Immunoreactivity against choline acetyltransferase, γ-aminobutyric acid, histamine, octopamine, and serotonin in the larval chemosensory system of Drosophila melanogaster

Journal of Comparative Neurology

Volumn 453, Issue 2, 2002, Pages 157-167

  Python, François ^a   Stocker, Reinhard F ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

Antennal lobe; Enhancer trap lines; Local interneurons; Neurotransmitters; Olfactory afferents; Projection neurons

Indexed keywords

4 AMINOBUTYRIC ACID; CHOLINE ACETYLTRANSFERASE; HISTAMINE; NORFENEFRINE; SEROTONIN;

ANIMAL TISSUE; ARTICLE; CHEMOSENSITIVITY; DROSOPHILA MELANOGASTER; ENHANCER REGION; ENZYME ACTIVATION; IMMUNOREACTIVITY; INTERNEURON; LARVAL DEVELOPMENT; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALS; ANTIBODIES; CHOLINE O-ACETYLTRANSFERASE; DROSOPHILA MELANOGASTER; GAMMA-AMINOBUTYRIC ACID; GANGLIA, INVERTEBRATE; HISTAMINE; IMMUNOHISTOCHEMISTRY; INTERNEURONS; LARVA; NEURAL PATHWAYS; NEUROTRANSMITTER AGENTS; OCTOPAMINE; OLFACTORY RECEPTOR NEURONS; SEROTONIN; TASTE;

EID: 0037064461     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10383     Document Type: Article

References (76)

1. Aronstein K, ffrench-Constant R. 1995. Immunocytochemistry of a novel GABA receptor subunit Rdl in Drosophila melanogaster. Invert Neurosci 1:25-31.
2. Bicker G. 1999. Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microsc Res Techn 45:174-183.
3. Bicker G. 2001. Sources and targets of nitric oxide signalling in insect nervous systems. Cell Tissue Res 303:137-146.
4. Blake AD, Anthony NM, Chen HH, Harrison JB, Nathanson NM, Sattelle DB. 1993. Drosophila nervous system muscarinic acetylcholine receptor: transient functional expression and localization by immunocytochemistry. Mol Pharmacol 44:716-724.
5. Blenau W, Baumann A. 2001. Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48:13-38.
6. Boeckh J, Distler P, Ernst KD, Hösl M, Malun D. 1990. Olfactory bulb and antennal lobe. In: Schild D, editor. Chemosensory information processing. NATO ASI Series H 39. NewYork: Springer. p 201-228.
7. Brand AH, Perrimon N. 1993, Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
8. 3H]choline uptake in the brain of Drosophila melanogaster. Neurosci Lett 42:25-31.
9. Buchner E, Buchner S, Crawford G, Mason WT, Salvaterra PM, Sattelle DB. 1986. Choline acetyltransferase-like immunoreactivity in the brain of Drosophila melanogaster. Cell Tissue Res 246:57-62.
10. Buchner E, Buchner S, Burg MG, Hofbauer A, Pak WL, Pollack I. 1993. Histamine is a major mechanosensory neurotransmitter candidate in Drosophila melanogaster. Cell Tissue Res 273:119-125.
11. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR. 1999. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327-338.
12. Cobb M. 1999. What and how do maggots smell? Biol Rev 74:425-459.
13. de Belle S, Kanzaki R. 1999. Protocerebral olfactory processing. In: Hansson BS, editor. Insect olfaction. NewYork: Springer. p 243-281.
14. Gorczyca MG, Hall JC. 1987. Immunohistochemical localization of choline acetyltransferase during development and in ChAT mutants of Drosophila melanogaster. J Neurosci 7:1361-1369.
15. Hammer M. 1993. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59-63.
16. Hansson BS. 1999. Insect olfaction. NewYork: Springer.
17. Harrison JB, Chen HH, Blake AD, Huskisson NS, Barker P, Sattelle DB. 1995. Localization in the nervous system of Drosophila melanogaster of a C-terminus antipeptide antibody to a cloned Drosophila muscarinic acetylcholine receptor. J Neuroendocrinol 7:347-352.
18. Harrison JB, Chen HH, Sattelle E, Barker PJ, Huskisson NS, Rauh JJ, Bai D, Sattelle DB. 1996. Immunocytochemical mapping of a C-terminus antipeptide antibody to the GABA receptor subunit, RDL in the nervous system in Drosophila melanogaster. Cell Tissue Res 284:269-278.
19. Heimbeck G, Bugnon V, Gendre N, Häberlin C, Stocker RF. 1999. Smell and taste perception in Drosophila melanogaster larva: toxin expression studies in chemosensory neurons. J Neurosci 19:6599-6609.
20. Heimbeck G, Bugnon V, Gendre N, Keller A, Stocker RF. 2001. A central neural circuit for experience-independent olfactory and courtship behavior in Drosophila melanogaster. Proc Natl Acad Sci USA 98:15336-15341.
21. Hildebrand JG. 1996. Olfactory control of behavior in moths: central processing of odor information and the functional significance of olfactory glomeruli. J Comp Physiol A178:5-19.
22. Homberg U. 1994. Distribution of neurotransmitters in the insect brain. Progress in zoology, vol 40. Stuttgart: Fischer.
23. Homberg U, Hildebrand JG. 1994. Postembryonic development of gamma-aminobutyric acid-like immunoreactivity in the brain of the sphinx moth Manduca sexta. J Comp Neurol 339:132-149.
24. Homberg U, Müller U. 1999. Neuroactive substances in the antennal lobe. In: Hansson BS, editor. Insect olfaction. NewYork: Springer. p 181-206.
25. Homberg U, Christensen TA, Hildebrand JG. 1989. Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34:477-501.
26. Homberg U, Hoskins SG, Hildebrand JG. 1995. Distribution of acetylcholinesterase activity in the deutocerebrum of the sphinx moth Manduca sexta. Cell Tissue Res 279:249-259.
27. Homberg U, Vitzthum H, Müller M, Binkle U. 1999. Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: identification of immunoreactive neurons and colocalization with neuropeptides. J Comp Neurol 409:495-507.
28. Hoskins SG, Homberg U, Kingan TG, Christensen TA, Hildebrand JG. 1986. Immunocytochemistry of GABA in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res 244:243-252.
29. Jefferis GSXE, Marin EC, Stocker RF, Luo LL. 2001. Target neuron pre-specification in the olfactory map of Drosophila. Nature 414:204-208.
30. Jonas PE, Phannavong B, Schuster R, Schroder C, Gundelfinger ED. 1994. Expression of the ligand-binding nicotinic acetylcholine receptor subunit D alpha 2 in the Drosophila central nervous system. J Neurobiol 25:1494-1508.
31. Kent KS, Hoskins SG, Hildebrand JG. 1987. A novel serotonin-immunoreactive neuron in the antennal lobe of the sphinx moth Manduca sexta persists throughout postembryonic life. J Neurobiol 18:451-465.
32. Kitamoto T, Ikeda K, Salvaterra PM. 1995. Regulation of choline acetyltransferase/lacZ fusion gene expression in putative cholinergic neurons of Drosophila melanogaster. J Neurobiol 28:70-81.
33. Kreissl S, Bicker G. 1989. Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J Comp Neurol 286:71-84.
34. Kreissl S, Eichmüller S, Bicker G, Rapus J, Eckert M. 1994. Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J Comp Neurol 348:583-595.
35. Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF. 1999. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543-552.
36. Lundell MJ, Hirsh J. 1994. Temporal and spatial development of serotonin and dopamine neurons in the Drosophila CNS. Dev Biol 165:385-396.
37. Malun D. 1991. Synaptic relationships between GABA-immunoreactive neurons and an identified uniglomerular projection neuron in the antennal lobe of Periplaneta americana: a double labeling electron microscopic study. Histochemistry 96:197-207.
38. Marin EC, Jefferis GSXE, Komiyama T, Zhu H, Luo L. 2002. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109:243-255.
39. Monastirioti M. 1999. Biogenic amine systems in the fruit fly Drosophila melanogaster. Microsc Res Techn 45:106-121.
40. Monastirioti M, Gorczyca M, Rapus J, Eckert M, White K, Budnik V. 1995. Octopamine immunoreactivity in the fruit fly Drosophila melanogaster. J Comp Neurol 356:275-287.
41. Müller U. 1997. The nitric oxide system in insects. Progr Neurobiol 51: 363-381.
42. Murray MJ, Merritt DJ, Brand AH, Whitington PM. 1998. In vivo dynamics of axon pathfinding in the Drosophila CNS: a time-lapse study of an identified motorneuron. J Neurobiol 37:607-621.
43. Nässel DR. 1999. Histamine in the brain of insects: a review. Microsc Res Techn 44:121-136.
44. Nässel DR. 2000. Functional roles of neuropeptides in the insect central nervous system. Naturwiss 87:439-449.
45. Nässel DR, Elekes K. 1992. Aminergic neurons in the brain of blowflies and Drosophila: dopamine- and tyrosine hydroxylase-immunoreactive neurons and their relationship with putative histaminergic neurons. Cell Tissue Res 267:147-167.
46. Nassel DR, Pirvola U, Panula P. 1990. Histaminelike immunoreactive neurons innervating putative neurohaemal areas and central neuropil in the thoracoabdominal ganglia of the flies Drosophila and Calliphora. J Comp Neurol 297:525-536.
47. Nayak SV, Singh RN. 1985. Primary sensory projections from the labella to the brain of Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 14:115-129.
48. Nishikawa K, Kidokoro Y. 1999. Octopamine inhibits synaptic transmission at the larval neuromuscular junction in Drosophila melanogaster. Brain Res 837:67-74.
49. Oland LA, Kirschenbaum SR, Pott WM, Mercer AR, Tolbert LP. 1995. Development of an identified serotonergic neuron in the antennal lobe of the moth and effects of reduction in serotonin during construction of olfactory glomeruli. J Neurobiol 28:248-267.
50. Oppliger FY, Guerin PM, Vlimant M. 2000. Neurophysiological and behavioural evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae. J Insect Physiol 46:135-144.
51. Osborne KA, Robichon A, Burgess E, Butland S, Shaw RA, Coulthard A, Pereira HS, Greenspan RJ, Sokolowski MB. 1997. Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277:834-836.
52. Pollack I, Hofbauer A. 1991. Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster. Cell Tissue Res 266:391-398.
53. Python F, Stocker RF. 2002. Adult-like complexity of the larval antennal lobe of D. melanogaster in spite of markedly low numbers of odorant receptor neurons. J Comp Neurol 445:374-387.
54. Ressler KJ, Sullivan SL, Buck LB. 1994. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79:1245-1255.
55. Salecker I, Distler P. 1990. Serotonin-immunoreactive neurons in the antennal lobes of the American cockroach Periplaneta americana: light- and electron-microscopic observations. Histochemistry 94:463-473.
56. Schäfer S, Bicker G. 1986. Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol 246:287-300.
57. Scott K, Brady R Jr, Cravchik A, Morozov P, Rzhetsky A, Zuker C, Axel R. 2001. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104:661-673.
58. Shaver SA, Varnam CJ, Hilliker AJ, Sokolowski MB. 1998. The foraging gene affects adult but not larval olfactory-related behavior in Drosophila melanogaster. Behav Brain Res 95:23-29.
59. Singh RN, Singh K. 1984. Fine structure of the sensory organs of Drosophila melanogaster Meigen larva (Diptera: Drosophilidae). Int J Insect Morphol Embryol 13:255-273.
60. Stocker RF. 1994. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3-26.
61. Stocker RF. 2001. Drosophila as a focus in olfactory research: mapping of olfactory sensilla by fine structure, odor specificity, odorant receptor expression, and central connectivity. Microsc Res Techn 55:284-296.
62. Stocker RF, Heimbeck G, Gendre N, de Belle JS. 1997. Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J Neurobiol 32:443-456.
63. Stopfer M, Bhagavan S, Smith BH, Laurent G. 1997. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70-74.
64. Taghert PH. 1999. FMRFamide neuropeptides and neuropeptide-associated enzymes in Drosophila. Microsc Res Techn 45:80-95.
65. Takagawa K, Salvaterra P. 1996. Analysis of choline acetyltransferase protein in temperature sensitive mutant flies using newly generated monoclonal antibody. Neurosci Res 24:237-243.
66. Tissot M, Gendre N, Hawken A, Störtkuhl KF, Stocker RF. 1997. Larval chemosensory projections and invasion of adult afferents in the antennal lobe of Drosophila. J Neurobiol 32:281-297.
67. Vallés AM, White K. 1986. Development of serotonin-containing neurons in Drosophila mutants unable to synthesize serotonin. J Neurosci 6:1482-1491.
68. Vallés AM, White K. 1988. Serotonin-containing neurons in Drosophila melanogaster: development and distribution. J Comp Neurol 268:414-428.
69. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R. 1999. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725-736.
70. Vosshall LB, Wong AM, Axel R. 2000. An olfactory sensory map in the fly brain. Cell 102:147-159.
71. Wong AM, Wang JW, Axel R. 2002. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229-241.
72. Yasuyama K, Salvaterra PM. 1999. Localization of choline acetyltransferase-expressing neurons in Drosophila nervous system. Microsc Res Techn 45:65-79.
73. Yasuyama K, Kitamoto T, Salvaterra PM. 1995. Immunocytochemical study of choline acetyltransferase in Drosophila melanogaster: an analysis of cis-regulatory regions controlling expression in the brain of cDNA-transformed flies. J Comp Neurol 361:25-37.
74. Yasuyama K, Kitamoto T, Salvaterra PM. 1996. Differential regulation of choline acetyltransferase expression in adult Drosophila melanogaster brain. J Neurobiol 30:205-218.
75. Yeh E, Gustafson K, Boulianne GL. 1995. Green fluorescent protein as a vital marker and reporter of gene expression in Drosophila. Proc Natl Acad Sci USA 92:7036-7040.
76. Yusuyama K, Meinertzhagen IA, Schürmann, FW. 2002. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J Comp Neurol 445:211-226.