Structure-function studies of the myosin motor domain: Importance of the 50-kDa cleft

Molecular Biology of the Cell

Volumn 7, Issue 7, 1996, Pages 1123-1136

  Ruppel, Kathleen M ^a,b   Spudich, James A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; MUTANT PROTEIN; MYOSIN;

ACTIN MYOSIN INTERACTION; ARTICLE; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; ENERGY TRANSFER; MOTOR ACTIVITY; MUSCLE CONTRACTION; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE;

EID: 0030035665     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.7.7.1123     Document Type: Article

References (49)

1. Botts, J., Thomason, J.F., and Morales, M.F. (1989). On the origin and transmission of force in actomyosin. Proc. Natl. Acad. Sci. USA 86, 2204-2208.
2. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
3. Clarke, M., and Spudich, J.A. (1974). Biochemical and structural studies of the actomyosin-like proteins from nonmuscle cells. Isolation and characterization of myosin from amoebae of Dictyostelium discoideum. J. Mol. Biol. 86, 209-222.
4. Dayhoff, M.O. (1978). Atlas of Protein Sequence and Structure, Washington, DC: National Biomedical Research Foundation.
5. De Lozanne, A., and Spudich, J.A. (1987). Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science, 236, 1086-1091.
6. Egelhoff, T.T., Lee, R.J., and Spudich, J.A. (1993). Dictyostelium myosin heavy chain phosphorylation sites regulate myosin filament assembly and localization in vivo. Cell 75, 363-371.
7. Egelhoff, T.T., Manstein, D.J., and Spudich, J.A. (1990). Complementation of myosin null mutants in Dictyostelium discoideum by direct functional selection. Dev. Biol. 137, 359-367.
8. Egelhoff, T.T., Titus, M.A., Manstein, D.J., Ruppel, K.M., and Spudich, J.A. (1991). Molecular genetic tools for study of the cytoskeleton in Dictyostelium. Methods Enzymol. 196, 319-334.
9. Fisher, A.J., Smith, C.A., Thoden, J., Smith, R., Sutoh, K., Holden, H.M., and Rayment, I. (1995). Structural studies of myosin/nucleotide complexes: a revised model for the molecular basis of contraction. Biophys. J. 68, 195-285.
10. Griffith, L.M., Downs, S.M., and Spudich, J.A. (1987). Myosin light chain kinase and myosin light chain phosphatase: effects of reversible phosphorylation on myosin structure and function. J. Cell Biol. 104, 1309-1323.
11. Holmes, K.C., Popp, D., Gebhard, W., and Kabsch, W. (1990). Atomic model of the actin filament. Nature 347, 44-49.
12. Huxley, H.E. (1969). The mechanism of muscular contraction. Science 164, 1356-1366.
13. Huxley, H.E., and Kress, M. (1985). Cross-bridge behavior during muscle contraction. J. Muscle Res. Cell Motil. 6, 153-161.
14. Itakura, S., Yamakawa, H., Toyoshima, Y.Y., Ishijima, A., Kojima, T., Harada, Y., Yanagida, T., Wakabayashi, T., and Sutoh, K. (1993). Force-generating domain of myosin motor. Biochem. Biophys. Res. Commun. 196, 1504-1510.
15. Jontes, J.D., Kubalek, E.M.W., and Milligan, R.A. (1995). A 32° tail swing in brush border myosin I on ADP release. Nature 378, 751-753.
16. Kabsch, W., Mannherz, H.G., Suck, D., Pai, E.F., and Holmes, K.C. (1990). Atomic structure of the actin/DNase I complex. Nature 347, 37-44.
17. Kishino, A., and Yanagida, T. (1988). Force measurements by micromanipulation of a single-actin filament by glass needles. Nature 334, 74-76.
18. Knecht, D.A., and Loomis, W.F. (1987). Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum. Science 236, 1081-1086.
19. Kraulis, P.J. (1991). MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
20. Kronert, W.A., O'Donnell, P.T., and Bernstein, S.I. (1994). A charge change in an evolutionarily conserved region of the myosin globular head prevents myosin and thick filament accumulation in Drosophila. J. Mol. Biol. 236, 697-702.
21. Kubalek, E.W., Uyeda, T.Q.P., and Spudich, J.A. (1992). A Dictyostelium myosin II lacking a proximal 58-kDa portion of the tail is functional in vivo and in vitro. Mol. Biol. Cell 3, 1455-1462.
22. Kunkel, T.A., Roberts, J.D., and Zakour, R.A. (1987). Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154, 367-382.
23. Lowey, S., Waller, G.S., and Trybus, K.M. (1993). Skeletal muscle myosin light chains are essential for physiological speeds of shortening. Nature 365, 454-456.
24. Lymn, R.W., and Taylor, E.W. (1971). Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10, 4617-4624.
25. Manstein, D.J., Titus, M.A., De Lozanne, A., and Spudich, J.A. (1989). Gene replacement in Dictyostelium: generation of myosin null mutants. EMBO J. 8, 923-932.
26. Margossian, S.S., and Lowey, S. (1982). Preparation of myosin and its subfragments from rabbit skeletal muscle. Methods Enzymol. 85, 55-71.
27. Maruta, H., and Korn, E.D. (1981). Direct photoaffinity labeling by nucleotides of the apparent catalytic site on the heavy chains of smooth muscle and Acanthamoeba myosins. J. Biol. Chem. 256, 499-502.
28. Patterson, B., and Spudich, J.A. (1996). Cold-sensitive mutations of Dictyostelium myosin heavy chain highlight functional domains of the myosin motor. Genetics 143, 801-810.
29. Peltz, G., Spudich, J.A., and Parham, P. (1985). Monoclonal antibodies against seven sites on the head and tail of Dictyostelium myosin. J. Cell Biol. 100, 1016-1023.
30. Perrie, W.T., Smillie, L.B., and Perry, S.V. (1973). A phosphorylated light chain component of myosin from skeletal muscle. Biochem. J. 135, 151-164.
31. Rayment, I., Holden, H.M., Whittaker, M., Yohn, C.B., Lorenz, M., Holmes, K.C., and Milligan, R.A. (1993a). Structure of the actin-myosin complex and its implications for muscle contraction. Science 261, 58-65.
32. Rayment, I., Rypniewski, W., Schmidt-Base, K., Smith, R., Tomchick, D., Benning, M.M., Winkelmann, D.A., Wesenberg, G., and Holden, H.M. (1993b). The three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261, 50-58.
33. Reedy, M.K. (1993). Myosin-actin motors: the partnership goes atomic. Structure 1, 1-5.
34. Ruppel, K.M., Uyeda, T.Q.P., and Spudich, J.A. (1994). Role of highly conserved lysine 130 of myosin motor domain: in vivo and in vitro characterization of a site specifically mutated myosin. J. Biol. Chem. 269, 18773-18780.
35. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
36. Schroeder, R.R., Manstein, D.J., Jahn, W., Holden, H., Rayment, I., Holmes, K.C., and Spudich, J.A. (1993). Three-dimensional atomic model of F-actin decorated with Dictyostelium myosin S1. Nature 364, 171-174.
37. Sellers, J.R., and Goodson, H.V. (1995). Motor proteins 2: myosin. Protein Profile 1, 1323-1423.
38. Spudich, J.A. (1989). In pursuit of myosin function. Cell Regul. 1, 1-11.
39. Spudich, J.A., Finer, J., Simmons, B., Ruppel, K., Patterson, B., and Uyeda, T. (1995). Myosin structure and function. Cold Spring Harbor Symp. Quant. Biol. 60, 783-791.
40. Spudich, J.A., and Watt, S. (1971). The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246, 4866-4871.
41. Sutoh, K., Tokunaga, M., and Wakabayashi, T. (1989). Electron microscopic mappings of the myosin head with site-directed antibodies. J. Mol. Biol. 206, 357-363.
42. Toyoshima, Y.Y., Kron, S.J., McNally, E.M., Niebling, K.R., Toyoshima, C., and Spudich, J.A. (1987). Myosin subfragment-1 is sufficient to move actin filaments in vitro. Nature 328, 536-539.
43. Uyeda, T.Q.P., Abramson, P.D., and Spudich, J.A. (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.
44. Uyeda, T.Q.P., Kron, S.J., and Spudich, J.A. (1990). Myosin step size: estimation from slow sliding movement of actin over low densities of heavy meromyosin. J. Mol. Biol. 214, 699-710.
45. Uyeda, T.Q.P., Ruppel, K.M., and Spudich, J.A. (1994). Enzymatic activities correlate with chimaeric substitutions at the actin-binding face of myosin. Nature 368, 567-569.
46. Uyeda, T.Q.P., and Spudich, J.A. (1993). A functional recombinant myosin II lacking a regulatory light chain-binding site. Science 262, 1867-1870.
47. Warshaw, H.M., Derosiers, J.M., Work, S.S., and Trybus, K.M. (1990). Smooth muscle myosin cross-bridge interactions modulate actin filament sliding velocity in vitro. J. Cell Biol. 111, 453-463.
48. Whittaker, M., Kubalek, E.M.W., Smith, J.E., Faust, E., Milligan, R.A., and Sweeney, H.L. (1995). A 35-Å movement of smooth muscle myosin on ADP release. Nature 378, 748-751.
49. Yanisch-Perron, C., Vieira, J., and Messing, J. (1985). Improved M13 phage-cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103-119.