The structure of apo-kinesin bound to tubulin links the nucleotide cycle to movement

Nature Communications

Volumn 5, Issue , 2014, Pages

  Cao, Luyan ^a   Wang, Weiyi ^a,b   Jiang, Qiyang ^b,c   Wang, Chunguang ^b   Knossow, Marcel ^a   Gigant, Benoît ^a  

^a LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^b TONGJI UNIVERSITY   (China)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN; NUCLEOTIDE; TUBULIN; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; KIF5B PROTEIN, HUMAN;

DATA ACQUISITION; ENZYME ACTIVITY; MECHANICAL PROPERTY; PROTEIN;

ARTICLE; COMPARATIVE STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME RELEASE; ENZYME STRUCTURE; MOLECULAR DOCKING; NUCLEOTIDE BINDING SITE; HUMAN; METABOLISM; MICROTUBULE; MOVEMENT (PHYSIOLOGY); PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; HUMANS; KINESIN; MICROTUBULES; MOLECULAR DOCKING SIMULATION; MOVEMENT; NUCLEOTIDES; PROTEIN STRUCTURE, TERTIARY; TUBULIN;

EID: 84923365639     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6364     Document Type: Article

References (51)

1. Svoboda, K., Schmidt, C. F., Schnapp, B. J. & Block, S. M. Direct observation of kinesin stepping by optical trapping interferometry. Nature 365, 721-727 (1993).
2. Vale, R. D. & Fletterick, R. J. The design plan of kinesin motors. Ann. Rev. Cell Dev. Biol 13, 745-777 (1997).
3. Coy, D. L., Wagenbach, M. & Howard, J. Kinesin takes one 8-nm step for each ATP that it hydrolyzes. J. Biol. Chem. 274, 3667-3671 (1999).
4. Rice, S. et al. A structural change in the kinesin motor protein that drives motility. Nature 402, 778-784 (1999).
5. Kull, F. J., Sablin, E. P., Lau, R., Fletterick, R. J. & Vale, R. D. Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature 380, 550-555 (1996).
6. Sindelar, C. V. et al. Two conformations in the human kinesin power stroke defined by X-ray crystallography and EPR spectroscopy. Nat. Struct. Biol. 9, 844-848 (2002).
7. Song, Y. H. et al. Structure of a fast kinesin: implications for ATPase mechanism and interactions with microtubules. EMBO J. 20, 6213-6225 (2001).
8. Marx, A., Hoenger, A. & Mandelkow, E. Structures of kinesin motor proteins. Cell Motil. Cytoskeleton 66, 958-966 (2009).
9. Chang, Q., Nitta, R., Inoue, S. & Hirokawa, N. Structural basis for the ATP-induced isomerization of kinesin. J. Mol. Biol. 425, 1869-1880 (2013).
10. Parke, C. L., Wojcik, E. J., Kim, S. & Worthylake, D. K. ATP hydrolysis in Eg5 kinesin involves a catalytic two-water mechanism. J. Biol. Chem. 285, 5859-5867 (2010).
11. Gigant, B. et al. Structure of a kinesin-tubulin complex and implications for kinesin motility. Nat. Struct. Mol. Biol. 20, 1001-1007 (2013).
12. Bodey, A. J., Kikkawa, M. & Moores, C. A. 9-Angstrom structure of a microtubule-bound mitotic motor. J. Mol. Biol. 388, 218-224 (2009).
13. Peters, C. et al. Insight into the molecular mechanism of the multitasking kinesin-8 motor. EMBO J. 29, 3437-3447 (2010).
14. Sindelar, C. V. & Downing, K. H. An atomic-level mechanism for activation of the kinesin molecular motors. Proc. Natl Acad. Sci. USA 107, 4111-4116 (2010).
15. Skiniotis, G. et al. Nucleotide-induced conformations in the neck region of dimeric kinesin. EMBO J. 22, 1518-1528 (2003).
16. Cross, R. A. The kinetic mechanism of kinesin. Trends Biochem. Sci. 29, 301-309 (2004).
17. Binz, H. K. et al. High-affinity binders selected from designed ankyrin repeat protein libraries. Nat. Biotechnol. 22, 575-582 (2004).
18. Pecqueur, L. et al. A designed ankyrin repeat protein selected to bind to tubulin caps the microtubule plus end. Proc. Natl Acad. Sci. USA 109, 12011-12016 (2012).
19. Crevel, I. M., Lockhart, A. & Cross, R. A. Weak and strong states of kinesin and ncd. J. Mol. Biol. 257, 66-76 (1996).
20. Shipley, K. et al. Structure of a kinesin microtubule depolymerization machine. EMBO J. 23, 1422-1432 (2004).
21. Arora, K. et al. KIF14 binds tightly to microtubules and adopts a rigor-like conformation. J. Mol. Biol. 426, 2997-3015 (2014).
22. Nitta, R., Okada, Y. & Hirokawa, N. Structural model for strain-dependent microtubule activation of Mg-ADP release from kinesin. Nat. Struct. Mol. Biol. 15, 1067-1075 (2008).
23. Case, R. B., Rice, S., Hart, C. L., Ly, B. & Vale, R. D. Role of the kinesin neck linker and catalytic core in microtubule-based motility. Curr. Biol. 10, 157-160 (2000).
24. Clancy, B. E., Behnke-Parks, W. M., Andreasson, J. O., Rosenfeld, S. S. & Block, S. M. A universal pathway for kinesin stepping. Nat. Struct. Mol. Biol. 18, 1020-1027 (2011).
25. Yun, M., Zhang, X., Park, C. G., Park, H. W. & Endow, S. A. A structural pathway for activation of the kinesin motor ATPase. EMBO J. 20, 2611-2618 (2001).
26. Woehlke, G. et al. Microtubule interaction site of the kinesin motor. Cell 90, 207-216 (1997).
27. Kull, F. J., Vale, R. D. & Fletterick, R. J. The case for a common ancestor: kinesin and myosin motor proteins and G proteins. J. Muscle Res. Cell Motil. 19, 877-886 (1998).
28. Coureux, P. D., Sweeney, H. L. & Houdusse, A. Three myosin V structures delineate essential features of chemo-mechanical transduction. EMBO J. 23, 4527-4537 (2004).
29. Coureux, P. D. et al. A structural state of the myosin V motor without bound nucleotide. Nature 425, 419-423 (2003).
30. Reubold, T. F., Eschenburg, S., Becker, A., Kull, F. J. & Manstein, D. J. A structural model for actin-induced nucleotide release in myosin. Nat. Struct. Biol. 10, 826-830 (2003).
31. Kull, F. J. & Endow, S. A. Force generation by kinesin and myosin cytoskeletal motor proteins. J. Cell Sci. 126, 9-19 (2013).
32. Sindelar, C. V. A seesaw model for intermolecular gating in the kinesin motor protein. Biophys. Rev. 3, 85-100 (2011).
33. Boriack-Sjodin, P. A., Margarit, S. M., Bar-Sagi, D. & Kuriyan, J. The structural basis of the activation of Ras by Sos. Nature 394, 337-343 (1998).
34. Mittal, R., Ahmadian, M. R., Goody, R. S. & Wittinghofer, A. Formation of a transition-state analog of the Ras GTPase reaction by Ras-GDP, tetrafluoroaluminate, and GTPase-activating proteins. Science 273, 115-117 (1996).
35. Hackney, D. D., Baek, N. & Snyder, A. C. Half-site inhibition of dimeric kinesin head domains by monomeric tail domains. Biochemistry 48, 3448-3456 (2009).
36. Kaan, H. Y., Hackney, D. D. & Kozielski, F. The structure of the kinesin-1 motor-tail complex reveals the mechanism of autoinhibition. Science 333, 883-885 (2011).
37. Rosenfeld, S. S., Jefferson, G. M. & King, P. H. ATP reorients the neck linker of kinesin in two sequential steps. J. Biol. Chem. 276, 40167-40174 (2001).
38. Hahlen, K. et al. Feedback of the kinesin-1 neck-linker position on the catalytic site. J. Biol. Chem. 281, 18868-18877 (2006).
39. Castoldi, M. & Popov, A. V. Purification of brain tubulin through two cycles of polymerization-depolymerization in a high-molarity buffer. Protein Expr. Purif. 32, 83-88 (2003).
40. Correia, J. J., Baty, L. T. & Williams, Jr. R. C. Mg2 + dependence of guanine nucleotide binding to tubulin. J. Biol. Chem. 262, 17278-17284 (1987).
41. Huang, T. G. & Hackney, D. D. Drosophila kinesin minimal motor domain expressed in Escherichia coli. Purification and kinetic characterization. J. Biol. Chem. 269, 16493-16501 (1994).
42. Cheng, J.-Q., Jiang, W. & Hackney, D. D. Interaction of mant-adenosine nucleotides and magnesium with kinesin. Biochemistry 37, 5288-5295 (1998).
43. Foster, K. A. & Gilbert, S. P. Kinetic studies of dimeric Ncd: evidence that Ncd is not processive. Biochemistry 39, 1784-1791 (2000).
44. Ma, Y. Z. & Taylor, E. W. Kinetic mechanism of kinesin motor domain. Biochemistry 34, 13233-13241 (1995).
45. Kabsch, W. Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
46. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
47. Bricogne, G. et al. BUSTER v. 2.10.0 (Global Phasing Ltd., 2011).
48. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
49. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
50. Mosca, R. & Schneider, T. R. RAPIDO: a web server for the alignment of protein structures in the presence of conformational changes. Nucleic Acids Res. 36, W42-W46 (2008).
51. Schrodinger, L. L. C. The PyMOL Molecular Graphics System, Version 1.3r1 (2010).