The C-terminus of tubulin increases cytoplasmic dynein and kinesin processivity

Biophysical Journal

Volumn 78, Issue 4, 2000, Pages 1955-1964

  Wang, Zhaohui ^a   Sheetz, Michael P ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; POTASSIUM CHLORIDE; SUBTILISIN; TUBULIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIFFUSION; EMBRYO; IONIC STRENGTH; MICROTUBULE; MICROTUBULE ASSEMBLY; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN DOMAIN; VELOCITY;

TRIXIS;

EID: 0034079578     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(00)76743-9     Document Type: Article

References (47)

1. Berliner, E., E. C. Young, K. Anderson, H. K. Mahtani, and J. Gelles. 1995. Failure of a single-headed kinesin to track parallel to microtubule protofilaments. Nature. 373:718-721.
2. Bhattacharyya, B., D. L. Sachett, and J. Wolff. 1985. Tubulin, hybrid dimers, and tubulin S. J. Biol. Chem. 260:10208-10216.
3. Block, S. M., L. S. Goldstein, and B. J. Schnapp. 1990. Bead movement by single kinesin molecules studied with optical tweezers. Nature. 348: 348-352.
4. Chandra, R., S. A. Endow, and E. D. Salmon. 1993. An N-terminal truncation of the ncd motor protein supports diffusional movement of microtubules in motility assays. J. Cell Sci. 104:899-906.
5. Coppin, C. M., J. T. Finer, J. A. Spudich, and R. D. Vale. 1996. Detection of sub-8-nm movements of kinesin by high-resolution optical-trap microscopy. Proc. Natl. Acad. Sci. USA. 93:1913-1917.
6. Coppin, C. M., D. W. Pierce, L. Hsu, and R. D. Vale. 1997. The load dependence of kinesin's mechanical cycle. Proc. Natl. Acad. Sci. USA. 94:8539-8544.
7. Gelles, J., B. J. Schnapp, and M. P. Sheetz. 1988. Tracking kinesin-driven movements with nanometre-scale precision. Nature. 331:450-453.
8. Hackney, D. D. 1995. Highly processive microtubule-stimulated ATP hydrolysis by dimeric kinesin head domains. Nature. 377:448-450.
9. Hackney, D. D. 1996. The kinetic cycles of myosin, kinesin, and dynein. Annu. Rev. Physiol. 58:731-750.
10. Hagiwara, H., H. Yorifuji, R. Sato-Yoshitake, and N. Hirokawa. 1994. Competition between motor molecules (kinesin and cytoplasmic dynein) and fibrous microtubule-associated proteins in binding to microtubules. J. Biol. Chem. 269:3581-3589.
11. Hancock, W. O., and J. Howard. 1998. Processivity of the motor protein kinesin requires two heads. J. Cell Biol. 140:1395-1405.
12. Heins, S., Y. H. Song, H. Wille, E. Mandelkow, and E. M. Mandelkow. 1991. Effect of MAP2, MAP2c, and tau on kinesin-dependent microtubule motility. J. Cell Sci. (Suppl.) 14:121-124.
13. Hirose, K., J. Fan, and L. A. Amos. 1995. Re-examination of the polarity of microtubules and sheets decorated with kinesin motor domain. J. Mol. Biol. 251:329-333.
14. Hirose, K., A. Lockhart, R. A. Cross, and L. A. Amos. 1996. Three-dimensional cryoelectron microscopy of dimeric kinesin and ncd motor domains on microtubules. Proc. Natl. Acad. Sci. USA. 93:9539-9544.
15. Hoenger, A., and R. A. Milligan. 1997. Motor domains of kinesin and ncd interact with microtubule protofilaments with the same binding geometry. J. Mol. Biol. 265:553-564.
16. Hunt, A. J., F. Gittes, and J. Howard. 1994. The force exerted by a single kinesin molecule against a viscous load. Biophys. J. 67:766-781.
17. Krauhs, E., M. Little, T. Kempf, R. Hofer-Warbineki, and H. Ponstingl. 1981. Complete amino acid sequence of beta-tubulin from porcine brain. Proc. Natl. Acad. Sci. USA. 78:4156-4160.
18. Kull, F. J., E. P. Sablin, R. Lau, R. J. Fletterick, and R. D. Vale. 1996. Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature. 380:550-555.
19. Li, Q., and H. C. Joshi. 1995. Gamma-tubulin is a minus end-specific microtubule binding protein. J. Cell Biol. 131:207-214.
20. Little, M., E. Krauhs, and H. Ponstingl. 1981. Tubulin sequence conservation. Biosystems. 14:239-246.
21. Lopez, L. A., and M. P. Sheetz. 1993. Steric inhibition of cytoplasmic dynein and kinesin motility by MAP2. Cell Motil. Cytoskeleton. 24: 1-16.
22. Marya, P. K., Z. Syed, P. E. Fraylich, and P. A. Eagles. 1994. Kinesin and tau bind to distinct sites on microtubules. J. Cell Sci. 107:399-344.
23. Mitchison, T. J. 1993. Localization of an exchangeable GTP binding site at the plus end of microtubules. Science. 261:1044-1047.
24. Nogales, E., S. G. Wolf, and K. H. Downing. 1998. Structure of the αβ tubulin dimer by electron crystallography. Nature. 391:199-203.
25. Paschal, B. M., R. A. Obar, and R. B. Vallee. 1989. Interaction of brain cytoplasmic dynein and MAP2 with a common sequence at the C terminus of tubulin. Nature. 342:569-572.
26. Ponstingl, H., E. Krauhs, M. Little, and T. Kempf. 1981. Complete amino acid sequence ot alpha-tubulin from porcine brain. Proc. Natl. Acad. Sci. USA. 78:2757-2761.
27. Rodionov, V. I., F. K. Gyoeva, A. S. Kashina, S. A. Kuznetsov, and V. I. Gelfand. 1990. Microtubule-associated proteins and microtubule-based translocators have different binding sites on tubulin molecule. J. Biol. Chem. 265:5702-5707.
28. Romberg, L., D. W. Pierce, and R. D. Vale. 1998. Role of the kinesin neck region in processive microtubule-based motility. J. Cell Biol. 140: 1407-1416.
29. Roopnarine, O., and D. D. Thomas. 1996. Orientation of intermediate nucleotide states of indane dione spin-labeled myosin heads in muscle fibers. Biophys. J. 70:2795-2806.
30. Sablin, E. P., F. J. Kull, R. Cooke, R. D. Vale, and R. J. Fletterick. 1996. Crystal structure of the motor domain of the kinesin-related motor ncd. Nature. 380:555-559.
31. Sackett, D. L., B. Bhattacharyya, and J. Wolff. 1985. Tubulin subunit carboxyl termini determine polymerization efficiency. J. Biol. Chem. 260:43-45.
32. Sackett, D. L., and J. Wolff. 1986. Proteolysis of tubulin and the substructure of the tubulin dimer. J. Biol. Chem. 261:9070-9076.
33. Schroer, T. A., E. R. Steuer, and M. P. Sheetz, 1989. Cytoplasmic dynein is a minus-end directed motor for membranous organelles. Cell. 56: 937-946.
34. Serrano, L., J. Avila, and R. B. Maccioni. 1984a. Controlled proteolysis of tubulin by subtilisin: localization of the site for MAP2 interaction. Biochemistry. 23:4675-4681.
35. Serrano, L., J. De La Torre, R. B. Maccioni, and J. Avila. 1984b. Involvement of the carboxyl-terminal domain of tubulin in the regulation of its assembly. Proc. Natl. Acad. Sci. USA. 81:5989-5993.
36. Steuer, E. R., L. Wordeman, T. A. Schroer, and M. P. Sheetz. 1990. Localization of cytoplasmic dynein to mitotic spindles and kinetochores. Nature. 345:266-268.
37. Svoboda, K., P. P. Mitra, and S. M. Block. 1994. Fluctuation analysis of motor protein movement and single enzyme kinetics. Proc. Natl. Acad. Sci. USA. 91:11782-11786.
38. 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.
39. Tripet, B., R. D. Vale, and R. S. Hodges. 1997. Demonstration of coiled-coil interactions within the kinesin neck region using synthetic peptides. Implications for motor activity. J. Biol. Chem. 272:8946-8956.
40. Tucker, C., and L. S. B. Goldstein. 1997. Probing the kinesin-microtubule interaction. J. Biol. Chem. 272:9481-9488.
41. Vale, R. D., T. Funatsu, D. W. Pierce, L. Romberg, Y. Harada, and T. Yanagida. 1996. Direct observation of single kinesin molecules moving along microtubules. Nature. 380:451-453.
42. Van Dijk, J., C. Fernandez, and P. Chaussepied. 1998. Effect of ATP analogues on the actin-myosin interface. Biochemistry. 37:8385-8394.
43. Wade, R. H., and D. Chretien. 1993. Cryoelectron microscopy of microtubules. J. Struct. Biol. 110:1-27.
44. Wang, Z., S. Khan, and M. P. Sheetz. 1995. Single cytoplasmic dynein molecule movements: characterization and comparison with kinesin. Biophys. J. 69:2011-2023.
45. Wang, Z., and M. P. Sheetz. 1999. One-dimensional diffusion on microtubules of particles coated with cytoplasmic dynein and immunoglobulins. Cell Struct. Fund. 24:373-383.
46. White, E. A., P. R. Burton, and R. H. Himes. 1987. Polymorphic assembly of subtilisin-cleaved tubulin. Cell Motil. Cytoskeleton. 7:31-38.
47. Woehlke, G., A. K. Ruby, C. L. Hart, B. Ly, N. Hom-Booher, and R. D. Vale. 1997. Microtubule interaction site of the kinesin motor. Cell. 90:207-216.