Image reconstructions of microtubules decorated with monomeric and dimeric kinesins: Comparison with x-ray structure and implications for motility

Journal of Cell Biology

Volumn 141, Issue 2, 1998, Pages 419-430

  Hoenger, A ^a,c   Sack, S ^b   Thormahlen M ^b   Marx, A ^b   Muller J ^b   Gross, H ^a   Mandelkow, E ^b  

^a ETH ZURICH   (Switzerland)

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

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN; TUBULIN;

ARTICLE; CELL MOTILITY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; MICROTUBULE; MICROTUBULE ASSEMBLY; PRIORITY JOURNAL; STOICHIOMETRY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; IMAGE PROCESSING, COMPUTER-ASSISTED; KINESIN; MICROSCOPY, ELECTRON; MICROTUBULES; PROTEIN CONFORMATION; RATS; TUBULIN;

EID: 0032550175     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.2.419     Document Type: Article

References (74)

1. Amos, L.A., and K. Hirose. 1997. The structure of microtubule-motor complexes. Curr. Opin. Cell Biol. 9:4-11.
2. Anson, M., M.A. Geeves, S.E. Kurzawa, and D.J. Manstein. 1996. Myosin motors with artificial lever arms. EMBO (Eur. Mol. Biol. Organ.) J. 15:6069-6074.
3. Arnal, I., F. Metoz, S. DeBonis, and R.H. Wade. 1996. Three-dimensional structure of functional motor proteins on microtubules. Curr. Biol. 6:1265-1270.
4. 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.
5. Brady, S.T. 1995. A kinesin medley: biochemical and functional heterogeneity. Trends Cell Biol. 5:159-164.
6. Case, R.B., D.W. Pierce, N. Hom-Booher, C.L. Hart, and R.D. Vale. 1997. The directional preference of kinesin motors is specified by an element outside of the motor catalytic domain. Cell. 90:959-966.
7. Cole, D., and J.M. Scholey. 1995. Structural variations among the kinesins. Trends Cell Biol. 5:259-262.
8. Coppin, C.M., J.T. Finer, J.A. Spudich, and R.D. Vale. 1996. Detection of sub8-nm movements of kinesin by high-resolution optical-trap microscopy. Proc. Natl. Acad. Sci. USA. 93:1913-1917.
9. Correia, J.J., S.P. Gilbert, M.L. Moyer, and K.A. Johnson. 1995. Sedimentation studies on the kinesin motor domain constructs K401, K366, and K341. Biochemistry. 34:4898-4907.
10. Crevel, I.M., A. Lockhart, and R. A. Cross. 1996. Weak and strong states of kinesin and ncd. J. Mol. Biol. 257:66-76.
11. Cross, R.A. 1995. On the hand-over-hand footsteps of kinesin heads. J. Muscle Res. Cell Motil. 16:91-94.
12. Dubochet, J., M. Adrian, J. Lepault, and A.W. McDowall. 1985. Cryo-electron microscopy of vitrified biological specimens. Trends Biochem. Sci. 10:143-146.
13. Fisher, A.J., C.A. Smith, J.B. Thoden, R. Smith, K. Sutoh, H.M. Holden, and I. Rayment. 1995. X-ray structures of the myosin motor domain of Dictyostelium discoideum complexed with MgADP.BeFx and MgADP.AlF4. Biochemistry. 34:8960-8972.
14. Gilbert, S.P., M.R. Webb, M. Brune, and K.A. Johnson. 1995. Pathway of processive ATP hydrolysis by kinesin. Nature. 373:671-676.
15. Gilbert, S.P., M.L. Moyer, and K.A. Johnson. 1998. Alternating site mechanism of the kinesin ATPase. Biochemistry. 37:792-799.
16. Goldstein, L.S.B. 1993. With apologies to Scheherazade: Tails of 1001 kinesin motors. Annu. Rev. Genet. 27:319-351.
17. Gross, H., K. Krusche, and P. Tittmann. 1990. Recent progress in high resolution shadowing for biological TEM. X11th Intl. Cong. Electron Microsc. Seattle, WA. 510-511.
18. Hackney, D.D. 1994. Evidence for alternating head catalysis by kinesin during microtubule-stimulated ATP hydrolysis. Proc. Natl. Acad. Sci. USA. 91: 6865-6869.
19. Harrison, B.C., S.P. Marchese-Ragona, S.P. Gilbert, N. Cheng, A.C. Steven, and K.A. Johnson. 1993. Decoration of the microtubule surface by one kinesin head per tubulin heterodimer. Nature. 362:73-75.
20. Henningsen, U., and M. Schliwa. 1997. Reversal of the direction of movement of a molecular motor. Nature. 389:93-96.
21. Hessler, D., S.J., Young, and M.H. Ellisman. 1996. A flexible environment for the visualization of three-dimensional biological structures. J. Struct. Biol. 116:113-119.
22. Hirose, K., A. Lockhart, R.A. Cross, and L.A. Amos. 1995. Nucleotide dependent angular change in kinesin motor domain bound to tubulin. Nature. 376: 277-279.
23. 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.
24. Hoenger, A., and R.A. Milligan. 1996. Polarity of 2-D and 3-D maps of tubulin sheets and motor decorated sheets. J. Mol. Biol. 263:114-119.
25. Hoenger, A., and R.A. Milligan. 1997. Motor domains of kinesin and ncd interact wilh microtubule protofilaments with the same binding geometry. J. Mol. Biol. 265:553-564.
26. Hoenger, A., E.P. Sablin, R.D. Vale, R.J. Fletterick, and R.A. Milligan. 1995. Three-dimensional structure of a tubulin-motor-protein complex. Nature. 376:271-274.
27. Holmes, K.C. 1997. The swinging lever-arm hypothesis of muscle contraction. Curr. Biol. 7:112-118.
28. Howard, J. 1996. The movement of kinesin along microtubules. Annu. Rev. Physiol. 58:703-729.
29. Hua, W., E.C. Young, M.L. Fleming, and J. Gelles. 1997. Coupling of kinesin steps to ATP hydrolysis. Nature. 388:390-393.
30. 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.
31. 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.
32. Jiang, W., M.F. Stock, X. Li, and D.D. Hackney. 1997. Influence of the kinesin neck domain on dimerization and ATPase kinetics. J. Biol. Chem. 272:7626-7632.
33. Jones, T.A., J.Y. Zou, S.W. Cowan, and M. Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A. 47:110-119.
34. Kikkawa, M., T. Ishikawa, T. Wakabayashi, and N. Hirokawa. 1995. Three-dimensional structure of the kinesin head-microtubule complex. Nature. 376: 274-277.
35. Kozielski, F., S. Sack, A. Marx, M. Thormählen, E. Schönbrunn, V. Biou, A. Thompson, E.-M. Mandelkow, and E. Mandelkow. 1997a. The crystal structure of dimeric kinesin and implications for microtubule-dependent motility. Cell. 91:985-994.
36. Kozielski, F., E. Schönbrunn, S. Sack, J. Müller, S.T. Brady, and E. Mandelkow. 1997b. Crystallization and preliminary X-ray analysis of the single-headed and double-headed motor protein kinesin. J. Struct. Biol. 119:28-34.
37. Kull, F.J., E. Sablin, P. Lau, R. Fletterick, and R. Vale. 1996. Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature. 380:550-554.
38. Lockhart, A., I.M. Crevel, and R.A. Cross. 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. Lupas, A., M. Van Dyke, and J. Stock. 1991. Predicting coiled coils from protein sequences. Science. 252:1162-1164.
40. Ma, Y.Z., and E.W. Taylor. 1997. Interacting head mechanism of microtubulekinesin ATPase. J. Biol. Chem. 272:724-30.
41. Mandelkow, E.-M., and E. Mandelkow. 1985. Unstained microtubules studied by cryo-electron microscopy: substructure, supertwist and disassembly. J. Mol. Biol. 181:123-135.
42. Mandelkow, E.-M., M. Herrmann, and U. Rühl. 1985. Tubulin domains probed by limited proteolysis and subunit-specific antibodies. J. Mol. Biol. 185:311-327.
43. Mandelkow, E.-M., R. Schultheiss, R. Rapp, M. Müller, and E. Mandelkow, 1986. On the surface lattice of microtubules: Helix starts, protofilament number, seam and handedness. J. Cell Biol. 102:1067-1073.
44. Marx, A., M. Thormählen, S. Sack, and E. Mandelkow. 1998. Crystal structure of kinesin and interaction with microtubules. Eur. Biophysics J. In press.
45. Morii, H., T. Takenawa, F. Arisaka, and T. Shimizu. 1997. Identification of kinesin neck region as a stable alpha-helical coiled coil and its thermodynamic characterization. Biochemistry. 36:1933-1942.
46. Nangaku, M., R. Sato-Yoshitake, Y. Okada, Y. Noda, R. Takemura, H. Yamazaki, and N. Hirokawa. 1994. KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell. 79:1209-1220.
47. Okada, Y., H. Yamazaki, Y. Sekine-Aizawa, and N. Hirokawa. 1995. The neuron-specific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors. Cell. 81: 769-780.
48. Ray, S., E. Meyhofer, R.A. Milligan, and J. Howard. 1993. Kinesin follows the microtubule's protofilament axis. J. Cell Biol. 121:1083-1093.
49. Rayment, I. 1996. Kinesin and myosin: molecular motors with similar engines. Structure. 4:501-504.
50. 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.
51. 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.
52. Sack, S., J. Müller, A. Marx, M. Thormählen, E.-M. Mandelkow, S.T. Brady, and E. Mandelkow. 1997. X-ray structure of motor and neck domains from rat brain kinesin. Biochemistry. 36:16155-16165.
53. Schnitzer, M.J., and S.M. Block. 1997. Kinesin hydrolyses one ATP per 8-nm step. Nature. 388:386-90.
54. Schroeter, J., and J.-P. Bretaudiere. 1996. SUPRIM: easily modified image processing software. J. Struct. Biol. 116:131-137.
55. Smith, C.A., and I. Rayment. 1996. X-ray structure of the magnesium(II).ADP.vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 Å resolution. Biochemistry. 35:5404-5417.
56. Song, H., and S.A. Endow. 1996. Binding sites on microtubules of kinesin motors of the same or opposite polarity. Biochemistry. 35:11203-11209.
57. Song, Y.H., and E. Mandelkow. 1993. Recombinant kinesin motor domain binds to β-tubulin and decorates microtubules with a B surface lattice. Proc. Natl. Acad. Sci. USA. 90:1671-1675.
58. Sosa, H., and R.A. Milligan. 1996. Three-dimensional structure of ncd-decorated microtubules obtained by a back-projection method. J. Mol. Biol. 260: 743-755.
59. Sosa, H., D.P. Dias, A. Hoenger, M. Whittaker, E. Wilson-Kubalek, E. Sablin, R.J. Fletterick, R.D. Vale, and R.A. Milligan. 1997a. A model for the microtubule-Ncd motor protein complex obtained by cryo-electron microscopy and image analysis. Cell. 90:217-224.
60. Sosa, H., A. Hoenger, and R.A. Milligan. 1997b. Three different approaches for calculating the 3-dimensional structure of microtubules decorated with kinesin motor domains. J. Struct. Biol. 118:149-158.
61. 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.
62. Thormählen, M., A. Marx, S.A. Müller, Y.-H. Song, E.-M. Mandelkow, U. Aebi, and E. Mandelkow. 1998a. Interaction of monomeric and dimeric kinesin with microtubules. J. Mol. Biol. 275:795-809.
63. Thormählen, M., A. Marx, S. Sack, and E. Mandelkow. 1998b. The coiled-coil helix in the neck of kinesin. J. Struct. Biol. In press.
64. 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.
65. Tucker, C., and L.S.B. Goldstein. 1997. Probing the kinesin-microtubule interaction. J. Biol. Chem. 272:9481-9488.
66. Uyeda, T.Q., P.D. Abramson, and J.A. Spudich. 1996. The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc. Natl. Acad. Sci. USA. 93:4459-4464.
67. Vale, R.D.. and R.J. Fletterick. 1997. The design plan of kinesin motors. Annu. Rev. Cell Dev. Biol. 13:745-777.
68. 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.
69. Wade, R.H., D. Chrètien, and D. Job. 1990. Characterization of microtubule protofilament numbers; how does the surface lattice accommodate? J. Mol. Biol. 212:775-786.
70. Wade, R.H., R. Horowitz, and R.A. Milligan. 1995. Toward understanding the structure and interactions of microtubules and motor proteins. PROTEINS: structure, function, and genetics 23:502-509.
71. Walker, R.A. 1995. Ncd and kinesin motor domains interact with both alpha- and beta-tubulin. Proc. Natl. Acad. Sci. USA. 92:5960-5964.
72. Whittaker, M., B.O. Carragher, and R.A. Milligan. 1995a. PHOELIX: a package for semi-automated helical reconstruction. Ultramicroscopy. 58:245-259.
73. Whittaker, M., E.M. Wilson-Kubalek, J.E. Smith, L. Faust, R.A. Milligan, and H.L. Sweeney. 1995b. A 35Å movement of smooth muscle myosin on ADP release. Nature. 378:748-751.
74. 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.