A structural perspective on the dynamics of kinesin motors

Biophysical Journal

Volumn 101, Issue 11, 2011, Pages 2749-2759

  Hyeon, Changbong ^a   Onuchic, José N ^b  

^a Korea Institute for Advanced Study   (South Korea)

^b RICE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; KINESIN;

ARTICLE; BIOMECHANICS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MICROTUBULE; PLIABILITY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; THERMODYNAMICS;

ADENOSINE TRIPHOSPHATE; BIOMECHANICS; KINESIN; MICROTUBULES; MODELS, MOLECULAR; PLIABILITY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; THERMODYNAMICS;

EID: 82955169485     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.10.037     Document Type: Article

References (78)

1. R.P. Feynman Miniaturization 1961 Reinhold New York
2. B. Alberts The cell as a collection of protein machines: preparing the next generation of molecular biologists Cell 92 1998 291 294
3. N. Hirokawa Kinesin and dynein superfamily proteins and the mechanism of organelle transport Science 279 1998 519 526
4. R.D. Vale The molecular motor toolbox for intracellular transport Cell 112 2003 467 480
5. J. Harms, and F. Schluenzen A. Yonath High resolution structure of the large ribosomal subunit from a mesophilic eubacterium Cell 107 2001 679 688
6. P. Nissen, and J. Hansen T.A. Steitz The structural basis of ribosome activity in peptide bond synthesis Science 289 2000 920 930
7. B. Alberts, and A. Johnson P. Walter Molecular Biology of the Cell 5th ed. 2008 Garland Science New York
8. B. Alberts, and R. Miake-Lye Unscrambling the puzzle of biological machines: the importance of the details Cell 68 1992 415 420
9. S.M. Block Kinesin motor mechanics: binding, stepping, tracking, gating, and limping Biophys. J. 92 2007 2986 2995
10. W.J. Greenleaf, M.T. Woodside, and S.M. Block High-resolution, single-molecule measurements of biomolecular motion Annu. Rev. Biophys. Biomol. Struct. 36 2007 171 190
11. 1-ATPase Proc. Natl. Acad. Sci. USA 103 2006 5367 5372
12. C. Hyeon, G.H. Lorimer, and D. Thirumalai Dynamics of allosteric transitions in GroEL Proc. Natl. Acad. Sci. USA 103 2006 18939 18944
13. C. Hyeon, and J.N. Onuchic Internal strain regulates the nucleotide binding site of the kinesin leading head Proc. Natl. Acad. Sci. USA 104 2007 2175 2180
14. C. Hyeon, and J.N. Onuchic Mechanical control of the directional stepping dynamics of the kinesin motor Proc. Natl. Acad. Sci. USA 104 2007 17382 17387
15. J. Chen, S.A. Darst, and D. Thirumalai Promoter melting triggered by bacterial RNA polymerase occurs in three steps Proc. Natl. Acad. Sci. USA 107 2010 12523 12528
16. R. Tehver, and D. Thirumalai Rigor to post-rigor transition in myosin V: link between the dynamics and the supporting architecture Structure 18 2010 471 481
17. M. Takano, T.P. Terada, and M. Sasai Unidirectional Brownian motion observed in an in silico single molecule experiment of an actomyosin motor Proc. Natl. Acad. Sci. USA 107 2010 7769 7774
18. A. Kravats, M. Jayasinghe, and G. Stan Unfolding and translocation pathway of substrate protein controlled by structure in repetitive allosteric cycles of the ClpY ATPase Proc. Natl. Acad. Sci. USA 108 2011 2234 2239
19. P.W. Anderson Basic Notions of Condensed Matter Physics 1997 Westview Press Boulder, CO
20. C. Hyeon, and D. Thirumalai Capturing the essence of folding and functions of biomolecules using coarse-grained models Nat Commun. 2 2011 487
21. J.N. Onuchic, and P.G. Wolynes Theory of protein folding Curr. Opin. Struct. Biol. 14 2004 70 75
22. E. Shakhnovich Protein folding thermodynamics and dynamics: where physics, chemistry, and biology meet Chem. Rev. 106 2006 1559 1588
23. K.A. Dill, and S.B. Ozkan T.R. Weikl The protein folding problem Annu. Rev. Biophys. 37 2008 289 316
24. D. Thirumalai, and E.P. O'Brien C. Hyeon Theoretical perspectives on protein folding Annu. Rev. Biophys. 39 2010 159 183
25. P.G. de Gennes Scaling Concepts in Polymer Physics 1979 Cornell University Press Ithaca, New York
26. C.L. Asbury, A.N. Fehr, and S.M. Block Kinesin moves by an asymmetric hand-over-hand mechanism Science 302 2003 2130 2134
27. M. Nishiyama, E. Muto, Y. Inoue, T. Yanagida, and H. Higuchi Substeps within the 8-nm step of the ATPase cycle of single kinesin molecules Nat. Cell Biol. 3 2001 425 428
28. A. Yildiz, and M. Tomishige P.R. Selvin Kinesin walks hand-over-hand Science 303 2004 676 678
29. C.V. Sindelar, and K.H. Downing An atomic-level mechanism for activation of the kinesin molecular motors Proc. Natl. Acad. Sci. USA 107 2010 4111 4116
30. Y.Z. Ma, and E.W. Taylor Interacting head mechanism of microtubule-kinesin ATPase J. Biol. Chem. 272 1997 724 730
31. R.A. Cross, and I. Crevel L.A. Amos The conformational cycle of kinesin Philos. Trans. R. Soc. Lond. B Biol. Sci. 355 2000 459 464
32. J. Xing, and W. Wriggers S.S. Rosenfeld Kinesin has three nucleotide-dependent conformations. Implications for strain-dependent release J. Biol. Chem. 275 2000 35413 35423
33. N.R. Guydosh, and S.M. Block Backsteps induced by nucleotide analogs suggest the front head of kinesin is gated by strain Proc. Natl. Acad. Sci. USA 103 2006 8054 8059
34. S.P. Gilbert, and K.A. Johnson Pre-steady-state kinetics of the microtubule-kinesin ATPase Biochemistry 33 1994 1951 1960
35. D.D. Hackney The tethered motor domain of a kinesin-microtubule complex catalyzes reversible synthesis of bound ATP Proc. Natl. Acad. Sci. USA 102 2005 18338 18343
36. C. Hyeon, S. Klumpp, and J.N. Onuchic Kinesin's backsteps under mechanical load Phys. Chem. Chem. Phys. 11 2009 4899 4910
37. J.J. Hopfield Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity Proc. Natl. Acad. Sci. USA 71 1974 4135 4139
38. C. Hyeon, and P.A. Jennings J.N. Onuchic Ligand-induced global transitions in the catalytic domain of protein kinase A Proc. Natl. Acad. Sci. USA 106 2009 3023 3028
39. C.L. Parke, and E.J. Wojcik D.K. Worthylake ATP hydrolysis in Eg5 kinesin involves a catalytic two-water mechanism J. Biol. Chem. 285 2010 5859 5867
40. S. Rice, and A.W. Lin R.D. Vale A structural change in the kinesin motor protein that drives motility Nature 402 1999 778 784
41. C.V. Sindelar, and M.J. Budny R. Cooke Two conformations in the human kinesin power stroke defined by x-ray crystallography and EPR spectroscopy Nat. Struct. Biol. 9 2002 844 848
42. S. Rice, and Y. Cui R. Cooke Thermodynamic properties of the kinesin neck-region docking to the catalytic core Biophys. J. 84 2003 1844 1854
43. W. Hwang, M.J. Lang, and M. Karplus Force generation in kinesin hinges on cover-neck bundle formation Structure 16 2008 62 71
44. A.S. Khalil, and D.C. Appleyard M.J. Lang Kinesin's cover-neck bundle folds forward to generate force Proc. Natl. Acad. Sci. USA 105 2008 19247 19252
45. A. Czövek, G.J. Szöllosi, and I. Derényi Neck-linker docking coordinates the kinetics of kinesin's heads Biophys. J. 100 2011 1729 1736
46. F. Oosawa The loose coupling mechanism in molecular machines of living cells Genes Cells 5 2000 9 16
47. C.M. Coppin, and J.T. Finer R.D. Vale Detection of sub-8-nm movements of kinesin by high-resolution optical-trap microscopy Proc. Natl. Acad. Sci. USA 93 1996 1913 1917
48. N.J. Carter, and R.A. Cross Mechanics of the kinesin step Nature 435 2005 308 312
49. A. Yildiz, and M. Tomishige R.D. Vale Intramolecular strain coordinates kinesin stepping behavior along microtubules Cell 134 2008 1030 1041
50. R. Nitta, and M. Kikkawa N. Hirokawa KIF1A alternately uses two loops to bind microtubules Science 305 2004 678 683
51. J. Helenius, and G. Brouhard J. Howard The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends Nature 441 2006 115 119
52. R.D. Astumian Thermodynamics and kinetics of a Brownian motor Science 276 1997 917 922
53. J. Roostalu, and C. Hentrich T. Surrey Directional switching of the kinesin Cin8 through motor coupling Science 332 2011 94 99
54. C. Branden, and J. Tooze Introduction to Protein Structure 1991 Garland Publishing New York
55. E. Fischer Einfluss der configuration auf die wirkung der enzyme Ber. Dt. Chem. Biol. 27 1894 2985 2993
56. D.E. Koshland Application of a Theory of Enzyme Specificity to Protein Synthesis Proc. Natl. Acad. Sci. USA 44 1958 98 104
57. B.A. Shoemaker, J.J. Portman, and P.G. Wolynes Speeding molecular recognition by using the folding funnel: the fly-casting mechanism Proc. Natl. Acad. Sci. USA 97 2000 8868 8873
58. O. Miyashita, J.N. Onuchic, and P.G. Wolynes Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins Proc. Natl. Acad. Sci. USA 100 2003 12570 12575
59. Y. Levy, and S.S. Cho P.G. Wolynes A survey of flexible protein binding mechanisms and their transition states using native topology based energy landscapes J. Mol. Biol. 346 2005 1121 1145
60. R.S. Spolar, and M.T. Record Jr. Coupling of local folding to site-specific binding of proteins to DNA Science 263 1994 777 784
61. H.J. Dyson, and P.E. Wright Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 6 2005 197 208
62. A.K. Dunker, and C.J. Brown Z. Obradović Intrinsic disorder and protein function Biochemistry 41 2002 6573 6582
63. W.O. Hancock, and J. Howard Kinesin's processivity results from mechanical and chemical coordination between the ATP hydrolysis cycles of the two motor domains Proc. Natl. Acad. Sci. USA 96 1999 13147 13152
64. S. Uemura, and S. Ishiwata Loading direction regulates the affinity of ADP for kinesin Nat. Struct. Biol. 10 2003 308 311
65. M.L. Moyer, S.P. Gilbert, and K.A. Johnson Pathway of ATP hydrolysis by monomeric and dimeric kinesin Biochemistry 37 1998 800 813
66. Y. Miyazono, and M. Hayashi H. Tadakuma Strain through the neck linker ensures processive runs: a DNA-kinesin hybrid nanomachine study EMBO J. 29 2010 93 106
67. T. Hugel, and N.B. Holland H.E. Gaub Single-molecule optomechanical cycle Science 296 2002 1103 1106
68. M.L. Kutys, J. Fricks, and W.O. Hancock Monte Carlo analysis of neck linker extension in kinesin molecular motors PLOS Comput. Biol. 6 2010 e1000980
69. J.D. Bryngelson, and J.N. Onuchic P.G. Wolynes Funnels, pathways, and the energy landscape of protein folding: a synthesis Proteins 21 1995 167 195
70. R.D. Astumian Thermodynamics and kinetics of molecular motors Biophys. J. 98 2010 2401 2409
71. D.D. Hackney, and M.F. Stock R.A. Patterson Modulation of kinesin half-site ADP release and kinetic processivity by a spacer between the head groups Biochemistry 42 2003 12011 12018
72. B.E. Clancy, and W.M. Behnke-Parks S.M. Block A universal pathway for kinesin stepping Nat. Struct. Mol. Biol. 18 2011 1020 1027
73. S.A. Endow, and H. Higuchi A mutant of the motor protein kinesin that moves in both directions on microtubules Nature 406 2000 913 916
74. Y. Okada, and N. Hirokawa Mechanism of the single-headed processivity: diffusional anchoring between the K-loop of kinesin and the C terminus of tubulin Proc. Natl. Acad. Sci. USA 97 2000 640 645
75. S. Lakämper, and E. Meyhöfer The E-hook of tubulin interacts with kinesin's head to increase processivity and speed Biophys. J. 89 2005 3223 3234
76. 1)-ATPase so high? J. Bioenerg. Biomembr. 32 2000 459 469
77. K. Kinosita Jr., and R. Yasuda K. Adachi A rotary molecular motor that can work at near 100% efficiency Philos. Trans. R. Soc. Lond. B Biol. Sci. 355 2000 473 489
78. I. Derényi, M. Bier, and R.D. Astumian Generalized efficiency and its application to microscopic engines Phys. Rev. Lett. 83 1999 903 906