Directed binding: A novel physical mechanism that describes the directional motion of two-headed kinesin motor proteins

Cell Biochemistry and Biophysics

Volumn 42, Issue 2, 2005, Pages 95-119

  Bolterauer, H ^a   Tuszynski, J A ^b   Unger, E ^c  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b UNIVERSITY OF ALBERTA   (Canada)

^c FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

Fokker Planck equation; Kinesin; Langevin equation; Motor protein; Ncd; Reaction kinetics

Indexed keywords

EID: 24644443289     PISSN: 10859195     EISSN: None     Source Type: Journal    
DOI: 10.1385/cbb:42:2:095     Document Type: Article

References (66)

1. Schliwa, M., ed. (2003) Molecular Motors, Wiley-VCH, Weinheim.
2. Howard, J. (2001) Mechanics of Motor Proteins and the Cytoskeleton, Sinauer Associates Inc., Sunderland, MA.
3. Kozielski, F., Sack, S., Marx, A., Thormahlen, M., Schonbrunn, E., Biou, V., Thompson, A., Mandelkow, E.-M., and Mandelkow, E. (1997) The crystal structure of dimeric kinesin and implications for microtubule-dependent motility. Cell 91, 985-994.
4. Bloom, G. S., Wagner, M. C., Pfister, K. K., and Brady, S. T. (1988) Native structure and physical properties of bovine brain kinesin and identification of the ATP-binding subunit polypeptide. Biochem 27, 3409-3416.
5. Kuznetsov, S. A. and Gelfand, V. I. (1986) Bovine brain kinesin is a microtubule-activated ATPase. Proc. Natl. Acad. Sci. USA 83, 8530-8534.
6. Scholey, J. M., Heusner, J., Yang, J. T., and Goldstein, L. S. (1989) Identification of globular mechanochemical heads of kinesin. Nature 338, 355-357.
7. Hirokawa, N., Pfister, K. K., Yorifuji, H., Wagner, M. C., Brady, S. T., and Bloom, G. S. (1989) Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration. Cell 56, 867-878.
8. Amos, L. A. and Cross, R. (1997) Structure and dynamics of molecular motors. Curr. Opin. Struct. Biol. 7, 239-246.
9. Verhey, K. J., Lizotte, D. L., Abramson, T., Barenboim, L., Schnapp, B. J., and Rapoport, T. (1998) Light chain-dependent regulation of kinesin's interaction with microtubules. J. Cell Biol. 143, 1053-1066.
10. Song, Y. H., Marx, A., Muller, J., Woelke, G., Schliewa, M., Krebs, A., Hoenger, A., and Mandelkow, E. (2001) Structure of fast kinesin: implications for ATPase mechanism and interactions with microtubules. EMBO J. 15, 6213-6225.
11. Han, Y., Sablin, E. P., Nogales, E., and Downing, R. J. F. K. H. (1999) Visualizing a new binding site of Ncd-motor domain on tubulin. J. Struct. Biol. 128, 26-33.
12. Block, S. M., Goldstein, L. S., and Schnapp, B. J. (1990) Bead movement by single kinesin molecules studied with optical tweezers. Nature 348, 348-352.
13. Crevel, I. M., Lockhart, A., and Cross, R. A. (1997) Kinetic evidence for low chemical processivity in Ncd and Eg5. J. Mol. Biol. 273, 160-170.
14. Hancock, W. O. and Howard, J. (1998) Processivity of the motor protein kinesin requires two heads. J. Cell Biol. 140, 1395-1405.
15. Howard, J., Hudspeth, A. J., and Vale, R. D. (1989) Movement of microtubules by single kinesin molecules. Nature 342, 154-158.
16. Mandelkow, E. and Johnson, K. A. (1998) The structural and mechanochemical cycle of kinesin. Trends Biochem. Sci. 23, 429-433.
17. Boehm, K. J., Steinmetzer, P., Daniel, A., Vater, W., Baum, M., and Unger, E. (1997) Kinesin-driven microtubule motility in the presence of alkaline-earth metal ions: indication for calcium ion-dependent motility. Cell Motil. Cytoskeleton 37, 226-231.
18. Vale, R. D., Reese, T. S., and Sheetz, M. P. (1985) Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42, 39-50.
19. von Massow, A., Mandelkow, E. M., and Mandelkow, E. (1989) Interaction between kinesin, microtubules, and microtubule-associated protein 2. Cell Motil Cytoskeleton 14, 562-571.
20. Cole, D. G. and Scholey J. M. (1995) Structural variations among the kinesins. Trends Cell Biol. 5, 259-262.
21. Hackney, D. D. (1995) Motor proteins. Polar explorations. Nature 376, 215-216.
22. Hackney, D. D. (1996) The kinetic cycles of myosin, kinesin, and dynein. Annu. Rev. Physiol. 58, 731-750.
23. Coy, D. L., Wagenbach, M., and Howard, J. (1999) Kinesin takes one 8-nm step for each ATP that it hydrolyzes. J. Biol. Chem. 274, 3667-3671.
24. Ray, S., Meyhoefer, E., Milligan, R. A., and Howard, J. (1993) Kinesin follows the microtubule's protofilament axis. J. Cell. Biol. 121, 1083-1093.
25. Young, E. C., Mahtani, H. K., and Gelles, J. (1998) One-headed kinesin derivatives move by a non-processive, low duty ratio mechanism unlike that of two-headed kinesin. Biochemistry 37, 3467-3479.
26. Inoue, Y., Iwane, A. H., Miyai, T., Muto, E., and Yanagida, T. (2001) Motility of single one-headed kinesin molecules along microtubules. Biophys. J. 81, 2838-2850.
27. Tomishige, M., Klopfenstein, D. R., and Vale, R. (2002) Conversion of Unc104/KIF1A kinesin into a processive motor after dimerization. Science 297, 2263-2267.
28. Okada, Y. and Hirokawa, N. (2000) 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, 640-645.
29. Magnasco, M. O. (1993) Forced thermal ratchets. Phys. Rev. Lett. 71, 1477-1481.
30. Magnasco, M. O. (1994) Molecular combustion motors. Phys. Rev. Lett. 72, 2656-2659.
31. Huxley, A. F. (1957) Muscle structure and theories of contraction. Biophys. Chem. J. 7, 257-318.
32. Leibler, S. and Huse, D. A. (1993) Porters versus rowers: a unified stochastic model of motor proteins. J. Cell Biol. 121, 1357-1368.
33. Schnitzer, M. J., Visscher, K., and Block, S. (2000) Force production by single kinesin motors. Nature Cell Biol 2, 718-723.
34. Fisher, M. E. and Kolomeisky A. B. (1999) The force exerted by a molecular motor. Proc. Natl. Acad. Sci. U S A 96, 6597-6602.
35. Peskin, C. S. and Oster, G. (1995) Coordinated hydrolysis explains the mechanical behavior of kinesin. Biophys. J. 68, 202S-211S.
36. Mogilner, A., Fisher, A. J., and Baskin, R. J. (2001) Structural changes in the neck linker of kinesin explain the load dependence of the motor's mechanical cycle. J. Theor. Biol. 211, 143-157.
37. Block, S. M. (1995) Nanometres and piconewtons: the macoromolecular mechanics of kinesin. Trends Cell Biol. 5, 169-175.
38. Hancock, W. O. and Howard, J. (2003) Kinesin: processivity and chemomechanical coupling, in Molecular Motors (Schliwa, M., ed.), Wiley-VCI, Weinheim, pp. 243-269.
39. Keller, D. and Bustamante, C. (2000) The mechanochemistry of molecular motors. Biophys. J. 78, 541-556.
40. Cross, R. A. (2004) The kinetic mechanism of kinesin. Trends Biochem. Sci. 29, 301-309.
41. Doering, C. R., Horsthemke, W., and Riordan, J. (1994) Nonequilibrium fluctuation-induced transport. Phys. Rev. Lett. 72, 2984-2987.
42. Astumian, R. D. and Bier, M. (1994) Fluctuation driven ratchets: molecular motors. Phys. Rev. Lett. 72, 1766-1769.
43. Prost, J., Chauwin, J. P., Peliti, L., and Ajdari, A. (1994) Asymmetric pumping of particles. Phys Rev Lett 72, 2652-2655.
44. Bier, M. and Astumian, R. D. (1996) Biased brownian motion as the operating principle for microscopic engines. Bioelectrochem. Bioenerg. 39, 67-75.
45. Astumian, R. D. (1997) Thermodynamics and kinetics of a brownian motor. Science 276, 917-922.
46. Jülicher, F., Adjari, A., and Prost, J. (1997) Modeling molecular motors. Rev. Mod. Phys. 69, 1269-1282.
47. Abad, E. and Mielke, A. (1998) Ann. Phys. 7, 9-23.
48. Derényi, I. and Vicsek, T. (1996) The kinesin walk: a dynamic model with elastically coupled heads. Proc. Natl. Acad. Sci. USA 93, 6775-6779.
49. Visscher, K., Schnitzer, M. J., and Block, S. M. (1999) Single kinesin molecules studied with a molecular force clamp. Nature 400, 184-189.
50. Lipowsky, R. and Harms, T. (2000) Molecular motors and nonuniform ratchets. Eur. Biophys. J. 29, 542-548.
51. Coppin, C. M., Pierce, D. W., Hsu, L., and Vale, R. D. (1997) The load dependence of kinesin's mechanical cycle. Proc. Natl Acad. Sci USA 94, 8539-8544.
52. Astumian, R. D. and Derenyi, I. (1999) A chemically reversible brownian motor: application to kinesin and Ncd. Biophys. J. 77, 993-1002.
53. Ajdari, A. (1994) Force free motion in asymmetric environment: a simple model for structured objects. J. Phys. I (France) 4, 1577-1582.
54. Duke, T. and Leibler, S. (1996) Motor protein mechanics: a stochastic model with minimal mechanochemical coupling. Biophys. J. 71, 1235-1247.
55. Endow, S. A. (1999) C-terminal motor kinesin proteins, in Guidebook to the Cytoskeletal and Motor Proteins, (Kreis, T. and Vale, R., eds.), Oxford University Press, Oxford, pp. 365-486.
56. Endow, S. A. (2003) Molecular Motors, Wiley-VCI, Weinheim, chap. Molecular Motor Directionality.
57. Arnal, I. and Wade, R. H. (1998) Nucleotide-dependent conformations of the KN dimer interacting with microtubules. Structure 6, 33-38.
58. Hirose, K., Henningsen, U., Schliwa, M., Toyoshima, C., Shimizu, T., Alonso, M., Cross, R. A., and Amos, L. A. (2000) Structural comparison of dimeric Eg5, Neurospora kinesin (Nkin) and Ncd head-Nkin neck chimera with conventional kinesin. EMBO J. 19, 5308-5314.
59. Mandelkow, E. and Hoenger, A. (1999) Structures of kinesin and kinesin-microtubule interactions. Curr. Opin. Cell. Biol. 11, 34-44.
60. Boal, D. (2002) Mechanics of the Cell, Cambridge University Press, Cambridge.
61. Bolterauer, H. and Tuszynski, J. A. (2002) A model of directed binding to microtubules by kinesin and Ncd motor proteins. Intl J Nonlin Sci Numerical Simulation (IJNSNS) 3, 185-190.
62. Meyhöfer, E. and Howard, J. (1995) The force generated by a single kinesin molecule against an elastic load. Proc. Natl. Acad. Sci. USA 92, 574-578.
63. Svoboda, K. and Block, S. M. (1994) Force and velocity measured for single kinesin molecules. Cell 77, 773-784.
64. Hua, W., Chung, J., and Gelles, J. (2002) Distinguishing inchworm and hand-over-hand processive kinesin movement by neck rotaion measurements. Science 295, 844-848.
65. Asbury C. L., Fehr, A. N., and Block, S. M. (2003) Kinesin moves by an asymmetric hand-over-hand mechanism. Science 3002, 2130-2134.
66. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MolMol: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55, 29-32.