Journal of Muscle Research & Cell Motility

, Volume 12, Issue 4, pp 340–354 | Cite as

Structurally differentDrosophila striated muscles utilize distinct variants of Z-band-associated proteins

  • Jim O. Vigoreaux
  • Judith D. Saide
  • Mary Lou Pardue


Monoclonal antibodies raised against four proteins from insect asynchronous flight muscle have been used to characterize the cross-reacting proteins in synchronous muscle ofDrosophila melanogaster. Two proteins,α-actinin and Z(400/600), are found at the Z-band of every muscle examined. A larger variant ofα-actinin is specific for the perforated Z-bands of supercontractile muscle. A third Z-band protein, Z(210), has a very limited distribution. It is found only in the asynchronous muscle and in the large cells of the jump muscle (tergal depressor of the trochanter). The absence of Z(210) from the anterior four small cells of the jump muscle demonstrates that cells within the same muscle do not have identical Z-band composition. The fourth protein, projectin, > 600 kDa polypeptide component of the connecting filaments in asynchronous muscle, is also detected in all synchronous muscles studied. Surprisingly, projectin is detected in the region of the thick filaments in synchronous muscles, rather than between the thick filaments and the Z-band, as in asynchronous muscles. Despite their different locations, the projectins of synchronous and asynchronous muscles are very similar, but not identical, as judged by SDS-PAGE and by peptide mapping. Projectin shows immunological cross-reactivity with twitchin, a nematode giant protein that is a component of the body wall A-band and shares similarities with vertebrate titin.


Peptide Polypeptide Limited Distribution Body Wall Distinct Variant 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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.PubMedGoogle Scholar
  2. Basi, G. S., Boardman, M. &Storti, R. V. (1984) Alternative splicing of a Drosophila tropomyosin gene generates muscle tropomyosin isoforms with different carboxyterminal ends.Mol. Cell Biol. 4, 2828–36.PubMedGoogle Scholar
  3. Bechtel, P. (1979) Identification of a high molecular weight actin-binding protein in skeletal muscle.J. Biol. Chem. 254, 1755–8.PubMedGoogle Scholar
  4. Benian, G. M., Kiff, J. E., Neckelmann, N., Moerman, D. G. &Waterston, R. H. (1989) Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans.Nature 342, 45–50.PubMedGoogle Scholar
  5. Bernstein, S. I., Hansen, C. J., Becker, K. D., Wassenberg, D. R. II, Roche, E. S., Donady, J. J. &Emerson, C. P., Jr. (1986) Alternative RNA splicing generates transcripts encoding a thorax-specific isoform of Drosophila myosin heavy chain.Mol. Cell Biol. 6, 2511–19.PubMedGoogle Scholar
  6. Chun, M. &Falkenthal, S. (1988) Ifm(2)2 is a myosin heavy chain allele that disrupts myofibrillar assembly only in the indirect flight muscle ofDrosophila melanogaster.J. Cell Biol. 107, 2613–21.PubMedGoogle Scholar
  7. Cleveland, D. W., Fischer, S. G., Kirschner, M. W. &Laemmli, U. K. (1977) Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis.J. Biol. Chem.252, 1102–6.PubMedGoogle Scholar
  8. Crossley, A. C. (1978) Morphology and development of the Drosophila muscular system. InThe Genetics and Biology of Drosophila, Volume 2b (edited by Ashbumer, M. & Wright, T. R. F.), pp. 499–560. London: Academic Press.Google Scholar
  9. Deak, I. I. (1977) A histochemical study of the muscles ofDrosophila melanogaster. J. Morphol.153, 307–16.PubMedGoogle Scholar
  10. Deak, I. I., Bellamy, P. R., Bienz, M., Dubuis, Y., Fenner, E., Gollin, M, Rahmi, A., Ramp, T., Reinhardt, C.A. &Cotton, B. (1982) Mutations affecting the indirect flight muscles ofDrosophila melanogaster.J. Embryol. Exp. Morphol.69, 61–81.PubMedGoogle Scholar
  11. Duhaiman, A. S. &Bamburg, J. R. (1984) Isolation of brain alpha-actinin. Its characterization and a comparison of its properties with those of muscle alpha-actinins.Biochemistry 23, 1600–8.PubMedGoogle Scholar
  12. Endo, T. &Masaki, T. (1982) Molecular properties and functionsin vitro of chicken smooth muscle alpha-actinin in comparison with those of striated muscle alpha-actinins.J. Biochem. Japan92, 1457–68.Google Scholar
  13. Fyrberg, E. A., Kelly, M., Ball, E., Fyrberg, C. &Reedy, M. C. (1990) Molecular genetics ofDrosophila alpha-actinin: mutant alleles disrupt Z disc integrity and muscle insertions.J. Cell Biol.110, 1999–2011.PubMedGoogle Scholar
  14. George, E. L., Ober, M. B. &Emerson, C. P., Jr. (1989) Functional domains of theDrosophila melanogaster muscle myosin heavy chain gene are encoded by alternatively spliced exons.Mol. Cell. Biol. 9, 2957–74.PubMedGoogle Scholar
  15. Gomer, R. H. &Lazarides, E. (1981) The synthesis and de-ployment of filamin in chicken skeletal muscle.Cell 23 524–32.PubMedGoogle Scholar
  16. Gomer,R. H. &Lazarides, E. (1983) Highly homologous filamin polypeptides have different distributions in avian slow and fast muscle fibers.J. Cell Biol. 97, 818–23.PubMedGoogle Scholar
  17. Horowits, R., Kempner, E. S., Bisher, M. E.&,Podolsky, R. J. (1986) A physiological role for Htin and nebulin in skeletal muscle.Nature 323, 160–4.PubMedGoogle Scholar
  18. Horowits, R. &Podolsky, R. J. (1987) The positional stability of thick filaments in activated skeletal muscle depends on sarcomere length: Evidence for the role of titin filaments.J. Cell Biol. 105, 2217–23.PubMedGoogle Scholar
  19. Horowits, R., Maruyama, K. &Podolsky, R. J. (1989) Elastic behavior of connecting filaments during thick filament movement in activated skeletal muscle.J. Cell Biol. 109, 2169–76.PubMedGoogle Scholar
  20. Karlik, C. C., Coutu, M. D. &Fyrberg, E. A. (1984) A nonsense mutation within the act88F actin gene disrupts myofibril formation inDrosophila indirect flight muscles.Cell 38, 711–19.PubMedGoogle Scholar
  21. Karlik, C. C. &Fyrberg, E. A. (1985) An insertion within a variably splicedDrosophila tropomyosin gene blocks accumulation of only one encoded isoform.Cell 41, 57–66.PubMedGoogle Scholar
  22. Karlik, C. C. &Fyrberg, E. A. (1986) TwoDrosophila melanogaster tropomyosin genes: structural and functional aspects.Mol. Cell Biol. 6, 1965–73.PubMedGoogle Scholar
  23. Kimura, K., Shimozawa, T. &Tanimura, T. (1986) Muscle degeneration in the posteclosional development of aDrosophila mutant, abnormal proboscis extension reflex C (aper C).Develop. Biol 117, 194–203.PubMedGoogle Scholar
  24. Kobayashi, R., Itoh, H. &Tashima, Y. (1983) Polymorphism of alpha-actinin.Eur. J. Biochem.133, 607–11.PubMedGoogle Scholar
  25. Koteliansky, V. E., Glukhova, M. A., Shirinsky, V. P., Babaer, V. R., Kandelenko, V. F., Rukosver, V. S. &Smirnov, V. N. (1981) Filamin-like protein in chick heart muscle.FEBS Lett. 125, 44–8.PubMedGoogle Scholar
  26. Labeit, S., Barlow, D. P., Gautel, M., Gibson, T., Holt, J., Hsieh, C.-L., Francke, U., Leonard, K., Wardale, J., Whiting, A. &Trinick, J. (1990) A regular pattern of two types of 100 residue motif in the sequence of titin.Nature 345, 273–6.PubMedGoogle Scholar
  27. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Nature 270, 680–5.Google Scholar
  28. Lakey, A., Ferguson, C., Labeit, S., Reedy, M., Larkins, A., Butcher, G., Leonard, K. &,Bullard, B. (1990) Identification and localization of high molecular weight proteins in insect flight and leg muscle.EMBO J.9, 3459–67.PubMedGoogle Scholar
  29. Locker, R. H. &Wild, D. J. C. (1986) A comparative study of high molecular weight proteins in various types of muscle across the animal kingdom.J. Biochem.99, 1473–84.PubMedGoogle Scholar
  30. Mahaffey, J. W., Coutu, M. D., Fyrberg, E. A. &Inwood, W. (1985) The flightlessDrosophila mutantraised has distinct genetic lesions affecting accumulation of myofibrillar proteins in flight muscles.Cell 40, 101–10.PubMedGoogle Scholar
  31. Miller, A. (1950) The internal anatomy and histology of the imago ofDrosophila rnelanogaster. InThe biology of Drosophila (edited by Demerec, M.), pp. 420–534. New York: John Wiley.Google Scholar
  32. Moerman, D. G., Plurad, S., Waterston, R. H. &Baillie, D. L. (1982) Mutations in the unc-54 myosin heavy chain gene ofCaenorhabditis elegans that alter contractility but not muscle structure.Cell 29, 773–81.PubMedGoogle Scholar
  33. Moerman, D. G., Benian, G. M., Barstead, R. J., Schriefer, L. A. &Waterston, R. H. (1988) Identification and intracellular localization of the unc-22 gene product ofCaenorhabditis elegans.Genes Dev.2, 93–105.PubMedGoogle Scholar
  34. Mogami, K. &Hotta, Y. (1981) Isolation ofDrosophila flightless mutants which affect myofibrillar proteins of indirect flight muscles.Mol. Gen. Genet.183, 409–17.PubMedGoogle Scholar
  35. Mogami, K., Fujita, S. C. &Hotta, Y. (1982) Identification ofDrosophila indirect flight muscle myofibrillar proteins by means of two-dimensional electrophoresis.J. Biochem. 91, 643–50.PubMedGoogle Scholar
  36. Nave, R. &Weber, K. (1990) A myofibrillar protein of insect muscle related to vertebrate titin connects Z band and A band: purification and molecular characterization of invertebrate mini-titin.J. Cell Sci. 95, 535–44.PubMedGoogle Scholar
  37. Neville, D. M. (1971) Molecular weight determination of protein-dodecyl sulfate complexes by gel electrophoresis in a discontinuous buffer system.J. Biol. Chem. 246, 6328–34.PubMedGoogle Scholar
  38. O'donnell, P. T., Collier, V. L., Mogami, K. &Bernstein, S. I. (1989) Ultrastructural and molecular analyses of homozygous-viableDrosophila melanogaster muscle mutants indicate there is a complex pattern of myosin heavy chain isoform distribution.Genes Dev. 3, 1233–46.PubMedGoogle Scholar
  39. Peckham, M., Molloy, J. E., Sparrow, J. C. &White, D. C. S. (1990) Physiological properties of the dorsal longitudinal flight muscle and the tergal depressor of the trochanter muscle ofDrosophila melanogaster.J. Muscle Res. Cell Motil. 11, 203–15.PubMedGoogle Scholar
  40. Pringle, J. W. S. (1978) Stretch activation of muscle: function and mechanism.Proc. R. Soc. London B 201, 107–30.Google Scholar
  41. Pringle, J. W. S. (1981) The Bidder Lecture, 1980. The evolution of fibrillar muscle in insects.J. Exp. Biol.94, 1–14.Google Scholar
  42. Robson, R. M. &Zeece, M. G. (1973) Comparative studies of alpha-actinin from porcine cardiac and skeletal muscle.Biochim. Biophys. Acta 295, 208–24.PubMedGoogle Scholar
  43. Saide, J. D. (1981) Identification of a connecting filament protein in insect fibrillar flight muscle.J. Mol. Biol. 153, 661–79.PubMedGoogle Scholar
  44. Saide, J. D., Chin-Bow, S., Hogan-Sheldon, J., Busquets-Turner, L., Vigoreaux, J. O., Valgeirsdottir, K. &Pardue, M. L. (1989) Characterization of components of Z-bands in the fibrillar flight muscle ofDrosophila melanogaster.J. Cell Biol.109, 2157–67.PubMedGoogle Scholar
  45. Saide, J. D., Chin-Bow, S., Hogan-Sheldon, J. &Busquets-Turner, L. (1990) Z band proteins in the flight muscle and leg muscle of the honeybee.J. Muscle Res. Cell Motil. 11, 125–36.PubMedGoogle Scholar
  46. Schachat, F. H., Canine, A. C., Briggs, M. M. &Reedy, M. C. (1985) The presence of two skeletal muscle alpha-actinins correlates with troponin-tropomyosin expression and Z-line width.J. Cell Biol.101, 1001–8.PubMedGoogle Scholar
  47. Schouest, L. P., Jr., Anderson, M. &Miller, T. A. (1986) The ultrastructure and physiology of the tergotrochanteral depressor muscle of the housefly,Musca domestica. J. Exp. Zool. 239, 147–58.PubMedGoogle Scholar
  48. Suzuki, A., Goll, D. E., Stromer, M. H., Singh, I. &Temple, J. (1973) Alpha-actinin from red and white porcine muscle.Biochim. Biophys. Acta 295, 188–207.PubMedGoogle Scholar
  49. Tregear, R. T. (1977) Insect flight muscle.Proceedings of the Oxford Symposium. Amsterdam: North-Holland.Google Scholar
  50. Wang, K., Ash, J. F. &Singer, S. J. (1975) Filamin, a new high molecular weight protein found in smooth muscle and nonmuscle cells.Proc. Nail Acad. Sci. USA72, 4483–6.Google Scholar
  51. Wang, K. (1977) Filamin, a new high-molecular-weight protein found in smooth muscle and nonmuscle cells. Purification and properties of chicken gizzard filamin.Biochemistry 16, 1857–65.PubMedGoogle Scholar
  52. Wang, K., McClure, J. &Tu, A. (1979) Titin: major myofibrillar components of striated muscle.Proc. Natl Acad. Sci. USA76, 3698–702.PubMedGoogle Scholar
  53. Wang, K. (1985) Sarcomere-associated cytoskeletal lattices in striated muscle.Cell Muscle Motil.6, 315–69.PubMedGoogle Scholar
  54. Wang, K. &Wright, J. (1988) Architecture of the sarcomere matrix of skeletal muscle: immunoelectron microscopic evidence that suggests a set of parallel inextensible nebulin filaments anchored at the Z line.J. Cell Biol. 107, 2199–212.PubMedGoogle Scholar
  55. Wray, J. S. (1979) Filament geometry and the activation of insect flight muscles.Nature 280, 325–6.Google Scholar

Copyright information

© Chapman and Hall Ltd 1991

Authors and Affiliations

  • Jim O. Vigoreaux
    • 1
  • Judith D. Saide
    • 2
  • Mary Lou Pardue
    • 1
  1. 1.Department of BiologyMassachusetts Institute of TechnologyCambridgeUSA
  2. 2.Department of PhysiologyBoston University School of MedicineBostonUSA

Personalised recommendations