Characterization of a hypercontraction-induced myopathy in Drosophila caused by mutations in Mhc

Journal of Cell Biology

Volumn 164, Issue 7, 2004, Pages 1045-1054

  Montana, Enrico S ^a   Littleton, J Troy ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cardiomyopathy; Drosophila; Dystrophy; Myosin; Neuromuscular

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; MYOSIN HEAVY CHAIN; TROPONIN I; TROPONIN T;

ADOLESCENT; ALLELE; ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CARDIOMYOPATHY; DROSOPHILA; ELECTROPHYSIOLOGY; EXTRACELLULAR CALCIUM; FLIGHT MUSCLE; GENE; GENE LOCUS; GENE MUTATION; GENETIC ANALYSIS; HYDROLYSIS; HYPERCONTRACTION INDUCED MYOPATHY; INTRACELLULAR RECORDING; LARVA; MALE; MHC GENE; MUSCLE ATROPHY; MUSCLE CONTRACTION; MUSCULAR DYSTROPHY; MYOPATHY; NERVE CELL; NERVE CELL STIMULATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; SEIZURE; TEMPERATURE SENSITIVE MUTANT;

ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; CALCIUM; DROSOPHILA; DROSOPHILA PROTEINS; FLIGHT, ANIMAL; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; POINT MUTATION;

ANIMALIA;

EID: 1842456978     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200308158     Document Type: Article

References (47)

1. Beall, C.J., and E. Fyrberg. 1991. Muscle abnormalities in Drosophila melanogaster heldup mutants are caused by missing or aberrant troponin-I isoforms. J. Cell Biol. 114:941-951.
2. Bernstein, S.I., K. Mogami, J.J. Donady, and C.P. Emerson, Jr. 1983. Drosophila muscle myosin heavy chain encoded by a single gene in a cluster of muscle mutations. Nature. 302:393-397.
3. Collier, V.L., W.A. Kronert, P.T. O'Donnell, K.A. Edwards, and S.I. Bernstein. 1990. Alternative myosin hinge regions are utilized in a tissue-specific fashion that correlates with muscle contraction speed. Genes Dev. 4:885-895.
4. Davis, G.W., A. DiAntonio, S.A. Petersen, and C.S. Goodman. 1998. Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. Neuron. 20:305-315.
5. Deak, I.I., P.R. Bellamy, M. Bienz, Y. Dubuis, E. Fenner, M. Gollin, A. Rahmi, T. Ramp, C.A. Reinhardt, and B. Cotton. 1982. Mutations affecting the indirect flight muscles of Drosophila melanogaster. J. Embryol. Exp. Morphol. 69: 61-81.
6. Engel, J.E., and C.F. Wu. 1992. Interactions of membrane excitability mutations affecting potassium and sodium currents in the flight and giant fiber escape systems of Drosophila. J. Comp. Physiol. [A]. 171:93-104.
7. Fekete, E., and J. Szidonya. 1979. Abnormalities of ultrastructure and calcium distribution in the flight muscle of a flightless mutant of Drosophila melanogaster. Acta Biol. 30:47-57.
8. Ferrus, A., A. Acebes, M.C. Marin, and A. Hernandez-Hernandez. 2000. A genetic approach to detect muscle protein interactions in vivo. Trends Cardiovasc. Med. 10:293-298.
9. 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.
10. Fyrberg, E.A., S.I. Bernstein, and K. Vijay Raghavan. 1994. Basic methods for Drosophila muscle biology. Methods Cell Biol. 44:237-258.
11. Ganeczky, B., and C.F. Wu. 1983. Neurogenetic analysis of potassium currents in Drosophila: synergistic effects on neuromuscular transmission in double mutants. J. Neurogenet. 1:17-28.
12. George, E.L., M.B. Ober, and C.P. Emerson, 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.
13. Gramates, L.S., and V. Budnik. 1999. Assembly and maturation of the Drosophila larval neuromuscular junction. Int. Rev. Neurobiol. 43:93-117.
14. Hess, N.K., and S.I. Bernstein. 1991. Developmentally regulated alternative splicing of Drosophila myosin heavy chain transcripts: in vivo analysis of an unusual 3′ splice site. Dev. Biol. 146:339-344.
15. Homyk, T., Jr., and C.P. Emerson, Jr. 1988. Functional interactions between unlinked muscle genes within haploinsufficient regions of the Drosophila genome. Genetics. 119:105-121.
16. Homyk, T., Jr., J. Szidonya, and D.T. Suzuki. 1980. Behavioral mutants of Drosophila melanogaster. III. Isolation and mapping of mutations by direct visual observations of behavioral phenotypes. Mol. Gen. Genet. 177:553-565.
17. Hong, C.S., and B. Ganetzky. 1994. Spatial and temporal expression patterns of two sodium channel genes in Drosophila. J. Neurosci. 14:5160-5169.
18. Huxley, A.F. 2000. Cross-bridge action: present views, prospects, and unknowns. J. Biomech. 33:1189-1195.
19. Jarecki, J., and H. Keshishian. 1995. Role of neural activity during synaptogenesis in Drosophila. J. Neurosci. 15:8177-8190.
20. Kronert, W.A., P.T. O'Donnell, A. Fieck, A. Lawn, J.O. Vigoreaux, J.C. Sparrow, and S.I. Bernstein. 1995. Defects in the Drosophila myosin rod permit sarcomere assembly but cause flight muscle degeneration. J. Mol. Biol. 249:111-125.
21. Kronert, W.A., A. Acebes, A. Ferrus, and S.I. Bernstein. 1999. Specific myosin heavy chain mutations suppress troponin I defects in Drosophila muscles. J. Cell Biol. 144:989-1000.
22. Lamb, G.D. 2000. Excitation-contraction coupling in skeletal muscle: comparisons with cardiac muscle. Clin. Exp. Pharmacol. Physiol. 27:216-224.
23. Lehrer, S.S., and M.A. Geeves. 1998. The muscle thin filament as a classical cooperative/allosteric regulatory system. J. Mol. Biol. 277:1081-1089.
24. Littleton, J.T., H.J. Bellen, and M.S. Perin. 1993. Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse. Development. 118:1077-1088.
25. Littleton, J.T., E.R. Chapman, R. Kreber, M.B. Garment, S.D. Carlson, and B. Ganetzky. 1998. Temperature-sensitive paralytic mutations demonstrate that synaptic exocytosis requires SNARE complex assembly and disassembly. Neuron. 21:401-413.
26. Mogami, K., and Y. Hotta. 1981. Isolation of Drosophila flightless mutants which affect myofibrillar proteins of indirect flight muscle. Mol. Gen. Genet. 183: 409-417.
27. Naimi, B., A. Harrison, M. Cummins, U. Nongthomba, S. Clark, I. Canal, A. Ferrus, and J.C. Sparrow. 2001., A tropomyosin-2 mutation suppresses a troponin I myopathy in Drosophila. Mol. Biol. Cell. 12:1529-1539.
28. Nongthomba, U., M. Cummins, S. Clark, J.O. Vigoreaux, and J.C. Sparrow. 2003. Suppression of muscle hypercontraction by mutations in the myosin heavy chain gene of Drosophila melanogaster. Genetics. 164:209-222.
29. Petersen, S.A., R.D. Fetter, J.N. Noordermeer, C.S. Goodman, and A. DiAntonio. 1997. Generic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron. 19:1237-1248.
30. Poage, R.E., and S.D. Meriney. 2002. Presynaptic calcium influx, neurotransmitter release, and neuromuscular disease. Physiol. Behav. 77:507-512.
31. Pollard, T.D. 2000. Reflections on a quarter century of research on contractile systems. Trends Biochem. Sci. 25:607-611.
32. Rafael, J.A., E.R. Townsend, S.E. Squire, A.C. Potter, J.S. Chamberlain, and K.E. Davies. 2000. Dystrophin and utrophin influence fiber type composition and post-synaptic membrane structure. Hum. Mol. Genet. 9:1357-1367.
33. Rayment, I., W.R. Rypniewski, K. Schmidt-Base, R. Smith, D.R. Tomchick, M.M. Benning, D.A. Winkelmann, G. Wesenberg, and H.M. Holden. 1993. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science. 261:50-58.
34. 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 cardiomyoparhy. Proc. Natl. Acad. Sci. USA. 92:3864-3868.
35. Reedy, M.C., B. Bullard, and J.O. Vigoreaux. 2000. Flightin is essential for thick filament assembly and sarcomere stability in Drosophila flight muscles. J. Cell Biol. 151:1483-1500.
36. Rivlin, P.K., R.M. St Clair, I. Vilinsky, and D.L. Deitcher. 2004. Morphology and molecular organization of the adult neuromuscular junction of Drosophila. J. Comp. Neurol. 468:596-613.
37. Rozek, C.E., and N. Davidson. 1983. Drosophila has one myosin heavy-chain gene with three developmentally regulated transcripts. Cell. 32:23-34.
38. Ruff, R.L. 2003. Neurophysiology of the neuromuscular junction: overview. Ann. NY Acad. Sci. 998:1-10.
39. Seidman, J.G., and C. Seidman. 2001. The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell. 104:557-567.
40. Simpson, P. 1983. Maternal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos. Genetics. 105:615-632.
41. Spradling, A.C., D. Stern, A. Beaton, E.J. Rhem, T. Laverty, N. Mozden, S. Misra, and G.M. Rubin. 1999. The Berkeley Drosophila Genome Project gene disruption project: single P-element insertions mutating 25% of vital Drosophila genes. Genetics. 153:135-177.
42. Stewart, B.A., H.L. Atwood, J.J. Renger, J. Wang, and C.F. Wu. 1994. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J. Comp. Physiol. [A]. 175:179-191.
43. Suzuki, D.T., T. Grigliatti, and R. Williamson, 1971. Temperature-sensitive mutations in Drosophila melanogaster. VII. A mutation (para-ts) causing reversible adult paralysis. Proc. Natl. Acad. Sci. USA. 68:890-893.
44. Vigoreaux, J.O. 2001. Genetics of the Drosophila flight muscle myofibril: a window into the biology of complex systems. Bioessays. 23:1047-1063.
45. Wassenberg, D.R., II, W.A. Kronert, P.T. O'Donnell, and S.I. Bernstein. 1987. Analysis of the 5′ end of the Drosophila muscle myosin heavy chain gene. Alternatively spliced transcripts initiate at a single site and intron locations are conserved compared to myosin genes of other organisms. J. Biol. Chem. 262: 10741-10747.
46. Wu, C.F., B. Ganetzky, F.N. Haugland, and A.X. Liu. 1983. Potassium currents in Drosophila: different components affected by mutations of two genes. Science. 220: 1076-1078.
47. Zhang, S., and S.I. Bernstein. 2001. Spatially and temporally regulated expression of myosin heavy chain alternative exons during Drosophila embryogenesis. Mech. Dev. 101:35-45.