Temporal and spatial expression patterns of two G-protein coupled receptors in Drosophila melanogaster

Invertebrate Neuroscience

Volumn 2, Issue 1, 1996, Pages 71-83

  Hannan, Frances ^a,b   Hall, Linda M ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

Antennal lobes; Developmental profile; In situ hybridization; mRNA transport; Muscarinic acetylcholine receptor; Octopamine tyramine receptor

Indexed keywords

COMPLEMENTARY DNA; GUANINE NUCLEOTIDE BINDING PROTEIN; MESSENGER RNA; MUSCARINIC RECEPTOR; NORSYNEPHRINE RECEPTOR; RECEPTOR; TYRAMINE RECEPTOR;

ANIMAL; ANIMAL EMBRYO; ARTICLE; CENTRAL NERVOUS SYSTEM; DROSOPHILA MELANOGASTER; FEMALE; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; NORTHERN BLOTTING; PRENATAL DEVELOPMENT; TIME; TISSUE DISTRIBUTION;

ANIMALS; BLOTTING, NORTHERN; CENTRAL NERVOUS SYSTEM; DNA, COMPLEMENTARY; DROSOPHILA MELANOGASTER; EMBRYO, NONMAMMALIAN; FEMALE; GTP-BINDING PROTEINS; IN SITU HYBRIDIZATION; RECEPTORS, BIOGENIC AMINE; RECEPTORS, MUSCARINIC; RNA, MESSENGER; TIME FACTORS; TISSUE DISTRIBUTION;

EID: 0030154604     PISSN: 13542516     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02336662     Document Type: Article

References (90)

1. Abdallah, E. A. M., Eldefrawi, M. E. and Eldefrawi, A. T. (1991) Pharmacologic characterization of muscarinic receptors of insect brains. Arch. Insect Biochem. Physiol., 17, 107-118.
2. Arakawa, S., Gocayne, J. D., McCombie, W. R., Urquhart, D. A., Hall, L. M., Fraser, C. M. and Venter J. C. (1990) Cloning, localization, and permanent expression of a Drosophila octopamine receptor. Neuron, 4, 343-354.
3. Ashburner, M. and Thompson, J. N. Jr. (1978) The laboratory culture of Drosophila. In The Genetics and Biology of Drosophila, Vol. 2a, ed. M. Ashburner and T. R. F. Wright, pp 1-109. New York: Academic Press.
4. Bainbridge, S. P. and Bownes, M. (1981) Staging the metamorphosis of Drosophila melanogaster. J. Embryol. Exp. Morphol., 66, 57-80.
5. Barber, R. P., Sugihara, H., Lee, M., Vaughn, J. E. and Salvaterra, P. M. (1989) Localization of Drosophila neurons that contain choline acetyltransferase messenger RNA: an in situ hybridization study. J. Comp. Neurol., 280, 533-543.
6. Blake, A. D., Anthony, N. M., Chen, H. H., Harrison, J. B., Nathanson, N. M. and Sattelle, D. B. (1993) Drosophila nervous system muscarinic acetylcholine receptor: transient functional expression and localization by immunocytochemistry. Mol. Pharmacol., 44, 716-724.
7. Bodnaryk, R. P. (1980) Changes in brain octopamine levels during metamorphosis of the moth Mamestra configurata Wlk. Insect Biochem., 10, 169-173.
8. Bossy, B., Ballivet, M. and Spierer, P. (1988) Conservation of neural nicotinic acetylcholine receptors from Drosophila to vertebrate central nervous systems. EMBO J., 7, 611-618.
9. 3H]choline uptake in the brain of Drosophila melanogaster. Neurosci. Lett., 42, 25-31.
10. Buchner, E., Buchner, S., Crawford, G., Mason, W. T., Salvaterra, P. M. and Sattelle, D. B. (1986) Choline acetyltransferase-like immunoreactivity in the brain of Drosophila melanogaster. Cell Tissue Res., 246, 57-62.
11. Campos-Ortega, J. A. and Hartenstein, V. (1985) The Embryonic Development of Drosophila melanogaster. Berlin; Heidelberg: Springer-Verlag.
12. Carbini, L. A., Maines, V. J. M. and Salvaterra, P. M. (1990) Developmental expression of choline acetyltransferase mRNA in Drosophila. Neurochem. Res., 15, 1089-1096.
13. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162, 156-159.
14. Cox, K. H., DeLeon, D. V., Angerer, L. M. and Angerer, R. C. (1984) Detection of mRNAs in sea urchin embryos by in situ hybridization using asymmetric RNA probes. Dev. Biol., 101, 485-502.
15. Davenport, A. P. and Wright, D. J. (1986) Octopamine distribution in the larvae and adults of two species of moth Spodoptera littoralis and Manduca sexta. J. Insect Physiol., 32, 987-993.
16. David, J. -C. and Coulon, J. -F. (1985) Octopamine in invertebrates and vertebrates. A review. Prog. Neurobiol., 24, 457-462.
17. Davis, R. L. (1993) Mushroom bodies and Drosophila learning. Neuron, 11, 1-14.
18. Dewhurst, S. A. and Seecof, R. L. (1975) Development of acetylcholine metabolizing enzymes in Drosophila embryos and in cultures of embryonic Drosophila cells. Comp. Biochem. Physiol., 50C, 53-58.
19. Dewhurst, S. A., McCaman, R. E. and Kaplan, W. D. (1970) The time course of development of acetylcholinesterase and choline acetyltransferase in Drosophila melanogaster. Biochem. Genet., 4, 499-508.
20. Downer, R. G. H., Orr, G. L., Gole, J. W. D. and Orchard, I. (1984) The role of octopamine and cyclic AMP in regulating hormone release from corpora cardiaca of the American cockroach. J. Insect Physiol., 30, 457-462.
21. Dudai, Y., Buxbaum, J., Corfas, G. and Ofarim, M. (1987) Formamidines interact with Drosophila octopamine receptors, alter the flies' behaviour and reduce their learning ability. J. Comp. Physiol. A, 161, 739-746.
22. Erber, J., Kloppenburg, P. and Scheidler, A (1993) Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology. Experientia, 49, 1073-1083.
23. Evans, P. D. (1981) Multiple receptor types for octopamine in the locust. J. Physiol. (Lond.), 318, 99-122.
24. Evans, P. D. (1985) Octopamine. In Comprehensive Insect Physiology Biochemistry and Pharmacology, ed. G. A. Kerkut and L. I. Gilbert, pp 499-530. Oxford: Pergamon.
25. Evans, P. D. (1993) Molecular studies on insect octopamine receptors. In Comparative Molecular Neurobiology. ed. Y. Pichon, pp 286-296. Basel; Boston; Berlin: Birkhäuser Verlag.
26. Evans, P. D. and O'Shea, M. (1977) The identification of an octopaminergic neurone which modulates neuromuscular transmission in the locust. Nature, 270, 257-259.
27. Fields, P. E., and Woodring, J. P. (1991) Octopamine mobilization of lipids and carbohydrates in the house cricket, Acheta domesticus. J. Insect Physiol., 37, 193-199.
28. Fryxell, K. J. (1995) The evolutionary divergence of neurotransmitter receptors and second-messenger pathways. J. Mol. Evol., 41, 85-97.
29. Goodman, C. S., O'Shea, M., McCaman, R. and Spitzer, N. C. (1979) Embryonic development of identified neurons: temporal pattern of morphological and biochemical differentiation. Science, 204, 1219-1222.
30. ts mutants of Drosophila melanogaster. J. Neurosci., 7, 1361-1369.
31. Gorczyca, M. G., Budnik, V., White, K. and Wu, C. -F. (1991) Dual muscarinic and nicotinic action on a motor program in Drosophila. J. Neurobiol., 22, 391-404.
32. Hafen, E. and Levine, M. (1986) The localization of RNAs in Drosophila tissue sections by in situ hybridization. In Basic Drosophila Care and Techniques, ed. D. B. Roberts, pp 139-157. Oxford: IRL Press.
33. Hanesch, U., Fischbach, K. -F. and Heisenberg, M. (1989) Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res., 257, 343-366.
34. Hannan, F. and Hall, L. M. (1993) Muscarinic acetylcholine receptors in invertebrates: comparisons with homologous receptors from vertebrates. In Comparative Molecular Neurobiology, ed. Y. Pichon, pp 98-145. Basel; Boston; Berlin: Birkhauser Verlag.
35. Harrison, J. B., Chen, H. H., Blake, A. D., Huskisson, N. S., Barker, P. and Sattelle, D. B. (1995) Localization in the nervous system of Drosophila melanogaster of a C-terminus anti-peptide antibody to a cloned Drosophila muscarinic acetylcholine receptor. J. Neuroendocrinol., 7, 347-352.
36. Henikoff, S. and Eghtedarzadeh, M. K. (1987) Conserved arrangement of nested genes at the Drosophila Gart locus. Genetics, 117, 711-725.
37. Hermans-Borgmeyer, I., Hoffmeister, S., Sawruk, E., Betz, H., Schmitt, B. and Gundelfinger, E. D. (1989) Neuronal acetylcholine receptors in Drosophila: mature and immature transcripts of the ard gene in the developing central nervous system. Neuron, 2, 1147-1156.
38. 125I-α-bungarotoxin binding sites in normal and deafferented antennal lobes of Manduca sexta. Proc. Natl. Acad. Sci. USA, 76, 499-503.
39. Hille, B. (1992) G protein-coupled mechanisms and nervous signalling. Neuron, 9, 187-195.
40. Homberg, U. and Hildebrand, J. G. (1991) Histamine-immunoreactive neurons in the midbrain and suboesophageal ganglion of the sphinx moth Manduca sexta. J. Comp. Neurol., 307, 647-657.
41. Johansen, J., Halpern, M. E., Johansen, K. M. and Keshishian, H. (1989) Stereotypic morphology of glutamatergic synapses on identified muscle cells of Drosophila larvae. J. Neurosci., 9, 710-725.
42. Jonas, P., Baumann, A., Merz, B. and Gundelfinger, E. D. (1990) Structure and developmental expression of the Dα2 gene encoding a novel nicotinic acetylcholine receptor protein of Drosophila melanogaster. FEBS Lett., 269, 264-268.
43. Jonas, P. E., Phannavong, B, Schuster, R., Schroder, C. and Gundelfinger, E. D. (1994) Expression of the ligand-binding nicotinic acetylcholine receptor subunit Dα2 in the Drosophila central nervous system. J. Neurobiol., 25, 1494-1508.
44. Kankel, D. R., Ferrus, A., Garen, S. H., Harte, P. J. and Lewis, P. E. (1980) The structure and development of the nervous system. In The Genetics and Biology of Drosophila, Vol 2d, ed. M. Ashburner and T. R. F. Wright, pp 295-368. New York: Academic Press.
45. Lange, A. B. and Orchard, I. (1986) Ventral neurons in an abdominal ganglion of the locust Locusta migratoria, with properties similar to dorsal unpaired median neurons. Can. J. Zool., 64, 264-267.
46. Lindsley, D. L. and Zimm, G. G. (1992) The Genome of Drosophila melanogaster. New York: Academic Press.
47. Livingstone, M. S. and Tempel, B. L. (1983) Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. Nature, 303, 67-70.
48. 3H]scopolamine binding sites in the central nervous system of the cockroach Periplaneta americana. Arch. Insect Biochem. Physiol., 3, 339-347.
49. Lundell, M. J. and Hirsh, J. (1994) Temporal and spatial development of serotonin and dopamine neurons in the Drosophila CNS. Dev. Biol., 165, 385-396.
50. Lutz, E. M. and Tyrer, N. M. (1987) Immunohistochemical localization of choline acetyltransferase in the central nervous system of the locust. Brain Res., 407, 173-179.
51. Martin-Morris, L. E. and White, K. (1990) The Drosophila transcript encoded by the β-amyloid precursor-like gene is restricted to the nervous system. Development, 110, 185-195.
52. Mercer, A. R. and Menzel, R. (1982) The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera. J. Comp. Physiol. A, 145, 363-368.
53. Miller, A. (1950) The internal anatomy and histology of the imago of Drosophila melanogaster. In Biology of Drosophila, ed. M. Demerec, pp 420-534. New York: Wiley.
54. Milligan, G. (1993) Mechanisms of multifunctional signalling by G-protein-linked receptors. Trends Pharmocol. Sci., 14, 239-244.
55. Monastirioti, M., Gorczyca, M., Rapus, J., Eckert, M., White, K. and Budnik, V. (1995) Octopamine immunoreactivity in the fruitfly Drosophila melanogaster. J. Comp. Neurol., 356, 275-287.
56. Nassel, D. R. (1993) Neuropeptides in the insect brain: a review. Cell Tissue Res., 273, 1-29.
57. Nassel, D. R. and 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.
58. O'Connell, P. and Rosbash, M. (1984) Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res., 12, 5495-5513.
59. O'Dell, K. M. C. (1993) The effect of the inactive mutation on longevity, sex, rhythm and resistance to p-cresol in Drosophila melanogaster. Heredity, 70, 393-399.
60. O'Dell, K., Coulon, J.-F., David, J. -C., Papin, C., Fuzeau-Braesch, S. and Jallon, J. -M. (1987) La mutation inactive produit une diminution marquee d'octopamine dans le cerveau des Drosophiles. C. R. Acad. Sci. III, 305, 199-202.
61. Onai, T., Fitzgerald, M. G., Arakawa, S., Gocayne, J. D., Urquhart, D. A., Hall, L. M., Fraser, C. M., McCombie, W. R. and Venter, J. C. (1989) Cloning, sequence analysis and chromosome localization of a Drosophila muscarinic acetylcholine receptor. FEBS Lett., 255, 219-225.
62. Orr, G. L., Orr, N. and Hollingworth, R. M. (1991) Distribution and pharmacological characterization of muscarinic-cholinergic receptors in the cockroach brain. Arch. Insect Biochem. Physiol., 16, 107-122.
63. Power, M. E. (1943) The brain of Drosophila melanogaster. J. Morphol., 72, 517-559.
64. Ready, D. F., Hanson, T. E. and Benzer, S. (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol., 53, 217-240.
65. Robb, S., Cheek, T. R., Venter, J. C., Midgley, J. M. and Evans P. D. (1991) The mode of action and pharmacology of a cloned Drosophila phenolamine receptor. Pest. Sci., 32, 369-371.
66. Robb, S., Cheek, T. R., Hannan, F. L., Hall, L. M., Midgley, J. M and Evans P. D. (1994) Agonist specific coupling of a cloned Drosophila octopamine/tyramine receptor to multiple second messenger systems. EMBO J., 13, 1325-1330.
67. Robinow, S. and White, K. (1988) The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev. Biol., 126, 294-303.
68. Roeder, T. (1994) Biogenic amines and their receptors in insects. Comp. Biochem. Physiol., 107C, 1-12.
69. 3H]quinuclidinyl-benzilate binding in central nervous systems of different species. J. Neurochem., 32, 1509-1517.
70. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
71. Sanes, J. R., Prescott, D. J. and Hildebrand, J. G. (1977) Cholinergic neurochemical development of normal and deafferented antennal lobes during metamorphosis of the moth, Manduca sexta. Brain Res., 119, 389-402.
72. Sattelle, D. B. (1980) Acetylcholine receptors of insects. Adv. Insect Physiol., 15, 215-315.
73. Saudou, F., Amlaiky, N., Plassat, J. -L., Borrelli, E. and Hen, R. (1990) Cloning and characterization of a Drosophila tyramine receptor. EMBO J., 9, 3611-3617.
74. Sawruk, E., Schloss, P., Betz, H. and Schmitt, B. (1990a) Heterogeneity of Drosophila nicotinic acetylcholine receptors: SAD, a novel developmentally regulated α-subunit. EMBO J., 9, 2671-2677.
75. Sawruk, E., Udri, C., Betz, H. and Schmitt, B. (1990b) SBD, a novel structural subunit of the Drosophila nicotinic acetylcholine receptor, shares its genomic localization with two α-subunits. FEBS Lett., 273, 177-181.
76. Schmidt-Nielsen, B. K., Gepner, J. I., Teng, N. N. H. and Hall, L. M. (1977) Characterization of an α-bungarotoxin binding component from Drosophila melanogoster. J. Neurochem., 29, 1013-1029.
77. Shapiro, R. A., Wakimoto, B. T., Subers, E. M. and Nathanson, N. M. (1989) Characterization and functional expression in mammalian cells of genomic and cDNA clones encoding a Drosophila muscarinic acetylcholine receptor. Proc. Natl. Acad. Sci. USA, 86, 9039-9043.
78. Stevenson, P. A. and Sporehase-Eichmann, U. (1995) Localization of octopaminergic neurones in insects. Comp. Biochem. Physiol., 110A, 203-215.
79. Stocker, R. F. (1982) Genetically displaced sensory neurons in the head of Drosophila project via different pathways into the same specific brain regions. Dev. Biol., 94, 31-40.
80. Stocker, R. F. (1995) Morphogenesis and cellular proliferation pattern in the developing antennal lobe of Drosophila melanogaster. Roux's Arch. Dev. Biol., 205, 62-72.
81. Strosberg, A. D. (1991) Structure/function relationship of proteins belonging to the family of receptors coupled to GTP-binding proteins. Eur. J. Biochem., 196, 1-10.
82. 32P-labelled blots. Biotechniques, 5, 672-678.
83. Tautz, D. and Pfeifle, C. (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosome, 98, 81-85.
84. Technau, G. and Heisenberg, M. (1982) Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature, 295, 405-407.
85. Trimmer, B. A. (1995) Current excitement from insect muscarinic receptors. Trends Neurosci., 18, 104-111.
86. Truman, J. W. (1990) Metamorphosis of the central nervous system of Drosophila. J. Neurobiol., 21, 1072-1084.
87. Valles, A. M. and White, K. (1988) Serotonin-containing neurons in Drosophila melanogaster: development and distribution. J. Comp. Neurol., 268, 414-428.
88. Venter, J. C., DiPorzio, U., Robinson, D. A., Shreeve, S. M., Lai, J., Kerlavage, A. R., Fracek, S. P. Jr., Lentes, K.-U. and Fraser, C. M. (1988) Evolution of neurotransmitter receptor systems. Prog. Neurobiol., 30, 105-169
89. Wadsworth, S. C., Rosenthal, L. S., Kammermeyer, K. L., Potter, M. B. and Nelson, D. J. (1988) Expression of a Drosophila melanogaster acetylcholine receptor-related gene in the central nervous system. Mol. Cell. Biol., 8, 778-785.
90. Zheng, W., Feng, G., Ren, D., Eberl, D. F., Hannan, F., Dubald, M. and Hall, L. M. (1995) Cloning and characterization of a calcium channel α1 subunit from Drosophila melanogaster with similarity to the rat brain type D isoform. J. Neurosci., 15, 1132-1143.