Myosin transducer mutations differentially affect motor function, myofibril structure, and the performance of skeletal and cardiac muscles

Molecular Biology of the Cell

Volumn 19, Issue 2, 2008, Pages 553-562

  Cammarato, Anthony ^a,b   Dambacher, Corey M ^a,c   Knowles, Aileen F ^a   Kronert, William A ^a   Bodmer, Rolf ^b   Ocorr, Karen ^b   Bernstein, Sanford I ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b BURNHAM INSTITUTE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATASE; MYOSIN;

ANIMAL TISSUE; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; D45 GENE; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; FEMALE; GENE; GENE MUTATION; HEART; HEART MUSCLE; MHC GENE; MOTOR PERFORMANCE; MUSCLE CONTRACTILITY; MUSCLE DISEASE; MUSCLE FIBRIL; MUSCLE FUNCTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SKELETAL MUSCLE;

AGING; AMINO ACID SEQUENCE; ANIMALS; BIOMECHANICS; DROSOPHILA MELANOGASTER; GENES, INSECT; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; MUTANT PROTEINS; MUTATION; MYOCARDIUM; MYOFIBRILS; MYOSINS; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

DROSOPHILA MELANOGASTER; VERTEBRATA;

EID: 39449118905     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-09-0890     Document Type: Article

References (63)

1. Ahmad, F., Seidman, J. G., and Seidman, C. E. (2005). The genetic basis for cardiac remodeling. Annu. Rev. Genomics Hum. Genet. 6, 185-216.
2. Baker, G. T., 3rd. (1976). Insect flight muscle: maturation and senescence. Gerontology 22, 334-361.
3. Beall, C. J., and Fyrberg, E. (1991). Muscle abnormalities in Drosophila melanogaster heldup mutants are caused by missing or aberrant troponin-I isoforms. J. Cell Biol. 114, 941-951.
4. Bernstein, S. I., Mogami, K., Donady, J. J., and Emerson, C. P., Jr. (1983). Drosophila muscle myosin heavy chain encoded by a single gene in a cluster of muscle mutations. Nature 302, 393-397.
5. Brown, J. H., and Cohen, C. (2005). Regulation of muscle contraction by tropomyosin and troponin: how structure illuminates function. Adv. Protein Chem. 71, 121-159.
6. Cammarato, A., Hatch, V., Saide, J., Craig, R., Sparrow, J. C., Tobacman, L. S., and Lehman, W. (2004). Drosophila muscle regulation characterized by electron microscopy and three-dimensional reconstruction of thin filament mutants. Biophys. J. 86, 1618-1624.
7. Chang, A. N., and Potter, J. D. (2005). Sarcomeric protein mutations in dilated cardiomyopathy. Heart Fail. Rev. 10, 225-235.
8. Clark, R., Ansari, M. A., Dash, S., Geeves, M. A., and Coluccio, L. M. (2005). Loop 1 of transducer region in mammalian class I myosin, Myo1b, modulates actin affinity, ATPase activity, and nucleotide access. J. Biol. Chem. 280, 30935-30942.
9. Coureux, P. D., Sweeney, H. L., and Houdusse, A. (2004). Three myosin V structures delineate essential features of chemo-mechanical transduction. EMBO J. 23, 4527-4537.
10. Coureux, P. D., Wells, A. L., Menetrey, J., Yengo, C. M., Morris, C. A., Sweeney, H. L., and Houdusse, A. (2003). A structural state of the myosin V motor without bound nucleotide. Nature 425, 419-423.
11. Cripps, R. M., Becker, K. D., Mardahl, M., Kronert, W. A., Hodges, D., and Bernstein, S. I. (1994). Transformation of Drosophila melanogaster with the wild-type myosin heavy-chain gene: rescue of mutant phenotypes and analysis of defects caused by overexpression. J. Cell Biol. 126, 689-699.
12. 2+-independent mechanical tone and acute myocyte remodeling. Circ. Res. 100, 1494-1502.
13. Debold, E. P., Schmitt, J. P., Patlak, J. B., Beck, S. E., Moore, J. R., Seidman, J. G., Seidman, C., and Warshaw, D. M. (2007). Hypertrophic and dilated cardiomyopathy mutations differentially affect the molecular force generation of mouse alpha-cardiac myosin in the laser trap assay. Am. J. Physiol. 293, H284-H291.
14. Drummond, D. R., Hennessey, E. S., and Sparrow, J. C. (1991). Characterisation of missense mutations in the Act88F gene of Drosophila melanogaster. Mol. Gen. Genet. 226, 70-80.
15. Fatkin, D., and Graham, R. M. (2002). Molecular mechanisms of inherited cardiomyopathies. Physiol. Rev. 82, 945-980.
16. Finch, C. E., and Ruvkun, G. (2001). The genetics of aging. Annu. Rev. Genomics Hum. Genet. 2, 435-462.
17. Friedberg, M. K., and Silverman, N. H. (2006). The systolic to diastolic duration ratio in children with heart failure secondary to restrictive cardiomyopathy. J. Am. Soc. Echocardiogr. 19, 1326-1331.
18. Geeves, M. A., Fedorov, R., and Manstein, D. J. (2005). Molecular mechanism of actomyosin-based motility. Cell Mol. Life Sci. 62, 1462-1477.
19. Geeves, M. A., and Holmes, K. C. (1999). Structural mechanism of muscle contraction. Annu. Rev. Biochem. 68, 687-728.
20. Geeves, M. A., and Holmes, K. C. (2005). The molecular mechanism of muscle contraction. Adv. Protein Chem. 71, 161-193.
21. George, E. L., Ober, M. B., and Emerson, C. P., Jr. (1989). Functional domains of the Drosophila melanogaster muscle myosin heavy-chain gene are encoded by alternatively spliced exons. Mol. Cell. Biol. 9, 2957-2974.
22. Gomes, A. V., Liang, J., and Potter, J. D. (2005). Mutations in human cardiac troponin I that are associated with restrictive cardiomyopathy affect basal ATPase activity and the calcium sensitivity of force development. J. Biol. Chem. 280, 30909-30915.
23. Gordon, A. M., Homsher, E., and Regnier, M. (2000). Regulation of contraction in striated muscle. Physiol. Rev. 80, 853-924.
24. Hinken, A. C., and Solaro, R. J. (2007). A dominant role of cardiac molecular motors in the intrinsic regulation of ventricular ejection and relaxation. Physiology 22, 73-80.
25. Kamisago, M. et al. (2000). Mutations in sarcomere protein genes as a cause of dilated cardiomyopathy. N. Engl. J. Med. 343, 1688-1696.
26. Kronert, W. A., Acebes, A., Ferrus, A., and Bernstein, S. I. (1999). Specific myosin heavy chain mutations suppress troponin I defects in Drosophila muscles. J. Cell Biol. 144, 989-1000.
27. Kurzawa-Goertz, S. E., Perreault-Micale, C. L., Trybus, K. M., Szent-Gyorgyi, A. G., and Geeves, M. A. (1998). Loop I can modulate ADP affinity, ATPase activity, and motility of different scallop myosins. Transient kinetic analysis of S1 isoforms. Biochemistry 37, 7517-7525.
28. Kushwaha, S. S., Fallon, J. T., and Fuster, V. (1997). Restrictive cardiomyopathy. N. Engl. J. Med. 336, 267-276.
29. Laing, N. G., and Nowak, K. J. (2005). When contractile proteins go bad: the sarcomere and skeletal muscle disease. Bioessays 27, 809-822.
30. Levine, R. L., and Stadtman, E. R. (2001). Oxidative modification of proteins during aging. Exp. Gerontol. 36, 1495-1502.
31. Magwere, T., Pamplona, R., Miwa, S., Martinez-Diaz, P., Portero-Otin, M., Brand, M. D., and Partridge, L. (2006). Flight activity, mortality rates, and lipoxidative damage in Drosophila. J. Gerontol. A Biol. Sci. Med. Sci. 61, 136-145.
32. Margossian, S. S., and Lowey, S. (1982). Structural and contractile proteins. In: Methods in Enzymology, Vol. 85, ed. L. W. Cunningham and D. W. Frederiksen, New York: Academic Press, 55-70.
33. McKillop, D. F., and Geeves, M. A. (1993). Regulation of the interaction between actin and myosin subfragment 1, evidence for three states of the thin filament. Biophys. J. 65, 693-701.
34. Miller, A. (1950). The internal anatomy and histology of the imago of Drosophila melanogaster. In: Biology of Drosophila, ed. M. Demerec, New York: Wiley, 420-534.
35. Mogensen, J., Kubo, T., Duque, M., Uribe, W., Shaw, A., Murphy, R., Gimeno, J. R., Elliott, P., and McKenna, W. J. (2003). Idiopathic restrictive cardiomyopathy is part of the clinical expression of cardiac troponin I mutations. J. Clin. Invest. 111, 209-216.
36. Montana, E. S., and Littleton, J. T. (2004). Characterization of a hypercontraction-induced myopathy in Drosophila caused by mutations in Mhc. J. Cell Biol. 164, 1045-1054.
37. Moss, R. L., Razumova, M., and Fitzsimons, D. P. (2004). Myosin crossbridge activation of cardiac thin filaments: implications for myocardial function in health and disease. Circ. Res. 94, 1290-1300.
38. Murphy, R. T., Mogensen, J., Shaw, A., Kubo, T., Hughes, S., and McKenna, W. J. (2004). Novel mutation in cardiac troponin I in recessive idiopathic dilated cardiomyopathy. Lancet 363, 371-372.
39. Nongthomba, U., Cummins, M., Clark, S., Vigoreaux, J. O., and Sparrow, J. C. (2003). Suppression of muscle hypercontraction by mutations in the myosin heavy chain gene of Drosophila melanogaster. Genetics 164, 209-222.
40. Ocorr, K., Reeves, N. L., Wessells, R. J., Fink, M., Chen, H. S., Akasaka, T., Yasuda, S., Metzger, J. M., Giles, W., Posakony, J. W., and Bodmer, R. (2007). KCNQ potassium channel mutations cause cardiac arrhythmias in Drosophila that mimic the effects of aging. Proc. Natl. Acad. Sci. USA 104, 3943-3948.
41. Oldfors, A. (2007). Hereditary myosin myopathies. Neuromuscul. Disord. 17, 355-367.
42. Oldfors, A., Tajsharghi, H., Darin, N., and Lindberg, C. (2004). Myopathies associated with myosin heavy chain mutations. Acta Myol. 23, 90-96.
43. Pardee, J. D., and Spudich, J. A. (1982). Structural and contractile proteins. In: Methods in Enzymology, Vol. 85, ed. L. W. Cunningham and D. W. Frederiksen, New York: Academic Press, 164-179.
44. Parkes, T. L., Hilliker, A. J., and Phillips, J. P. (1999). Motorneurons, reactive oxygen, and life span in Drosophila. Neurobiol. Aging 20, 531-535.
45. Paternostro, G., Vignola, C., Bartsch, D. U., Omens, J. H., McCulloch, A. D., and Reed, J. C. (2001). Age-associated cardiac dysfunction in Drosophila melanogaster. Circ. Res. 88, 1053-1058.
46. Poole, K. J., Lorenz, M., Evans, G., Rosenbaum, G., Pirani, A., Craig, R., Tobacman, L. S., Lehman, W., and Holmes, K. C. (2006). A comparison of muscle thin filament models obtained from electron microscopy reconstructions and low-angle X-ray fibre diagrams from non-overlap muscle. J. Struct. Biol. 155, 273-284.
47. Redowicz, M. J. (2002). Myosins and pathology: genetics and biology. Acta Biochim. Pol. 49, 789-804.
48. Root, D. D., and Wang, K. (1994). Calmodulin-sensitive interaction of human nebulin fragments with actin and myosin. Biochemistry 33, 12581-12591.
49. Rozek, C. E., and Davidson, N. (1983). Drosophila has one myosin heavy-chain gene with three developmentally regulated transcripts. Cell 32, 23-34.
50. Schmitt, J. P. et al. (2006). Cardiac myosin missense mutations cause dilated cardiomyopathy in mouse models and depress molecular motor function. Proc. Natl. Acad. Sci. USA 103, 14525-14530.
51. Sellers, J. R. (1999). Myosins, Oxford; New York: Oxford University Press.
52. Stadtman, E. R. (1992). Protein oxidation and aging. Science 257, 1220-1224.
53. Suggs, J. A., Cammarato, A., Kronert, W. A., Nikkhoy, M., Dambacher, C. M., Megighian, A., and Bernstein, S. I. (2007). Alternative S2 hinge regions of the myosin rod differentially affect muscle function, myofibril dimensions and myosin tail length. J. Mol. Biol. 367, 1312-1329.
54. Swank, D. M., Bartoo, M. L., Knowles, A. F., Iliffe, C., Bernstein, S. I., Molloy, J. E., and Sparrow, J. C. (2001). Alternative exon-encoded regions of Drosophila myosin heavy chain modulate ATPase rates and actin sliding velocity. J. Biol. Chem. 276, 15117-15124.
55. Swank, D. M., Knowles, A. F., Kronert, W. A., Suggs, J. A., Morrill, G. E., Nikkhoy, M., Manipon, G. G., and Bernstein, S. I. (2003). Variable N-terminal regions of muscle myosin heavy chain modulate ATPase rate and actin sliding velocity. J. Biol. Chem. 278, 17475-17482.
56. Sweeney, H. L., Rosenfeld, S. S., Brown, F., Faust, L., Smith, J., Xing, J., Stein, L. A., and Sellers, J. R. (1998). Kinetic tuning of myosin via a flexible loop adjacent to the nucleotide binding pocket. J. Biol. Chem. 273, 6262-6270.
57. Tardiff, J. C. (2005). Sarcomeric proteins and familial hypertrophic cardiomyopathy: linking mutations in structural proteins to complex cardiovascular phenotypes. Heart Fail. Rev. 10, 237-248.
58. Tatar, M., Bartke, A., and Antebi, A. (2003). The endocrine regulation of aging by insulin-like signals. Science 299, 1346-1351.
59. Tobacman, L. S. (1996). Thin filament-mediated regulation of cardiac contraction. Annu. Rev. Physiol. 58, 447-481.
60. Vibert, P., Craig, R., and Lehman, W. (1997). Steric-model for activation of muscle thin filaments. J. Mol. Biol. 266, 8-14.
61. Wessells, R. J., and Bodmer, R. (2007). Age-related cardiac deterioration: insights from Drosophila. Front. Biosci. 12, 39-48.
62. Wolf, M. J., Amrein, H., Izatt, J. A., Choma, M. A., Reedy, M. C., and Rockman, H. A. (2006). Drosophila as a model for the identification of genes causing adult human heart disease. Proc. Natl. Acad. Sci. USA 103, 1394-1399.
63. 2+ sensitization of myofilament associated with a small structural change in troponin I in inherited restrictive cardiomyopathy. Biochem. Biophys. Res. Commun. 338, 1519-1526.