Localization of choline acetyltransferase-expressing neurons in Drosophila nervous system

Microscopy Research and Technique

Volumn 45, Issue 2, 1999, Pages 65-79

  Yasuyama, Kouji ^a   Salvaterra, Paul M ^b  

^a KAWASAKI MEDICAL SCHOOL   (Japan)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

ChAT lacZ fusion gene; Cholinergic neurons; Immunocytochemistry; In situ hybridization

Indexed keywords

BIOCHEMISTRY; GENE EXPRESSION; MONOCLONAL ANTIBODIES; RNA;

ACETYL TRANSFERASE; ACETYLTRANSFERASES; CHOLINE ACETYLTRANSFERASE/LACZ FUSION GENE; CHOLINERGIC NEURON; DROSOPHILLA; FUSION GENES; IMMUNOCYTOCHEMISTRY; IN-SITU HYBRIDIZATION; LOCALISATION; NEURAL ELEMENT;

NEURONS;

ACETYLCHOLINE; BETA GALACTOSIDASE; CHOLINE ACETYLTRANSFERASE; MESSENGER RNA;

ACETYLCHOLINE RELEASE; ANIMAL CELL; ANIMAL TISSUE; BRAIN DEVELOPMENT; CELLULAR DISTRIBUTION; DROSOPHILA; EMBRYO DEVELOPMENT; ENZYME LOCALIZATION; GENE EXPRESSION REGULATION; IMMUNOCYTOCHEMISTRY; LARVAL DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; REVIEW;

EID: 0033561475     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(19990415)45:2<65::AID-JEMT2>3.0.CO;2-0     Document Type: Review

References (81)

1. Barber RP, Sugihara H, Lee M, Vaughn JE, Salvaterra PM. 1989. Localization of Drosophila neurons that contain choline acetyltrans-ferase messenger RNA: an in situ hybridization study. J Comp Neurol 180:533-543.
2. 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.
3. Bolwig N. 1946. Senses and sense organs of the anterior end of the house fly larvae. Vidensk Medd Dansk Naturh Foren 109:81-217.
4. Buchner E. 1991. Genes expressed in the adult brain of Drosophila and effects of their mutations on behavior: a survey of transmitter-and second messenger-related genes. J Neurogent 7:153-192.
5. 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.
6. Buchner E, Bader R, Buchner S, Cox J, Emson PC, Flory E, Heinzmann CW, Hemm S, Hofbauer A, Oertel WH. 1988. Cell-specific immuno-probes for the brain of normal and mutant Drosophila melanogaster. I. Wild type visual system. Cell Tissue Res 253: 357-370.
7. 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.
8. Carbini LA, Maines VJM, Salvaterra PM. 1990. Developmental expression of choline acetyltransferase mRNA in Drosophila. Neurochem Res. 15:1089-1096.
9. Chase BA, Kankel DR. 1988. On the role of acetylcholine metabolism in the formation and maintenance of the Drosophila nervous system. Dev Biol 125:361-380.
10. Cole ES, Palka J. 1982. The pattern of campaniform sensilla on the wing and haltere of Drosophila melanogaster and several of its homeotic mutants. J Embryol Exp Morphol 71:41-61.
11. Crawford G, Slemmon JR, Salvaterra PM. 1982. Monoclonal antibodies selective for Drosophila melanogaster choline acetyltransferase. J Biol Chem 257:3853-3856.
12. Datum K-H, Weiler R, Zettler F. 1986. Immunocytochemical demonstration of -amino butyric acid and glutamic acid decarboxylase in R7 photoreceptors and C2 centrifugal fibers in the blowfly visual system. J Comp Physiol A 159:241-249.
13. Duve H, Thorpe A. 1979. Immunofluorescent localization of insulin-like material in the median neurosecretory cells of the blowfly Calliphora vomitoria (Diptera). Cell Tissue Res 200:187-191.
14. Duve H, Thorpe A. 1981. Gastrin/cholecystokinin (CCK)-like immuno-reactive neurons in the brain of the blowfly Calliphora erythrocephala (Diptera). Gen Comp Endocrinol 43:381-391.
15. Duve H, Thorpe A. 1983. Immunocytochemical identification of-endorphin-like material in neurons of the brain and corpus cardiacum of the blowfly Calliphora vomitoria (Diptera). Cell Tissue Res 233: 415-426.
16. Ewing AW. 1978. The antenna as a "love song" receptor. Physiol Entomol 3:33-36.
17. Fischbach K-F, Dittrich APM. 1989. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441-475.
18. Geffard M, Vieillemaringe J, Heinrich-Rock A-M, Duris P. 1985. Anti-acetylcholine antibodies and first immunocytochemical application in insect brain. Neurosci Lett 57:1-6.
19. Ghysen A, Dambly-Chaudiere C, Aceves E, Jan LY, Van YN. 1986. Sensory neurons and peripheral pathways in Drosophila embryos. Roux's Arch Dev Biol 195:281-289.
20. Gorczyca MG, Hall JC. 1984. Identification of a cholinergic synapse in the giant fiber pathway of Drosophila using conditional mutations of acetylcholine synthesis. J Neurogenet 1:289-313.
21. ts of Drosophila melanogaster. J Neurosci 7:1361-1369,
22. Gorczyca MG, Budnik V, White K, Wu CF. 1991. Dual muscarinic and nicotinic action on a motor program in Drosophila. J Neurobiol 22:391-404.
23. Greenspan RJ. 1980. Mutations of choline acetyltransferase and associated neural defects in Drosophila melanogaster. J Comp Physiol 137:83-92.
24. Gundelfinger ED. 1992. How complex is the nicotinic receptor system of insect? Trends Neurosci 15:206-211.
25. Gundelfinger ED, Hess N. 1992. Nicotinic acetylcholine receptors of the central nervous system of Drosophila. Biochim Biophys Acta 1137:299-308.
26. Hall JC, Kankel DR. 1976. Genetics of acetylcholinesterase in Drosophila melanogaster. Gentics 83:517-535.
27. Hall LMC, Spierer P. 1986. The Ace locus of Drosophila melanogaster: structural gene for acetylcholinesterase with an usual 5' leader. EMBO J 5:2949-2954.
28. Hannan F, Hall LM. 1993. Muscarinic acetylcholine receptors in invertebrates: comparisons with homologous receptors from vertebrates. In: Pichon Y, editor. Comparative molecular neurobiology. Basel: Birkhauser Verlag; p 98-145.
29. Hartenstein V, Posakony JW. 1989. Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development 107:389-405.
30. 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.
31. Huang F, Dambly-Chaudiere C, Ghysen A. 1991. The emergence of sense organs in the wing disc of Drosophila. Development 111:1087-1095.
32. Ikeda K, Salvaterra PM. 1989. Immunocytochemical study of a temperature-sensitive choline acetyltransferase mutant of Drosophila melanogaster. J Comp Neurol 280:283-290.
33. Itoh N, Slemmon J R, Hawke DH, Williamson R, Morita E, Itakura K, Roberts E, Shively JE, Crawford GD, Salvaterra PM. 1986. Cloning of Drosophila choline acetyltransferase cDNA. Proc Natl Acad Sci USA 83:4081-4085.
34. Jan YN, Ghysen A, Christoph I, Barbel S, Jan LY. 1985. Formation of neuronal pathways in the imaginal discs of Drosophila melanogaster. J Neurosci 5:2453-2465.
35. Jonas P, Phannavong B, Schhuster R, Schröder C, Gundelfinger ED. 1994. Expression of the ligand-binding nicotinic acetylcholine receptor subunit Da2 in the Drosophila central nervous system. J Neurobiol 25:1494-1508.
36. Kankel DR, Ferrus A, Garen SH, Harte PJ, Lewis PE. 1980. The structure and development of the nervous system. In: Ashburner M, Wright TRF, editors. The genetics and biology of Drosophila, vol. 2. New York: Academic Press; p 295-368.
37. Kitamoto T, Salvaterra PM. 1993. Developmental regulatory elements in the 5' flanking DNA of the Drosophila choline acetyltransferase gene. Roux's Arch Dev Biol 202:159-169.
38. Kitamoto T, Ikeda K, Salvaterra PM. 1992. Analysis of cis-regulatory elements in the 5' flanking region of the Drosophila melanogaster choline acetyltransferase gene. J Neurosci 12:1628-1639.
39. Kitamoto T, Ikeda K, Salvaterra PM. 1995. Regulation of choline acetyltrasferase/lacZ fusion gene expression in putative cholinergic neurons of Drosophila melanogaster. J Neurobiol 28:70-81.
40. Kitamoto T, Wang W, Salvaterra PM. 1998. Structure and organization of the Drosophila cholinergic locus. J Biol Chem 273:2706-2713.
41. Lutz EM, Tyrer NM. 1988. Immunohistochemical localization of serotonin and choline acetyltransferase in sensory neurones of the locust. J Comp Neurol 267:335-342.
42. Meinertzhagen IA, O'Neil SD. 1991. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J Comp Neurol 305:232-263.
43. Merritt DJ, Murphey RK. 1992. Projections of leg proprioceptors within the CNS of the fly Phormia in relation to the generalized insect ganglion. J Comp Neurol 322:16-34.
44. Meyer EP, Matute C, Streit P, Nässel DR. 1986. Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry 84:207-216.
45. Miller A 1950. The internal anatomy and histology of the imago of Drosophila melanogaster. In: Demerec M, editor. Biology of Drosophila. New York: Hafner Publishing; p420-534.
46. Mindek G. 1968. Proliferations-und Transdeterminationsleistungen der weiblichen Genital-Imaginalscheiben von Drosophila melanogaster nach Kultur in vivo. Roux's Arch Dev Biol 161:249-280.
47. Murphey RK, Possidente D, Pollack G, Merritt DJ. 1989. Modality-specific axonal projections in the CNS of the flies Phormia and Drosophila. J Comp Neurol 290:185-200.
48. Nässel DR. 1991. Neurotransmitters and neuromodulators in the insect visual system. Prog Neurobiol 37:179-254.
49. Nässel DR. 1993. Neuropeptides in the brain: a review. Cell Tissue Res 273:1-29.
50. Nässel DR, O'Shea M. 1987. Proctolin-like immunoreactive neurons in the blowfly central nervous system. J Comp Neurol 265:437-454.
51. Nayak SV, Singh RN. 1983. Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 12:273-291
52. O'Brien MA, Schneider LE, Taghert PH. 1991. In situ hybridization analysis of the FMRFamide neuropeptide gene in Drosophila. II. Constancy in the cellular pattern of expression during metamorphosis. J Comp Neurol 304:623-638.
53. Palka J, Lawrence PA, Hart HS. 1979. Neural projection patterns from homeotic tissue of Drosophila studied in bithorax mutants and mosaics. Dev Biol 69:549-575.
54. Pollack I, Hofbauer A. 1991. Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster. Cell Tissue Res 266:391-398.
55. Power ME. 1948. The thoracico-abdominal nervous system of an adult insect Drosophila melanogaster. J Comp Neurol 88:347-409.
56. Restifo LL, White K. 1990. Molecular and genetic approaches to neruotransmitter and neruomodulator systems in Drosophila. Adv Insect Physiol 22:115-219.
57. Salvaterra PM, Vaughn JE. 1989. Regulation of choline acetyltransferase. Int Rev Neurobiol 31:81-143.
58. Schmidt M. 1997. Distribution of presumptive chemosensory afferents with FMRFamide-or substance P-like immunoreactivity in decapod crustaceans. Brain Res 746:71-84.
59. Schmidt M, Ache BW. 1994, FMRFamide-like immunoreactivity in presumptive chemosensory afferents of the spiny lobster Panulirus argus. Brain Res 315-324.
60. Schuster R, Phannavong B, Schröder C, Gundelfinger ED. 1993. Immunohistochemical localization of a ligand-binding and a structureal subunit of nicotinic acetylcholine receptors in the central nervous system of Drosophila melanogaster. J Comp Neurol 335: 149-162.
61. Shanbhag SR, Singh K, Singh RN. 1992. Ultrastructure of the femoral chordotonal organs and their novel synaptic organization in the legs of Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 21:311-322.
62. Singh RN, Nayak S. 1985. Fine structure and primary sensory projections of sensilla on the maxillary palp of Drosphila melanogaster Meigen (Diptera: Drosophilaidae). Int J Insect Morphol Embryol 14:291-306.
63. Smith SA, Shepherd D. 1996. Central afferent projections of proprioceptive sensory neurons in Drosophila revealed with the enhancer-trap technique. J Comp Neurol 364:311-323.
64. Steller H, Fischbach K-F, Rubin GM. 1987. disconnected: a locus required for neuronal pathway formation in the visual system of Drosophila. Cell 50:1139-1153.
65. Stengl M, Homberg U, Hildebrand JG. 1990. Acetylcholinesterase activity in antennal receptor neurons of the sphinx moth Manduca sexta. Cell Tissue Res 262:245-252.
66. Stocker RF. 1994. The organization of the chemosensory system in Drosophila melanogaster. a review. Cell Tissue Res 275:3-26.
67. Stocker RF, Schorderet M. 1981. Cobalt filling of sensory projections from internal and external mouthparts in Drosophila. Cell Tissue Res 216:513-523.
68. Stocker RF, Singh RN, Schorderet M, Siddiqi O. 1983. Projection patterns of different types of antennal sensilla in the antennal glomeruli of Drosophila melanogaster. Cell Tissue Res 232:237-248.
69. Stocker RF, Lienhard MC, Borst A, Fischbach K-F. 1990. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9-34.
70. Sugihara H, Andrisani V, Salvaterra PM. 1990. Drosophila choline actyltransferase uses a non-AUG initiation codon and full length RNA is inefficiently translated. J. Biol. Chem, 265:21714-21719.
71. Takagawa K, Salvaterra PM. 1996. Analysis of choline acetyltransferase protein in temperature sensitive mutant flies using newly generated monoclonal antibody. Neurosci Res 24:237-243.
72. Taylor B. 1989a. Sexually dimorphic neurons in the terminalia of Drosophila melanogaster: I. Development of sensory neruons in the genital disc during metamorphosis. J Neurogenet 5:173-192.
73. Taylor B. 1989b. Sexually dimorphic neurons of the terminalia of Drosophila melanogaster: II. Sex-specific axonal arborizations in the central nervous system. J Neurogenet 5:193-213.
74. Tix S, Minden JS, Technau GM. 1989. Pre-existing neuronal pathways in the developing optic lobes of Drosophila. Development 105:739-746.
75. Trimmer BA. 1995. Current excitement from insect muscarinic receptors. Trends Neurosci 18:104-111.
76. White K, Hurteau T, Punsal P. 1986. Neuropeptide-FMRFamide-like immunoreactivity in Drosophila: development and distribution. J Comp Neurol 247:430-438.
77. Wilczek M. 1967. The distribution and neuroanatomy of the labellar sense organs of the blowfly Phormia regina Meigen. J Morphol 122:175-201.
78. Yasuyama K, Kitamoto T, Salvaterra PM. 1995a. 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.
79. Yasuyama K, Kitamoto T, Salvaterra PM. 1995b. Localization of choline acetyltransferase-expressing neurons in the larval visual system of Drosophila melanogaster. Cell Tissue Res 282:193-202.
80. Yasuyama K, Kitamoto T, Salvaterra PM. 1996a. Differential regulation of choline acetyltransferase expression in adult Drosophila melanogaster Brain J Neurobiol 30:205-218.
81. Yasuyama K, Kitamoto T, Salvaterra PM. 1996b. Distribution and central projections of putative cholinergic leg sensory neurons in Drosophila. Zool Sci 13(Suppl):120.