Characterization of mutant myosins of Dictyostelium discoideum equivalent to human familial hypertrophic cardiomyopathy mutants: Molecular force level of mutant myosins may have a prognostic implication

Journal of Clinical Investigation

Volumn 99, Issue 5, 1997, Pages 1010-1015

  Fujita, Hideo ^a   Sugiura, Seiryo ^a   Momomura, Shin Ichi ^a   Omata, Masao ^a   Sugi, Haruo ^b   Sutoh, Kazuo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TEIKYO UNIVERSITY   (Japan)

Author keywords

dictyostelium; hypertrophic cardiomyopathy; myosin heavy chain; recombinant proteins; site directed mutagenesis

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATASE; MUTANT PROTEIN; MYOSIN HEAVY CHAIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; DICTYOSTELIUM DISCOIDEUM; ENZYME ACTIVITY; FAMILIAL DISEASE; FORCE; GENE MUTATION; HYPERTROPHIC CARDIOMYOPATHY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; SITE DIRECTED MUTAGENESIS;

EID: 0030899032     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119228     Document Type: Article

References (44)

1. Tanigawa, G., J.A. Jarcho, S. Kass, S.D. Solomon, H.P. Vosberg, J.G. Seidman, and C.E. Seidman. 1990. A molecular basis for familial hypertrophic cardiomyopathy: an alpha/beta cardiac myosin heavy chain hybrid gene. Cell. 62:991-998.
2. Geisterfer, L.A., S. Kass, G. Tanigawa, H.P. Vosberg, W. McKenna, C.E. Seidman, and J.G. Seidman. 1990. A molecular basis for familial hypertrophic cardiomyopathy: a beta cardiac myosin heavy chain gene missense mutation. Cell. 62:999-1006.
3. Seidman, C.E., and J.G. Seidman. 1991. Mutations in cardiac myosin heavy chain genes cause familial hypertrophic cardiomyopathy. Mol. Biol. Med. 8:159-166.
4. Thierfelder, L., H. Watkins, C. MacRae, R. Lamas, W. McKenna, H.P. Vosberg, J.G. Seidman, and C.E. Seidman. 1994. Alpha-tropomyosin and cardiac troponin T mutations cause familial hypertrophic cardiomyopathy: a disease of the sarcomere. Cell. 77:701-712.
5. Watkins, H., D. Conner, L. Thierfelder, J.A. Jarcho, C. MacRae, W.J. McKenna, B.J. Maron, J.G. Seidman, and C.E. Seidman. 1995. Mutations in the cardiac myosin binding protein-C gene on chromosome 11 cause familial hypertrophic cardiomyopathy. Nat. Genet. 11:434-437.
6. Watkins, H., W.J. McKenna, L. Thierfelder, H.J. Suk, R. Anan, A. O'Donoghue, P. Spirito, A. Matsumori, C.S. Moravec, J.G. Seidman, et al. 1995. Mutations in the genes for cardiac troponin T and alpha-tropomyosin in hypertrophic cardiomyopathy. N. Engl. J. Med. 332:1058-1064.
7. Watkins, H., C. MacRae, L. Thierfelder, Y.H. Chou, M. Frenneaux, W. McKenna, J.G. Seidman, and C.E. Seidman. 1993. A disease locus for familial hypertrophic cardiomyopathy maps to chromosome 1q3. Nat. Genet. 3:333-337.
8. Bonne, G., L. Carrier, J. Bercovici, C. Cruaud, P. Richard, B. Hainque, M. Gautel, S. Labeit, M. James, J. Beckmann, et al. 1995. Cardiac myosin binding protein-C gene splice acceptor site mutation is associated with familial hypertrophic cardiomyopathy. Nat Genet. 11:438-440.
9. Rayment, I., H.M. Holden, J.R. Sellers, L. Fananapazir, and N.D. Epstein. 1995. Structural interpretation of the mutations in the beta-cardiac myosin that have been implicated in familial hypertrophic cardiomyopathy. Proc. Natl. Acad. Sci. USA. 92:3864-3868.
10. Anan, R., G. Greve, L. Thierfelder, H. Walkins, W.J. McKenna, S. Solomon, C. Vecchio, H. Shono, S. Nakao, H. Tanaka, et al. 1994. Prognostic implications of novel beta cardiac myosin heavy chain gene mutations that cause familial hypertrophic cardiomyopathy [see comments]. J. Clin. Invest. 93:280-285.
11. 4. Biochemistry. 34:8960-8972.
12. 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 (Lond.). 380:555-559.
13. 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 (Lond.). 380:550-555.
14. Consevage, M.W., G.C. Salada, B.G. Baylen, R.L. Ladda, and P.K. Rogan. 1994. A new missense mutation. Arg719Gln, in the beta-cardiac heavy chain myosin gene of patients with familial hypertrophic cardiomyopathy. Hum. Mol. Genet. 3:1025-1026.
15. Watkins, H., L. Thierfelder, R. Anan, J. Jarcho, A. Matsumori, W. McKenna, J.G. Seidman, and C.E. Seidman. 1993. Independent origin of identical beta cardiac myosin heavy-chain mutations in hypertrophic cardiomyopathy. Am. J. Hum. Genet. 53:1180-1185.
16. Manstein, D.J., M.A. Titus, A. De Lozanne, and J.A. Spudich. 1989. Gene replacement in Dictyostelium: generation of myosin null mutants. EMBO (Eur. Mol. Biol. Organ.) J. 8:923-932.
17. Manstein, D.J., K.M. Ruppel, and J.A. Spudich. 1989. Expression and characterization of a functional myosin head fragment in Dictyostelium discoideum. Science (USA). 246:656-658.
18. Uyeda, T.Q., and J.A. Spudich. 1993. A functional recombinant myosin II lacking a regulatory light chain-binding site. Science (USA). 262:1867-1870.
19. Ruppel, K.M., T.Q. Uyeda, and J.A. Spudich. 1994. Role of highly conserved lysine 130 of myosin motor domain. In vivo and in vitro characterization of site specifically mutated myosin. J. Biol. Chem. 269:18773-18780.
20. Kunkel, T.A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA. 82:488-492.
21. Kunkel, T.A., J.D. Roberts, and R.A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154: 367-382.
22. Howard, P.K., K.G. Ahern, and R.A. Firtel. 1988. Establishment of a transient expression system for Dictyostelium discoideum. Nucleic Acids. Res. 16:2613-2623.
23. Ruppel, K.M., T.T. Egelhoff, and J.A. Spudich. 1990. Purification of a functional recombinant myosin fragment from Dictyostelium discoideum. Ann. NY Acad. Sci. 84:147-155.
24. Spudich, J.A., and S. Watt. 1971. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosintroponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246:4866-4871.
25. Miyata, H., H. Hakozaki, H. Yoshikawa, N. Suzuki, K. Kinoshita, T. Nishizawa, and S. Ishiwata. 1994. Stepwise motion of an actin filament over a small number of heavy meromyosin molecules is revealed in an in vitro motility assay. J. Biochem. 115:644-647.
26. Kamimura, S. 1987. Direct measurement of nanometric displacement under an optical microscope. Appl. Opt. 26:3425-3434.
27. Svoboda, K., and S.M. Block. 1994. Fluctuation analysis of motor protein movement and single enzyme kinetics. Proc. Natl. Acad. Sci. USA. 91: 11782-11786.
28. Kron, S.J., and J.A. Spudich. 1986. Fluorescent actin filaments move on myosin fixed to a glass surface. Proc. Natl. Acad. Sci. USA. 83:6272-6276.
29. Kodama, T., K. Fukui, and K. Kometani. 1986. The initial phosphate burst in ATP hydrolysis by myosin and subfragment-1 as studied by a modified malachite green method for determination of inorganic phosphate. J. Biochem. (Tokyo). 99:1465-1472.
30. 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 A resolution. Biochemistry. 35:5404-5417.
31. Lee, C. 1994. Predicting protein mutant energetics by self-consistent ensemble optimization. J. Mol. Biol. 236:918-939.
32. Uyeda, T.Q., S.J. Kron, and J.A. Spudich. 1990. Myosin step size. Estimation from slow sliding movement of actin over low densities of heavy meromyosin. J. Mol. Biol. 214:699-710.
33. Milligan, R.A. 1996. Protein-protein interactions in the rigor actomyosin complex. Proc. Natl. Acad. Sci. USA. 93:21-26.
34. Sweeney, H.L., A.J. Straceski, L.A. Leinwand, B.A. Tikunov, and L. Faust. 1994. Heterologous expression of a cardiomyopathic myosin that is defective in its actin interaction. J. Biol. Chem. 269:1603-1606.
35. Whittaker, M., E.M. Wilson-Kubalek, J.E. Smith, L. Faust, R.A. Milligan, and H.L. Sweeney. 1995. A 35-Å movement of smooth muscle myosin on ADP release. Nature (Lond.). 378:748-753.
36. 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.
37. Rayment, I., H.M. Holden, M. Whittaker, C. Yohn, B.M. Lorenz, K.C. Holes, and R.A. Milligan. 1993. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science (Wash. DC). 261:50-58.
38. Poetter, K., H. Jiang, S. Hassanzadeh, S.R. Master, A. Chang, M.C. Dalakas, I. Rayment, J.R. Sellers, L. Fananapazir, and N.D. Epstein. 1996. Mutations in either the essential or regulatory light chains of myosin are associated with a rare myopathy in human heart and skeletal muscle. Nat. Genet. 13:63-69.
39. Lankford, E.B., N.D. Epstein, L. Fananapazir, and H.L. Sweeney. 1995. Abnormal contractile properties of muscle fibers expressing beta-myosin heavy chain gene mutations in patients with hypertrophic cardiomyopathy. J. Clin. Invest. 95:1409-1414.
40. Sutoh, K., M. Andou, K. Sutoh, and Y.Y. Toyoshima. 1991. Site-directed mutations of Dictyostelium actin: Disruption of a negative charge cluster at the N terminus. Proc. Natl. Acad. Sci. USA. 88:7711-7714.
41. Johara, M., Y.Y. Toyoshima, A. Ishijima, H. Kojima, T. Yanagida, and K. Sutoh. 1993. Charge-reversion mutagenesis of Dictyostelium actin to map the surface recognized by myosin during ATP-driven sliding motion. Proc. Natl. Acad. Sci. USA. 90:2127-2131.
42. Duong, A.M., and E. Reisler. 1994. C-terminus on actin: spectroscopic and immunochemical examination of its role in actomyosin interactions. Adv. Exp. Med. Biol. 358:59-70.
43. Miller, C.J., and E. Reisler. 1995. Role of charged amino acid pairs in subdomain-1 of actin in interactions with myosin. Biochemistry. 34:2694-2700.
44. Miller, C.J., P. Cheung, P. White, and E. Reisler. 1995. Actin's view of actomyosin interface. Biophys. J. 68:50S-54S.