Issue 2, 2009, Pages 218-224

  Bodey, Andrew J ^a   Kikkawa, Masahide ^b   Moores, Carolyn A ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

cancer; cryo electron microscopy; kinesin; microtubule; mitosis

Indexed keywords

ADENOSINE TRIPHOSPHATE; KINESIN; KINESIN 5; MOLECULAR MOTOR; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN;

ARTICLE; BINDING SITE; CELL DIVISION; CHROMOSOME SEGREGATION; CLINICAL RESEARCH; CRYOELECTRON MICROSCOPY; DRUG BINDING; IMAGE PROCESSING; IMAGE RECONSTRUCTION; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; ANIMAL; CHEMISTRY; METABOLISM; X RAY CRYSTALLOGRAPHY;

ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; CHROMOSOME SEGREGATION; CRYSTALLOGRAPHY, X-RAY; DROSOPHILA PROTEINS; KINESIN; MICROTUBULES; MITOSIS; MOLECULAR MOTOR PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 64049086564     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.03.008     Document Type: Article

References (46)

1. Wittmann T., Hyman A., and Desai A. The spindle: a dynamic assembly of microtubules and motors. Nat. Cell Biol. 3 (2001) E28-E34
2. Sawin K.E., LeGuellec K., Philippe M., and Mitchison T.J. Mitotic spindle organization by a plus-end-directed microtubule motor. Nature 359 (1992) 540-543
3. Goshima G., and Vale R.D. The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J. Cell Biol. 162 (2003) 1003-1016
4. Mayer T.U., Kapoor T.M., Haggarty S.J., King R.W., Schreiber S.L., and Mitchison T.J. Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286 (1999) 971-974
5. Kashina A.S., Baskin R.J., Cole D.G., Wedaman K.P., Saxton W.M., and Scholey J.M. A bipolar kinesin. Nature 379 (1996) 270-272
6. van den Wildenberg S.M., Tao L., Kapitein L.C., Schmidt C.F., Scholey J.M., and Peterman E.J. The homotetrameric kinesin-5 KLP61F preferentially crosslinks microtubules into antiparallel orientations. Curr. Biol. 18 (2008) 1860-1864
7. Kapitein L.C., Peterman E.J.G., Kwok B.H., Kim J.H., Kapoor T.M., and Schmidt C.F. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature 435 (2005) 114-118
8. Kaseda K., Crevel I., Hirose K., and Cross R.A. Single-headed mode of kinesin-5. EMBO Rep. 9 (2008) 761-765
9. Crevel I.M., Lockhart A., and Cross R.A. Kinetic evidence for low chemical processivity in ncd and Eg5. J. Mol. Biol. 273 (1997) 160-170
10. Valentine M.T., Fordyce P.M., Krzysiak T.C., Gilbert S.P., and Block S.M. Individual dimers of the mitotic kinesin motor Eg5 step processively and support substantial loads in vitro. Nat. Cell Biol. 8 (2006) 470-476
11. Kapitein L.C., Kwok B.H., Weinger J.S., Schmidt C.F., Kapoor T.M., and Peterman E.J.G. Microtubule cross-linking triggers the directional motility of kinesin-5. J. Cell Biol. 182 (2008) 421-428
12. Vale R.D., and Milligan R.A. The way things move: looking under the hood of molecular motor proteins. Science 288 (2000) 88-95
13. Crevel I.M., Alonso M.C., and Cross R.A. Monastrol stabilises an attached low-friction mode of Eg5. Curr. Biol. 14 (2004) R411-R412
14. Kwok B.H., Kapitein L.C., Kim J.H., Peterman E.J.G., Schmidt C.F., and Kapoor T.M. Allosteric inhibition of kinesin-5 modulates its processive directional motility. Nat. Chem. Biol. 2 (2006) 480-485
15. Yan Y., Sardana V., Xu B., Homnick C., Halczenko W., Buser C.A., et al. Inhibition of a mitotic motor protein: where, how, and conformational consequences. J. Mol. Biol. 335 (2004) 547-554
16. Maliga Z., and Mitchison T.J. Small-molecule and mutational analysis of allosteric Eg5 inhibition by monastrol. BMC Chem. Biol. 6 (2006) 2
17. Lad L., Luo L., Carson J.D., Wood K.W., Hartman J.J., Copeland R.A., and Sakowicz R. Mechanism of inhibition of human KSP by ispinesib. Biochemistry 47 (2008) 3576-3585
18. Sarli V., and Giannis A. Targeting the kinesin spindle protein: basic principles and clinical implications. Clin. Cancer Res. 14 (2008) 7583-7587
19. Myers K.A., and Baas P.W. Kinesin-5 regulates the growth of the axon by acting as a brake on its microtubule array. J. Cell Biol. 178 (2007) 1081-1091
20. Hirose K., Henningsen U., Schliwa M., Toyoshima C., Shimizu T., Alonso M., et al. Structural comparison of dimeric Eg5, Neurospora kinesin (Nkin) and Ncd head-Nkin neck chimera with conventional kinesin. EMBO J. 19 (2000) 5308-5314
21. Krzysiak T.C., Wendt T., Sproul L.R., Tittmann P., Gross H., Gilbert S.P., and Hoenger A. A structural model for monastrol inhibition of dimeric kinesin Eg5. EMBO J. 25 (2006) 2263-2273
22. Metlagel Z., Kikkawa Y.S., and Kikkawa M. Ruby-Helix: an implementation of helical image processing based on object-oriented scripting language. J. Struct. Biol. 157 (2007) 95-105
23. Löwe J., Li H., Downing K.H., and Nogales E. Refined structure of alpha beta-tubulin at 3.5 Å resolution. J. Mol. Biol. 313 (2001) 1045-1057
24. Nogales E., Wolf S.G., and Downing K.H. Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391 (1998) 199-203
25. Kikkawa M. The role of microtubules in processive kinesin movement. Trends Cell Biol. 18 (2008) 128-135
26. Li H., DeRosier D.J., Nicholson W.V., Nogales E., and Downing K.H. Microtubule structure at 8 Å resolution. Structure 10 (2002) 1317-1328
27. Wang Z., and Sheetz M.P. The C-terminus of tubulin increases cytoplasmic dynein and kinesin processivity. Biophys. J. 78 (2000) 1955-1964
28. Hammond J.W., Cai D., and Verhey K.J. Tubulin modifications and their cellular functions. Curr. Opin. Cell Biol. 20 (2008) 71-76
29. Moores C.A., Yu M., Guo J., Beraud C., Sakowicz R., and Milligan R.A. A mechanism for microtubule depolymerization by KinI kinesins. Mol. Cell 9 (2002) 903-909
30. Grant B.J., McCammon J.A., Caves L.S.D., and Cross R.A. Multivariate analysis of conserved sequence-structure relationships in kinesins: coupling of the active site and a tubulin-binding sub-domain. J. Mol. Biol. 368 (2007) 1231-1248
31. Notredame C., Higgins D.G., and Heringa J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302 (2000) 205-217
32. Sali A., and Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234 (1993) 779-815
33. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612
34. Kikkawa M., and Hirokawa N. High-resolution cryo-EM maps show the nucleotide binding pocket of KIF1A in open and closed conformations. EMBO J. 25 (2006) 4187-4194
35. Sindelar C.V., and Downing K.H. The beginning of kinesin's force-generating cycle visualized at 9-Å resolution. J. Cell Biol. 177 (2007) 377-385
36. Woehlke G., Ruby A.K., Hart C.L., Ly B., Hom-Booher N., and Vale R.D. Microtubule interaction site of the kinesin motor. Cell 90 (1997) 207-216
37. Nitta R., Kikkawa M., Okada Y., and Hirokawa N. KIF1A alternately uses two loops to bind microtubules. Science 305 (2004) 678-683
38. Naber N., Minehardt T.J., Rice S., Chen X., Grammer J., Matuska A., et al. Closing of the nucleotide pocket of kinesin-family motors upon binding to microtubules. Science 300 (2003) 798-801
39. Hirose K., Akimaru E., Akiba T., Endow S.A., and Amos L.A. Large conformational changes in a kinesin motor catalyzed by interaction with microtubules. Mol. Cell 23 (2006) 913-923
40. Cochran J.C., and Gilbert S.P. ATPase mechanism of Eg5 in the absence of microtubules: insight into microtubule activation and allosteric inhibition by monastrol. Biochemistry 44 (2005) 16633-16648
41. Brier S., Lemaire D., DeBonis S., Forest E., and Kozielski F. Molecular dissection of the inhibitor binding pocket of mitotic kinesin Eg5 reveals mutants that confer resistance to antimitotic agents. J. Mol. Biol. 360 (2006) 360-376
42. Rice S., Lin A.W., Safer D., Hart C.L., Naber N., Carragher B.O., et al. A structural change in the kinesin motor protein that drives motility. Nature 402 (1999) 778-784
43. Turner J., Anderson R., Guo J., Beraud C., Fletterick R., and Sakowicz R. Crystal structure of the mitotic spindle kinesin Eg5 reveals a novel conformation of the neck-linker. J. Biol. Chem. 276 (2001) 25496-25502
44. Maliga Z., Xing J., Cheung H., Juszczak L.J., Friedman J.M., and Rosenfeld S.S. A pathway of structural changes produced by monastrol binding to Eg5. J. Biol. Chem. 281 (2006) 7977-7982
45. Nitta R., Okada Y., and Hirokawa N. Structural model for strain-dependent microtubule activation of Mg-ADP release from kinesin. Nat. Struct. Mol. Biol. 15 (2008) 1067-1075
46. Cochran J.C., Sindelar C.V., Mulko N.K., Collins K.A., Kong S.E., Hawley R.S., and Kull F.J. ATPase cycle of the nonmotile kinesin NOD allows microtubule end tracking and drives chromosome movement. Cell 136 (2009) 110-122