Interaction of monomeric and dimeric kinesin with microtubules

Journal of Molecular Biology

Volumn 275, Issue 5, 1998, Pages 795-809

  Thormahlen M ^a   Marx, A ^a   Muller S A ^b   Song, Y H ^a   Mandelkow, E M ^a   Aebi, U ^b   Mandelkow, E ^a  

^a MAX PLANCK UNIT FOR STRUCTURAL MOLECULAR BIOLOGY   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Kinesin; Microtubule; Molecular motors; Tubulin

Indexed keywords

KINESIN;

ARTICLE; BIOCHEMISTRY; BIOPHYSICS; CONTROLLED STUDY; IMAGE RECONSTRUCTION; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN INTERACTION; RADIATION SCATTERING; STOICHIOMETRY; TRANSMISSION ELECTRON MICROSCOPY;

EID: 0039356659     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1503     Document Type: Article

References (57)

1. Amos, L. A., Henderson, R. & Unwin, P. N. (1982). Three-dimensional structure determination by electron microscopy of two-dimensional crystals. Prog. Biophys. Mol. Biol. 39, 183-231.
2. Amos, L. A. & Hirose, K. (1997). The structure of microtubule-motor complexes. Curr. Opin. Cell Biol. 9, 4-11.
3. Amrein, K. E., Takacs, B., Stieger, M., Molnos, J., Flint, N. A. & Burn, P. (1995). Purification and characterization of recombinant human p50csk protein-tyrosine kinase from an Escherichia coli expression system overproducing the bacterial chaperones GroES and GroEL. Proc. Natl Acad. Sci. USA, 92, 1048-1052.
4. Arnal, I., Metoz, F., DeBonis, S. & Wade, R. H. (1996). Three-dimensional structure of functional motor proteins on microtubules. Curr. Biol. 6, 1265-1270.
5. Bergen, L. G. & Borisy, G. G. (1980). Head-to-tail polymerization of microtubules in vitro. Electron microscope analysis of seeded assembly. J. Cell Biol. 84, 141-150.
6. Berliner, E., Young, E. C., Anderson, K., Mahtani, H. K. & Gelles, J. (1995). Failure of a single-headed kinesin to track parallel to microtubule protofilaments. Nature, 373, 718-721.
7. Binder, L. I., Dentler, W. L. & Rosenbaum, J. L. (1975). Assembly of chick brain tubulin onto flagellar microtubules from Chlamydomonas and sea urchin sperm. Proc. Natl Acad. Sci. USA, 72, 1122-1126.
8. Brady, S. T. (1995). A kinesin medley: biochemical and functional heterogeneity. Trends Cell Biol. 5, 159-164.
9. Chandrasekhar, G. N., Tilly, K., Woolford, C., Hendrix, R. & Georgopoulos, C. (1986). Purification and properties of the GroES morphogenetic protein of Escherichia coli. J. Biol. Chem. 261, 12414-12419.
10. Crevel, I. M., Lockhart, A. & Cross, R. A. (1996). Weak and strong states of kinesin and ncd. J. Mol. Biol. 257, 66-76.
11. Engel, A. (1978). Molecular weight determination by scanning transmission electron microscopy. Ultramicroscopy, 3, 273-281.
12. Erickson, H. P. (1974). Microtubule surface lattice and subunit structure and observations on reassembly. J. Cell Biol. 60, 153-67.
13. Fan, J., Griffiths, A. D., Lockhart, A., Cross, R. A. & Amos, L. A. (1996). Microtubule minus ends can be labelled with a phage display antibody specific to alpha-tubulin. J. Mol. Biol. 259, 325-330.
14. Gilbert, S., Moyer, M. & Johnson, K. A. (1998). Alternating site mechanism of the kinesin ATPase. Biochemistry, in the press.
15. Goodson, H. V., Valetti, C. & Kreis, T. E. (1997). Motors and membrane traffic. Curr. Opin. Cell Biol. 9, 18-28.
16. Hackney, D. D. (1994). Evidence for alternating head catalysis by kinesin during microtubule-stimulated ATP hydrolysis. Proc. Natl Acad. Sci. USA, 91, 6865-6869.
17. Harrison, B. C., Marchese-Ragona, S. P., Gilbert, S. P., Cheng, N., Steven, A. C. & Johnson, K. A. (1993). Decoration of the microtubule surface by one kinesin head per tubulin heterodimer. Nature, 362, 73-75.
18. Hirose, K., Lockhart, A., Cross, R. A. & Amos, L. A. (1995b). Nucleotide-dependent angular change in kinesin motor domain bound to tubulin. Nature, 376, 277-279.
19. Hirose, K., Fan, J. & Amos, L. A. (1995a). Re-examination of the polarity of microtubules and sheets decorated with kinesin motor domain. J. Mol. Biol. 251, 329-333.
20. Hirose, K., Lockhart, A., Cross, R. A. & Amos, L. A. (1996). Three-dimensional cryoelectron microscopy of dimeric kinesin and ncd motor domains on microtubules. Proc. Natl Acad. Sci. USA, 93, 9539-9544.
21. Hoenger, A. & Milligan, R. A. (1997). Motor domains of kinesin and ncd interact with microtubule protofilaments with the same binding geometry. J. Mol. Biol. 265, 553-564.
22. Hoenger, A. & Milligan, R. A. (1996). Polarity of 2-D and 3-D maps of tubulin sheets and motor decorated sheets. J. Mol. Biol. 263, 114-119.
23. Hoenger, A., Sablin, E. P., Vale, R. D., Fletterick, R. J. & Milligan, R. A. (1995). Three-dimensional structure of a tubulin-motor-protein complex. Nature, 376, 271-274.
24. Huang, T. G. & Hackney, D. D. (1994). Drosophila kinesin minimal motor domain expressed in Escherichia coli. Purification and kinetic characterization. J. Biol. Chem. 269, 16493-16501.
25. Huang, T. G., Suhan, J. & Hackney, D. D. (1994). Drosophila kinesin motor domain extending to amino acid position 392 is dimeric when expressed in Escherichia coli. J. Biol. Chem. 269, 16502-16507.
26. Inoue, Y., Toyoshima, Y. Y., Iwane, A. H., Morimoto, S., Higuchi, H. & Yanagida, T. (1997). Movements of truncated kinesin fragments with a short or an artificial flexible neck. Proc. Natl Acad. Sci. USA, 94, 7275-7280.
27. Jiang, W., Stock, M. F., Li, X. & Hackney, D. D. (1997). Influence of the kinesin neck domain on dimerization and ATPase kinetics. J. Biol. Chem. 272, 7626-7632.
28. Kikkawa, M., Ishikawa, T., Nakata, T., Wakabayashi, T. & Hirokawa, N. (1994). Direct visualization of the microtubule lattice seam both in vitro and in vivo. J. Cell Biol. 127, 1965-1971.
29. Kikkawa, M., Ishikawa, T., Wakabayashi, T. & Hirokawa, N. (1995). Three-dimensional structure of the kinesin head-microtubule complex. Nature, 376, 274-277.
30. Koch, M. J. H & Bordas, J. (1983). X-ray diffraction and scattering on disordered systems using synchrotron radiation. Nucl. Instrum. Methods, 208, 461-469.
31. Kosik, K. S., Orecchio, L. D., Schnapp, B., Inouye, H. & Neve, R. L. (1990). The primary structure and analysis of the squid kinesin heavy chain. J. Biol. Chem. 265, 3278-3283.
32. Kozielski, F. (1997). Die Röntgenstrukturanalyse des Motorproteins Kinesin. PhD thesis, Universität Hamburg, Germany.
33. Kozielski, F., Schönbrunn, E., Sack, S., Müller, J., Brady, S. T. & Mandelkow, E. (1997a). Crystallization and preliminary X-ray analysis of the single-headed and double-headed motor protein kinesin. J. Struct. Biol. 119, 28-34.
34. Kozielski, F., Sack, S., Marx, A., Thormählen, M., Schönbrunn, E., Biou, V., Thompson, A., Mandelkow, E.-M. & Mandelkow, E. (1997b). The crystal structure of dimeric kinesin and implications for microtubule-dependent motility. Cell, in the press.
35. Kull, F. J., Sablin, E. P., Lau, R., Fletterick, R. J. & Vale, R. D. (1996). Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature, 380, 550-555.
36. LeGendre, N. & Matsudaira, P. (1988). Direct protein microsequencing from Immobilon-P transfer membrane. Biotechniques, 6, 154-159.
37. Lewis, S. A., Tian, G., Vainberg, I. E. & Cowan, N. J. (1996). Chaperonin-mediated folding of actin and tubulin. J. Cell Biol. 132, 1-4.
38. Lockhart, A., Crevel, I. M. & Cross, R. A. (1995). Kinesin and ncd bind through a single head to microtubules and compete for a shared MT binding site. J. Mol. Biol. 249, 763-771.
39. Ma, Y. Z. & Taylor, E. W. (1997). Interacting head mechanism of microtubule-kinesin ATPase. J. Biol. Chem. 272, 724-30.
40. Mandelkow, E. M., Herrmann, M. & Ruhl, U. (1985). Tubulin domains probed by limited proteolysis and subunit-specific antibodies. J. Mol. Biol. 185, 311-327.
41. Marx, A., Jagla, A. & Mandelkow, E. (1990). Microtubule assembly and oscillations induced by flash photolysis of caged-GTP. Eur. Biophys. J. 19, 1-9.
42. Mitchison, T. J. (1993). Localization of an exchangeable GTP binding site at the plus end of microtubules. Science, 261, 1044-1047.
43. Morii, H., Takenawa, T., Arisaka, F. & Shimizu, T. (1997). Identification of kinesin neck region as a stable alpha-helical coiled coil and its thermodynamic characterization. Biochemistry, 36, 1933-1942.
44. Müller, S. A., Goldie, K. N., Bürki, R., Häring, R. & Engel, A. (1992). Factors influencing the precision of quantitative scanning transmission electron microscopy. Ultramicroscopy, 46, 317-334.
45. Murray, J. M. (1991). Structure of flagellar microtubules. Int. Rev. Cytol. 125, 47-93.
46. Sawin, K. E., Mitchison, T. J. & Wordeman, L. G. (1992). Evidence for kinesin-related proteins in the mitotic apparatus using peptide antibodies. J. Cell Sci. 101, 303-313.
47. Sack, S., Müller, J., Marx, A., Thormählen, M., Mandelkow, E.-M., Brady, S. T. & Mandelkow, E. (1997). X-ray structure of motor and neck domains from rat brain kinesin. Biochemistry, 36, 16155-16165.
48. Song, Y. H. & Mandelkow, E. (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.
49. Song, Y. H. & Mandelkow, E. (1995). The anatomy of flagellar microtubules: polarity, seam, junctions, and lattice. J. Cell Biol. 128, 81-94.
50. Studier, W. F., Rosenberg, A. H., Dunn, J. J. & Dubendorff, J. W. (1990). Use of T7 RNA polymerase to direct the expression of cloned genes. Methods Enzymol. 185, 60-89.
51. Svoboda, K., Schmidt, C. F., Schnapp, B. J. & Block, S. M. (1993). Direct observation of kinesin stepping by optical trapping interferometry. Nature, 365, 721-727.
52. Tripet, B., Vale, R. D. & Hodges, R. S. (1997). Demonstration of coiled-coil interactions within the kinesin neck region using synthetic peptides -implications for motor activity. J. Biol. Chem. 272, 8946-8956.
53. Tucker, C. & Goldstein, L. S. B. (1997). Probing the kinesin - microtubule interaction. J. Biol. Chem. 272, 9481-9488.
54. Wade, R. H. & Hyman, A. A. (1997). Microtubule structure and dynamics. Curr. Opin. Cell Biol. 9, 12-17.
55. Walker, R. A. (1995). Ned and kinesin motor domains interact with both alpha- and beta-tubulin. Proc. Natl Acad. Sci. USA, 92, 5960-5964.
56. Walker, R. A., Inoue, S. & Salmon, E. D. (1989). Asymmetric behavior of severed microtubule ends after ultraviolet-microbeam irradiation of individual microtubules in vitro. J. Cell Biol. 108, 931-937.
57. Yasukawa, T., Kanei-Ishii, C, Maekawa, T., Fujimoto, J., Yamamoto, T. & Ishii, S. (1995). Increase of solubility of foreign proteins in Escherichia coli by coproduction of the bacterial thioredoxin. J. Biol. Chem. 270, 25328-25331.