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Journal of Muscle Research & Cell Motility

, Volume 15, Issue 6, pp 607–616 | Cite as

Multiple isoelectric variants of flightin in Drosophila stretch-activated muscles are generated by temporally regulated phosphorylations

  • Jim O. Vigoreaux
  • Louise M. Perry
Papers

Summary

Drosophila stretch-activated flight muscles contain flightin, a novel myofibrillar protein that interacts with myosin filaments. We have identified elevent flightin isoelectric variants that can be subdivided into phosphorylated and non-phosphorylated subclasses. Flight muscles of late pupal stage P15, at which time myofibrillogenesis has been completed but the muscle has yet to be used, contain primarily non-phosphorylated variants. A dramatic increase in flightin phosphorylation occurs subsequent to eclosion. As the young adult matures, increasingly phosphorylated variants are generated following a precise ontogenetic progression. Adults 5–6 h old and older contain the entire set of flightin isoelectric variants. All nine phosphovariants remain metabolically active throughout adult life as evidence by their ability to incorporate radioactive phosphate in older adults. Our results suggest the possibility that all nine phosphorylated variants originate from a single precursor by sequential phosphorylation. Phosphorylation of flightin may thus serve both structural and regulatory functional roles.

Keywords

Phosphate Young Adult Functional Role Adult Life Pupal Stage 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. ABBOTT, R. H. & STEIGER, G. J. (1977) Temperature and amplitude dependence of tension transients in glycerinated skeletal and insect fibrillar muscle. J. Physiol. 266, 13–42.Google Scholar
  2. AHN, D. H., HATTORI, A. & TAKAHASHI, K. (1993) Structural changes in Z-disks of skeletal muscle myofibrils during growth of chicken. J. Biochem. 113, 383–8.Google Scholar
  3. BALL, E., KARLIK, C. C., BEALL, C. J., SAVILLE, D. L., SPARROW, J. C., BULLARD, B. & FYRBERG, E. A. (1987) Arthrin, a myofibrillar protein of insect flight muscle, is an actin-ubiquitin conjugate. Cell 51, 221–8.Google Scholar
  4. BOWNES, M. & REMBOLD, H. (1987) The titre of juvenile hormone during the pupal and adult stages of the life cycle of D. melanogaster. Eur. J. Biochem. 164, 709–12.Google Scholar
  5. BULLARD, B., LEONARD, K., LARKINS, A., BUTCHER, G., KARLIK, C. & FYRBERG, E. (1988) Troponin of asynchronous flight muscle. J. Mol. Biol. 204, 621–37.Google Scholar
  6. CHIEN, K. R., KNOWLTON, K. U., ZHU, H. & CHIEN, A. S. (1991) Regulation of cardiac gene expression during myocardial growth and hypertrophy: molecular studies of an adaptive physiologic response. FASEB J. 5, 3037–46.Google Scholar
  7. COOPER, J. A. (1991) Estimation of phosphorylation stoichiometry by separation of phosphorylated isoforms. Methods Enzymol. 201, 251–61.Google Scholar
  8. JEWELL, B. R. & RUEGG, J. C. (1966) Oscillatory contraction of insect fibrillar muscle after glycerol extraction. Proc. R. Soc. Lond. B164, 428–59.Google Scholar
  9. JOHNSON, S. A. & MILNER, M. J. (1987) The final stages of wing development in Drosophila melanogaster. Tissue Cell 19, 505–13.Google Scholar
  10. MORGAN, H. E. & BAKER, K. M. (1991) Cardiac hypertrophy. Mechanical, neural and endocrine dependence. Circulation 83, 13–25.Google Scholar
  11. O'FARRELL, P. H. (1975) High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007–21.Google Scholar
  12. PRINGLE, J. W. S. (1978) Stretch activation of muscle: function and mechanism. Proc. R. Soc. Lond. B201, 107–30.Google Scholar
  13. REEDY, M. C. & BEALL, C. (1993) Ultrastructure of developing flight muscle in Drosophila. I. Assembly of myofibrils. Develop. Biol. 160, 443–65.Google Scholar
  14. SAMAREL, A. M. & ENGELMANN, G. L. (1991) Contractile activity modulates myosin heavy chain-β expression in neonatal rat heart cells. Amer. J. Physiol. 261, H1067–77.Google Scholar
  15. STEIGER, G. J. (1971) Stretch activation and myogenic oscillation of isolated contractile structures of heart muscle. Pflüg Arch. 330, 347–61.Google Scholar
  16. TAKANO-OHMURO, H., TAKAHASHI, S., HIROSE, G. & MARUYAMA, K. (1990) Phosphorylated and dephosphorylated myosin light chains of Drosophila fly and larva. Comp. Biochem. Physiol. 95B, 171–7.Google Scholar
  17. THORSON, J. & WHITE, D. C. S. (1969) Distributed representations for actin-myosin interaction in the oscillatory contraction of muscle. Biophys. J. 9, 360–90.Google Scholar
  18. TRAUGH, J. A. & SHARP, S. B. (1977) Protein modification enzymes associated with the protein-synthesizing complex from rabbit reticulocytes. J. Biol. Chem. 252, 3738–44.Google Scholar
  19. TREGEAR, R. T., ed. (1977) Insect Flight Muscle. London: North Holland.Google Scholar
  20. VANDENBURGH, H. H., SWASDISON, S. & KARLISCH, P. (1991) Computer-aided mechanogenesis of skeletal muscle organs from single cells in vitro. FASEB J. 5, 2860–7.Google Scholar
  21. VIGOREAUX, J.O., SAIDE, J. D., VALGEIRSDÓTTIR, K. & PARDUE, M. L. (1993) Flightin, a novel myofibrillar protein of Drosophila stretch-activated muscles. J. Cell Biol. 121, 587–98.Google Scholar
  22. WANG, N., BUTLER, J. P. & INGBER, D. E. (1993) Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124–7.Google Scholar

Copyright information

© Chapman & Hall 1994

Authors and Affiliations

  • Jim O. Vigoreaux
    • 1
  • Louise M. Perry
    • 1
  1. 1.Department of ZoologyUniversity of VermontBurlingtonUSA

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