Single-molecule observations of neck linker conformational changes in the kinesin motor protein

Nature Structural and Molecular Biology

Volumn 13, Issue 10, 2006, Pages 887-894

  Tomishige, Michio ^a,b   Stuurman, Nico ^b   Vale, Ronald D ^b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN; MOLECULAR MOTOR;

ARTICLE; CONFORMATIONAL TRANSITION; FLUORESCENCE RESONANCE ENERGY TRANSFER; MICROTUBULE ASSEMBLY; MOLECULAR MODEL; MOTOR UNIT; MOVEMENT (PHYSIOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN;

BINDING SITES; DIMERIZATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; KINESIN; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR MOTOR PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; STAINING AND LABELING; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 33749515974     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1151     Document Type: Article

References (43)

1. Vale, R.D. The molecular motor toolbox for intracellular transport. Cell 112, 467-480 (2003).
2. Hirokawa, N. & Takemura, R. Molecular motors and mechanisms of directional transport in neurons. Nat. Rev. Neurosci. 6, 201-214 (2005).
3. 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).
4. Hackney, D.D. Evidence for alternating head catalysis by kinesin during microtubule-stimulated ATP hydrolysis. Proc. Natl. Acad. Sci. USA 91, 6865-6869 (1994).
5. Vale, R.D. et al. Direct observation of single kinesin molecules moving along microtubules. Nature 380, 451-453 (1996).
6. 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).
7. Kikkawa, M. et al. Switch-based mechanism of kinesin motors. Nature 411, 439-445 (2001).
8. Nitta, R., Kikkawa, M., Okada, Y. & Hirokawa, N. KIF1A alternatively use two loops to bind microtubules. Science 305, 678-683 (2004).
9. Sack, S. et al. X-ray structure of motor and neck domains from rat brain kinesin. Biochemistry 36, 16155-16165 (1997).
10. Kozielski, F. et al. The crystal structure of dimeric kinesin and implications for microtubule-dependent motility. Cell 91, 985-994 (1997).
11. 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).
12. Rice, S. et al. A structural change in the kinesin motor protein that drives motility. Nature 402, 778-784 (1999).
13. Vale, R.D. & Milligan, R.A. The way things move: looking under the hood of molecular motor proteins. Science 288, 88-95 (2000).
14. Yildiz, A., Tomishige, M., Vale, R.D. & Selvin, P.R. Kinesin walks hand-over-hand. Science 303, 676-678 (2004).
15. Rice, S. et al. Thermodynamic properties of the kinesin neck-region docking to the catalytic core. Biophys. J. 84, 1844-1854 (2003).
16. Skiniotis, G. et al. Nucleotide-induced conformations in the neck region of dimeric kinesin. EMBO J. 22, 1518-1528 (2003).
17. 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).
18. Rosenfeld, S.S., Xing, J., Jefferson, G.M., Cheung, H.C. & King, P.H. Measuring kinesin's first step. J. Biol. Chem. 277, 36731-36739 (2002).
19. Rosenfeld, S.S., Fordyce, P.M., Jefferson, G.M., King, P.H. & Block, S.M. Stepping and stretching: how kinesin uses internal strain to walk processively. J. Biol. Chem. 278, 18550-18556 (2003).
20. Asenjo, A.B., Krohn, N. & Sosa, H. Configuration of the two kinesin motor domains during ATP hydrolysis. Nat. Struct. Biol. 10, 836-842 (2003).
21. Asenjo, A.B., Weinberg, Y. & Sosa, H. Nucleotide binding and hydrolysis induces a disorder-order transition in the kinesin neck-linker region. Nat. Struct. Mol. Biol. 13, 648-654 (2006).
22. 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).
23. Tomishige, M. & Vale, R.D. Controlling kinesin by reversible disulfide cross-linking: identifying the motility-producing conformational change. J. Cell Biol. 151, 1081-1092 (2000).
24. Schief, W.R. & Howard, J. Conformational changes during kinesin motility. Curr. Opin. Cell Biol. 13, 19-28 (2001).
25. Carter, N.J. & Cross, R.A. Kinesin's moonwalk. Curr. Opin. Cell Biol. 18, 61-67 (2006).
26. Sablin, E.P. & Fletterick, R.J. Coordination between motor domains in processive kinesins. J. Biol. Chem. 279, 15707-15710 (2004).
27. Kawaguchi, K. & Ishiwata, S. Nucleotide-dependent single- to double-headed binding of kinesin. Science 291, 667-669 (2001).
28. Skerra, A. & Schmidt, T.G. Applications of a peptide ligand for streptavidin: the Streptag. Biomol. Eng. 16, 79-86 (1999).
29. Tomishige, M., Klopfenstein, D.R. & Vale, R.D. Conversion of Unc104/KIF1A kinesin into a processive motor after dimerization. Science 297, 2263-2267 (2002).
30. Carter, N.J. & Cross, R.A. Mechanics of the kinesin step. Nature 435, 308-312 (2005).
31. Suzuki, Y., Yasunaga, T., Ohkura, R., Wakabayashi, T. & Sutoh, K. Swing of the lever arm of a myosin motor at the isomerization and phosphate-release steps. Nature 396, 380-383 (1998).
32. Shih, W.M., Gryczynski, Z., Lakowicz, J.R. & Spudich, J.A. A FRET-based sensor reveals large ATP hydrolysis-induced conformational changes and three distinct states of the molecular motor myosin. Cell 102, 683-694 (2000).
33. Forkey, J.N., Quinlan, M.E., Shaw, M.A., Corrie, J.E. & Goldman, Y.E. Three-dimensional structural dynamics of myosin V by single-molecule fluorescence polarization. Nature 422, 399-404 (2003).
34. Houdusse, A., Kalabokis, V.N., Himmel, D., Szent-Györgyi, A.G. & Cohen, C. Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell 97, 459-470 (1999).
35. Turner, J. et al. Crystal structure of the mitotic spindle kinesin Eg5 reveals a novel conformation of the neck-linker. J. Biol. Chem. 276, 25496-25502 (2001).
36. Kinosita, K., Jr. et al. How two-foot molecular motors may walk. Adv. Exp. Med. Biol. 565, 205-219 (2005).
37. Hackney, D.D. The tethered motor domain of a kinesin-microtubule complex catalyzes reversible synthesis of bound ATP. Proc. Natl. Acad. Sci. USA 102, 18338-18343 (2005).
38. Hua, W., Chung, J. & Gelles, J. Distinguishing inchworm and hand-over-hand processive kinesin movement by neck rotation measurements. Science 295, 844-848 (2002).
39. Asbury, C.L., Fehr, A.N. & Block, S.M. Kinesin moves by an asymmetric hand-over-hand mechanism. Science 302, 2130-2134 (2003).
40. Kaseda, K., Higuchi, H. & Hirose, K. Alternate fast and slow stepping of a heterodimeric kinesin molecule. Nat. Cell Biol. 5, 1079-1082 (2003).
41. Higuchi, H., Bronner, C.E., Park, H.-W. & Endow, S.A. Rapid double 8-nm steps by a kinesin mutant. EMBO J. 23, 2993-2999 (2004).
42. Ishii, Y., Yoshida, T., Funatsu, T., Wazawa, T. & Yanagida, T. Fluorescence resonance energy transfer between single fluorophores attached to a coiled-coil protein in aqueous solution. Chem. Phys. 247, 163-173 (1999).
43. Gelles, J., Schnapp, B.J. & Sheetz, M.P. Tracking kinesin-driven movements with nanometre-scale precision. Nature 331, 450-453 (1988).