The nicotinic acetylcholine receptor Da7 is required for an escape behavior in Drosophila

PLoS Biology

Volumn 4, Issue 3, 2006, Pages 0420-0431

  Fayyazuddin, Amir ^a   Zaheer, Mahira A ^a   Hiesinger, P Robin ^a   Bellen, Hugo J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINIC RECEPTOR; RECEPTOR SUBUNIT; COMPLEMENTARY DNA; DROSOPHILA PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; NACRALPHA 18C PROTEIN, DROSOPHILA; NACRALPHA-18C PROTEIN, DROSOPHILA;

ANALYTIC METHOD; ARTICLE; CHOLINERGIC SYNAPSE; DENDRITE; DROSOPHILA; ELECTROPHYSIOLOGY; ESCAPE BEHAVIOR; GENE FREQUENCY; GENE MUTATION; GENETIC SCREENING; MOTONEURON; MUTANT; NERVE CELL NETWORK; NONHUMAN; PROTEIN FUNCTION; SENSORY STIMULATION; SIGNAL TRANSDUCTION; ALLELE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; GENOME; METABOLISM; MOLECULAR CLONING; MUTATION; PHYSIOLOGY; PROTEIN QUATERNARY STRUCTURE; SYNAPSE;

HEXAPODA;

ALLELES; ANIMALS; CLONING, MOLECULAR; DENDRITES; DNA, COMPLEMENTARY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ELECTROPHYSIOLOGY; ESCAPE REACTION; GENE EXPRESSION REGULATION; GENOME, INSECT; GLIAL FIBRILLARY ACIDIC PROTEIN; MODELS, MOLECULAR; MUTATION; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, NICOTINIC; SYNAPSES;

EID: 33644986233     PISSN: 15457885     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0040063     Document Type: Article

References (56)

1. Grauso M, Reenan RA, Culetto E, Sattelle DB (2002) Novel putative nicotinic acetylcholine receptor subunit genes, Dα5, Dα6 and Dα7, in Drosophila melanogaster identify a new and highly conserved target of adenosine deaminase acting on RNA-mediated A-to-I pre-mRNA editing. Genetics 160: 1519-1533.
2. Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain α7: A nicotinic cation channel highly permeable to calcium. J Neurosci 13: 596-604.
3. Couturier S, Bertrand D, Matter JM, Hernandez MC, Bertrand S, et al. (1990) A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5: 847-856.
4. Ballivet M, Alliod C, Bertrand S, Bertrand D (1996) Nicotinic acetylcholine receptors in the nematode Caenorhabditis elegans. J Mol Biol 258: 261-269.
5. Wyman RJ, Thomas JB, Salkoff L, King DG (1984) The Drosophila giant fiber system. In: Eaton RC, editor. Neural mechanisms of startle behavior. New York: Plenum Press. pp. 133-161.
6. Bacon JP, Strausfeld NJ (1986) The dipteran "Giant fibre" pathway: Neurons and signals. J Comp Physiol [A] 158: 529-548.
7. Holmqvist MH (1994) A visually elicited escape response in the fly that does not use the giant fiber pathway. Vis Neurosci 11: 1149-1161.
8. Milde JJ, Strausfeld NJ (1990) Cluster organization and response characteristics of the giant fiber pathway of the blowfly Calliphora erythrocephala. J Comp Neurol 294: 59-75.
9. Fischbach KF, Dittrich APM (1989) The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258: 441-475.
10. Hausen K, Strausfeld NJ (1980) Sexually dimorphic interneuron arrangements in the fly visual system. Proc R Soc Lond B 208: 57-71.
11. Gilbert C, Strausfeld NJ (1991) The functional organization of male-specific visual neurons in flies. J Comp Physiol [A] 169: 395-411.
12. Strausfeld NJ, Bassemir UK (1983) Cobalt-coupled neurons of a giant fibre system in Diptera. J Neurocytol 12: 971-991.
13. Yasuyama K, Salvaterra PM (1999) Localization of choline acetyltransferase-expressing neurons in Drosophila nervous system. Microsc Res Tech 45: 65-79.
14. Pringle JWS (1957) Insect flight. Cambridge: Cambridge University Press.
15. Gorczyca M, 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.
16. Harcombe ES, Wyman RJ (1977) Output pattern generation by Drosophila flight motoneurons. J Neurophysiol 40: 1066-1077.
17. Koenig JH, Ikeda K (1983) Reciprocal excitation between identified flight motor neurons in Drosophila and its effect on pattern generation. J Comp Physiol A 150: 305-317.
18. Wang D, Keng ZC, Hsu K, Tan CC (1989) Drosophila mutants with progressive atrophy in dorsal longitudinal muscles. J Neurogenet 6: 27-39.
19. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
20. Lansdell SJ, Millar NS (2004) Molecular characterization of Dα6 and Dα7 nicotinic acetylcholine receptor subunits from Drosophila: Formation of a high-affinity α-bungarotoxin binding site revealed by expression of subunit chimeras. J Neurochem 90: 479-489.
21. Bellen HJ, Levis RW, Liao G, He Y, Carlson JW, et al. (2004) The BDGP gene disruption project: Single transposon insertions associated with 40% of Drosophila genes. Genetics 167: 761-781.
22. Hayashi S, Ito K, Sado Y, Taniguchi M, Akimoto A, et al. (2002) GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 34: 58-61.
23. Sepp KJ, Auld VJ (1999) Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. Genetics 151: 1093-1101.
24. Drummond DR, Hennessey ES, Sparrow JC (1991) Characterisation of missense mutations in the Act88F gene of Drosophila melanogaster. Mol Gen Genet 226: 70-80.
25. Nelson HB, Heiman RG, Bolduc C, Kovalick GE, Whitley P, et al. (1997) Calmodulin point mutations affect Drosophila development and behavior. Genetics 147: 1783-1798.
26. Woodard C, Huang T, Sun H, Helfand SL, Carlson J (1989) Genetic analysis of olfactory behavior in Drosophila: A new screen yields the ota mutants. Genetics 123: 315-326.
27. Alawi AA, Pak WL (1971) On-transient of insect electroretinogram: Its cellular origin. Science 172: 1055-1057.
28. Greenspan RJ, Finn JA Jr., Hall JC (1980) Acetylcholinesterase mutants in Drosophila and their effects on the structure and function of the central nervous system. J Comp Neurol 189: 741-774.
29. Benzer S (1967) Behavioral mutants of Drosophila isolated by counter-current distribution. Proc Natl Acad Sci U S A 58: 1112-1119.
30. Connolly JB, Tully T (1998) Behaviour, learning, and memory. In: Roberts DB, editor. Drosophila. 2nd ed. Oxford: Oxford University Press. pp. 265-317.
31. Thomas JB, Wyman RJ (1984) Mutations altering synaptic connectivity between identified neurons in Drosophila. J Neurosci 4: 530-538.
32. Allen MJ, Drummond JA, Moffat KG (1998) Development of the giant fiber neuron of Drosophila melanogaster. J Comp Neurol 397: 519-531.
33. Unwin N (2003) Structure and action of the nicotinic acetylcholine receptor explored by electron microscopy. FEBS Lett 555: 91-95.
34. Lester HA, Dibas MI, Dahan DS, Leite JF, Dougherty DA (2004) Cys-loop receptors: New twists and turns. Trends Neurosci 27: 329-336.
35. Unwin N (2005) Refined structure of the nicotinic acetylcholine receptor at 4Å resolution. J Mol Biol 346: 967-989.
36. Engel AG, Sine SM (2005) Current understanding of congenital myasthenic syndromes. Curr Opin Pharmacol 5: 308-321.
37. King DG, Wyman RJ (1980) Anatomy of the giant fibre pathway in Drosophila. I. Three thoracic components of the pathway. J Neurocytol 9: 753-770.
38. Egger MD, Nowakowski RS, Peng B, Wyman RJ (1997) Patterns of connectivity in a Drosophila nerve. J Comp Neurol 387: 63-72.
39. Fayyazuddin A, Dickinson MH (1999) Convergent mechanosensory input structures the firing phase of a steering motor neuron in the blowfly, Calliphora. J Neurophysiol 82: 1916-1926.
40. Douglass JK, Strausfeld NJ (2003) Anatomical organization of retinotopic motion-sensitive pathways in the optic lobes of flies. Microsc Res Tech 62: 132-150.
41. Levine JD, Tracey D (1973) Structure and function of the giant motorneuron of Drosophila melanogaster. J Comp Physiol 87: 213-235.
42. Trimarchi JR, Schneiderman AM (1993) Giant fiber activation of an intrinsic muscle in the mesothoracic leg of Drosophila melanogaster. J Exp Biol 177: 149-167.
43. Lin M, Nash HA (1996) Influence of general anesthetics on a specific neural pathway in Drosophila melanogaster. Proc Natl Acad Sci U S A 93: 10446-10451.
44. Tanouye MA, Wyman RJ (1980) Motor outputs of giant nerve fiber in Drosophila. J Neurophysiol 44: 405-421.
45. Engel JE, Wu CF (1996) Altered habituation of an identified escape circuit in Drosophila memory mutants. J Neurosci 16: 3486-3499.
46. Godenschwege TA, Simpson JH, Shan X, Bashaw GJ, Goodman CS, et al. (2002) Ectopic expression in the giant fiber system of Drosophila reveals distinct roles for roundabout (Robo), Robo2, and Robo3 in dendritic guidance and synaptic connectivity. J Neurosci 22: 3117-3129.
47. Sala F, Mulet J, Sala S, Gerber S, Criado M (2005) Charged amino acids of the N-terminal domain are involved in coupling binding and gating in a7 nicotinic receptors. J Biol Chem 280: 6642-6647.
48. Schuster R, Phannavong B, Schroder C, Gundelfinger ED (1993) Immunohistochemical localization of a ligand-binding and a structural subunit of nicotinic acetylcholine receptors in the central nervous system of Drosophila melanogaster. J Comp Neurol 335: 149-162.
49. Xu W, Orr-Urtreger A, Nigro F, Gelber S, Sutcliffe CB, et al. (1999) Multiorgan autonomic dysfunction in mice lacking the β2 and the β4 subunits of neuronal nicotinic acetylcholine receptors. J Neurosci 19: 9298-9305.
50. Marubio LM, Paylor R (2004) Impaired passive avoidance learning in mice lacking central neuronal nicotinic acetylcholine receptors. Neuroscience 129: 575-582.
51. Cavener DR (1987) Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res 15: 1353-1361.
52. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
53. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
54. Levine JD, Hughes M (1973) Stereotaxic map of the muscle fibers in the indirect flight muscles of Drosophila melanogaster. J Morphology 140: 153-158.
55. Baines RA, Bate M (1998) Electrophysiological development of central neurons in the Drosophila embryo. J Neurosci 18: 4673-4683.
56. Humphrey W, Dalke A, Schulten K (1996) VMD: Visual molecular dynamics. J Mol Graph 14: 27-38.