Neurotransmitter-induced changes in the intracellular calcium concentration suggest a differential central modulation of CCAP neuron subsets in Drosophila

Developmental Neurobiology

Volumn 67, Issue 6, 2007, Pages 792-808

  Vömel, Matthias ^a   Wegener, Christian ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Calcium imaging; Crustacean cardioactive peptide; Insect ecdysis; Neuronal network signaling; Peptide release

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; ACETYLCHOLINE; CALCIUM; CHOLINERGIC RECEPTOR; CHOLINERGIC RECEPTOR STIMULATING AGENT; CRUSTACEAN CARDIOACTIVE PEPTIDE; GLUTAMATE RECEPTOR; GLUTAMIC ACID; NEUROTRANSMITTER; NICOTINE; PEPTIDE HORMONE; UNCLASSIFIED DRUG; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; DROSOPHILA PROTEIN; NEUROPEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA MELANOGASTER; GENOME; IN VITRO STUDY; INVERTEBRATE; MOLTING; NEUROMERE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; ANIMAL; CELL CULTURE; CENTRAL NERVOUS SYSTEM; CHEMISTRY; CONFOCAL MICROSCOPY; IMMUNOHISTOCHEMISTRY; INTRACELLULAR FLUID; METABOLISM; NERVE CELL; THREE DIMENSIONAL IMAGING; ULTRASTRUCTURE;

ANIMALS; CALCIUM; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; IMAGING, THREE-DIMENSIONAL; IMMUNOHISTOCHEMISTRY; INTRACELLULAR FLUID; MICROSCOPY, CONFOCAL; NEURONS; NEUROPEPTIDES; NEUROTRANSMITTER AGENTS;

EID: 34250829606     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.20392     Document Type: Article

References (50)

1. Albert JL, Lingle CJ. 1993. Activation of nicotinic acetylcholine receptors on cultured Drosophila and other insect neurons. J Physiol 463:605-630.
2. Baker JD, McNabb SL, Truman JW. 1999. The hormonal coordination of behavior and physiology at adult ecdysis in Drosophila melanogaster. J Exp Biol 202:3037-3048.
3. Bogdanik L, Mohrmann R, Ramaekers A, Bockaert J, Grau Y, Broadie K, Parmentier ML. 2004. The Drosophila metabotropic glutamate receptor DmGluRA regulates activity-dependent synaptic facilitation and fine synaptic morphology. J Neurosci 24:9105-9116.
4. Buckingham SD, Biggin PC, Sattelle BM, Brown LA, Sattelle DB. 2005. Insect GABA receptors: Splicing, editing, and targeting by antiparasitics and insecticides. Mol Pharmacol 68:942-951.
5. Chiba A. 1999. Early development of the Drosophila neuromuscular junction: A model for studying neuronal networks in development. In: Budnik V, Sian Gramates L, editors. Neuromuscular Junctions in Drosophila. New York: Academic Press, pp 1-24.
6. Clark AC, del Campo ML, Ewer J. 2004. Neuroendocrine control of larval ecdysis behavior in Drosophila: Complex regulation by partially redundant neuropeptides. J Neurosci 24:4283-4292.
7. Cordova D, Delpech VR, Sattelle DB, Rauh JJ. 2003. Spatiotemporal calcium signaling in a Drosophila melanogaster cell line stably expressing a Drosophila muscarinic acetylcholine receptor. Invert Neurosci 5:19-28.
8. Daniels RW, Collins CA, Gelfand MV, Dant J, Brooks ES, Krantz DE, DiAntonio A. 2004. Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J Neurosci 24:10466-10474.
9. Diegelmann S, Fiala A, Leibold C, Spall T, Buchner E. 2002. Transgenic flies expressing the fluorescence calcium sensor Cameleon 2.1 under UAS control. Genesis 34:95-98.
10. Dircksen H. 1998. Conserved crustacean cardioactive peptide (CCAP) neuronal networks and functions in arthropod evolution. In: Webster SG, Coast GM, editors. Recent Advances in Arthropod Endocrinology. Cambridge: Cambridge University Press, pp 302-333.
11. Donini A, Ngo C, Lange AB. 2002. Evidence for crustacean cardioactive peptide-like innervation of the gut in Locusta migratoria. Peptides 23:1915-1923.
12. Dulcis D, Levine RB, Ewer J. 2005. Role of the neuropeptide CCAP in Drosophila cardiac function. J Neurobiol 64:259-274.
13. Engelmann M, Bull PM, Brown CH, Landgraf R, Horn TF, Singewald N, Ludwig M, et al. 2004. GABA selectively controls the secretory activity of oxytocin neurons in the rat supraoptic nucleus. Eur J Neurosci 19:601-608.
14. Ewer J. 2005. Behavioral actions of neuropeptides in invertebrates: Insights from Drosophila. Horm Behav 48:418-429.
15. Ewer J, Truman JW. 1996. Increases in cyclic 3′,5′- guanosinemonophosphate (cGMP) occur at ecdysis in an evolutionarily conserved crustacean cardioactive peptide-immunoreactive insect neuronal network. J Comp Neurol 370:330-341.
16. Ewer J, Truman JW. 1997. Invariant association of ecdysis with increases in cyclic 3′,5′-guanosinemonophosphate immunoreactivity in a small network of peptidergic neurons in the hornworm, Manduca sexta. J Comp Physiol [A] 181:319-330.
17. Featherstone DE, Rushton E, Rohrbough J, Liebl F, Karr J, Sheng Q, Rodesch CK, et al. 2005. An essential Drosophila glutamate receptor subunit that functions in both central neuropil and neuromuscular junction. J Neurosci 25:3199-3208.
18. Fuse M, Truman JW. 2002. Modulation of ecdysis in the moth Manduca sexta: The roles of the subesophageal and thoracic ganglia. J Exp Biol 205:1047-1058.
19. Garside S, Mazurek MF. 1997. Role of glutamate receptor subtypes in the differential release of somatostatin, neuropeptide Y, and substance P in primary serum-free cultures of striatal neurons. Synapse 27:161-167.
20. Godenschwege TA, Reisch D, Diegelmann S, Eberle K, Funk N, Heisenberg M, Hoppe V, et al. 2004. Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour. Eur J Neurosci 20:611-622.
21. Gorczyca M, Augart C, Budnik V. 1993. Insulin-like receptor and insulin-like peptide are localized at neuromuscular junctions in Drosophila. J Neurosci 13:3692-3704.
22. Hinoi E, Ogita K, Takeuchi Y, Ohashi H, Maruyama T, Yoneda Y. 2000. Direct radiolabeling by [3H]quisqualic acid of group I metabotropic glutamate receptor in rat brain synaptic membranes. Brain Res 881:199-203.
23. Hodge JJ, Choi JC, O'Kane CJ, Griffith LC. 2005. Shaw potassium channel genes in Drosophila. J Neurobiol 63:235-254.
24. Jan LY, Jan YN. 1976. Properties of the larval neuromuscular junction in Drosophila melanogaster. J Physiol 262:189-214.
25. Jia XX, Gorczyca M, Budnik V. 1993. Ultrastructure of neuromuscular junctions in Drosophila: Comparison of wild type and mutants with increased excitability. J Neurobiol 24:1025-1044.
26. Kim YJ, Zitnan D, Galizia CG, Cho KH, Adams ME. 2006. A command chemical triggers an innate behavior by sequential activation of multiple peptidergic ensembles. Curr Biol 16:1395-1407.
27. Krenz WD, Nguyen D, Perez-Acevedo NL, Selverston AI. 2000. Group I, II, and III mGluR compounds affect rhythm generation in the gastric circuit of the crustacean stomatogastric ganglion. J Neurophysiol 83:1188-1201.
28. Küppers B, Sanchez-Soriano N, Letzkus J, Technau GM, Prokop A. 2003. In developing Drosophila neurones the production of γ-amino butyric acid is tightly regulated downstream of glutamate decarboxylase translation and can be influenced by calcium. J Neurochem 84:939-951.
29. Landgraf M, Sanchez-Soriano N, Technau GM, Urban J, Prokop A. 2003. Charting the Drosophila neuropile: A strategy for the standardised characterisation of genetically amenable neurites. Dev Biol 260:207-225.
30. Lapchak PA, Beaudet A. 1990. Cholinergic regulation of vasoactive intestinal peptide content and release in rat frontal cortex and hippocampus. J Neurochem 55:1340-1345.
31. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461.
32. Luan H, Lemon WC, Peabody NC, Pohl JB, Zelensky PK, Wang D, Nitabach MN, et al. 2006. Functional dissection of a neuronal network required for cuticle tanning and wing expansion in Drosophila. J Neurosci 26:573-584.
33. McNabb SL, Baker JD, Agapite J, Steller H, Riddiford LM, Truman JW. 1997. Disruption of a behavioral sequence by targeted death of peptidergic neurons in Drosophila. Neuron 19:813-823.
34. Mitri C, Parmentier ML, Pin JP, Bockaert J, Grau Y. 2004. Divergent evolution in metabotropic glutamate receptors. A new receptor activated by an endogenous ligand different from glutamate in insects. J Biol Chem 279:9313-9320.
35. Park JH, Schroeder AJ, Helfrich-Forster C, Jackson FR, Ewer J. 2003. Targeted ablation of CCAP neuropeptide-containing neurons of Drosophila causes specific defects in execution and circadian timing of ecdysis behavior. Development 130:2645-2656.
36. Park Y, Filippov V, Gill SS, Adams ME. 2002. Deletion of the ecdysis-triggering hormone gene leads to lethal ecdysis deficiency. Development 129:493-503.
37. Reiff DF, Ihring A, Guerrero G, Isacoff EY, Joesch M, Nakai J, Borst A. 2005. In vivo performance of genetically encoded indicators of neural activity in flies. J Neurosci 25:4766-4778.
38. Rohrbough J, Broadie K. 2002. Electrophysiological analysis of synaptic transmission in central neurons of Drosophila larvae. J Neurophysiol 88:847-860.
39. Sattelle DB, Jones AK, Sattelle BM, Matsuda K, Reenan R, Biggin PC. 2005. Edit, cut and paste in the nicotinic acetylcholine receptor gene family of Drosophila melanogaster. Bioessays 27:366-376.
40. Shirai Y, Jiang Y, Yoshioka S, Aizono Y. 2001. The release of an insect neuropeptide hormone, bombyxin, is regulated by muscarinic transmission in the brain- corpus cardiacum-corpus allatum complex of the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Appl Entomol Zool 36:431-438.
41. Sprengel R, Aronoff R, Volkner M, Schmitt B, Mosbach R, Kuner T. 2001. Glutamate receptor channel signatures. Trends Pharmacol Sci 22:7-10.
42. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF. 1994. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol [A] 175:179-191.
43. Su H, O'Dowd DK. 2003. Fast synaptic currents in Drosophila mushroom body Kenyon cells are mediated by α-bungarotoxin-sensitive nicotinic acetylcholine receptors and picrotoxin-sensitive GABA receptors. J Neurosci 23:9246-9253.
44. Treherne JE, Smith DS. 1965. The metabolism of acetylcholine in the intact central nervous system of an insect (Periplaneta americana I.). J Exp Biol 43:441-454.
45. Usherwood PNR. 1994. Insect glutamate receptors. Adv Insect Physiol 24:309-341.
46. Washio H. 2002. Glutamate receptors on the somata of dorsal unpaired median neurons in cockroach, Periplaneta americana, thoracic ganglia. Zoolog Sci 19:153-162.
47. 2+ via nicotinic receptors in cultured PDF-containing clock neurons of Drosophila. J Neurophysiol 91:912-923.
48. Yasuyama K, Salvaterra PM. 1999. Localization of choline acetyltransferase-expressing neurons in Drosophila nervous system. Microsc Res Tech 45:65-79.
49. Zitnan D, Adams ME. 2000. Excitatory and inhibitory roles of central ganglia in initiation of the insect ecdysis behavioural sequence. J Exp Biol 203:1329-1340.
50. Zitnan D, Adams ME. 2004. Neuroendocrine regulation of insect ecdysis. In: Lawrence IG, Kostas I, Sarjeet SG, editors. Comprehensive Molecular Insect Science. Amsterdam: Elsevier, pp 1-60.