Passive stiffness in Drosophila indirect flight muscle reduced by disrupting paramyosin phosphorylation, but not by embryonic myosin S2 hinge substitution

Biophysical Journal

Volumn 91, Issue 12, 2006, Pages 4500-4506

  Hao, Yudong ^a   Miller, Mark S ^b   Swank, Douglas M ^b,d   Liu, Hongjun ^c,e   Bernstein, Sanford I ^c   Maughan, David W ^b   Pollack, Gerald H ^a  

^a University of Washington   (United States)

^b UNIVERSITY OF VERMONT   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

^d RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^e NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; MYOSIN; PARAMYOSIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DROSOPHILA; ELASTICITY; FLIGHT MUSCLE; IMAGING SYSTEM; MUSCLE CELL; MUSCLE FIBRIL; MUSCLE FUNCTION; MUSCLE STIFFNESS; MYOFILAMENT; NONHUMAN; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SARCOMERE; TRANSGENIC ANIMAL; TRANSMISSION ELECTRON MICROSCOPY; VALIDATION STUDY;

HEXAPODA;

EID: 33845397160     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.088492     Document Type: Article

References (37)

1. Josephson, R. K., J. G. Malamud, and D. R. Stokes. 2000. Asynchronous muscle: a primer. J. Exp. Biol. 203:2713-2722.
2. Peckham, M., J. E. Molloy, J. C. Sparrow, and D. C. White. 1990. Physiological properties of the dorsal longitudinal flight muscle and the tergal depressor of the trochanter muscle of Drosophila melanogaster. J. Muscle Res. Cell Motil. 11:203-215.
3. Henkin, J. A., D. W. Maughan, and J. O. Vigoreaux. 2004. Mutations that affect flightin expression in Drosophila alter the viscoelastic properties of flight muscle fibers. Am. J. Physiol. Cell Physiol. 286:C65-C72.
4. Moore, J. R., J. O. Vigoreaux, and D. W. Maughan. 1999. The Drosophila projectin mutant, bentD, has reduced stretch activation and altered indirect flight muscle kinetics. J. Muscle Res. Cell Motil. 20:797-806.
5. Moore, J. R., M. H. Dickinson, J. O. Vigoreaux, and D. W. Maughan. 2000. The effect of removing the N-terminal extension of the Drosophila myosin regulatory light chain upon flight ability and the contractile dynamics of indirect flight muscle. Biophys. J. 78:1431-1440.
6. Tohtong, R., H. Yamashita, M. Graham, J. Haeberle, A. Simcox, and D. Maughan. 1995. Impairment of muscle function caused by mutations of phosphorylation sites in myosin regulatory light chain. Nature. 374:650-653.
7. Maughan, D. W., and J. O. Vigoreaux. 1999. An integrated view of insect flight muscle: genes, motor molecules, and motion. News Physiol. Sci. 14:87-92.
8. Dickinson, M., G. Farman, M. Frye, T. Bekyarova, D. Gore, D. Maughan, and T. Irving. 2005. Molecular dynamics of cyclically contracting insect flight muscle in vivo. Nature. 433:330-334.
9. Chan, W. P., and M. H. Dickinson. 1996. In vivo length oscillations of indirect flight muscles in the fruit fly Drosophila virilis. J. Exp. Biol. 199:2767-2774.
10. Granzier, H. L., and K. Wang. 1993. Passive tension and stiffness of vertebrate skeletal and insect flight muscles: the contribution of weak cross-bridges and elastic filaments. Biophys. J. 65:2141-2159.
11. White, D. C. 1983. The elasticity of relaxed insect fibrillar flight muscle. J. Physiol. 343:31-57.
12. Saide, J. D., S. Chin-Bow, J. Hogan-Sheldon, L. Busquets-Turner, J. O. Vigoreaux, K. Valgeirsdottir, and M. L. Pardue. 1989. Characterization of components of Z-bands in the fibrillar flight muscle of Drosophila melanogaster. J. Cell Biol. 109:2157-2167.
13. Kulke, M., C. Neagoe, B. Kolmerer, A. Minajeva, H. Hinssen, B. Bullard, and W. A. Linke. 2001. Kettin, a major source of myofibrillar stiffness in Drosophila indirect flight muscle. J. Cell Biol. 154:1045-1057.
14. Lakey, A., C. Ferguson, S. Labeit, M. Reedy, A. Larkins, G. Butcher, K. Leonard, and B. Bullard. 1990. Identification and localization of high molecular weight proteins in insect flight and leg muscle. EMBO J. 9:3459-3467.
15. Clayton, J. D., R. M. Cripps, J. C. Sparrow, and B. Bullard. 1998. Interaction of troponin-H and glutathione S-transferase-2 in the indirect flight muscles of Drosophila melanogaster. J. Muscle Res. Cell Motil. 19:117-127.
16. Granzier, H. L., and K. Wang. 1993. Interplay between passive tension and strong and weak binding cross-bridges in insect indirect flight muscle. A functional dissection by gelsolin-mediated thin filament removal. J. Gen. Physiol. 101:235-270.
17. Suggs, J. A. 2003. The function of the S2 hinge of myosin heavy chain in Drosophila melanogaster. Masters thesis. San Diego State University, San Diego, CA.
18. Liu, H., M. S. Miller, D. M. Swank, W. A. Kronert, D. W. Maughan, and S. I. Bernstein. 2005. Paramyosin phosphorylation site disruption affects indirect flight muscle stiffness and power generation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA. 102:10522-10527.
19. Hao, Y., S. I. Bernstein, and G. H. Pollack. 2004. Passive stiffness of Drosophila IFM myofibrils: a novel, high accuracy measurement method. J. Muscle Res. Cell Motil. 25:359-366.
20. 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.
21. Dickinson, M. H., C. J. Hyatt, F. O. Lehmann, J. R. Moore, M. C. Reedy, A. Simcox, R. Tohtong, J. O. Vigoreaux, H. Yamashita, and D. W. Maughan. 1997. Phosphorylation-dependent power output of transgenic flies: an integrated study. Biophys. J. 73:3122-3134.
22. Barton, B., G. Ayer, N. Heymann, D. W. Maughan, F. O. Lehmann, and J. O. Vigoreaux. 2005. Flight muscle properties and aerodynamic performance of Drosophila expressing a flightin transgene. J. Exp. Biol. 208:549-560.
23. Lupas, A., M. Van Dyke, and J. Stock. 1991. Predicting coiled coils from protein sequences. Science. 252:1162-1164.
24. Dunaway, D., M. Fauver, and G. Pollack. 2002. Direct measurement of single synthetic vertebrate thick filament elasticity using nanofabricated cantilevers. Biophys. J. 82:3128-3133.
25. Huxley, H. E., A. Stewart, H. Sosa, and T. Irving. 1994. X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys. J. 67:2411-2421.
26. Liu, X., and G. H. Pollack. 2002. Mechanics of F-actin characterized with microfabricated cantilevers. Biophys. J. 83:2705-2715.
27. Wakabayashi, K., Y. Sugimoto, H. Tanaka, Y. Ueno, Y. Takezawa, and Y. Amemiya. 1994. X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys. J. 67:2422-2435.
28. 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.
29. Lu, R. C. 1980. Identification of a region susceptible to proteolysis in myosin subfragment-2. Proc. Natl. Acad. Sci. USA. 77:2010-2013.
30. Becker, K. D., P. T. O'Donnell, J. M. Heitz, M. Vito, and S. I. Bernstein. 1992. Analysis of Drosophila paramyosin: identification of a novel isoform which is restricted to a subset of adult muscles. J. Cell Biol. 116:669-681.
31. Kagawa, H., K. Gengyo, A. D. McLachlan, S. Brenner, and J. Karn. 1989. Paramyosin gene (unc-15) of Caenorhabditis elegans. Molecular cloning, nucleotide sequence and models for thick filament structure. J. Mol. Biol. 207:311-333.
32. Vinos, J., A. Domingo, R. Marco, and M. Cervera. 1991. Identification and characterization of Drosophila melanogaster paramyosin. J. Mol. Biol. 220:687-700.
33. Schriefer, L. A., and R. H. Waterson. 1989. Phosphorylation of the N-terminal region of Caenorhabditis elegans paramyosin. J. Mol. Biol. 207:451-454.
34. Watabe, S., T. Tsuchiya, and D. J. Hartshorne. 1989. Phosphorylation of paramyosin. Comp. Biochem. Physiol. B. 94:813-821.
35. Maroto, M., J. Arredondo, D. Goulding, R. Marco, B. Bullard, and M. Cervera. 1996. Drosophila paramyosin/miniparamyosin gene products show a large diversity in quantity, localization, and isoform pattern: a possible role in muscle maturation and function. J. Cell Biol. 134:81-92.
36. Royuela, M., R. Garcia-Anchuelo, M. I. Arenas, M. Cervera, B. Fraile, and R. Paniagua. 1996. Immunocytochemical electron microscopic study and western blot analysis of paramyosin in different invertebrate muscle cell types of the fruit fly Drosophila melanogaster, the earthworm Eisenia foetida, and the snail Helix aspersa. Histochem. J. 28:247-255.
37. Epstein, H. F., G. Y. Lu, P. R. Deitiker, I. Oritz, and M. F. Schmid. 1995. Preliminary three-dimensional model for nematode thick filament core. J. Struct. Biol. 115:163-174.