The propensity for consuming ethanol in Drosophila requires rutabaga adenylyl cyclase expression within mushroom body neurons

Genes, Brain and Behavior

Volumn 11, Issue 6, 2012, Pages 727-739

  Xu, S ^a   Chan, T ^b,c   Shah, V ^a   Zhang, S ^a   Pletcher, S D ^b,c   Roman, G ^a,d  

^a University of Houston   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d UNIVERSITY OF HOUSTON   (United States)

Author keywords

CAMP; Drosophila; Ethanol self administration; Learning; Mushroom body

Indexed keywords

ADENYLATE CYCLASE; ALCOHOL; SUGAR;

ALCOHOL CONSUMPTION; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APPETITE; ARTICLE; AVERSIVE BEHAVIOR; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; FEMALE; FOOD PREFERENCE; MALE; MUSHROOM BODY; NERVE CELL; NONHUMAN; OLFACTORY MEMORY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REINFORCEMENT; RUTABAGA; WILD TYPE;

ADENYLATE CYCLASE; ALCOHOL DRINKING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ETHANOL; FEEDING BEHAVIOR; FEMALE; MALE; MUSHROOM BODIES; NEURONS; REINFORCEMENT (PSYCHOLOGY);

BASIDIOMYCOTA; BRASSICA NAPUS VAR. NAPOBRASSICA; DROSOPHILA MELANOGASTER;

EID: 84864145151     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2012.00810.x     Document Type: Article

References (48)

1. Aso, Y., Grubel, K., Busch, S., Friedrich, A.B., Siwanowicz, I. & Tanimoto, H. (2009) The mushroom body of adult Drosophila characterized by GAL4 drivers. J Neurogenet 23, 156-172.
2. Belknap, J.K., Crabbe, J.C. & Young, E.R. (1993) Voluntary consumption of ethanol in 15 inbred mouse strains. Psychopharmacology (Berl) 112, 503-510.
3. Blum, A.L., Li, W., Cressy, M. & Dubnau, J. (2009) Short- and long-term memory in Drosophila require cAMP signaling in distinct neuron types. Curr Biol 19, 1341-1350.
4. Burke, C.J. & Waddell, S. (2011) Remembering nutrient quality of sugar in Drosophila. Curr Biol 21, 746-750.
5. Byers, D., Davis, R.L. & Kiger, J.A. Jr. (1981) Defect in cyclic AMP phosphodiesterase due to the dunce mutation of learning in Drosophila melanogaster. Nature 289, 79-81.
6. Cicero, T. (1980) Alcohol self-administration, tolerance, and withdrawal in humans and animals: theoretical and methodological issues. In Rigter, H. & Crabbe, J. (eds), Alcohol Tolerance and Dependence. Elsvier/North Holland Biomedical Press, Amsterdam, pp. 1-51.
7. Colomb, J., Kaiser, L., Chabaud, M.A. & Preat, T. (2009) Parametric and genetic analysis of Drosophila appetitive long-term memory and sugar motivation. Genes Brain Behav 8, 407-415.
8. Devineni, A.V. & Heberlein, U. (2009) Preferential ethanol consumption in Drosophila models features of addiction. Curr Biol 19, 2126-2132.
9. Feany, M.B. & Quinn, W.G. (1995) A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science 268, 869-873.
10. Fujita, M. & Tanimura, T. (2011) Drosophila evaluates and learns the nutritional value of sugars. Curr Biol 21, 751-755.
11. Gervasi, N., Tchenio, P. & Preat, T. (2010) PKA dynamics in a Drosophila learning center: coincidence detection by rutabaga adenylyl cyclase and spatial regulation by dunce phosphodiesterase. Neuron 65, 516-529.
12. Gibson, J.B., May, T.W. & Wilks, A.V. (1981) Genetic variation at the alcohol dehydrogenase locus in Drosophila melanogaster in relation to environmental variation: ethanol levels in breeding sites and allozyme frequencies. Oecologia 51, 191-198.
13. Ja, W.W., Carvalho, G.B., Mak, E.M., de la Rosa, N.N., Fang, A.Y., Liong, J.C., Brummel, T. & Benzer, S. (2007) Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci U S A 104, 8253-8256.
14. Kaun, K.R., Azanchi, R., Maung, Z., Hirsh, J. & Heberlein, U. (2011) A Drosophila model for alcohol reward. Nat Neurosci 14, 612-619.
15. Kim, M.S., Repp, A. & Smith, D.P. (1998) LUSH odorant-binding protein mediates chemosensory responses to alcohols in Drosophila melanogaster. Genetics 150, 711-721.
16. Kim, M.S. & Smith, D.P. (2001) The invertebrate odorant-binding protein LUSH is required for normal olfactory behavior in Drosophila. Chem Senses 26, 195-199.
17. Kimura, K., Shimoawa, T. & Tanimura, T. (1986) Muscle degeneration in the posteclosional development of a Drosophila mutant, abnormal proboscis extension reflex C (aperC). Dev Biol 117, 194-203.
18. King, I., Tsai, L.T., Pflanz, R., Voigt, A., Lee, S., Jackle, H., Lu, B. & Heberlein, U. (2011) Drosophila tao controls mushroom body development and ethanol-stimulated behavior through par-1. J Neurosci 31, 1139-1148.
19. Krashes, M.J., Keene, A.C., Leung, B., Armstrong, J.D. & Waddell, S. (2007) Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53, 103-115.
20. Larsson, M.C., Domingos, A.I., Jones, W.D., Chiappe, M.E., Amrein, H. & Vosshall, L.B. (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703-714.
21. Laughlin, J.D., Ha, T.S., Jones, D.N. & Smith, D.P. (2008) Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133, 1255-1265.
22. Levin, L.R., Han, P.L., Hwang, P.M., Feinstein, P.G., Davis, R.L. & Reed, R.R. (1992) The Drosophila learning and memory gene rutabaga encodes a Ca2+/Calmodulin-responsive adenylyl cyclase. Cell 68, 479-489.
23. Libert, S., Zwiener, J., Chu, X., Vanvoorhies, W., Roman, G. & Pletcher, S.D. (2007) Regulation of Drosophila life span by olfaction and food-derived odors. Science 315, 1133-1137.
24. Liu, G., Seiler, H., Wen, A., Zars, T., Ito, K., Wolf, R., Heisenberg, M. & Liu, L. (2006) Distinct memory traces for two visual features in the Drosophila brain. Nature 439, 551-556.
25. Maas, J.W. Jr. Vogt, S.K., Chan, G.C., Pineda, V.V., Storm, D.R. & Muglia, L.J. (2005) Calcium-stimulated adenylyl cyclases are critical modulators of neuronal ethanol sensitivity. J Neurosci 25, 4118-4126.
26. Masek, P. & Scott, K. (2010) Limited taste discrimination in Drosophila. Proc Natl Acad Sci U S A 107, 14833-14838.
27. Moore, M.S., DeZazzo, J., Luk, A.Y., Tully, T., Singh, C.M. & Heberlein, U. (1998) Ethanol intoxication in Drosophila: Genetic and pharmacological evidence for regulation by the cAMP signaling pathway. Cell 93, 997-1007.
28. Morse, R.M. & Flavin, D.K. (1992) The definition of alcoholism. The Joint Committee of the National Council on Alcoholism and Drug Dependence and the American Society of Addiction Medicine to Study the Definition and Criteria for the Diagnosis of Alcoholism. JAMA 268, 1012-1014.
29. Ofstad, T.A., Zuker, C.S. & Reiser, M.B. (2011) Visual place learning in Drosophila melanogaster. Nature 474, 204-207.
30. Osterwalder, T., Yoon, K.S., White, B.H. & Keshishian, H. (2001) A conditional tissue-specific transgene expression system using inducible GAL4. Proc Natl Acad Sci U S A 98, 12596-12601.
31. Rodd, Z.A., Bell, R.L., Sable, H.J., Murphy, J.M. & McBride, W.J. (2004) Recent advances in animal models of alcohol craving and relapse. Pharmacol Biochem Behav 79, 439-450.
32. Roman, G. (2004) The genetics of Drosophila transgenics. Bioessays 26, 1243-1253.
33. Roman, G. & Davis, R.L. (2002) Conditional expression of UAS-transgenes in the adult eye with a new gene-switch vector system. Genesis 34, 127-131.
34. Roman, G., Endo, K., Zong, L. & Davis, R.L. (2001) P[Switch], a system for spatial and temporal control of gene expression in Drosophila melanogaster. Proc Natl Acad Sci U S A 98, 12602-12607.
35. Schwaerzel, M., Monastirioti, M., Scholz, H., Friggi-Grelin, F., Birman, S. & Heisenberg, M. (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23, 10495-10502.
36. Stocker, R.F., Heimbeck, G., Gendre, N. & de Belle, J.S. (1997) Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J Neurobiol 32, 443-456.
37. Tempel, B.L., Bonini, N., Dawson, D.R. & Quinn, W.G. (1983) Reward learning in normal and mutant Drosophila. Proc Natl Acad Sci U S A 80, 1482-1486.
38. Thiele, T.E., Willis, B., Stadler, J., Reynolds, J.G., Bernstein, I.L. & McKnight, G.S. (2000) High ethanol consumption and low sensitivity to ethanol-induced sedation in protein kinase A-mutant mice. J Neurosci 20, RC75.
39. Thum, A.S., Jenett, A., Ito, K., Heisenberg, M. & Tanimoto, H. (2007) Multiple memory traces for olfactory reward learning in Drosophila. J Neurosci 27, 11132-11138.
40. Tomchik, S.M. & Davis, R.L. (2009) Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron 64, 510-521.
41. Tully, T. & Quinn, W.G. (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol [A] 157, 263-277.
42. Wand, G., Levine, M., Zweifel, L., Schwindinger, W. & Abel, T. (2001) The cAMP-protein kinase A signal transduction pathway modulates ethanol consumption and sedative effects of ethanol. J Neurosci 21, 5297-5303.
43. Wolf, F.W., Rodan, A.R., Tsai, L.T. & Heberlein, U. (2002) High-resolution analysis of ethanol-induced locomotor stimulation in Drosophila. J Neurosci 22, 11035-11044.
44. Wu, J.S. & Luo, L. (2006) A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat Protoc 1, 2110-2115.
45. Zars, T. (2011) Short-term memories in Drosophila are governed by general and specific genetic systems. Learn Mem 17, 246-251.
46. Zars, T., Fischer, M., Schulz, R. & Heisenberg, M. (2000a) Localization of a short-term memory in Drosophila. Science 288, 672-675.
47. Zars, T., Wolf, R., Davis, R. & Heisenberg, M. (2000b) Tissue-specific expression of a type I adenylyl cyclase rescues the rutabaga mutant memory defect: in search of the engram. Learn Mem 7, 18-31.
48. Zhong, Y. & Wu, C.F. (1993) Differential modulation of potassium currents by cAMP and its long-term and short-term effects: dunce and rutabaga mutants of Drosophila. J Neurogenet 9, 15-27.