The E-hook of tubulin interacts with kinesin's head to increase processivity and speed

Biophysical Journal

Volumn 89, Issue 5, 2005, Pages 3223-3234

  Lakämper, Stefan ^a,b,c   Meyhöfer, Edgar ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; DIMER; KINESIN; MOLECULAR MOTOR; MONOMER; TUBULIN;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; FORCE; MICROTUBULE; MOLECULAR INTERACTION; NEUROSPORA CRASSA; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; VELOCITY;

NEUROSPORA CRASSA;

EID: 27744552948     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.057505     Document Type: Article

References (55)

1. Vale, R. D. 2003. The molecular motor toolbox for intracellular transport. Cell. 112:467-480.
2. Vale, R. D., T. S. Reese, and M. P. Sheetz. 1985. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell. 42:39-50.
3. Brady, S. T. 1985. A novel brain ATPase with properties expected for the fast axonal transport motor. Nature. 317:73-75.
4. Kuznetsov, S. A., E. A. Vaisberg, N. A. Shanina, N. N. Magretova, V. Y. Chernyak, and V. I. Gelfand. 1988. The quaternary structure of bovine brain kinesin. EMBO J. 7:353-356.
5. Scholey, J. M., J. Heuser, J. T. Yang, and L. S. Goldstein. 1989. Identification of globular mechanochemical heads of kinesin. Nature. 338:355-357.
6. Bloom, G. S., M. C. Wagner, K. K. Pfister, and S. T. Brady. 1988. Native structure and physical properties of bovine brain kinesin and identification of the ATP-binding subunit polypeptide. Biochemistry. 27:3409-3416.
7. de Cuevas, M., T. Tao, and L. S. Goldstein. 1992. Evidence that the stalk of Drosophila kinesin heavy chain is an alpha-helical coiled coil. J. Cell Biol. 116:957-965.
8. Kosik, K. S., L. D. Orecchio, B. Schnapp, H. Inouye, and R. L. Neve. 1990. The primary structure and analysis of the squid kinesin heavy chain. J. Biol. Chem. 265:3278-3283.
9. Grummt, M., G. Woehlke, U. Henningsen, S. Fuchs, M. Schleicher, and M. Schliwa. 1998. Importance of a flexible hinge near the motor domain in kinesin-driven motility. EMBO J. 17:5536-5542.
10. Hackney, D. D., J. D. Levitt, and J. Suhan. 1992. Kinesin undergoes a 9 S to 6 S conformational transition. J. Biol. Chem. 267:8696-8701.
11. Hackney, D. D., and M. F. Stock. 2000. Kinesin's IAK tail domain inhibits initial microtubule-stimulated ADP release. Nat. Cell Biol. 2: 257-260.
12. Seiler, S., J. Kirchner, C. Horn, A. Kallipolitou, G. Woehlke, and M. Schliwa. 2000. Cargo binding and regulatory sites in the tail of fungal conventional kinesin. Nat. Cell Biol. 2:333-338.
13. Hackney, D. D. 1995. Highly processive microtubule-stimulated ATP hydrolysis by dimeric kinesin head domains. Nature. 377:448-450.
14. Huang, T. G., J. Suhan, and D. D. Hackney. 1994. Drosophila kinesin motor domain extending to amino acid position 392 is dimeric when expressed in Escherichia coli. J. Biol. Chem. 269:16502-16507.
15. Gilbert, S. P., M. L. Moyer, and K. A. Johnson. 1998. Alternating site mechanism of the kinesin ATPase. Biochemistry. 37:792-799.
16. Howard, J., A. J. Hudspeth, and R. D. Vale. 1989. Movement of microtubules by single kinesin molecules. Nature. 342:154-158.
17. Vale, R. D., T. Funatsu, D. W. Pierce, I. Romberg, Y. Harada, and T. Yanagida. 1996. Direct observation of single kinesin molecules moving along microtubules. Nature. 380:451-453.
18. Svoboda, K., C. F. Schmidt, B. J. Schnapp, and S. M. Block. 1993. Direct observation of kinesin stepping by optical trapping interferometry. Nature. 365:721-727.
19. Hua, W., E. C. Young, M. L. Fleming, and J. Gelles. 1997. Coupling of kinesin steps to ATP hydrolysis. Nature. 388:390-393.
20. Schnitzer, M. J., and S. M. Block. 1997. Kinesin hydrolyses one ATP per 8-nm step. Nature. 388:386-390.
21. Yildiz, A., M. Tomishige, R. D. Vale, and P. R. Selvin. 2004. Kinesin walks hand-over-hand. Science. 303:676-678.
22. Hancock, W. O., and J. Howard. 1999. Kinesin's processivity results from mechanical and chemical coordination between the ATP hydrolysis cycles of the two motor domains. Proc. Natl. Acad. Sci. USA. 96:13147-13152.
23. Rosenfeld, S. S., P. M. Fordyce, G. M. Jefferson, P. H. King, and S. M. Block. 2003. Stepping and stretching. How kinesin uses internal strain to walk processively. J. Biol. Chem. 278:18550-18556.
24. Lakämper, S., A. Kallipolitou, G. Woehlke, M. Schliwa, and E. Meyhöfer. 2003. Single fungal kinesin motor molecules move processively along microtubules. Biophys. J. 84:1833-1843.
25. Howard, J. 1993. Molecular motors. One giant step for kinesin. Nature. 365:696-697.
26. Wang, Z., and M. P. Sheetz. 2000. The C-terminus of tubulin increases cytoplasmic dynein and kinesin processivity. Biophys. J. 78:1955-1964.
27. Thorn, K. S., J. A. Ubersax, and R. D. Vale. 2000. Engineering the processive run length of the kinesin motor. J. Cell Biol. 151:1093-1100.
28. Redeker, V., R. Melki, D. Prome, J. P. Le Caer, and J. Rossier. 1992. Structure of tubulin C-terminal domain obtained by subtilisin treatment. The major alpha and beta tubulin isotypes from pig brain are glutamylated. FEBS Lett. 313:185-192.
29. Nogales, E., S. G. Wolf, and K. H. Downing. 1998. Structure of the alpha beta tubulin dimer by electron crystallography. Nature. 391: 199-203.
30. Mandelkow, E. M., M. Herrmann, and U. Ruhl. 1985. Tubulin domains probed by limited proteolysis and subunit-specific antibodies. J. Mol. Biol. 185:311-327.
31. Bhattacharyya, B., D. L. Sackett, and J. Wolff. 1985. Tubulin, hybrid dimers, and tubulin S. Stepwise charge reduction and polymerization. J. Biol. Chem. 260:10208-10216.
32. Steinberg, G., and M. Schliwa. 1996. Characterization of the biophysical and motility properties of kinesin from the fungus Neurospora crassa. J. Biol. Chem. 271:7516-7521.
33. Crevel, I., N. Carter, M. Schliwa, and R. Cross. 1999. Coupled chemical and mechanical reaction steps in a processive Neurospora kinesin. EMBO J. 18:5863-5872.
34. Kallipolitou, A., D. Deluca, U. Majdic, S. Lakamper, R. Cross, E. Meyhofer, L. Moroder, M. Schliwa, and G. Woehlke. 2001. Unusual properties of the fungal conventional kinesin neck domain from. Neurospora crassa. EMBO J. 20:6226-6235.
35. Schafer, F., D. Deluca, U. Majdic, J. Kirchner, M. Schliwa, L. Moroder, and G. Woehlke. 2003. A conserved tyrosine in the neck of a fungal kinesin regulates the catalytic motor core. EMBO J. 22: 450-458.
36. Inoue, Y., A. Hikikoshi Iwane, T. Miyai, E. Muto, and T. Yanagida 2001. Motility of single one-headed kinesin molecules along microtubules. Biophys. J. 81:2838-2850.
37. Inoue, Y., Y. Y. Toyoshima, A. H. Iwane, S. Morimoto, H. Higuchi, and T. Yanagida. 1997. Movements of truncated kinesin fragments with a short or an artificial flexible neck. Proc. Natl. Acad. Sci. USA. 94:7275-7280.
38. Huang, T. G., and D. D. Hackney. 1994. Drosophila kinesin minimal motor domain expressed in Escherichia coli. Purification and kinetic characterization. J. Biol. Chem. 269:16493-16501.
39. Grummt, M., S. Pistor, F. Lottspeich, and M. Schliwa. 1998. Cloning and functional expression of a 'fast' fungal kinesin. FEBS Lett. 427:79-84.
40. Klumpp, L. M., K. M. Brendza, J. M. Rosenberg, A. Hoenger, and S. P. Gilbert. 2003. Motor domain mutation traps kinesin as a microtubule rigor complex. Biochemistry. 42:2595-2606.
41. Skiniotis, G., J. C. Cochran, J. Muller, E. Mandelkow, S. P. Gilbert, and A. Hoenger. 2004. Modulation of kinesin binding by the C-termini of tubulin. EMBO J. 23:989-999.
42. Mandelkow, E., and A. Hoenger. 1999. Structures of kinesin and kinesin-microtubule interactions. Curr. Opin. Cell Biol. 11:34-44.
43. Song, Y. H., and E. Mandelkow. 1993. Recombinant kinesin motor domain binds to beta-tubulin and decorates microtubules with a B surface lattice. Proc. Natl. Acad. Sci. USA. 90:1671-1675.
44. Visscher, K., M. J. Schnitzer, and S. M. Block. 1999. Single kinesin molecules studied with a molecular force clamp. Nature. 400:184-189.
45. Hancock, W. O., and J. Howard. 1998. Processivity of the motor protein kinesin requires two heads. J. Cell Biol. 140:1395-1405.
46. Moyer, M. L., S. P. Gilbert, and K. A. Johnson. 1996. Purification and characterization of two monomeric kinesin constructs. Biochemistry. 35:6321-6329.
47. Ma, Y. Z., and E. W. Taylor. 1995. Kinetic mechanism of kinesin motor domain. Biochemistry. 34:13233-13241.
48. Steinberg, G., and M. Schliwa. 1995. The Neurospora organelle motor: a distant relative of conventional kinesin with unconventional properties. Mol. Biol. Cell. 6:1605-1618.
49. Kozielski, F., S. Sack, A. Marx, M. Thormahlen, E. Schonbrunn, V. Biou, A. Thompson, E. M. Mandelkow, and E. Mandelkow. 1997. The crystal structure of dimeric kinesin and implications for microtubule-dependent motility. Cell. 91:985-994.
50. Jimenez, M. A., J. A. Evangelio, C. Aranda, A. Lopez-Brauet, D. Andreu, M. Rico, R. Lagos, J. M. Andreu, and O. Monasterio. 1999. Helicity of alpha(404-451) and beta(394-445) tubulin C-terminal recombinant peptides. Protein Sci. 8:788-799.
51. Tomishige, M., and R. D. Vale. 2000. Controlling kinesin by reversible disulfide cross-linking. Identifying the motility-producing conformational change. J. Cell Biol. 151:1081-1092.
52. Kirchner, J., S. Seiler, S. Fuchs, and M. Schliwa. 1999. Functional anatomy of the kinesin molecule in vivo. EMBO J. 18:4404-4413.
53. Tripet, B., and R. S. Hodges. 2002. Helix capping interactions stabilize the N-terminus of the kinesin neck coiled-coil. J. Struct. Biol. 137: 220-235.
54. Westermann, S., and K. Weber. 2003. Post-translational modifications regulate microtubule function. Nat. Rev. Mol. Cell Biol. 4: 938-947.
55. Rosenbaum, J. 2000. Cytoskeleton: functions for tubulin modifications at last. Curr. Biol. 10:R801-R803.