A pair of dopamine neurons target the D1-like dopamine receptor dopr in the central complex to promote ethanol-stimulated locomotion in drosophila

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Kong, Eric C ^a   Woo, Katherine ^b   Li, Haiyan ^c   Lebestky, Tim ^d   Mayer, Nasima ^b   Sniffen, Melissa R ^b   Heberlein, Ulrike ^a,b   Bainton, Roland J ^b   Hirsh, Jay ^c   Wolf, Fred W ^a  

^a UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; DOPAMINE 1 RECEPTOR; TETANUS TOXIN; TRANSCRIPTION FACTOR GAL4; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; CENTRAL DEPRESSANT AGENT; DOPAMINE; DOPAMINE RECEPTOR; DOPR PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DROSOPHILA; HYPERACTIVITY; INNERVATION; LOCOMOTION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEDATION; SIGNAL TRANSDUCTION; STARTLE REFLEX; TRANSPOSON; ANIMAL; ANIMAL BEHAVIOR; DRUG EFFECT; METABOLISM; MOTOR ACTIVITY; NERVE CELL; PHYSIOLOGY;

MAMMALIA;

ANIMALS; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DOPAMINE; DROSOPHILA; DROSOPHILA PROTEINS; ETHANOL; LOCOMOTION; MOTOR ACTIVITY; NEURONS; RECEPTORS, DOPAMINE;

EID: 77956157366     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009954     Document Type: Article

References (78)

1. Mayfield RD, Harris RA, Schuckit MA (2008) Genetic factors influencing alcohol dependence. Br J Pharmacol 154: 275-287.
2. Risinger FO, Malott DH, Prather LK, Niehus DR, Cunningham CL (1994) Motivational properties of ethanol in mice selectively bred for ethanolinduced locomotor differences. Psychopharmacology (Berl) 116: 207-216.
3. Waller MB, Murphy JM, McBride WJ, Lumeng L, Li TK (1986) Effect of low dose ethanol on spontaneous motor activity in alcohol-preferring and-nonpreferring lines of rats. Pharmacol Biochem Behav 24: 617-623.
4. Berridge KC (2007) The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl) 191: 391-431.
5. Fields HL, Hjelmstad GO, Margolis EB, Nicola SM (2007) Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 30: 289-316.
6. El-Ghundi M, George SR, Drago J, Fletcher PJ, Fan T, et al. (1998) Disruption of dopamine D1 receptor gene expression attenuates alcohol-seeking behavior. Eur J Pharmacol 353: 149-158.
7. Gonzales RA, Job MO, Doyon WM (2004) The role of mesolimbic dopamine in the development and maintenance of ethanol reinforcement. Pharmacol Ther 103: 121-146.
8. Phillips TJ, Brown KJ, Burkhart-Kasch S, Wenger CD, Kelly MA, et al. (1998) Alcohol preference and sensitivity are markedly reduced in mice lacking dopamine D2 receptors. Nat Neurosci 1: 610-615.
9. Wolf FW, Heberlein U (2003) Invertebrate models of drug abuse. J Neurobiol 54: 161-178.
10. Moore MS, DeZazzo J, Luk AY, Tully T, Singh SM, et al. (1998) Ethanol Intoxication in Drosophila: Genetic and Pharmacological Evidence for Regulation by the cAMP Signaling Pathway. Cell 93: 997-1007.
11. Wolf FW, Rodan AR, Tsai LT, Heberlein U (2002) High-resolution analysis of ethanol-induced locomotor stimulation in Drosophila. J Neurosci 22: 11035-11044.
12. Berger KH, Heberlein U, Moore MS (2004) Rapid and chronic: two distinct forms of ethanol tolerance in Drosophila. Alcohol Clin Exp Res 28: 1469-1480.
13. Kong EC, Allouche L, Chapot PA, Vranizan K, Moore MS, et al. (2009) Ethanol-Regulated Genes That Contribute to Ethanol Sensitivity and Rapid Tolerance in Drosophila. Alcohol Clin Exp Res.
14. Scholz H, Ramond J, Singh CM, Heberlein U (2000) Functional ethanol tolerance in Drosophila. Neuron 28: 261-271.
15. Devineni AV, Heberlein U (2009) Preferential ethanol consumption in Drosophila models features of addiction. Curr Biol 19: 2126-2132.
16. Bainton RJ, Tsai LT-Y, Singh CM, Moore MS, Neckameyer WS, et al. (2000) Dopamine modulates acute responses to cocaine, nicotine, and ethanol in Drosophila. Curr Biol 10: 187-194.
17. Chang HY, Grygoruk A, Brooks ES, Ackerson LC, Maidment NT, et al. (2006) Overexpression of the Drosophila vesicular monoamine transporter increases motor activity and courtship but decreases the behavioral response to cocaine. Mol Psychiatry 11: 99-113.
18. Li H, Chaney S, Forte M, Hirsh J (2000) Ectopic G-protein expression in dopmaine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster. Curr Biol 11: 211-214.
19. Andretic R, van Swinderen B, Greenspan RJ (2005) Dopaminergic modulation of arousal in Drosophila. Curr Biol 15: 1165-1175.
20. Friggi-Grelin F, Coulom H, Meller M, Gomez D, Hirsh J, et al. (2003) Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J Neurobiol 54: 618-627.
21. Kim YC, Lee HG, Han KA (2007) D1 dopamine receptor dDA1 is required in the mushroom body neurons for aversive and appetitive learning in Drosophila. J Neurosci 27: 7640-7647.
22. Kume K, Kume S, Park SK, Hirsh J, Jackson FR (2005) Dopamine is a regulator of arousal in the fruit fly. J Neurosci 25: 7377-7384.
23. Neckameyer WS (1998) Dopamine and mushroom bodies in Drosophila: experience-dependent and-independent aspects of sexual behavior. Learn Mem 5: 157-165.
24. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, et al. (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23: 10495-10502.
25. Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H, et al. (2009) Writing memories with light-addressable reinforcement circuitry. Cell 139: 405-415.
26. Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, et al. (2009) A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139: 416-427.
27. Lebestky T, Chang JS, Dankert H, Zelnik L, Kim YC, et al. (2009) Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64: 522-536.
28. Riemensperger T, Voller T, Stock P, Buchner E, Fiala A (2005) Punishment prediction by dopaminergic neurons in Drosophila. Curr Biol 15: 1953-1960.
29. Mao Z, Davis RL (2009) Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front Neural Circuits 3: 5.
30. Nassel 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.
31. Sweeney ST, Broadie K, Keane J, Niemann H, O'Kane CJ (1995) Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14: 341-351.
32. Thimgan MS, Berg JS, Stuart AE (2006) Comparative sequence analysis and tissue localization of members of the SLC6 family of transporters in adult Drosophila melanogaster. J Exp Biol 209: 3383-3404.
33. Johnson WA, McCormick CA, Bray SJ, Hirsh J (1989) A neuron-specific enhancer of the Drosophila dopa decarboxylase gene. Genes Dev 3: 676-686.
34. Budnik V, White K (1988) Catecholamine-containing neurons in Drosophila melanogaster: distribution and development. J Comp Neurol 268: 400-413.
35. Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, et al. (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454: 217-220.
36. Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12: 633-638.
37. Urizar NL, Yang Z, Edenberg HJ, Davis RL (2007) Drosophila homer is required in a small set of neurons including the ellipsoid body for normal ethanol sensitivity and tolerance. J Neurosci 27: 4541-4551.
38. Strauss R, Heisenberg M (1993) A higher control center of locomotor behavior in the Drosophila brain. Journal of Neuroscience J Neurosci 13: 1852-1861.
39. Martin JR, Ernst R, Heisenberg M (1998) Mushroom bodies suppress locomotor activity in Drosophila melanogaster. Learn Mem 5: 179-191.
40. Rodan AR, Kiger JA, Jr., Heberlein U (2002) Functional dissection of neuroanatomical loci regulating ethanol sensitivity in Drosophila. J Neurosci 22: 9490-9501.
41. Zars T, Fischer M, Schulz R, Heisenberg M (2000) Localization of a short-term memory in Drosophila. Science 288: 672-675.
42. Booker R, Quinn WG (1981) Conditioning of leg position in normal and mutant Drosophila. Proc Natl Acad Sci USA 78: 3940-3944.
43. Konopka RJ, Kyriacou CP, Hall JC (1996) Mosaic analysis in the Drosophila CNS of circadian and courtship-song rhythms affected by a period clock mutation. J Neurogenet 11: 117-139.
44. Corl AB, Rodan AR, Heberlein U (2005) Insulin signaling in the nervous system regulates ethanol intoxication in Drosophila melanogaster. Nat Neurosci 8: 18-19.
45. Kim YC, Lee HG, Seong CS, Han KA (2003) Expression of a D1 dopamine receptor dDA1/DmDOP1 in the central nervous system of Drosophila melanogaster. Gene Expr Patterns 3: 237-245.
46. Stowers RS, Isacoff EY (2007) Drosophila huntingtin-interacting protein 14 is a presynaptic protein required for photoreceptor synaptic transmission and expression of the palmitoylated proteins synaptosome-associated protein 25 and cysteine string protein. J Neurosci 27: 12874-12883.
47. Fadda F, Rossetti ZL (1998) Chronic ethanol consumption: From neuroadaptation to neurodegeneration. Prog Neurobiol 56: 385-431.
48. Gotzes F, Baumann A (1996) Functional properties of Drosophila dopamine D1-receptors are not altered by the size of the N-terminus. Biochem Biophys Res Commun 222: 121-126.
49. Xu M, Hu XT, Cooper DC, Moratalla R, Graybiel AM, et al. (1994) Elimination of cocaine-induced hyperactivity and dopamine-mediated neurophysiological effects in dopamine D1 receptor mutant mice. Cell 79: 945-955.
50. Neckameyer W, O'Donnell J, Huang Z, Stark W (2001) Dopamine and sensory tissue development in Drosophila melanogaster. J Neurobiol 47: 280-294.
51. Hanesch U, Fishbach K-F, Heisenberg M (1989) Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 257: 343-366.
52. Ito K, Suzuki K, Estes P, Ramaswami M, Yamamoto D, et al. (1998) The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learning and Memory Learn Mem 5: 52-77.
53. Meyer PJ, Meshul CK, Phillips TJ (2009) Ethanol-and cocaine-induced locomotion are genetically related to increases in accumbal dopamine. Genes Brain Behav 8: 346-355.
54. Borue X, Condron B, Jill Venton B (2010) Both synthesis and reuptake are critical for replenishing the releasable serotonin pool in Drosophila. J Neurochem doi:10.1111/j.1471-4159.2010.06588.x.
55. Martin JR, Raabe T, Heisenberg M (1999) Central complex substructures are required for the maintenance of locomotor activity in Drosophila melanogaster. J Comp Physiol [A] 185: 277-288.
56. Ilius M, Wolf R, Heisenberg M (2007) The central complex of Drosophila melanogaster is involved in flight control: studies on mutants and mosaics of the gene ellipsoid body open. J Neurogenet 21: 321-338.
57. Neuser K, Triphan T, Mronz M, Poeck B, Strauss R (2008) Analysis of a spatial orientation memory in Drosophila. Nature 453: 1244-1247.
58. Wang Z, Pan Y, Li W, Jiang H, Chatzimanolis L, et al. (2008) Visual pattern memory requires foraging function in the central complex of Drosophila. Learn Mem 15: 133-142.
59. Wu CL, Xia S, Fu TF, Wang H, Chen YH, et al. (2007) Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body. Nat Neurosci 10: 1578-1586.
60. Lima SQ, Miesenbock G (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121: 141-152.
61. Feng G, Hannan F, Reale V, Hon YY, T. KC, et al. (1996) Cloning and functional characterization of a novel dopamine receptor from Drosophila melanogaster. J Neurosci 16: 3925-3933.
62. Han KA, Millar NS, Grotewiel MS, Davis RL (1996) DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron 16: 1127-1135.
63. Hearn MG, Ren Y, McBride EW, Reveillaud I, Beinborn M, et al. (2002) A Drosophila dopamine 2-like receptor: Molecular characterization and identification of multiple alternatively spliced variants. Proc Natl Acad Sci U S A 99: 14554-14559.
64. Srivastava DP, Yu EJ, Kennedy K, Chatwin H, Reale V, et al. (2005) Rapid, nongenomic responses to ecdysteroids and catecholamines mediated by a novel Drosophila G-protein-coupled receptor. J Neurosci 25: 6145-6155.
65. Crabbe JC, Phillips TJ, Harris RA, Arends MA, Koob GF (2006) Alcoholrelated genes: contributions from studies with genetically engineered mice. Addict Biol 11: 195-269.
66. Tupala E, Tiihonen J (2004) Dopamine and alcoholism: neurobiological basis of ethanol abuse. Prog Neuropsychopharmacol Biol Psychiatry 28: 1221-1247.
67. Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29: 565-598.
68. Szumlinski KK, Ary AW, Lominac KD (2008) Homers regulate drug-induced neuroplasticity: implications for addiction. Biochem Pharmacol 75: 112-133.
69. Daniels RW, Gelfand MV, Collins CA, DiAntonio A (2008) Visualizing glutamatergic cell bodies and synapses in Drosophila larval and adult CNS. J Comp Neurol 508: 131-152.
70. Enell L, Hamasaka Y, Kolodziejczyk A, Nassel DR (2007) gamma-Aminobutyric acid (GABA) signaling components in Drosophila: immunocytochemical localization of GABA(B) receptors in relation to the GABA(A) receptor subunit RDL and a vesicular GABA transporter. J Comp Neurol 505: 18-31.
71. Amalric M, Koob GF (1993) Functionally selective neurochemical afferents and efferents of the mesocorticolimbic and nigrostriatal dopamine system. Prog Brain Res 99: 209-226.
72. Di Chiara G, Imperato A (1986) Preferential stimulation of dopamine release in the nucleus accumbens by opiates, alcohol, and barbiturates: studies with transcerebral dialysis in freely moving rats. Ann N Y Acad Sci 473: 367-381.
73. Rocha BA, Fumagalli F, Gainetdinov RR, Jones SR, Ator R, et al. (1998) Cocaine self-administration in dopamine-transporter knockout mice. Nat Neurosci 1: 132-137.
74. Sora I, Wichems C, Takahashi N, Li X-F, Zeng Z, et al. (1998) Cocaine reward models: Conditioned place preference can be established in dopamine-and in serotonin-transporter knockout mice. Proc Natl Acad Sci USA 95: 7699-7704.
75. Morgan BA, Johnson WA, Hirsh J (1986) Regulated splicing produces different forms of dopa decarboxylase in the central nervous system and hypoderm of Drosophila melanogaster. Embo J 5: 3335-3342.
76. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
77. Rubin GM, Spradling AC (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218: 348-353.
78. Spradling AC, Rubin GM (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218: 341-347.