Skip to main content

Neuromuscular Development

Connectivity and Plasticity

  • Chapter
Muscle Development in Drosophila

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

  • 963 Accesses

Abstract

The Drosophila neuromuscular junction provides an excellent model system in which to study synaptic development. Axon outgrowth, target selection, and synaptogenesis have been extremely well characterized and occur with remarkable precision. Coupled with the powerful molecular genetic approaches available in Drosophila, this has lead to the identification of many genes involved in these processes. In this review, we examine the cellular and molecular mechanisms of guidance, target selection and synaptogenesis at the neuromuscular junction. We will also discuss how these synaptic contacts are refined and modified during periods of synaptic plasticity.

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. Gramates LS, Budnik V. Assembly and maturation of the Drosophila larval neuromuscular junction. Int Rev Neurobiol 1999; 43:93–117.

    PubMed  CAS  Google Scholar 

  2. Keshishian H, Broadie K, Chiba A et al. The Drosophila neuromuscular junction: A model system for studying synaptic development and function. Annu Rev Neurosci 1996; 19:545–575.

    Article  PubMed  CAS  Google Scholar 

  3. Hoang B, Chiba A. Single-cell analysis of Drosophila larval neuromuscular synapses. Dev Biol 2001; 229(1):55–70.

    Article  PubMed  CAS  Google Scholar 

  4. Rubin GM, Lewis EB. A brief history of Drosophila’s contributions to genome research. Science 2000; 287(5461):2216–2218.

    Article  PubMed  CAS  Google Scholar 

  5. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993; 118(2):401–415.

    PubMed  CAS  Google Scholar 

  6. Osterwalder T, Yoon KS, White BH et al. A conditional tissue-specific transgene expression system using inducible GAL4. Proc Natl Acad Sci USA 2001; 98(22):12596–12601.

    Article  PubMed  CAS  Google Scholar 

  7. Singh S, Wu CF. Ionic currents in larval muscles of Drosophila. Int Rev Neurobiol 1999;43:191–220.

    Article  PubMed  CAS  Google Scholar 

  8. Ng M, Roorda RD, Lima SQ et al. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 2002; 36(3):463–474.

    Article  PubMed  CAS  Google Scholar 

  9. Fiala A, Spall T, Diegelmann S et al. Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr Biol 2002; 12(21):1877–1884.

    Article  PubMed  CAS  Google Scholar 

  10. Yu D, Baird GS, Tsien RY et al. Detection of calcium transients in Drosophila mushroom body neurons with camgaroo reporters. J Neurosci 2003; 23(1):64–72.

    PubMed  Google Scholar 

  11. Halpern ME, Chiba A, Johansen J et al. Growth cone behavior underlying the development of stereotypic synaptic connections in Drosophila embryos. J Neurosci 1991; 11(10):3227–3238.

    PubMed  CAS  Google Scholar 

  12. Sink H, Whitington PM. Location and connectivity of abdominal motoneurons in the embryo and larva of Drosophila melanogaster. J Neurobiol 1991; 22(3):298–311.

    Article  PubMed  CAS  Google Scholar 

  13. Landgraf M, Bossing T, Technau GM et al. The origin, location, and projections of the embryonic abdominal motorneurons of Drosophila. J Neurosci 1997; 17(24):9642–9655.

    PubMed  CAS  Google Scholar 

  14. Atwood HL, Govind CK, Wu CF. Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J Neurobiol 1993; 24(8):1008–1024.

    Article  PubMed  CAS  Google Scholar 

  15. Jia XX, Gorczyca M, Budnik V. Ultrastructure of neuromuscular junctions in Drosophila: Comparison of wild type and mutants with increased excitability. J Neurobiol 1993; 24(8):1025–1044.

    Article  PubMed  CAS  Google Scholar 

  16. Johansen J, Halpern ME, Keshishian H. Axonal guidance and the development of muscle fiber-specific innervation in Drosophila embryos. Journal of Neuroscience 1989; 9(12):4318–4332.

    PubMed  CAS  Google Scholar 

  17. Gorczyca M, Augart C, Budnik V. Insulin-like receptor and insulin-like peptide are localized at neuromuscular junctions in Drosophila. J Neurosci 1993; 13(9):3692–3704.

    PubMed  CAS  Google Scholar 

  18. Jan LY, Jan YN. L-glutamate as an excitatory transmitter at the Drosophila larval neuromuscular junction. J Physiol 1976; 262(1):215–236.

    PubMed  CAS  Google Scholar 

  19. Johansen J, Halpern ME, Keshishian H. Axonal guidance and the development of muscle fiber-specific innervation in Drosophila embryos. J Neurosci 1989; 9(12):4318–4332.

    PubMed  CAS  Google Scholar 

  20. Monastirioti M, Gorczyca M, Rapus J et al. Octopamine immunoreactivity in the fruit fly Drosophila melanogaster. J Comp Neurol 1995; 356(2):275–287.

    Article  PubMed  CAS  Google Scholar 

  21. Anderson MS, Halpern ME, Keshishian H. Identification of the neuropeptide transmitter proctolin in Drosophila larvae: Characterization of muscle fiber-specific neuromuscular endings. J Neurosci 1988; 8(1):242–255.

    PubMed  CAS  Google Scholar 

  22. Zhong Y, Pena LA. A novel synaptic transmission mediated by a PACAP-like neuropeptide in Drosophila. Neuron 1995; 14(3):527–536.

    Article  PubMed  CAS  Google Scholar 

  23. Bossing T, Udolph G, Doe CQ et al. The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev Biol 1996; 179(1):41–64.

    Article  PubMed  CAS  Google Scholar 

  24. Schmid A, Chiba A, Doe CQ. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 1999; 126(21):4653–4689.

    PubMed  CAS  Google Scholar 

  25. Landgraf M, Jeffrey V, Fujioka M et al. Embryonic origins of a motor system: Motor dendrites form a myotopic mapin Drosophila. PLoS Biol 2003; 1(2):E41.

    Article  PubMed  CAS  Google Scholar 

  26. Burrows M. The Neurobiology of an Insect Brain. Oxford: Oxford University Press, 1996.

    Google Scholar 

  27. Bacon JP, Murphey RK. Receptive fields of cricket giant interneurones are related to their dendritic structure. J Physiol 1984; 352:601–623.

    PubMed  CAS  Google Scholar 

  28. Sink H, Whitington PM. Early ablation of target muscles modulates the arborisation pattern of an identified embryonic Drosophila motor axon. Development 1991; 113(2):701–707.

    PubMed  CAS  Google Scholar 

  29. Cash S, Chiba A, Keshishian H. Alternate neuromuscular target selection following the loss of single muscle fibers in Drosophila. J Neurosci 1992; 12(6):2051–2064.

    PubMed  CAS  Google Scholar 

  30. O’Connor TP, Duerr JS, Bentley D. Pioneer growth cone steering decisions mediated by single filopodial contacts in situ. J Neurosci 1990; 10(12):3935–3946.

    PubMed  CAS  Google Scholar 

  31. Thor S, Andersson SG, Tomlinson A et al. A LIM-homeodomain combinatorial code for motor-neuron pathway selection. Nature 1999; 397(6714):76–80.

    Article  PubMed  CAS  Google Scholar 

  32. Landgraf M, Roy S, Prokop A et al. Even-skipped determines the dorsal growth of motor axons in Drosophila. Neuron 1999; 22(1):43–52.

    Article  PubMed  CAS  Google Scholar 

  33. Landgraf M, Baylies M, Bate M. Muscle founder cells regulate defasciculation and targeting of motor axons in the Drosophila embryo. Curr Biol 1999; 9(11):589–592.

    Article  PubMed  CAS  Google Scholar 

  34. Vactor DV, Sink H, Fambrough D et al. Genes that control neuromuscular specificity in Drosophila. Cell 1993; 73(6):1137–1153.

    Article  PubMed  CAS  Google Scholar 

  35. Grenningloh G, Rehm EJ, Goodman CS. Genetic analysis of growth cone guidance in Drosophila: Fasciclin II functions as a neuronal recognition molecule. Cell 1991; 67(1):45–57.

    Article  PubMed  CAS  Google Scholar 

  36. Nose A, Mahajan VB, Goodman CS. Connectin: A homophilic cell adhesion molecule expressed on a subset of muscles and the motoneurons that innervate them in Drosophila. Cell 1992; 70(4):553–567.

    Article  PubMed  CAS  Google Scholar 

  37. Lin DM, Fetter RD, Kopczynski C et al. Genetic analysis of Fasciclin II in Drosophila: Defasciculation, refasciculation, and altered fasciculation. Neuron 1994; 13(5):1055–1069.

    Article  PubMed  CAS  Google Scholar 

  38. Lin DM, Goodman CS. Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 1994; 13(3):507–523.

    Article  PubMed  CAS  Google Scholar 

  39. Yu HH, Araj HH, Rails SA et al. The transmembrane semaphorin sema I is required in Drosophila for embryonic motor and CNS axon guidance. Neuron 1998; 20(2):207–220.

    Article  PubMed  CAS  Google Scholar 

  40. Winberg ML, Mitchell KJ, Goodman CS. Genetic analysis of the mechanisms controlling target selection: Complementary and combinatorial functions of netrins, semaphorins, and IgCAMs. Cell 1998; 93(4):581–591.

    Article  PubMed  CAS  Google Scholar 

  41. Yu HH, Huang AS, Kolodkin AL. Semaphorin-la acts in concert with the cell adhesion molecules fasciclin II and connectin to regulate axon fasciculation in Drosophila. Genetics 2000; 156(2):723–731.

    PubMed  CAS  Google Scholar 

  42. Winberg ML, Noordermeer JN, Tamagnone L et al. Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 1998; 95(7):903–916.

    Article  PubMed  CAS  Google Scholar 

  43. Fambrough D, Goodman CS. The Drosophila beaten path gene encodes a novel secreted protein that regulates defasciculation at motor axon choice points. Cell 1996; 87(6):1049–1058.

    Article  PubMed  CAS  Google Scholar 

  44. Sink H, Rehm EJ, Richstone L et al. Sidestep encodes a target-derived attractant essential for motor axon guidance in Drosophila. Cell 2001; 105(1):57–67.

    Article  PubMed  CAS  Google Scholar 

  45. Krueger NX, Van Vactor D, Wan HI et al. The transmembrane tyrosine phosphatase DLAR controls motor axon guidance in Drosophila. Cell 1996; 84(4):611–622.

    Article  PubMed  CAS  Google Scholar 

  46. Desai CJ, Gindhart Jr JG, Goldstein LS et al. Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo. Cell 1996; 84(4):599–609.

    Article  PubMed  CAS  Google Scholar 

  47. Schindelholz B, Knirr M, Warrior R et al. Regulation of CNS and motor axon guidance in Drosophila by the receptor tyrosine phosphatase DPTP52F. Development 2001; 128(21):4371–4382.

    PubMed  CAS  Google Scholar 

  48. Sun Q, Schindelholz B, Knirr M et al. Complex genetic interactions among four receptor tyrosine phosphatases regulate axon guidance in Drosophila. Mol Cell Neurosci 2001; 17(2):274–291.

    Article  PubMed  CAS  Google Scholar 

  49. Desai CJ, Krueger NX, Saito H et al. Competition and cooperation among receptor tyrosine phosphatases control motoneuron growth cone guidance in Drosophila. Development 1997; 124(10):1941–1952.

    PubMed  CAS  Google Scholar 

  50. Johnson KG, Van Vactor D. Receptor protein tyrosine phosphatases in nervous system development. Physiol Rev 2003; 83(1):1–24.

    PubMed  CAS  Google Scholar 

  51. Wills Z, Bateman J, Korey CA et al. The tyrosine kinase Abl and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 1999; 22(2):301–312.

    Article  PubMed  CAS  Google Scholar 

  52. Lanier LM, Gertler FB. From Abl to actin: Abl tyrosine kinase and associated proteins in growth cone motility. Curr Opin Neurobiol 2000; 10(1):80–87.

    Article  PubMed  CAS  Google Scholar 

  53. Chiba A, Hing H, Cash S et al. Growth cone choices of Drosophila motoneurons in response to muscle fiber mismatch. J Neurosci 1993; 13(2):714–732.

    PubMed  CAS  Google Scholar 

  54. Chiba A, Snow P, Keshishian H et al. Fasciclin III as a synaptic target recognition molecule in Drosophila. Nature 1995; 374(6518):166–168.

    Article  PubMed  CAS  Google Scholar 

  55. Shishido E, Takeichi M, Nose A. Drosophila synapse formation: Regulation by transmembrane protein with Leu-rich repeats, CAPRICIOUS. Science 1998; 280(5372):2118–2121.

    Article  PubMed  CAS  Google Scholar 

  56. Nose A, Umeda T, Takeichi M. Neuromuscular target recognition by a homophilic interaction of connectin cell adhesion molecules in Drosophila. Development 1997; 124(8):1433–1441.

    PubMed  CAS  Google Scholar 

  57. Nose A, Takeichi M, Goodman CS. Ectopic expression of connectin reveals a repulsive function during growth cone guidance and synapse formation. Neuron 1994; 13(3):525–539.

    Article  PubMed  CAS  Google Scholar 

  58. Kose H, Rose D, Zhu X et al. Homophilic synaptic target recognition mediated by immunoglobulin-like cell adhesion molecule Fasciclin III. Development 1997; 124(20):4143–4152.

    PubMed  CAS  Google Scholar 

  59. Mitchell KJ, Doyle JL, Serafini T et al. Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 1996; 17(2):203–215.

    Article  PubMed  CAS  Google Scholar 

  60. Kolodziej PA, Timpe LC, Mitchell KJ et al. Frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 1996; 87(2):197–204.

    Article  PubMed  CAS  Google Scholar 

  61. Halfon MS, Hashimoto C, Keshishian H. The Drosophila toll gene functions zygotically and is necessary for proper motoneuron and muscle development. Dev Biol 1995; 169(1):151–167.

    Article  PubMed  CAS  Google Scholar 

  62. Rose D, Zhu X, Kose H et al. Toll, a muscle cell surface molecule, locally inhibits synaptic initiation of the RP3 motoneuron growth cone in Drosophila. Development 1997; 124(8):1561–1571.

    PubMed  CAS  Google Scholar 

  63. Keleman K, Rajagopalan S, Cleppien D et al. Comm sorts robo to control axon guidance at the Drosophila midline. Cell 2002; 110(4):415–427.

    Article  PubMed  CAS  Google Scholar 

  64. Wolf B, Seeger MA, Chiba A. Commissureless endocytosis is correlated with initiation of neuromuscular synaptogenesis. Development 1998; 125(19):3853–3863.

    PubMed  CAS  Google Scholar 

  65. Kolodkin AL, Matthes DJ, Goodman CS. The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 1993; 75(7):1389–1399.

    Article  PubMed  CAS  Google Scholar 

  66. Murray MJ, Merritt DJ, Brand AH et al. In vivo dynamics of axon pathfinding in the Drosophilia CNS: A time-lapse study of an identified motorneuron. J Neurobiol 1998; 37(4):607–621.

    Article  PubMed  CAS  Google Scholar 

  67. Davis GW, Schuster CM, Goodman CS. Genetic analysis of the mechanisms controlling target selection: Target-derived Fasciclin II regulates the pattern of synapse formation. Neuron 1997; 19(3):561–573.

    Article  PubMed  CAS  Google Scholar 

  68. Rose D, Chiba A. A single growth cone is capable of integrating simultaneously presented and functionally distinct molecular cues during target recognition. J Neurosci 1999; 19(12):4899–4906.

    PubMed  CAS  Google Scholar 

  69. Keshishian H, Chiba A. Neuromuscular development in Drosophila: Insights from single neurons and single genes. Trends Neurosci 1993; 16(7):278–283.

    Article  PubMed  CAS  Google Scholar 

  70. Broadie K, Bate M. Innervation directs receptor synthesis and localization in Drosophila embryo synaptogenesis. Nature 1993; 361(6410):350–353.

    Article  PubMed  CAS  Google Scholar 

  71. Yoshihara M, Rheuben MB, Kidokoro Y. Transition from growth cone to functional motor nerve terminal in Drosophila embryos. J Neurosci 1997; 17(21):8408–8426.

    PubMed  CAS  Google Scholar 

  72. Keshishian H, Chiba A, Chang TN et al. Cellular mechanisms governing synaptic development in Drosophila melanogaster. J Neurobiol 1993; 24(6):757–787.

    Article  PubMed  CAS  Google Scholar 

  73. Murray MJ, Whitington PM. Effects of roundabout on growth cone dynamics, filopodial length, and growth cone morphology at the midline and throughout the neuropile. J Neurosci 1999; 19(18):7901–7912.

    PubMed  CAS  Google Scholar 

  74. Suzuki E, Rose D, Chiba A. The ultrastructural interactions of identified pre and postsynaptic cells during synaptic target recognition in Drosophila embryos. J Neurobiol 2000; 42(4):448–459.

    Article  PubMed  CAS  Google Scholar 

  75. Ritzenthaler S, Suzuki E, Chiba A. Postsynaptic filopodia in muscle cells interact with innervating motoneuron axons. Nat Neurosci 2000; 3(10):1012–1017.

    Article  PubMed  CAS  Google Scholar 

  76. Broadie KS, Bate M. Development of the embryonic neuromuscular synapse of Drosophila melanogaster. J Neurosci 1993; 13(1):144–166.

    PubMed  CAS  Google Scholar 

  77. Saitoe M, Tanaka S, Takata K et al. Neural activity affects distribution of glutamate receptors during neuromuscular junction formation in Drosophila embryos. Dev Biol 1997; 184(1):48–60.

    Article  PubMed  CAS  Google Scholar 

  78. Broadie K, Bate M. Activity-dependent development of the neuromuscular synapse during Drosophila embryogenesis. Neuron 1993; 11(4):607–619.

    Article  PubMed  CAS  Google Scholar 

  79. Anderson MJ, Cohen MW, Zorychta E. Effects of innervation on the distribution of acetylcholine receptors on cultured muscle cells. J Physiol 1977; 268(3):731–756.

    PubMed  CAS  Google Scholar 

  80. Davey DF, Cohen MW. Localization of acetylcholine receptors and cholinesterase on nerve-contacted and noncontacted muscle cells grown in the presence of agents that block action potentials. J Neurosci 1986; 6(3):673–680.

    PubMed  CAS  Google Scholar 

  81. Dahm LM, Landmesser LT. The regulation of synaptogenesis during normal development and following activity blockade. J Neurosci 1991; 11(1):238–255.

    PubMed  CAS  Google Scholar 

  82. Kopczynski CC, Davis GW, Goodman CS. A neural tetraspanin, encoded by late bloomer, that facilitates synapse formation. Science 1996; 271(5257):1867–1870.

    Article  PubMed  CAS  Google Scholar 

  83. Fradkin LG, Kamphorst JT, DiAntonio A et al. Genomewide analysis of the Drosophila tetraspanins reveals a subset with similar function in the formation of the embryonic synapse. Proc Natl Acad Sci USA 2002; 99(21):13663–13668.

    Article  PubMed  CAS  Google Scholar 

  84. Sink H, Whitington PM. Pathfinding in the central nervous system and periphery by identified embryonic Drosophila motor axons. Development 1991; 112(1):307–316.

    PubMed  CAS  Google Scholar 

  85. Broadie K, Sink H, Van Vactor D et al. From growth cone to synapse: The life history of the RP3 motor neuron. Dev Suppl 1993; 227–238.

    Google Scholar 

  86. Jarecki J, Keshishian H. Role of neural activity during synaptogenesis in Drosophila. J Neurosci 1995; 15(12):8177–8190.

    PubMed  CAS  Google Scholar 

  87. Chang TN, Keshishian H. Laser ablation of Drosophila embryonic motoneurons causes ectopic innervation of target muscle fibers. J Neurosci 1996; 16(18):5715–5726.

    PubMed  CAS  Google Scholar 

  88. White BH, Osterwalder TP, Yoon KS et al. Targeted attenuation of electrical activity in Drosophila using a genetically modified K(+) channel. Neuron 2001; 31(5):699–711.

    Article  PubMed  CAS  Google Scholar 

  89. Yoon KS, Wells DG, Keshishian H. Activity-dependent remodeling of Drosophila NMJ deopends on presynaptic as opposed to postsynaptic electrical excitability. Soc Neurosci Abstr 2003; 457–21.

    Google Scholar 

  90. Ming G, Henley J, Tessier-Lavigne M et al. Electrical activity modulates growth cone guidance by diffusible factors. Neuron 2001; 29(2):441–452.

    Article  PubMed  CAS  Google Scholar 

  91. Hu H, Marton TF, Goodman CS. Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron 2001; 32(1):39–51.

    Article  PubMed  CAS  Google Scholar 

  92. Matthes DJ, Sink H, Kolodkin AL et al. Semaphorin II can function as a selective inhibitor of specific synaptic arborizations. Cell 1995; 81(4):631–639.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Haig Keshishian .

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Eurekah.com and Springer Science+Business Media

About this chapter

Cite this chapter

Nicholson, L., Keshishian, H. (2006). Neuromuscular Development. In: Muscle Development in Drosophila. Molecular Biology Intelligence Unit. Springer, New York, NY. https://doi.org/10.1007/0-387-32963-3_10

Download citation

Publish with us

Policies and ethics