Skip to main content
SpringerLink
Log in

Glutamatergic Synthesis, Recycling, and Receptor Pharmacology at Drosophila and Crustacean Neuromuscular Junctions

  • Protocol
  • First Online:
Biochemical Approaches for Glutamatergic Neurotransmission

Part of the book series: Neuromethods ((NM,volume 130))

Abstract

Invertebrate glutamatergic synapses have been at the forefront of major discoveries into the mechanisms of neurotransmission. In this chapter we recount many of the neurophysiological advances that have been made using invertebrate model organisms, from receptor pharmacology to synaptic plasticity and glutamate recycling. We then direct your attention to the crayfish and fruit fly larva neuromuscular junctions, glutamatergic synapses that have been extraordinarily insightful, the crayfish because of its experimental tractability and Drosophila because of its extensive genetic and molecular resources. Detailed protocols with schematics and representative images are provided for both preparations, along with references to more advanced techniques that have been developed in these systems. The chapter concludes with a discussion of unresolved questions and future directions for which invertebrate neuromuscular junction preparations would be particularly well suited.

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

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
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

References

  1. Usherwood PN (1977) Glutamatergic synapses in invertebrates [proceedings]. Biochem Soc Trans 5(4):845–849

    Article  CAS  PubMed  Google Scholar 

  2. Duce IR (1988) Glutamate. In: Lunt GG, Olsen RW (eds) Comparative invertebrate neurochemistry. Springer US, Boston, MA, pp 42–89

    Chapter  Google Scholar 

  3. Greer JB, Khuri S, Fieber LA (2017) Phylogenetic analysis of ionotropic l-glutamate receptor genes in the Bilateria, with special notes on Aplysia californica. BMC Evol Biol 17(1):11

    Article  PubMed Central  PubMed  Google Scholar 

  4. Petroff OA (2002) GABA and glutamate in the human brain. Neuroscientist 8(6):562–573

    Article  CAS  PubMed  Google Scholar 

  5. Traynelis SF et al (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62(3):405–496

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Price MB, Jelesko J, Okumoto S (2012) Glutamate receptor homologs in plants: functions and evolutionary origins. Front Plant Sci 3:235

    Article  PubMed Central  PubMed  Google Scholar 

  7. Li Y et al (2016) Novel functional properties of Drosophila CNS glutamate receptors. Neuron 92(5):1036–1048

    Article  CAS  PubMed  Google Scholar 

  8. Hawkins RA, Vina JR (2016) How glutamate is managed by the blood-brain barrier. Biology (Basel) 5(4)

    Google Scholar 

  9. Anne C, Gasnier B (2014) Vesicular neurotransmitter transporters: mechanistic aspects. Curr Top Membr 73:149–174

    Article  CAS  PubMed  Google Scholar 

  10. Ziegler AB et al (2016) The amino acid transporter JhI-21 coevolves with glutamate receptors, impacts NMJ physiology, and influences locomotor activity in Drosophila larvae. Sci Rep 6:19692

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Ishibashi H et al (2013) Dynamic regulation of glycine-GABA co-transmission at spinal inhibitory synapses by neuronal glutamate transporter. J Physiol 591(16):3821–3832

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Vandenberg RJ, Ryan RM (2013) Mechanisms of glutamate transport. Physiol Rev 93(4):1621–1657

    Article  CAS  PubMed  Google Scholar 

  13. Littleton JT, Ganetzky B (2000) Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26(1):35–43

    Article  CAS  PubMed  Google Scholar 

  14. Pawlu C, DiAntonio A, Heckmann M (2004) Postfusional control of quantal current shape. Neuron 42(4):607–618

    Article  CAS  PubMed  Google Scholar 

  15. Featherstone DE et al (2005) An essential Drosophila glutamate receptor subunit that functions in both central neuropil and neuromuscular junction. J Neurosci 25(12):3199–3208

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Guerrero G et al (2005) Heterogeneity in synaptic transmission along a Drosophila larval motor axon. Nat Neurosci 8(9):1188–1196

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Rasse TM et al (2005) Glutamate receptor dynamics organizing synapse formation in vivo. Nat Neurosci 8(7):898–905

    Article  CAS  PubMed  Google Scholar 

  18. Logsdon S et al (2006) Regulation of synaptic vesicles pools within motor nerve terminals during short-term facilitation and neuromodulation. J Appl Physiol (1985) 100(2):662–671

    Article  CAS  Google Scholar 

  19. Shinozaki H, Shibuya I (1974) A new potent excitant, quisqualic acid: effects on crayfish neuromuscular junction. Neuropharmacology 13(7):665–672

    Article  CAS  PubMed  Google Scholar 

  20. Shinozaki H, Ishida M (1981) An attempt at an analysis of the factors determining the time course of the glutamate response in the crayfish neuromuscular junction. J Pharmacobiodyn 4(7):483–489

    Article  CAS  PubMed  Google Scholar 

  21. Anderson CR, Cull-Candy SG, Miledi R (1976) Glutamate and quisqualate noise in voltage-clamped locust muscle fibres. Nature 261(5556):151–153

    Article  CAS  PubMed  Google Scholar 

  22. Cull-Candy SG, Parker I (1983) Experimental approaches used to examine single glutamate-receptor ion channels in locust muscle fibers. In: Sakmann B, Neher E (eds) Single-channel recording. Springer US, Boston, MA, pp 389–400

    Chapter  Google Scholar 

  23. Jan LY, Jan YN (1976) Properties of the larval neuromuscular junction in Drosophila melanogaster. J Physiol 262(1):189–214

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Patlak JB, Gration KA, Usherwood PN (1979) Single glutamate-activated channels in locust muscle. Nature 278(5705):643–645

    Article  CAS  PubMed  Google Scholar 

  25. Gration KA et al (1981) Agonist potency determination by patch clamp analysis of single glutamate receptors. Brain Res 230(1-2):400–405

    Article  CAS  PubMed  Google Scholar 

  26. Loewi O (1921) Über humorale Übertragbarkeit der Herznervenwirkung i.v. Mitteilung. Pflügers Arch Ges Physiol 189:239–242

    Article  Google Scholar 

  27. Dale HH, Feldberg W, Vogt M (1936) Release of acetylcholine at voluntary motor nerve endings. J Physiol 86(4):353–380

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Minz B (1932) Pharmakologische Untersuchungen am Blutegelpräparat,zugleich eine Methode zum biologischen Nachweis von Acetylcholin bei Anwesenheit anderer pharmakologisch wirksamer körpereigener Stoffe. Arch Exp Pharmal 168:292–304

    Article  CAS  Google Scholar 

  29. Dudel J, Kuffler SW (1961) The quantal nature of transmission and spontaneous miniature potentials at the crayfish neuromuscular junction. J Physiol 155:514–529

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Cull-Candy SG (1984) Inhibitory synaptic currents in voltage-clamped locust muscle fibres desensitized to their excitatory transmitter. Proc R Soc Lond B Biol Sci 221(1224):375–383

    Article  CAS  PubMed  Google Scholar 

  31. Jones HC (1962) The action of l-glutamic acid and of structurally related compounds on the hind gut of the crayfish. J Physiol 164:295–300

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Florey E (1954) An inhibitory and an excitatory factor of mammalian central nervous system, and their action of a single sensory neuron. Arch Int Physiol 62(1):33–53

    CAS  PubMed  Google Scholar 

  33. Robbins J (1959) The excitation and inhibition of crustacean muscle by amino acids. J Physiol 148:39–50

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Van Harreveld A (1959) Compounds in brain extracts causing spreading depression of cerebral cortical activity and contraction of crustacean muscle. J Neurochem 3(4):300–315

    Article  Google Scholar 

  35. Van Harreveld A, Mendelson M (1959) Glutamate-induced contractions in crustacean muscle. J Cell Comp Physiol 54:85–94

    Article  Google Scholar 

  36. Harris-Warrick R (2005) Synaptic chemistry in single neurons: GABA is identified as an inhibitory neurotransmitter. J Neurophysiol 93(6):3029–3031

    Article  PubMed  Google Scholar 

  37. Florey E (1961) A new test preparation for bio-assay of factor I and gamma-aminobutyric acid. J Physiol 156:1–7

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Bazemore A, Elliott KA, Florey E (1956) Factor I and gamma-aminobutyric acid. Nature 178(4541):1052–1053

    Article  CAS  PubMed  Google Scholar 

  39. Kuffler SW, Edwards C (1958) Mechanism of gamma aminobutyric acid (GABA) action and its relation to synaptic inhibition. J Neurophysiol 21(6):589–610

    CAS  PubMed  Google Scholar 

  40. Boistel J, Fatt P (1958) Membrane permeability change during inhibitory transmitter action in crustacean muscle. J Physiol 144(1):176–191

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Kravitz EA (1962) Enzymic formation of gamma-aminobutyric acid in the peripheral and central nervous system of lobsters. J Neurochem 9:363–370

    Article  CAS  PubMed  Google Scholar 

  42. Kravitz EA, Kuffler SW, Potter DD (1963) Gamma-aminobutyric acid and other blocking compounds in crustacea: III. Their relative concentrations in separated motor and inhibitory axons. J Neurophysiol 26:739–751

    CAS  PubMed  Google Scholar 

  43. Kravitz EA et al (1963) Gamma-aminobutyric acid and other blocking compounds in crustacea: II. Peripheral nervous system. J Neurophysiol 26:729–738

    CAS  PubMed  Google Scholar 

  44. Kravitz EA, Potter DD (1965) A further study of the distribution of gamma-aminobutyric acid between excitatory and inhibitory axons of the lobster. J Neurochem 12:323–328

    Article  CAS  PubMed  Google Scholar 

  45. Dudel J, Kuffler SW (1961) Presynaptic inhibition at the crayfish neuromuscular junction. J Physiol 155:543–562

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Kerkut GA et al (1965) The presence of glutamate in nerve-muscle perfusates of Helix, Carcinus and Periplaneta. Comp Biochem Physiol 15(4):485–502

    Article  CAS  PubMed  Google Scholar 

  47. Crawford AC, McBurney RN (1976) Proceedings: The time course of action of L-glutamate at the excitatory neuromuscular junction in Maia squinado. J Physiol 254(1):47P–48P

    CAS  PubMed  Google Scholar 

  48. King AE, Wheal HV (1984) The excitatory actions of kainic acid and some derivatives at the crab neuromuscular junction. Eur J Pharmacol 102(1):129–134

    Article  CAS  PubMed  Google Scholar 

  49. Gray SR et al (1991) Solubilization and purification of a putative quisqualate-sensitive glutamate receptor from crustacean muscle. Biochem J 273(Pt 1):165–171

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Fiszer de Plazas S, De Robertis E (1974) Isolation of hydrophobic proteins binding neurotransmitter aminoacids. Glutamate receptor of the shrimp muscle. J Neurochem 23(6):1115–1120

    Article  CAS  PubMed  Google Scholar 

  51. Chiba C, Tazaki K (1992) Glutamatergic motoneurons in the stomatogastric ganglion of the mantis shrimp Squilla oratoria. J Comp Physiol A 170(6):773–786

    Article  CAS  PubMed  Google Scholar 

  52. Sakurai A, Yamagishi H (2000) Graded neuromuscular transmission in the heart of the isopod crustacean Ligia exotica. J Exp Biol 203(Pt 9):1447–1457

    CAS  PubMed  Google Scholar 

  53. Lunt GG (1973) Hydrophobic proteins from locust (Shistocerca gregaria) muscle with glutamate receptor properties. Comp Gen Pharmacol 4(13):75–79

    Article  CAS  Google Scholar 

  54. Issberner JP et al (2002) Combined imaging and chemical sensing of L-glutamate release from the foregut plexus of the lepidopteran, Manduca sexta. J Neurosci Methods 120(1):1–10

    Article  CAS  PubMed  Google Scholar 

  55. Gardiner RB et al (2002) Cellular distribution of a high-affinity glutamate transporter in the nervous system of the cabbage looper Trichoplusia ni. J Exp Biol 205(Pt 17):2605–2613

    CAS  PubMed  Google Scholar 

  56. Grigor'ev VV, Ragulin VV (1988) Action of phosphorus-containing aminocarboxylic acids on neuromuscular transmission in the blowfly. Neirofiziologiia 20(2):256–258

    PubMed  Google Scholar 

  57. Gallus L et al (2010) NMDA R1 receptor distribution in the cyprid of Balanus amphitrite (=Amphibalanus amphitrite) (Cirripedia, Crustacea). Neurosci Lett 485(3):183–188

    Article  CAS  PubMed  Google Scholar 

  58. Huxley TH (1880) The crayfish: an introduction to the study of zoology. By T.H. Huxley. With eighty-two illustrations. D. Appleton and Company, New York

    Book  Google Scholar 

  59. Richet C (1879) Contribution a la physiologic des centres nerveux et des muscles de l'ecrevisse. Arch Physiol 6(262–299):522–576

    Google Scholar 

  60. Richet C (1881) Physiologie des muscles et des nerfs. Le ons prof sees la Facult de m decine en 1881, par Charles Richet. G. Bailli re, Paris

    Google Scholar 

  61. Cooper AS, Cooper RL (2009) Historical view and physiology demonstration at the NMJ of the crayfish opener muscle. J Vis Exp (33):1595

    Google Scholar 

  62. Ringer S (1882) Concerning the influence exerted by each of the constituents of the blood on the contraction of the ventricle. J Physiol 3(5–6):380–393

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Ringer S (1882) Regarding the action of hydrate of soda, hydrate of ammonia, and hydrate of potash on the ventricle of the frog’s heart. J Physiol 3(3–4):195–202.6

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Van Harreveld A (1936) A physiological solution for freshwater crustaceans. Proc Soc Exp Biol Med 34(4):428–432

    Article  Google Scholar 

  65. Katz B, Kuffler SW (1946) Excitation of the nerve-muscle system in Crustacea. Proc R Soc Lond B Biol Sci 133:374–389

    Article  CAS  PubMed  Google Scholar 

  66. Katz B (1949) Neuro-muscular transmission in invertebrates. Biol Rev Camb Philos Soc 24(1):1–20

    Article  CAS  PubMed  Google Scholar 

  67. Wiersma CA (1949) Synaptic facilitation in the crayfish. J Neurophysiol 12(4):267–275

    CAS  PubMed  Google Scholar 

  68. Fatt P, Katz B (1953) The effect of inhibitory nerve impulses on a crustacean muscle fibre. J Physiol 121(2):374–389

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. Sherman RG, Atwood HL (1971) Synaptic facilitation: long-term neuromuscular facilitation in crustaceans. Science 171(3977):1248–1250

    Article  CAS  PubMed  Google Scholar 

  70. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232(2):331–356

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  71. Grundfest H, Reuben JP, Rickles WH Jr (1959) The electrophysiology and pharmacology of lobster neuromuscular synapses. J Gen Physiol 42(6):1301–1323

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  72. Takeuchi A, Takeuchi N (1964) Iontophoretic application of gamma-aminobutyric acid crayfish muscle. Nature 203:1074–1075

    Article  CAS  PubMed  Google Scholar 

  73. Takeuchi A, Takeuchi N (1964) The effect on crayfish muscle of iontophoretically applied glutamate. J Physiol 170:296–317

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Takeuchi A, Takeuchi N (1965) Localized action of gamma-aminobutyric acid on the crayfish muscle. J Physiol 177(2):225–238

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  75. Takeuchi A, Takeuchi N (1966) A study of the inhibitory action of gamma-amino-butyric acid on neuromuscular transmission in the crayfish. J Physiol 183(2):418–432

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  76. Barker JL (1975) Divalent cations: effects on post-synaptic pharmacology of invertebrate synapses. Brain Res 92(2):307–323

    Article  CAS  PubMed  Google Scholar 

  77. Shank RP, Freeman AR (1975) Cooperative interaction of glutamate and aspartate with receptors in the neuromuscular excitatory membrane in walking limbs of the lobster. J Neurobiol 6(3):289–303

    Article  CAS  PubMed  Google Scholar 

  78. McBain AE, Wheal HV, Collins JF (1984) The pharmacology of the piperidine dicarboxylates on the crustacean neuromuscular junction. Neuropharmacology 23(1):23–30

    Article  CAS  PubMed  Google Scholar 

  79. Van Harreveld A (1980) L-proline as a glutamate antagonist at a crustacean neuromuscular junction. J Neurobiol 11(6):519–529

    Article  PubMed  Google Scholar 

  80. Olsson T et al (2016) Hemolymph metabolites and osmolality are tightly linked to cold tolerance of Drosophila species: a comparative study. J Exp Biol 219(Pt 16):2504–2513

    Article  PubMed  Google Scholar 

  81. McBain AE, Wheal HV (1984) Further structure activity studies on the excitatory amino acid receptors of the crustacean neuromuscular junction. Comp Biochem Physiol C 77(2):357–362

    Article  CAS  PubMed  Google Scholar 

  82. Shinozaki H, Ishida M (1986) A new potent channel blocker: effects on glutamate responses at the crayfish neuromuscular junction. Brain Res 372(2):260–268

    Article  CAS  PubMed  Google Scholar 

  83. Shinozaki H, Ishida M, Mizuta T (1982) Glutamate inhibitors in the crayfish neuromuscular junction. Comp Biochem Physiol C 72(2):249–255

    Article  CAS  PubMed  Google Scholar 

  84. Shinozaki H, Ishida M (1983) Excitatory junctional responses and glutamate responses at the crayfish neuromuscular junction in the presence of chlorisondamine. Brain Res 273(2):325–333

    Article  CAS  PubMed  Google Scholar 

  85. Klose MK, Atkinson JK, Mercier AJ (2002) Effects of a hydroxy-cinnamoyl conjugate of spermidine on arthropod neuromuscular junctions. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 187(12):945–952

    Article  CAS  PubMed  Google Scholar 

  86. Onodera K, Takeuchi A (1977) Inhibitory effect of streptomycin and related antibiotics on the glutamate receptor of the crayfish neuromuscular junction. Neuropharmacology 16(3):171–177

    Article  CAS  PubMed  Google Scholar 

  87. Shinozaki H, Ishida M (1981) Electrophysiological studies of kainate, quisqualate, and ibotenate action on the crayfish neuromuscular junction. Adv Biochem Psychopharmacol 27:327–336

    CAS  PubMed  Google Scholar 

  88. Shinozaki H, Ishida M (1988) Stizolobic acid, a competitive antagonist of the quisqualate-type receptor at the crayfish neuromuscular junction. Brain Res 451(1–2):353–356

    Article  CAS  PubMed  Google Scholar 

  89. Schramm M, Dudel J (1997) Metabotropic glutamate autoreceptors on nerve terminals of crayfish muscle depress or facilitate release. Neurosci Lett 234(1):31–34

    Article  CAS  PubMed  Google Scholar 

  90. Stettmeier H, Finger W (1983) Excitatory postsynaptic channels operated by quisqualate in crayfish muscle. Pflugers Arch 397(3):237–242

    Article  CAS  PubMed  Google Scholar 

  91. Shinozaki H, Ishida M (1981) Quisqualate action on the crayfish neuromuscular junction. J Pharmacobiodyn 4(1):42–48

    Article  CAS  PubMed  Google Scholar 

  92. Dudel J, Franke C, Hatt H (1992) Rapid activation and desensitization of transmitter-liganded receptor channels by pulses of agonists. Ion Channels 3:207–260

    Article  CAS  PubMed  Google Scholar 

  93. Atwood HL (1982) 3—Synapses and neurotransmitters. In: The biology of crustacea. Academic Press, San Diego, pp 105–150

    Chapter  Google Scholar 

  94. Atwood HL, Cooper RL, Wojtowicz JM (1994) Nonuniformity and plasticity of quantal release at crustacean motor nerve terminals. Adv Second Messenger Phosphoprotein Res 29:363–382

    Article  CAS  PubMed  Google Scholar 

  95. Atwood HL, Cooper RL (1995) Functional and structural parallels in crustacean and Drosophila neuromuscular systems. Am Zool 35(6):556–565

    Article  Google Scholar 

  96. Atwood HL, Cooper RL (1996) Assessing ultrastructure of crustacean and insect neuromuscular junctions. J Neurosci Methods 69(1):51–58

    Article  CAS  PubMed  Google Scholar 

  97. Atwood HL, Cooper RL (1996) Synaptic diversity and differentiation: crustacean neuromuscular junctions. Invert Neurosci 1(4):291–307

    Article  Google Scholar 

  98. Dudel J, Franke C, Luboldt W (1993) Reaction scheme for the glutamate-ergic, quisqualate type, completely desensitizing channels on crayfish muscle. Neurosci Lett 158(2):177–180

    Article  CAS  PubMed  Google Scholar 

  99. Tour O, Parnas H, Parnas I (1995) The double-ticker: an improved fast drug-application system reveals desensitization of the glutamate channel from a closed state. Eur J Neurosci 7(10):2093–2100

    Article  CAS  PubMed  Google Scholar 

  100. Tour O, Parnas H, Parnas I (1998) Depolarization increases the single-channel conductance and the open probability of crayfish glutamate channels. Biophys J 74(4):1767–1778

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  101. Tour O, Parnas H, Parnas I (2000) On the mechanism of desensitization in quisqualate-type glutamate channels. J Neurophysiol 84(1):1–10

    CAS  PubMed  Google Scholar 

  102. Shinozaki H, Ishida M (1981) The recovery from desensitization of the glutamate receptor in the crayfish neuromuscular junction. Neurosci Lett 21(3):293–296

    Article  CAS  PubMed  Google Scholar 

  103. Thieffry M (1984) The effect of calcium ions on the glutamate response and its desensitization in crayfish muscle fibres. J Physiol 355:119–135

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  104. Hatt H, Franke C, Dudel J (1988) Calcium dependent gating of the L-glutamate activated, excitatory synaptic channel on crayfish muscle. Pflugers Arch 411(1):17–26

    Article  CAS  PubMed  Google Scholar 

  105. Stettmeier H, Finger W, Dudel J (1983) Effects of concanavalin A on glutamate operated postsynaptic channels in crayfish muscle. Pflugers Arch 397(1):20–24

    Article  CAS  PubMed  Google Scholar 

  106. Park H, Popescu A, Poo MM (2014) Essential role of presynaptic NMDA receptors in activity-dependent BDNF secretion and corticostriatal LTP. Neuron 84(5):1009–1022

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  107. Stewart BA et al (1994) Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol A 175(2):179–191

    Article  CAS  PubMed  Google Scholar 

  108. Macleod GT et al (2002) Fast calcium signals in Drosophila motor neuron terminals. J Neurophysiol 88(5):2659–2663

    Article  CAS  PubMed  Google Scholar 

  109. de Castro C et al (2014) Analysis of various physiological salines for heart rate, CNS function, and synaptic transmission at neuromuscular junctions in Drosophila melanogaster larvae. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 200(1):83–92

    Article  CAS  PubMed  Google Scholar 

  110. Pulver SR et al (2009) Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. J Neurophysiol 101(6):3075–3088

    Article  PubMed Central  PubMed  Google Scholar 

  111. Macleod GT (2012) Calcium imaging at the Drosophila larval neuromuscular junction. Cold Spring Harb Protoc 2012(7):758–766

    PubMed  Google Scholar 

  112. Budnik V, Ruiz-Canada C (2006) The fly neuromuscular junction: structure and function, 2nd edn. Elsevier Science, San Diego, CA

    Google Scholar 

  113. Menon KP, Carrillo RA, Zinn K (2013) Development and plasticity of the Drosophila larval neuromuscular junction. Wiley Interdiscip Rev Dev Biol 2(5):647–670

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  114. Harris KP, Littleton JT (2015) Transmission, development, and plasticity of synapses. Genetics 201(2):345–375

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  115. Marrus SB et al (2004) Differential localization of glutamate receptor subunits at the Drosophila neuromuscular junction. J Neurosci 24(6):1406–1415

    Article  CAS  PubMed  Google Scholar 

  116. Qin G et al (2005) Four different subunits are essential for expressing the synaptic glutamate receptor at neuromuscular junctions of Drosophila. J Neurosci 25(12):3209–3218

    Article  CAS  PubMed  Google Scholar 

  117. DiAntonio A (2006) Glutamate receptors at the Drosophila neuromuscular junction. Int Rev Neurobiol 75:165–179

    Article  CAS  PubMed  Google Scholar 

  118. Bhatt D, Cooper RL (2005) The pharmacological and physiological profile of glutamate receptors at the Drosophila larval neuromuscular junction. Physiol Entomol 30(2):205–210

    Article  CAS  Google Scholar 

  119. Lee JY et al (2009) Furthering pharmacological and physiological assessment of the glutamatergic receptors at the Drosophila neuromuscular junction. Comp Biochem Physiol C Toxicol Pharmacol 150(4):546–557

    Article  CAS  PubMed  Google Scholar 

  120. Han TH et al (2015) Functional reconstitution of Drosophila melanogaster NMJ glutamate receptors. Proc Natl Acad Sci U S A 112(19):6182–6187

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  121. Gratz SJ et al (2013) Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics 194(4):1029–1035

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  122. Abe T, Kawai N, Miwa A (1983) Effects of a spider toxin on the glutaminergic synapse of lobster muscle. J Physiol 339:243–252

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  123. Kawai N et al (1984) Spider toxin (JSTX) on the glutamate synapse. J Physiol (Paris) 79(4):228–231

    CAS  Google Scholar 

  124. Kawasaki F, Kita H (1996) Physiological and immunocytochemical determination of the neurotransmitter at cricket neuromuscular junctions. Zool Sci 13(4):503–507

    Article  CAS  Google Scholar 

  125. Frank CA et al (2006) Mechanisms underlying the rapid induction and sustained expression of synaptic homeostasis. Neuron 52(4):663–677

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  126. Frank CA (2014) Homeostatic plasticity at the Drosophila neuromuscular junction. Neuropharmacology 78:63–74

    Article  CAS  PubMed  Google Scholar 

  127. DiAntonio A et al (1999) Glutamate receptor expression regulates quantal size and quantal content at the Drosophila neuromuscular junction. J Neurosci 19(8):3023–3032

    CAS  PubMed  Google Scholar 

  128. Frank CA, Pielage J, Davis GW (2009) A presynaptic homeostatic signaling system composed of the Eph receptor, ephexin, Cdc42, and CaV2.1 calcium channels. Neuron 61(4):556–569

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  129. Jakawich SK et al (2010) Local presynaptic activity gates homeostatic changes in presynaptic function driven by dendritic BDNF synthesis. Neuron 68(6):1143–1158

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  130. Henry FE et al (2012) Retrograde changes in presynaptic function driven by dendritic mTORC1. J Neurosci 32(48):17128–17142

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  131. Penney J et al (2012) TOR is required for the retrograde regulation of synaptic homeostasis at the Drosophila neuromuscular junction. Neuron 74(1):166–178

    Article  CAS  PubMed  Google Scholar 

  132. Parmentier ML et al (1996) Cloning and functional expression of a Drosophila metabotropic glutamate receptor expressed in the embryonic CNS. J Neurosci 16(21):6687–6694

    CAS  PubMed  Google Scholar 

  133. Mitri C et al (2004) Divergent evolution in metabotropic glutamate receptors. A new receptor activated by an endogenous ligand different from glutamate in insects. J Biol Chem 279(10):9313–9320

    Article  CAS  PubMed  Google Scholar 

  134. Bogdanik L et al (2004) The Drosophila metabotropic glutamate receptor DmGluRA regulates activity-dependent synaptic facilitation and fine synaptic morphology. J Neurosci 24(41):9105–9116

    Article  CAS  PubMed  Google Scholar 

  135. Kurdyak P et al (1994) Differential physiology and morphology of motor axons to ventral longitudinal muscles in larval Drosophila. J Comp Neurol 350(3):463–472

    Article  CAS  PubMed  Google Scholar 

  136. Ormerod KG et al (2013) Action of octopamine and tyramine on muscles of Drosophila melanogaster larvae. J Neurophysiol 110(8):1984–1996

    Article  CAS  PubMed  Google Scholar 

  137. Jan LY, Jan YN (1976) l-Glutamate as an excitatory transmitter at the Drosophila larval neuromuscular junction. J Physiol 262(1):215–236

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  138. Delgado R et al (1989) l-Glutamate activates excitatory and inhibitory channels in Drosophila larval muscle. FEBS Lett 243(2):337–342

    Article  CAS  PubMed  Google Scholar 

  139. Chen K, Augustin H, Featherstone DE (2009) Effect of ambient extracellular glutamate on Drosophila glutamate receptor trafficking and function. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195(1):21–29

    Article  CAS  PubMed  Google Scholar 

  140. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355–405

    Article  CAS  PubMed  Google Scholar 

  141. Wu CF et al (1983) Potassium currents in Drosophila: different components affected by mutations of two genes. Science 220(4601):1076–1078

    Article  CAS  PubMed  Google Scholar 

  142. Peron S et al (2009) From action potential to contraction: neural control and excitation-contraction coupling in larval muscles of Drosophila. Comp Biochem Physiol A Mol Integr Physiol 154(2):173–183

    Article  CAS  PubMed  Google Scholar 

  143. Zhong Y, Wu CF (1991) Altered synaptic plasticity in Drosophila memory mutants with a defective cyclic AMP cascade. Science 251(4990):198–201

    Article  CAS  PubMed  Google Scholar 

  144. Wu Y, Kawasaki F, Ordway RW (2005) Properties of short-term synaptic depression at larval neuromuscular synapses in wild-type and temperature-sensitive paralytic mutants of Drosophila. J Neurophysiol 93(5):2396–2405

    Article  PubMed  Google Scholar 

  145. Sigrist SJ et al (2003) Experience-dependent strengthening of Drosophila neuromuscular junctions. J Neurosci 23(16):6546–6556

    CAS  PubMed  Google Scholar 

  146. Ataman B et al (2008) Rapid activity-dependent modifications in synaptic structure and function require bidirectional Wnt signaling. Neuron 57(5):705–718

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  147. Nesler KR et al (2013) The miRNA pathway controls rapid changes in activity-dependent synaptic structure at the Drosophila melanogaster neuromuscular junction. PLoS One 8(7):e68385

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  148. Nesler KR et al (2016) Presynaptic CamKII regulates activity-dependent axon terminal growth. Mol Cell Neurosci 76:33–41

    Article  CAS  PubMed  Google Scholar 

  149. Piccioli ZD, Littleton JT (2014) Retrograde BMP signaling modulates rapid activity-dependent synaptic growth via presynaptic LIM kinase regulation of cofilin. J Neurosci 34(12):4371–4381

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  150. Budnik V, Gorczyca M, Prokop A (2006) Selected methods for the anatomical study of Drosophila embryonic and larval neuromuscular junctions. Int Rev Neurobiol 75:323–365

    Article  CAS  PubMed  Google Scholar 

  151. Fuger P et al (2007) Live imaging of synapse development and measuring protein dynamics using two-color fluorescence recovery after photo-bleaching at Drosophila synapses. Nat Protoc 2(12):3285–3298

    Article  CAS  PubMed  Google Scholar 

  152. Sturgeon M et al (2016) The Notch ligand E3 ligase, Mind Bomb1, regulates glutamate receptor localization in Drosophila. Mol Cell Neurosci 70:11–21

    Article  CAS  PubMed  Google Scholar 

  153. Lee G, Schwarz TL (2016) Filamin, a synaptic organizer in Drosophila, determines glutamate receptor composition and membrane growth. Elife 5. doi:10.7554/eLife.19991

  154. Wang M et al (2016) Dbo/Henji modulates synaptic dPAK to gate glutamate receptor abundance and postsynaptic response. PLoS Genet 12(10):e1006362

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  155. Hussein NA et al (2016) The extracellular-regulated kinase effector Lk6 is required for glutamate receptor localization at the Drosophila neuromuscular junction. J Exp Neurosci 10:77–91

    Article  PubMed Central  PubMed  Google Scholar 

  156. Deivasigamani S et al (2015) A presynaptic regulatory system acts transsynaptically via Mon1 to regulate glutamate receptor levels in Drosophila. Genetics 201(2):651–664

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  157. Ramos CI et al (2015) Neto-mediated intracellular interactions shape postsynaptic composition at the Drosophila neuromuscular junction. PLoS Genet 11(4):e1005191

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  158. Ghosh R et al (2014) Kismet positively regulates glutamate receptor localization and synaptic transmission at the Drosophila neuromuscular junction. PLoS One 9(11):e113494

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  159. Kim MJ, O'Connor MB (2014) Anterograde Activin signaling regulates postsynaptic membrane potential and GluRIIA/B abundance at the Drosophila neuromuscular junction. PLoS One 9(9):e107443

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  160. Xing G et al (2014) Drosophila neuroligin3 regulates neuromuscular junction development and synaptic differentiation. J Biol Chem 289(46):31867–31877

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  161. Gardiol A, St Johnston D (2014) Staufen targets coracle mRNA to Drosophila neuromuscular junctions and regulates GluRIIA synaptic accumulation and bouton number. Dev Biol 392(2):153–167

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  162. Kerr KS et al (2014) Glial wingless/Wnt regulates glutamate receptor clustering and synaptic physiology at the Drosophila neuromuscular junction. J Neurosci 34(8):2910–2920

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  163. Parkinson W et al (2013) N-glycosylation requirements in neuromuscular synaptogenesis. Development 140(24):4970–4981

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  164. Lee J, Ueda A, Wu CF (2014) Distinct roles of Drosophila cacophony and Dmca1D Ca(2+) channels in synaptic homeostasis: genetic interactions with slowpoke Ca(2+)-activated BK channels in presynaptic excitability and postsynaptic response. Dev Neurobiol 74(1):1–15

    Article  CAS  PubMed  Google Scholar 

  165. Lee MJ et al (2013) Tbc1d15-17 regulates synaptic development at the Drosophila neuromuscular junction. Mol Cells 36(2):163–168

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  166. Lee HG et al (2013) Akt regulates glutamate receptor trafficking and postsynaptic membrane elaboration at the Drosophila neuromuscular junction. Dev Neurobiol 73(10):723–743

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  167. Staples J, Broadie K (2013) The cell polarity scaffold Lethal Giant Larvae regulates synapse morphology and function. J Cell Sci 126(Pt 9):1992–2003

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  168. Fukui A et al (2012) Lola regulates glutamate receptor expression at the Drosophila neuromuscular junction. Biol Open 1(4):362–375

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  169. Chen K, Featherstone DE (2011) Pre and postsynaptic roles for Drosophila CASK. Mol Cell Neurosci 48(2):171–182

    Article  CAS  PubMed  Google Scholar 

  170. Sun M et al (2007) Presynaptic contributions of chordin to hippocampal plasticity and spatial learning. J Neurosci 27(29):7740–7750

    Article  CAS  PubMed  Google Scholar 

  171. Chen K et al (2010) Neurexin in embryonic Drosophila neuromuscular junctions. PLoS One 5(6):e11115

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  172. Banovic D et al (2010) Drosophila neuroligin 1 promotes growth and postsynaptic differentiation at glutamatergic neuromuscular junctions. Neuron 66(5):724–738

    Article  CAS  PubMed  Google Scholar 

  173. Bachmann A et al (2010) A perisynaptic menage a trois between Dlg, DLin-7, and Metro controls proper organization of Drosophila synaptic junctions. J Neurosci 30(17):5811–5824

    Article  CAS  PubMed  Google Scholar 

  174. Wang D et al (2010) Drosophila twinfilin is required for cell migration and synaptic endocytosis. J Cell Sci 123(Pt 9):1546–1556

    Article  CAS  PubMed  Google Scholar 

  175. Owald D et al (2010) A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila. J Cell Biol 188(4):565–579

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  176. Morimoto T et al (2010) Subunit-specific and homeostatic regulation of glutamate receptor localization by CaMKII in Drosophila neuromuscular junctions. Neuroscience 165(4):1284–1292

    Article  CAS  PubMed  Google Scholar 

  177. Menon KP et al (2009) The translational repressors Nanos and Pumilio have divergent effects on presynaptic terminal growth and postsynaptic glutamate receptor subunit composition. J Neurosci 29(17):5558–5572

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  178. Bogdanik L et al (2008) Muscle dystroglycan organizes the postsynapse and regulates presynaptic neurotransmitter release at the Drosophila neuromuscular junction. PLoS One 3(4):e2084

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  179. Wairkar YP et al (2008) Synaptic defects in a Drosophila model of congenital muscular dystrophy. J Neurosci 28(14):3781–3789

    Article  CAS  PubMed  Google Scholar 

  180. Heckscher ES et al (2007) NF-kappaB, IkappaB, and IRAK control glutamate receptor density at the Drosophila NMJ. Neuron 55(6):859–873

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  181. Rohrbough J et al (2007) Presynaptic establishment of the synaptic cleft extracellular matrix is required for post-synaptic differentiation. Genes Dev 21(20):2607–2628

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  182. Haas KF et al (2007) The ubiquitin-proteasome system postsynaptically regulates glutamatergic synaptic function. Mol Cell Neurosci 35(1):64–75

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  183. Chen K et al (2005) The 4.1 protein coracle mediates subunit-selective anchoring of Drosophila glutamate receptors to the postsynaptic actin cytoskeleton. J Neurosci 25(28):6667–6675

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  184. Chen K, Featherstone DE (2005) Discs-large (DLG) is clustered by presynaptic innervation and regulates postsynaptic glutamate receptor subunit composition in Drosophila. BMC Biol 3:1

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  185. Menon KP et al (2004) The translational repressor Pumilio regulates presynaptic morphology and controls postsynaptic accumulation of translation factor eIF-4E. Neuron 44(4):663–676

    Article  CAS  PubMed  Google Scholar 

  186. Albin SD, Davis GW (2004) Coordinating structural and functional synapse development: postsynaptic p21-activated kinase independently specifies glutamate receptor abundance and postsynaptic morphology. J Neurosci 24(31):6871–6879

    Article  CAS  PubMed  Google Scholar 

  187. Chan YB et al (2003) Neuromuscular defects in a Drosophila survival motor neuron gene mutant. Hum Mol Genet 12(12):1367–1376

    Article  CAS  PubMed  Google Scholar 

  188. Renden RB, Broadie K (2003) Mutation and activation of Galpha s similarly alters pre- and postsynaptic mechanisms modulating neurotransmission. J Neurophysiol 89(5):2620–2638

    Article  CAS  PubMed  Google Scholar 

  189. Parnas D et al (2001) Regulation of postsynaptic structure and protein localization by the Rho-type guanine nucleotide exchange factor dPix. Neuron 32(3):415–424

    Article  CAS  PubMed  Google Scholar 

  190. Blunk AD et al (2014) Postsynaptic actin regulates active zone spacing and glutamate receptor apposition at the Drosophila neuromuscular junction. Mol Cell Neurosci 61:241–254

    Article  CAS  PubMed  Google Scholar 

  191. Morel V et al (2014) Drosophila Nesprin-1 controls glutamate receptor density at neuromuscular junctions. Cell Mol Life Sci 71(17):3363–3379

    Article  CAS  PubMed  Google Scholar 

  192. Saitoe M et al (2001) Absence of junctional glutamate receptor clusters in Drosophila mutants lacking spontaneous transmitter release. Science 293(5529):514–517

    Article  CAS  PubMed  Google Scholar 

  193. Verstreken P, Bellen HJ (2002) Meaningless minis? Mechanisms of neurotransmitter-receptor clustering. Trends Neurosci 25(8):383–385

    Article  CAS  PubMed  Google Scholar 

  194. Melom JE et al (2013) Spontaneous and evoked release are independently regulated at individual active zones. J Neurosci 33(44):17253–17263

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  195. Deitcher DL et al (1998) Distinct requirements for evoked and spontaneous release of neurotransmitter are revealed by mutations in the Drosophila gene neuronal-synaptobrevin. J Neurosci 18(6):2028–2039

    CAS  PubMed  Google Scholar 

  196. Ganesan S, Karr JE, Featherstone DE (2011) Drosophila glutamate receptor mRNA expression and mRNP particles. RNA Biol 8(5):771–781

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  197. Sigrist SJ et al (2000) Postsynaptic translation affects the efficacy and morphology of neuromuscular junctions. Nature 405(6790):1062–1065

    Article  CAS  PubMed  Google Scholar 

  198. Titlow JS et al. Super-resolution single molecule FISH at the Drosophila neuromsucular junction. Methods Mol Biol, in press

    Google Scholar 

  199. Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509–547

    Article  CAS  PubMed  Google Scholar 

  200. Wu WH, Cooper RL (2012) The regulation and packaging of synaptic vesicles as related to recruitment within glutamatergic synapses. Neuroscience 225:185–198

    Article  CAS  PubMed  Google Scholar 

  201. Rizzoli SO, Betz WJ (2005) Synaptic vesicle pools. Nat Rev Neurosci 6(1):57–69

    Article  CAS  PubMed  Google Scholar 

  202. Fredj NB, Burrone J (2009) A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat Neurosci 12(6):751–758

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  203. Denker A et al (2011) A small pool of vesicles maintains synaptic activity in vivo. Proc Natl Acad Sci U S A 108(41):17177–17182

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  204. Denker A et al (2011) The reserve pool of synaptic vesicles acts as a buffer for proteins involved in synaptic vesicle recycling. Proc Natl Acad Sci U S A 108(41):17183–17188

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  205. Akbergenova Y, Bykhovskaia M (2009) Stimulation-induced formation of the reserve pool of vesicles in Drosophila motor boutons. J Neurophysiol 101(5):2423–2433

    Article  PubMed Central  PubMed  Google Scholar 

  206. Johnstone AFM, Viele K, Cooper RL (2011) Structure/function assessment of synapses at motor nerve terminals. Synapse 65(4):287–299

    Article  CAS  PubMed  Google Scholar 

  207. Wu WH, Cooper RL (2013) Physiological separation of vesicle pools in low- and high-output nerve terminals. Neurosci Res 75(4):275–282

    Article  CAS  PubMed  Google Scholar 

  208. Walrond JP, Govind CK, Huestis SE (1993) Two structural adaptations for regulating transmitter release at lobster neuromuscular synapses. J Neurosci 13(11):4831–4845

    CAS  PubMed  Google Scholar 

  209. Mykles DL et al (2002) Myofibrillar protein isoform expression is correlated with synaptic efficacy in slow fibres of the claw and leg opener muscles of crayfish and lobster. J Exp Biol 205(Pt 4):513–522

    CAS  PubMed  Google Scholar 

  210. Dudel J, Schramm M (2003) A receptor for presynaptic glutamatergic autoinhibition is a glutamate transporter. Eur J Neurosci 18(4):902–910

    Article  PubMed  Google Scholar 

  211. Pinard A et al (2003) Glutamatergic modulation of synaptic plasticity at a PNS vertebrate cholinergic synapse. Eur J Neurosci 18(12):3241–3250

    Article  PubMed  Google Scholar 

  212. Kim WM et al (2016) The role of inversely operating glutamate transporter in the paradoxical analgesia produced by glutamate transporter inhibitors. Eur J Pharmacol 793:112–118

    Article  CAS  PubMed  Google Scholar 

  213. Koles K et al (2012) Mechanism of evenness interrupted (Evi)-exosome release at synaptic boutons. J Biol Chem 287(20):16820–16834

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  214. Spring AM, Brusich DJ, Frank CA (2016) C-terminal Src kinase gates homeostatic synaptic plasticity and regulates fasciclin II expression at the Drosophila neuromuscular junction. PLoS Genet 12(2):e1005886

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  215. Deshpande M, Rodal AA (2016) The crossroads of synaptic growth signaling, membrane traffic and neurological disease: insights from Drosophila. Traffic 17(2):87–101

    Article  CAS  PubMed  Google Scholar 

  216. Petralia RS, Mattson MP, Yao PJ (2014) Communication breakdown: the impact of ageing on synapse structure. Ageing Res Rev 14:31–42

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  217. Cooper AS, Johnstone AFM, Cooper RL (2013) Motor nerve terminal morphology with unloading and reloading of muscle in Procambarus clarkii. Journal of Crustacean Biology 33(6):818–827

    Article  Google Scholar 

  218. Morrison JH, Baxter MG (2012) The ageing cortical synapse: hallmarks and implications for cognitive decline. Nat Rev Neurosci 13(4):240–250

    CAS  PubMed Central  PubMed  Google Scholar 

  219. Picconi B, Piccoli G, Calabresi P (2012) Synaptic dysfunction in Parkinson’s disease. Adv Exp Med Biol 970:553–572

    Article  CAS  PubMed  Google Scholar 

  220. Yeoman M, Scutt G, Faragher R (2012) Insights into CNS ageing from animal models of senescence. Nat Rev Neurosci 13(6):435–445

    Article  CAS  PubMed  Google Scholar 

  221. Badre NH, Martin ME, Cooper RL (2005) The physiological and behavioral effects of carbon dioxide on Drosophila melanogaster larvae. Comp Biochem Physiol A Mol Integr Physiol 140(3):363–376

    Article  CAS  PubMed  Google Scholar 

  222. Bierbower SM, Cooper RL (2010) The effects of acute carbon dioxide on behavior and physiology in Procambarus clarkii. J Exp Zool A Ecol Genet Physiol 313(8):484–497

    Article  CAS  PubMed  Google Scholar 

  223. Bierbower SM, Cooper RL (2013) The mechanistic action of carbon dioxide on a neural circuit and NMJ communication. J Exp Zool A Ecol Genet Physiol 319(6):340–354

    Article  CAS  PubMed  Google Scholar 

  224. Sugahara M, Sakamoto F (2009) Heat and carbon dioxide generated by honeybees jointly act to kill hornets. Naturwissenschaften 96(9):1133–1136

    Article  CAS  PubMed  Google Scholar 

  225. Eisele JH, Eger EI 2nd, Muallem M (1967) Narcotic properties of carbon dioxide in the dog. Anesthesiology 28(5):856–865

    Article  CAS  PubMed  Google Scholar 

  226. Traynelis SF, Cull-Candy SG (1990) Proton inhibition of N-methyl-D-aspartate receptors in cerebellar neurons. Nature 345(6273):347–350

    Article  CAS  PubMed  Google Scholar 

  227. Tong CK, Chesler M (2000) Modulation of spreading depression by changes in extracellular pH. J Neurophysiol 84(5):2449–2457

    CAS  PubMed  Google Scholar 

  228. Williams K et al (2003) Pharmacology of delta2 glutamate receptors: effects of pentamidine and protons. J Pharmacol Exp Ther 305(2):740–748

    Article  CAS  PubMed  Google Scholar 

  229. Low CM et al (2003) Molecular determinants of proton-sensitive N-methyl-D-aspartate receptor gating. Mol Pharmacol 63(6):1212–1222

    Article  CAS  PubMed  Google Scholar 

  230. He P et al (1999) Role of alpha-SNAP in promoting efficient neurotransmission at the crayfish neuromuscular junction. J Neurophysiol 82(6):3406–3416

    CAS  PubMed  Google Scholar 

  231. Kandel ER (2012) The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Mol Brain 5:14

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  232. Martin A et al (2016) CRISPR/Cas9 mutagenesis reveals versatile roles of Hox genes in crustacean limb specification and evolution. Curr Biol 26(1):14–26

    Article  CAS  PubMed  Google Scholar 

  233. LaFramboise WA et al (2000) Muscle type-specific myosin isoforms in crustacean muscles. J Exp Zool 286(1):36–48

    Article  CAS  PubMed  Google Scholar 

  234. Griffis B, Moffett SB, Cooper RL (2001) Muscle phenotype remains unaltered after limb autotomy and unloading. J Exp Zool 289(1):10–22

    Article  CAS  PubMed  Google Scholar 

  235. Sohn J, Mykles DL, Cooper RL (2000) Characterization of muscles associated with the articular membrane in the dorsal surface of the crayfish abdomen. J Exp Zool 287(5):353–377

    Article  CAS  PubMed  Google Scholar 

  236. Strawn JR, Neckameyer WS, Cooper RL (2000) The effects of 5-HT on sensory, central and motor neurons driving the abdominal superficial flexor muscles in the crayfish. Comp Biochem Physiol B Biochem Mol Biol 127(4):533–550

    Article  CAS  PubMed  Google Scholar 

  237. Baierlein B et al (2011) Membrane potentials, synaptic responses, neuronal circuitry, neuromodulation and muscle histology using the crayfish: student laboratory exercises. J Vis Exp (47)

    Google Scholar 

  238. Wu WH, Cooper RL (2010) Physiological recordings of high- and low-output NMJs on the crayfish leg extensor muscle. J Vis Exp (45)

    Google Scholar 

  239. Cooper RL et al (1996) Synaptic structural complexity as a factor enhancing probability of calcium-mediated transmitter release. J Neurophysiol 75(6):2451–2466

    CAS  PubMed  Google Scholar 

  240. Winslow JL, Cooper RL, Atwood HL (2002) Intracellular ionic concentration by calibration from fluorescence indicator emission spectra, its relationship to the Kd, Fmin, Fmax formula, and use with Na-Green for presynaptic sodium. J Neurosci Methods 118(2):163–175

    Article  PubMed  Google Scholar 

  241. Majeed ZR et al (2015) New insights into the acute actions from a high dosage of fluoxetine on neuronal and cardiac function: Drosophila, crayfish and rodent models. Comp Biochem Physiol C Toxicol Pharmacol 176–177:52–61

    Article  CAS  PubMed  Google Scholar 

  242. Cooper RL et al (1995) Quantal measurement and analysis methods compared for crayfish and Drosophila neuromuscular junctions, and rat hippocampus. J Neurosci Methods 61(1-2):67–78

    Article  CAS  PubMed  Google Scholar 

  243. Cooper RL, Hampson DR, Atwood HL (1995) Synaptotagmin-like expression in the motor nerve terminals of crayfish. Brain Res 703(1–2):214–216

    Article  CAS  PubMed  Google Scholar 

  244. Magrassi L, Purves D, Lichtman JW (1987) Fluorescent probes that stain living nerve terminals. J Neurosci 7(4):1207–1214

    CAS  PubMed  Google Scholar 

  245. Cooper RL, Marin L, Atwood HL (1995) Synaptic differentiation of a single motor neuron: conjoint definition of transmitter release, presynaptic calcium signals, and ultrastructure. J Neurosci 15(6):4209–4222

    CAS  PubMed  Google Scholar 

  246. Muller KJ, Nicholls JG, Stent GS (1981) Neurobiology of the leech. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  247. Cooper AS et al (2009) Monitoring heart function in larval Drosophila melanogaster for physiological studies. J Vis Exp (33). doi:10.3791/1596

  248. Verstreken P, Ohyama T, Bellen HJ (2008) FM 1-43 labeling of synaptic vesicle pools at the Drosophila neuromuscular junction. Methods Mol Biol 440:349–369

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  249. Imlach W, McCabe BD (2009) Electrophysiological methods for recording synaptic potentials from the NMJ of Drosophila larvae. J Vis Exp (24). doi:10.3791/1109

  250. Zhang B, Stewart B (2010) Electrophysiological recording from Drosophila larval body-wall muscles. Cold Spring Harb Protoc 2010(9):pdb prot5487

    Google Scholar 

  251. Brent J, Werner K, McCabe BD (2009) Drosophila larval NMJ immunohistochemistry. J Vis Exp (25)

    Google Scholar 

  252. Ramachandran P, Budnik V (2010) Immunocytochemical staining of Drosophila larval body-wall muscles. Cold Spring Harb Protoc 2010(8):pdb prot5470

    Google Scholar 

  253. Andlauer TF, Sigrist SJ (2012) Quantitative analysis of Drosophila larval neuromuscular junction morphology. Cold Spring Harb Protoc 2012(4):490–493

    PubMed  Google Scholar 

  254. Nijhof B et al (2016) A new Fiji-based algorithm that systematically quantifies nine synaptic parameters provides insights into Drosophila NMJ morphometry. PLoS Comput Biol 12(3):e1004823

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  255. Sanhueza M, Kubasik-Thayil A, Pennetta G (2016) Why quantification matters: characterization of phenotypes at the Drosophila larval neuromuscular junction. J Vis Exp (111). doi:10.3791/53821

  256. Juge N et al (2010) Metabolic control of vesicular glutamate transport and release. Neuron 68(1):99–112

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. J. Troy Littleton (Massachusetts Institute of Technology, Cambridge, MA, USA) for editorial comments and suggestions on improving this chapter. J.S.T. is supported by a Wellcome Trust Senior Basic Biomedical Research Fellowship (096144) awarded to Professor Ilan Davis.

Author information

Authors and Affiliations

  1. Department of Biochemistry, University of Oxford, Oxford, UK

    Joshua S. Titlow

  2. Department of Biology and Center for Muscle Biology, University of Kentucky, Lexington, KY, USA

    Robin L. Cooper

Authors
  1. Joshua S. Titlow
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robin L. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Joshua S. Titlow or Robin L. Cooper .

Editor information

Editors and Affiliations

  1. Lyon Neuroscience Research Center, University Lyon 1, Lyon, France

    Sandrine Parrot

  2. Lyon Neuroscience Research Center, University Lyon 1, Lyon, France

    Luc Denoroy

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Science+Business Media LLC

About this protocol

Cite this protocol

Titlow, J.S., Cooper, R.L. (2018). Glutamatergic Synthesis, Recycling, and Receptor Pharmacology at Drosophila and Crustacean Neuromuscular Junctions. In: Parrot, S., Denoroy, L. (eds) Biochemical Approaches for Glutamatergic Neurotransmission. Neuromethods, vol 130. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7228-9_9

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-7228-9_9

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-7227-2

  • Online ISBN: 978-1-4939-7228-9

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation