Flight muscle properties and aerodynamic performance of Drosophila expressing a flightin transgene

Journal of Experimental Biology

Volumn 208, Issue 3, 2005, Pages 549-560

  Barton, Byron ^a   Ayer, Gretchen ^a   Heymann, Nicole ^b   Maughan, David W ^a   Lehmann, Fritz Olaf ^b   Vigoreaux, Jim O ^a  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

Flightin; Insect flight muscle; Stretch activation; Thick filaments

Indexed keywords

DROSOPHILA PROTEIN; FLN PROTEIN, DROSOPHILA; MUSCLE PROTEIN;

ANIMAL; ARTICLE; BIOMECHANICS; BIOSYNTHESIS; DROSOPHILA MELANOGASTER; FLYING; GENE EXPRESSION; GENETICS; HISTOLOGY; MUSCLE CELL; MUSCLE CONTRACTION; PHYSIOLOGY; SKELETAL MUSCLE; TRANSGENIC ANIMAL; ULTRASTRUCTURE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOMECHANICS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FLIGHT, ANIMAL; GENE EXPRESSION; MUSCLE CONTRACTION; MUSCLE FIBERS; MUSCLE PROTEINS; MUSCLE, SKELETAL;

INSECTA;

EID: 14644419657     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.01425     Document Type: Article

References (41)

1. Arredondo, J. J., Mardahl-Dumesnil, M., Cripps, R. M., Cervera, M. and Bernstein, S. I. (2001). Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster. J. Muscle Res. Cell Motil. 22, 287-299.
2. Atkinson, S. J. and Stewart, M. (1991). Molecular basis of myosin assembly: coiled-coil interactions and the role of charged periodicities. J. Cell Sci. Suppl. 14, 7-10.
3. Ayer, G. and Vigoreaux, J. O. (2003). Flightin is a myosin rod binding protein. Cell Biochem. Biophys. 38, 41-54.
4. Bainbridge, S. P. and Bownes, M. (1981). Staging the metamorphosis of Drosophila melanogaster. J. Embryol. Exp. Morph. 66, 57-80.
5. Bernstein, S. I., O'Donnell, P. T. and Cripps, R. M. (1993). Molecular genetic analysis of muscle development, structure and function in Drosophila. Int. Rev. Cytol. 143, 63-152.
6. Cripps, R. M. (2004). The contributions of genetics to the study of insect flight muscle function. In Nature's Versatile Engine: Insect Flight Muscle Inside and Out, in press (ed. J. Vigoreaux). Georgetown, TX: Landes Bioscience.
7. 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.
8. Cripps, R. M., Suggs, J. A. and Bernstein, S. I. (1999). Assembly of thick filaments and myofibrils occurs in the absence of the myosin head. EMBO J. 18, 1793-1804.
9. Dickinson, M. H., Hyatt, C. J., Lehmann, F.-O., Moore, J. R., Reedy, M. C., Simcox, A., Tohtong, R., Vigoreaux, J. O., Yamashita, H. and Maughan, D. W. (1997). Phosphorylation-dependent power output of transgenic flies: an integrated study. Biophys. J. 73, 3122-3134.
10. Dickinson, M. H., Lehmann, F. O. and Sane, S. P. (1999). Wing rotation and the aerodynamic basis of insect flight. Science 284, 1954-1960.
11. Ellington, C. P. (1984). The aerodynamics of insect flight. IV. Aerodynamic mechanisms. Phil. Trans. R. Soc. Lond. B 305, 79-113.
12. Fernandes, J., Bate, M. and Vijayraghavan, K. (1991). Development of the indirect flight muscles of Drosophila. Development 113, 67-77.
13. Geyer, P. K. and Fyrberg, E. A. (1986). 5′-flanking sequence required for regulated expression of a muscle-specific Drosophila melanogaster actin gene. Mol. Cell Biol. 6, 3388-3396.
14. Henkin, J. A., Maughan, D. W. and Vigoreaux, J. O. (2004). Mutations that affect flightin expression in Drosophila alter the viscoelastic properties of flight muscle fibers. Am. J. Physiol. Cell Physiol. 286, C65-C72.
15. Hiromi, Y., Okamoto, H., Gehring, W. J. and Hotta, Y. (1986). Germline transformation with Drosophila mutant actin genes induces constitutive expression of heat shock genes. Cell 44, 293-301.
16. Klemenz, R., Weber, U. and Gehring, W. J. (1987). The white gene as a marker in a new P element vector for gene transfer in Drosophila. Nucleic Acids Res. 15, 3947-3959.
17. Kreuz, A. J., Simcox, A. and Maughan, D. (1996). Alterations in flight muscle ultrastructure and function in Drosophila tropomyosin mutants. J. Cell Biol. 135, 673-687.
18. Kronert, W. A., O'Donnell, P. T., Fieck, A., Lawn, A., Vigoreaux, J. O., Sparrow, J. C. and Bernstein, S. I. (1995). Defects in the Drosophila myosin rod permit sarcomere assembly but cause flight muscle degeneration. J. Mol. Biol. 249, 111-125.
19. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 270, 680-685.
20. Lehmann, F. O. and Dickinson, M. H. (1998). The control of wing kinematics and flight forces in fruit flies (Drosophila spp.). J. Exp. Biol. 201, 385-401.
21. Lehmann, F.-O. and Dickinson, M. H. (1997). The changes in power requirements and muscle efficiency during elevated flight force production in the fruit fly, Drosophila. J. Exp. Biol. 200, 1133-1143.
22. Liu, H., Mardahl-Dumesnil, M., Sweeney, S. T., O'Kane, C. J. and Bernstein, S. I. (2003). Drosophila paramyosin is important for myoblast fusion and essential for myofibril formation. J. Cell Biol. 160, 899-908.
23. Mardahl-Dumesnil, M. and Fowler, V. M. (2001). Thin filaments elongate from their pointed ends during myofibril assembly in Drosophila indirect flight muscle. J. Cell Biol. 155, 1043-1053.
24. McLachlan, A. D. and Karn, J. (1982). Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature 299, 226-231.
25. Miller, B. M. and Bernstein, S. I. (2004). Myosin. In Nature's Versatile Engine: Insect Flight Muscle Inside and Out, in press (ed. J. Vigoreaux). Georgetown, TX: Landes Bioscience.
26. Miller, R. C., Schaaf, R., Maughan, D. W. and Tansey, T. R. (1993). A non-flight muscle isoform of Drosophila tropomyosin rescues an indirect flight muscle tropomyosin mutant. J. Muscle Res. Cell Motil. 14, 85-98.
27. Nongthomba, U. and Ramachandra, N. B. (1999). A direct screen identifies new flight muscle mutants on the Drosophila second chromosome. Genetics 153, 261-274.
28. Reedy, M. C. and Beall, C. (1993). Ultrastructure of developing flight muscle in Drosophila. I. Assembly of myofibrils. Dev. Biol. 160, 443-465.
29. Reedy, M. C., Bullard, B. and Vigoreaux, J. O. (2000). Flightin is essential for thick filament assembly and sarcomere stability in Drosophila flight muscles. J. Cell Biol. 151, 1483-1499.
30. Rubin, G. M. and Spradling, A. C. (1983). Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res. 11, 6341-6351.
31. Sanchez, F., Tobin, S. L., Rdest, U., Zulauf, E. and McCarthy, B. J. (1983). Two Drosophila actin genes in detail. Gene structure, protein structure and transcription during development. J. Mol. Biol. 163, 533-551.
32. Sebat, J. et al. (2004). Large-scale copy number polymorphism in the human genome. Science 305, 525-528.
33. Spradling, A. C. and Rubin, G. M. (1982). Transposition of cloned P elements into Drosophila germ-line chromosomes. Science 218, 341-347.
34. Swank, D. M., Wells, L., Kronert, W. A., Morrill, G. E. and Bernstein, S. I. (2000). Determining structure/function relationships for sarcomeric myosin heavy chain by genetic and transgenic manipulation of Drosophila. Micro. Res. Tech. 50, 430-442.
35. Vigoreaux, J. O. (1994). Alterations in flightin phosphorylation in Drosophila flight muscles are associated with myofibrillar defects engendered by actin and myosin heavy chain mutant alleles. Biochem. Genet. 32, 301-314.
36. Vigoreaux, J. O. (2001). Genetics of the Drosophila flight muscle myofibril: a window into the biology of complex systems. BioEssays 23, 1047-1063.
37. Vigoreaux, J. O. and Perry, L. M. (1994). Multiple isoelectric variants of flightin in Drosophila stretch-activated muscles are generated by temporally regulated phosphorylations. J. Muscle Res. Cell Motil. 15, 607-616.
38. Vigoreaux, J. O. and Swank, D. M. (2004). The development of the flight and leg muscle. In Comprehensive Molecular Insect Science, vol. 2 (eds. L. I. Gilbert, K. Iatrou and S. Gill), pp. 45-84. Oxford, UK: Elsevier.
39. Vigoreaux, J. O., Saide, J. D. and Pardue, M. L. (1991). Structurally different Drosophila striated muscles utilize distinct variants of Z-band-associated proteins. J. Muscle Res. Cell Motil. 12, 340-354.
40. Vigoreaux, J. O., Saide, J. D., Valgeirsdottir, K. and Pardue, M. L. (1993). Flightin, a novel myofibrillar protein of Drosophila stretch-activated muscles. J. Cell Biol. 121, 587-598.
41. Vigoreaux, J. O., Hernandez, C., Moore, J., Ayer, G. and Maughan, D. (1998). A genetic deficiency that spans the flightin gene of Drosophila melanogaster affects the ultrastructure and function of the flight muscles. J. Exp. Biol. 201, 2033-2044.