Skip to main content

Molecular Basis of Muscle Structure

  • Chapter
Muscle Development in Drosophila

Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

Abstract

The flight muscle myofibril is a precisely assembled cytoskeletal network of contractile proteins that produces high power to sustain flight. This chapter will focus on myofibrillar assembly during development of the indirect flight muscles. Studies in Drosophila melanogaster have combined genetics with microscopy to elucidate the series of steps that lead to the formation of the sarcomere and the role that individual myofibrillar proteins may play in this process. Despite much progress, the broad characterization of many of the mutants’ effects has yet to uncover the mechanisms that regulate and dictate the assembly of the myofibril.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Crossley AC. The morphology and development of the Drosophila muscular system. In: Ashburner M, Wright TRF, eds. The Genetics and Biology of Drosophila, Vol. 2b. London: Academic Press, 1978:499–560.

    Google Scholar 

  2. Deak II, Bellamy PR, Bienz M et al. Mutations affecting the indirect flight muscles of Drosophila melanogaster. J Embryol Exp Morphol 1982; 69:61–81.

    PubMed  CAS  Google Scholar 

  3. Mogami K, Hotta Y. Isolation of Drosophila flightless mutants which affect myofibrillar proteins of indirect flight muscle. Mol Gen Genet 1981; 183:409–417.

    Article  PubMed  CAS  Google Scholar 

  4. Bernstein SI, O’Donnell PT, Cripps RM. Molecular genetic analysis of muscle development, structure and function in Drosophila. Int Rev Cytol 1993; 143:63–152.

    Article  PubMed  CAS  Google Scholar 

  5. Vigoreaux JO. Genetics of the Drosophila flight muscle myofibril: A window into the biology of complex systems. Bioessays 2001; 23:1047–1063.

    Article  PubMed  CAS  Google Scholar 

  6. Vigoreaux JO, Swank DM. The development of the flight and leg muscle. In: Gilbert LI, Iatrou K, Gill S, eds. Comprehensive Molecular Insect Science. Oxford: Elsevier, 2004:in press.

    Google Scholar 

  7. Reedy MC, Beall C. Ultrastructure of developing flight muscle in Drosophila. I. Assembly of myofibrils. Develop Biol 1993; 160:443–465.

    Article  PubMed  CAS  Google Scholar 

  8. Yu Q, Hipolito LC, Kronert WA et al. Characterization and functional analysis of the Drosophila melanogaster unc-45 (dunc-45) gene. Mol Biol Cell 2003; 14(S):45a.

    Google Scholar 

  9. Swank DM, Wells L, Kronert WA et al. Determining structure/function relationships for sarcomeric myosin heavy chain by genetic and transgenic manipulation of Drosophila. Microsc Res Tech 2000; 50(6):430–442.

    Article  PubMed  CAS  Google Scholar 

  10. Fyrberg E, Beall C. Genetic approaches to myofibril form and function in Drosophila. TIG 1990; 6(4):126–131.

    PubMed  CAS  Google Scholar 

  11. Chun M, Falkenthal S. Ifm(2)2 is a myosin heavy chain allele that disrupts myofibrillar assembly only in the indirect flight muscle of Drosophila melanogaster. J Cell Biol 1988; 107:2613–2621.

    Article  PubMed  CAS  Google Scholar 

  12. Mogami K, O’Donnell PT, Bernstein SI et al. Mutations of the Drosophila myosin heavy-chain gene: Effects on transcription, myosin accumulation, and muscle function. Proc Natl Acad Sci USA 1986; 83(5):1393–1397.

    Article  PubMed  CAS  Google Scholar 

  13. Beall CJ, Sepanski MA, Fyrberg EA. Genetic dissection of Drosophila myofibril formation: Effects of actin and myosin heavy chain null alleles. Genes Dev 1989; 3:131–140.

    PubMed  CAS  Google Scholar 

  14. Cripps RM, Becker KD, Mardahl M et al. 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 1994; 126(3):689–699.

    Article  PubMed  CAS  Google Scholar 

  15. Homyk T, Emerson CP. Functional interactions between unlinked muscle genes within haploinsufficient regions of the Drosophila genome. Genetics 1988; 119:105–121.

    PubMed  Google Scholar 

  16. Kronert WA, O’Donnell PT, Fieck A et al. Defects in the Drosophila myosin rod permit sarcomere assembly but cause flight muscle degeneration. J Mol Biol 1995; 249:111–125.

    Article  PubMed  CAS  Google Scholar 

  17. Bernstein SI, Milligan RA. Fine tuning a molecular motor: The location of alternative domains in the Drosophila myosin head. J Mol Biol 1997; 271(1):1–6.

    Article  PubMed  CAS  Google Scholar 

  18. O’Donnell PT, Collier VL, Mogami K et al. Ultrastructural and molecular analyses of homozygous-viable Drosophila melanogaster muscle mutants indicate there is a complex pattern of myosin heavy-chain isoform distribution. Genes Dev 1989; 3(8):1233–1246.

    PubMed  CAS  Google Scholar 

  19. Kronert WA, O’Donnell PT, Bernstein SI. A charge change in an evolutionarily-conserved region of the myosin globular head prevents myosin and thick filament accumulation in Drosophila. J Mol Biol 1994; 236(3):697–702.

    Article  PubMed  CAS  Google Scholar 

  20. Cripps RM, Suggs JA, Bernstein SI. Assembly of thick filaments and myofibrils occurs in the absence of the myosin head. EMBO J 1999; 18(7):1793–1804.

    Article  PubMed  CAS  Google Scholar 

  21. Swank DM, Bartoo ML, Knowles AF et al. Alternative exon-encoded regions of Drosophila myosin heavy chain modulate ATPase rates and actin sliding velocity. J Biol Chem 2001; 276(18):15117–15124.

    Article  PubMed  CAS  Google Scholar 

  22. Swank DM, Knowles AF, Kronert WA et al. Variable N-terminal regions of muscle myosin heavy chain modulate ATPase rate and actin sliding velocity. J Biol Chem 2003; 278(19):17475–17482.

    Article  PubMed  CAS  Google Scholar 

  23. Wells L, Edwards KA, Bernstein SI. Myosin heavy chain isoforms regulate muscle function but not myofibril assembly. EMBO J 1996; 15(17):4454–4459.

    PubMed  CAS  Google Scholar 

  24. Warmke J, Yamakawa M, Molloy J et al. Myosin light chain-2 mutation affects flight, wing beat frequency and indirect flight muscle contraction kinetics in Drosophila. J Cell Biol 1992; 119:1523–1539.

    Article  PubMed  CAS  Google Scholar 

  25. Takano-Ohmuro H, Takahashi S, Hirose G et al. Phosphorylated and dephosphorylated myosin light chains of Drosophila fly and larva. Comp Biochem Physiol 1990; 95B:171–177.

    CAS  Google Scholar 

  26. Tohtong R, Yamashita H, Graham M et al. Impairment of muscle function caused by mutations of phosphorylation sites in myosin regulatory light chain. Nature 1995; 374:650–655.

    Article  PubMed  CAS  Google Scholar 

  27. Dickinson MH, Hyatt CJ, Lehmann F-O et al. Phosphorylation-dependent power output of transgenic flies: An integrated study. Biophys J 1997; 73:3122–3134.

    PubMed  CAS  Google Scholar 

  28. Tohtong R, Rodriguez D, Maughan D et al. Analysis of cDNAs encoding Drosophila melanogaster myosin light chain kinase. J Muscle Res Cell Motil 1997; 18(1):43–56.

    Article  PubMed  CAS  Google Scholar 

  29. Moore JR, Dickinson MH, Vigoreaux JO et al. 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 muscles. Biophys J 2000; 78:1431–1440.

    PubMed  CAS  Google Scholar 

  30. Arredondo JJ, Mardahl-Dumesnil M, Cripps RM et al. Overexpression of miniparamyosin causes muscle dysfunction and age-dependant myofibril degeneration in the indirect flight muscles of Drosophila melanogaster. J Muscle Res Cell Motil 2001; 22(3):287–299.

    Article  PubMed  CAS  Google Scholar 

  31. Liu H, Mardahl-Dumesnil M, Sweeney ST et al. Drosophila paramyosin is important for myoblast fusion and essential for myofibril formation. J Cell Biol 2003; 160(6):899–908.

    Article  PubMed  CAS  Google Scholar 

  32. Maroto M, Arredondo J, Goulding D et al. 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 1996; 134(1):81–92.

    Article  PubMed  CAS  Google Scholar 

  33. Reedy MC, Bullard B, Vigoreaux JO. Flightin is essential for thick filament assembly and sarcomere stability in Drosophila flight muscles. J Cell Biol 2000; 151:1483–1499.

    Article  PubMed  CAS  Google Scholar 

  34. Nongthomba U, Cummins M, Clark S et al. Suppression of muscle hypercontraction by mutations in the myosin heavy chain gene of Drosophila melanogaster. Genetics 2003; 164(1):209–222.

    PubMed  CAS  Google Scholar 

  35. Fernandes J, Bate M, Vijayraghavan K. Development of the indirect flight muscles of Drosophila. Development 1991; 113(1):67–77.

    PubMed  CAS  Google Scholar 

  36. Barton BE, Ayer G, Cajigas IJ et al. Defects in flight muscle ultrastructure and function in transgenic Drosophila with mutations of phosphorylation sites in flightin. Mol Biol Cell 2002; 13S:319a.

    Google Scholar 

  37. Vigoreaux JO, Hernandez C, Moore J et al. A genetic deficiency that spans the flightin gene of Drosophila melanogaster affects the ultrastructure and function of the flight muscles. J Exp Biol 1998; 201:2033–2044.

    PubMed  CAS  Google Scholar 

  38. Vigoreaux JO, Saide JD, Valgeirsdottir K et al. Flightin, a novel myofibrillar protein of Drosophila stretch-activated muscles. J Cell Biol 1993; 121(3):587–598.

    Article  PubMed  CAS  Google Scholar 

  39. Vigoreaux JO, Perry LM. Multiple isoelectric variants of flightin in Drosophila stretch-activated muscles are generated by temporally regulated phosphorylation. J Muscle Res Cell Motil 1994;15:607–616.

    Article  PubMed  CAS  Google Scholar 

  40. Cammarato A, Hatch V, Saide J et al. Drosophila muscle regulation characterized by electron microscopy and three-dimensional reconstruction of thin filament mutants. Biophys J 2004; 86(3):1618–1624.

    Article  PubMed  CAS  Google Scholar 

  41. Drummond DR, Hennessey ES, Sparrow JC. Characterisation of missense mutations in the Act88F gene of Drosophila melanogaster. Mol Gen Genet 1991; 226:70–80.

    Article  PubMed  CAS  Google Scholar 

  42. Okamoto H, Hiromi Y, Ishikawa E et al. Molecular characterization of mutant actin genes which induce heat-shock proteins in Drosophila flight muscles. EMBO J 1986; 5(3):589–596.

    PubMed  CAS  Google Scholar 

  43. Hiromi Y, Okamoto H, Gehring WJ et al. Germline transformation with Drosophila mutant actin genes induces constitutive expression of heat shock genes. Cell 1986; 44(2):293–301.

    Article  PubMed  CAS  Google Scholar 

  44. Sparrow J, Reedy M, Ball E et al. Functional and ultrastructural effects of a missense mutation in the indirect flight muscle-specific actin gene of Drosophila melanogaster. J Mol Biol 1991;222:963–982.

    Article  PubMed  CAS  Google Scholar 

  45. Reedy MC, Beall C, Fyrberg E. Formation of reverse rigor chevrons by myosin heads. Nature 1989; 339:481–483.

    Article  PubMed  CAS  Google Scholar 

  46. Nongthomba U, Cummins M, Clark S et al. Suppression of the muscle hypercontraction phenotype by mutations in the myosin heavy chain gene of Drosophila melanogaster. Genetics 2003;164:209–222.

    PubMed  CAS  Google Scholar 

  47. An H, Mogami K. Isolation of 88F actin mutants of Drosophila melanogaster and possible alterations in the mutant actin structures. J Mol Biol 1996; 260:492–505.

    Article  PubMed  CAS  Google Scholar 

  48. Sakai Y, Okamoto H, Mogami K et al. Actin with tumor-related mutation is antimorphic in Drosophila muscle: Two distinct modes of myofibrillar disruption by antimorphic actins. J Biochem (Tokyo) 1990; 107(3):499–505.

    PubMed  CAS  Google Scholar 

  49. Brault V, Reedy MC, Sauder U et al. Substitution of flight muscle-specific actin by human (beta)-cytoplasmic actin in the indirect flight muscle of Drosophila. J Cell Sci 1999; 112 (Pt 21):3627–3639.

    PubMed  CAS  Google Scholar 

  50. Fyrberg EA, Fyrberg CC, Biggs JR et al. Functional nonequivalence of Drosophila actin isoforms. Biochem Genet 1998; 36(7–8):271–287.

    Article  PubMed  CAS  Google Scholar 

  51. Schmitz S, Clayton J, Nongthomba U et al. Drosophila ACT88F indirect flight muscle-specific actin is not N-terminally acetylated: A mutation in N-terminal processing affects actin function. J Mol Biol 2000; 295(5):1201–1210.

    Article  PubMed  CAS  Google Scholar 

  52. Ball E, Karlik CC, Beall CJ et al. Arthrin, a myofibrillar protein of insect flight muscle, is an actin-ubiquitin conjugate. Cell 1987; 51:221–228.

    Article  PubMed  CAS  Google Scholar 

  53. Nongthomba U, Clark S, Cummins M et al. Troponin I is required for myofibrillogenesis and sarcomere formation in Drosophila flight muscle. J Cell Sci 2004; 117(9):1795–1805.

    Article  PubMed  CAS  Google Scholar 

  54. Fyrberg E, Fyrberg CC, Beall C et al. Drosophila melanogaster troponin-T mutations engender three distinct syndromes of myofibrillar abnormalities. J Mol Biol 1990; 216:657–675.

    Article  PubMed  CAS  Google Scholar 

  55. Barbas JA, Galceran J, Torroja L et al. Abnormal muscle development in the heldup3 mutant of Drosophila melanogaster is caused by a splicing defect affecting selected troponin I isoforms. Mol Cell Biol 1993; 13(3):1433–1439.

    PubMed  CAS  Google Scholar 

  56. Beall CJ, Fyrberg E. Muscle abnormalities in Drosophila melanogaster heldup mutants are caused by missing or aberrant troponin-I isoforms. J Cell Biol 1991; 114:941–951.

    Article  PubMed  CAS  Google Scholar 

  57. Kronert WA, Acebes A, Ferrus A et al. Specific myosin heavy chains mutations suppress troponin I defects in Drosophila muscles. J Cell Biol 1999; 144(5):989–1000.

    Article  PubMed  CAS  Google Scholar 

  58. Prado A, Canal I, Barbas JA et al. Functional recovery of troponin I in a Drosophila heldup mutant after a second site mutation. Mol Biol Cell 1995; 6(11):1433–1441.

    PubMed  CAS  Google Scholar 

  59. Naimi B, Harrison A, Cummins M et al. A tropomyosin-2 mutation suppresses a troponin I myopathy in Drosophila. Mol Biol Cell 2001; 12(5):1529–1539.

    PubMed  CAS  Google Scholar 

  60. Benoist P, Mas JA, Marco R et al. Differential muscle-type expression of the Drosophila troponin T gene. A 3-base pair microexon is involved in visceral and adult hypodermic muscle specification. J Biol Chem 1998; 273(13):7538–7546.

    Article  PubMed  CAS  Google Scholar 

  61. Domingo A, Gonzalez-Jurado J, Maroto M et al. Troponin-T is a calcium-binding protein in insect muscle: In vivo phosphorylation, muscle-specific isoforms and developmental profile in Drosophila melanogaster. J Muscle Res Cell Motil 1998; 19(4):393–403.

    Article  PubMed  CAS  Google Scholar 

  62. Miller RC, Schaaf R, Maughan DW et al. A nonflight muscle isoform of Drosophila tropomyosin rescues an indirect flight muscle tropomyosin mutant. J Muscle Res Cell Motil 1993; 14(1):85–98.

    Article  PubMed  CAS  Google Scholar 

  63. Karlik CC, Fyrberg EA. An insertion within a variably spliced Drosophila tropomyosin gene blocks accumulation of only one encoded isoform. Cell 1985; 41:57–66.

    Article  PubMed  CAS  Google Scholar 

  64. Kreuz AJ, Simcox A, Maughan D. Alterations in flight muscle ultrastructure and function in Drosophila tropomyosin mutants. J Cell Biol 1996; 135(3):673–687.

    Article  PubMed  CAS  Google Scholar 

  65. Mardahl-Dumesnil M, Fowler VM. Thin filaments elongate from their pointed ends during myofibril assembly in Drosophila indirect flight muscle. J Cell Biol 2001; 155(6):1043–1053.

    Article  PubMed  CAS  Google Scholar 

  66. Hakeda S, Endo S, Saigo K. Requirements of Kettin, a giant muscle protein highly conserved in overall structure in evolution, for normal muscle function, viability, and flight activity of Drosophila. J Cell Biol 2000; 148:101–114.

    Article  PubMed  CAS  Google Scholar 

  67. Roulier EM, Fyrberg C, Fyrberg E. Perturbations of Drosophila a-actinin cause muscle paralysis, weakness, and atrophy but do not confer obvious nonmuscle phenotypes. J Cell Biol 1992;116:911–922.

    Article  PubMed  CAS  Google Scholar 

  68. Fyrberg E, Kelly M, Ball E et al. Molecular genetics of Drosophila alpha-actinin: Mutant alleles disrupt Z disc integrity and muscle insertions. J Cell Biol 1990; 110:1999–2011.

    Article  PubMed  CAS  Google Scholar 

  69. Whiting A, Wardale J, Trinick J. Does titin regulate the length of muscle thick filaments? J Mol Biol 1989; 205(1):263–268.

    Article  PubMed  CAS  Google Scholar 

  70. Gregorio CC, Granzier H, Sorimachi H et al. Muscle assembly: A titanic achievement? Curr Opin Cell Biol 1999; 11(1);18–25.

    Article  PubMed  CAS  Google Scholar 

  71. Machado C, Sunkel CE, Andrew DJ. Human autoantibodies reveal titin as a chromosomal protein. J Cell Biol 1998; 141(2):321–334.

    Article  PubMed  CAS  Google Scholar 

  72. Kulke M, Neagoe C, Kolmerer B et al. Kettin, a major source of myofibrillar stiffness in Drosophila indirect flight muscle. J Cell Biol 2001; 154(5):1045–1057.

    Article  PubMed  CAS  Google Scholar 

  73. Zhang Y, Featherstone D, Davis W et al. Drosophila D-titin is required for myoblast fusion and skeletal muscle striation. J Cell Sci 2000; 113 (Pt 17):3103–3115.

    PubMed  CAS  Google Scholar 

  74. Machado C, Andrew DJ. D-Titin: A giant protein with Dual roles in chromosomes and muscles. J Cell Biol 2000; 151(3):639–652.

    Article  PubMed  CAS  Google Scholar 

  75. Henkin J, Vigoreaux JO. Mapping myofibrillar protein interactions by mutational proteomics. In: Vigoreaux JO, ed. Nature’s Versatile Engine: Insect Flight Muscle Inside and Out. Georgetown: Landes Bioscience, 2006:270–284.

    Google Scholar 

  76. White KP, Rifkin SA, Hurban P et al. Microarray analysis of Drosophila development during metamorphosis. Science 1999; 286(5447):2179–2184.

    Article  PubMed  CAS  Google Scholar 

  77. Arbeitman MN, Furlong EE, Imam F et al. Gene expression during the life cycle of Drosophila melanogaster. Science 2002; 297(5590):2270–2275.

    Article  PubMed  CAS  Google Scholar 

  78. Horn C, Offen N, Nystedt S et al. Piggybac-based insertional mutagenesis and enhancer detection as a tool for functional insect genomics. Genetics 2003; 163(2):647–661.

    PubMed  CAS  Google Scholar 

  79. Maughan D, Vigoreaux J. Nature’s strategy for optimizing power generation in insect flight muscle. In: Sugi H, ed. Mysteries About the Sliding Filament Mechanism: Fifty Years After its Proposal. New York: Kluwer/Plenum Press, 2004:in press.

    Google Scholar 

  80. Barton B, Ayer G, Heymann N et al. Flight muscle properties and aerodynamic performance of Drosophila expressing a flightin transgene. J Exp Biol 2005; 208:549–560.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Eurekah.com and Springer Science+Business Media

About this chapter

Cite this chapter

Vigoreaux, J.O. (2006). Molecular Basis of Muscle Structure. In: Muscle Development in Drosophila. Molecular Biology Intelligence Unit. Springer, New York, NY. https://doi.org/10.1007/0-387-32963-3_12

Download citation

Publish with us

Policies and ethics