Perception of sweet taste is important for voluntary alcohol consumption in mice

Genes, Brain and Behavior

Volumn 7, Issue 1, 2008, Pages 1-13

  Blednov, Y A ^a   Walker, D ^a   Martinez, M ^a   Levine, M ^a   Damak, S ^b   Margolskee, R F ^b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

gustducin; Alcohol intake; Knockout mice; Tas1r3; Trpm5

Indexed keywords

ALCOHOL; QUININE; SACCHARIN; SODIUM CHLORIDE;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; RIGHTING REFLEX; SWEETNESS; TASTE; TASTE AVERSION; TASTE BUD;

ALCOHOL DRINKING; ANIMALS; AVOIDANCE LEARNING; CONDITIONING, CLASSICAL; CROSSES, GENETIC; FEMALE; HETEROTRIMERIC GTP-BINDING PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, MUTANT STRAINS; QUININE; RECEPTORS, G-PROTEIN-COUPLED; SACCHARIN; TASTE; TRPM CATION CHANNELS;

MUS;

EID: 38349026426     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2007.00309.x     Document Type: Article

References (77)

1. Artigas, A.A., Sansa, J., Blair, C.A.J., Hall, G. Prados, J 2006) Enhanced discrimination between flavor stimuli: roles of salience modulation and inhibition. J Exp Psychol Anim Behav Process 32, 173 177.
2. Bachmanov, A.A., Reed, D.R., Tordoff, M.G., Price, R.A. Beauchamp, G.K 1996) Intake of ethanol, sodium chloride, sucrose, citric acid, and quinine hydrochloride solutions by mice: a genetic analysis. Behav Genet 26, 563 573.
3. Bachmanov, A.A., Reed, D.R., Li, X., Li, S., Beauchamp, G.K. Tordoff, M.G 2002) Voluntary ethanol consumption by mice: genome-wide analysis of quantitative trait loci and their interactions in a C57BL/6ByJ × 129P3/J F2 intercross. Genome Res 12, 1257 1268.
4. Bachmanov, A.A., Kiefer, S.W., Molina, J.C., Tordoff, M.G., Duffy, V.B., Bartoshuk, L.M. Mennella, J.A 2003) Chemosensory factors influencing alcohol perception, preferences, and consumption. Alcohol Clin Exp Res 27, 220 231.
5. Belknap, J.K., Crabbe, J.C. Young, E.R 1993) Voluntary consumption of ethanol in 15 inbred mouse strains. Psychopharmacology 112, 503 510.
6. Blednov, Y.A. Harris, R.A 2006) Why do mice drink or not drink alcohol? Lessons from null mutants. Alcohol Clin Exp Res 30 (Suppl S52.
7. Blednov, Y.A., Stoffel, M., Chang, S.R. Harris, R.A 2001) Potassium channels as targets for ethanol: studies of G-protein-coupled inwardly rectifying potassium channel 2 (GIRK2) null mutant mice. J Pharmacol Exp Ther 298, 521 530.
8. Blednov, Y.A., Walker, D., Alva, H., Creech, K., Findlay, G. Harris, R.A 2003) GABAA receptor alpha 1 and beta 2 subunit null mutant mice: behavioral responses to ethanol. J Pharmacol Exp Ther 305, 854 863.
9. Boughter, J.D., Pumplin, D.W., Yu, C., Christy, R.C. Smith, D.V 1997) Differential expression of alpha-gustducin in taste bud populations of the rat and hamster. J Neurosci 17, 2852 2858.
10. Chester, J.A. Cunningham, C.L 1998) Modulation of corticosterone does not affect the acquisition or expression of ethanol-induced conditioned place preference in DBA/2J mice. Pharmacol Biochem Behav 59, 67 75.
11. Chester, J.A. Cunningham, C.L 2002) GABA(A) receptor modulation of the rewarding and aversive effects of ethanol. Alcohol 26, 131 143.
12. Crabbe, J.C., Merrill, C. Belknap, J.K 1991) Acute dependence on depressant drugs is determined by common genes in mice. J Pharmacol Exp Ther 257, 663 667.
13. Cunningham, C.L 1993) Pavlovian drug conditioning. In van Haaren, F. (ed Methods in Behavioral Pharmacology. Elsevier, New York, pp. 349 381.
14. Damak, S., Rong, M., Yasumatsu, K., Kokrashvili, Z., Varadarajan, V., Zou, S., Jiang, P., Ninomiya, Y. Margolskee, R.F 2003) Detection of sweet and umami taste in the absence of taste receptor T1r3. Science 301, 850 853.
15. Damak, S., Rong, M., Yasumatsu, K., Kokrashvili, Z., Perez, C.A., Shigemura, N., Yoshida, R., Mosinger, B. Jr., Glendinning, J.I., Ninomiya, Y. Margolskee, R.F 2006) Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses 31, 253 264.
16. Dess, N.K., Badia-Elder, N.E., Thiele, T.E., Kiefer, S.W. Blizard, D.A 1998) Ethanol consumption in rats selectively bred for differential saccharin intake. Alcohol 16, 275 278.
17. Dudley, R 2000) Evolutionary origins of human alcoholism in primate frugivory. Q Rev Biol 75, 3 15.
18. Dudley, R 2002) Fermenting fruit and the historical ecology of ethanol ingestion: is alcoholism in modern humans an evolutionary hangover? Addiction 97, 381 388.
19. Edenberg, H.J. Foroud, T 2006) The genetics of alcoholism: identifying specific genes through family studies. Addict Biol 11, 386 396.
20. Forgie, M.L., Beyerstein, B.L. Alexander, B.K 1988) Contributions of taste factors and gender to opioid preference in C57BL and DBA mice. Psychopharmacology 95, 237 244.
21. Foroud, T., Bice, P., Castelluccio, P., Bo, R., Ritchotte, A., Stewart, R., Lumeng, L., Li, T.K. Carr, L 2002) Mapping of QTL influencing saccharin consumption in the selectively bred alcohol-preferring and -nonpreferring rat lines. Behav Genet 32, 57 67.
22. Gilbertson, T.A., Damak, S. Margolskee, R.F 2000) The molecular physiology of taste transduction. Curr Opin Neurobiol 10, 519 527.
23. Goodwin, F.L., Bergeron, N. Amit, Z 2000) Differences in the consumption of ethanol and flavored solutions in three strains of rats. Pharmacol Biochem Behav 65, 357 362.
24. Gosnell, B.A. Krahn, D.D 1992) The relationship between saccharin and alcohol intake in rats. Alcohol 9, 201 206.
25. Grigson, P.S 2000) Drugs of abuse and reward comparison: a brief review. Appetite 35, 89 91.
26. He, W., Danilova, V., Zou, S., Hellekant, G., Max, M., Margolskee, R.F. Damak, S 2002) Partial rescue of taste responses of alphagustducin null mice by transgenic expression of alpha-transducin. Chem Senses 27, 719 727.
27. He, W., Yasumatsu, K., Varadarajan, V., Yamada, A., Lem, J., Ninomiya, Y., Margolskee, R.F. Damak, S 2004) Umami taste responses are mediated by alpha-transducin and alpha-gustducin. J Neurosci 24, 7674 7680.
28. Higley, J.D. Bennett, A.J 1999) Central nervous system serotonin and personality as variables contributing to excessive alcohol consumption in non-human primates. Alcohol Alcohol 34, 402 418.
29. Hodge, C.W., Mehmert, K.K., Kelley, S.P., McMahon, T., Haywood, A., Olive, M.F., Wang, D., Sanchez-Perez, A.M. Messing, R.O 1999) Supersensitivity to allosteric GABA(A) receptor modulators and alcohol in mice lacking PKCepsilon. Nat Neurosci 2, 997 1002.
30. Hofer, D., Puschel, B. Drenckhahn, D 1996) Taste receptor-like cells in the rat gut identified by expression of alpha-gustducin. Proc Natl Acad Sci USA 93, 6631 6634.
31. Horne, J., Lawless, H.T., Speirs, W. Sposato, D 2002) Bitter taste of saccharin and acesulfame-K. Chem Senses 27, 31 38.
32. Kampov-Polevoy, A.B., Kasheffskaya O.P. Sinclair, J.D 1990) Initial acceptance of ethanol: gustatory factors and patterns of alcohol drinking. Alcohol 7, 83 85.
33. Kampov-Polevoy, A.B., Overstreet, D.H., Rezvani, A.H. Janowsky, D.S 1995) Suppression of ethanol intake in alcohol-preferring rats by prior voluntary saccharin consumption. Pharmacol Biochem Behav 52, 59 64.
34. Kampov-Polevoy, A.B., Garbutt, J.C. Janowsky, D.S 1997) Evidence of preference for a higher concentration sucrose solution in alcoholic men. Am J Psychiatry 154, 269 270.
35. Kampov-Polevoy, A.B., Garbutt, J.C. Janowsky, D.S 1999) Association between preference for sweets and excessive alcohol intake: a review of animal and human studies. Alcohol Alcohol 34, 386 395.
36. Kampov-Polevoy, A.B., Tzoi, M.V., Zvartau, E.E., Neznanov, N.G. Khalitov, E 2001) Sweet liking and family history of alcoholism in hospitalized alcoholic and non-alcoholic patients. Alcohol Alcohol 36, 165 170.
37. Kampov-Polevoy, A.B., Garbutt, J.C. Khalitov, E 2003a) Family history of alcoholism and response to sweets. Alcohol Clin Exp Res 27, 1743 1749.
38. Kampov-Polevoy, A.B., Ziedonis, D., Steinberg, M.L., Pinsky, I., Krejci, J., Eick, C., Boland, G., Khalitov, E. Crews, F.T 2003b) Association between sweet preference and paternal history of alcoholism in psychiatric and substance abuse patients. Alcohol Clin Exp Res 27, 1929 1936.
39. Kiefer, S.W 1995) Alcohol, palatability, and taste reactivity. Neurosci Biobehav Rev 19, 133 141.
40. Kiefer, S.W. Morrow, N.S 1991) Odor cue mediation of alcohol aversion learning in rats lacking gustatory neocortex. Behav Neurosci 105, 25 32.
41. Kim, M.R., Kusakabe, Y., Miura, H., Shindo, Y., Ninomiya, Y. Hino, A 2003) Regional expression patterns of taste receptors and gustducin in the mouse tongue. Biochem Biophys Res Commun 312, 500 506.
42. Kinnamon, S.C. Margolskee, R.F 1996) Mechanisms of taste transduction. Curr Opin Neurobiol 6, 506 513.
43. Kranzler, H.R., Sandstrom, K.A. Van Kirk, J 2001) Sweet preference as a risk factor for alcohol dependence. Am J Psychiatry 158, 813 815.
44. Lemon, C.H., Brasser, S.M. Smith, D.V 2004) Alcohol activates a sucrose-responsive gustatory neural pathway. J Neurophysiol 92, 536 544.
45. Lindemann, B 2001) Receptors and transduction in taste. Nature 413, 219 225.
46. Liu, D. Liman, E.R 2003) Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci USA 100, 15160 15165.
47. Lundquist, F 1959) The determination of ethyl alcohol in blood and tissue. Methods Biochem Anal 7, 217 251.
48. Lush, I.E., Hornigold, N., King, P. Stoye, J.P 1995) The genetics of tasting in mice. VII. Glycine revisited, and the chromosomal location of Sac and Soa. Genet Res 66, 167 174.
49. Margolskee, R.F 2002) Molecular mechanisms of bitter and sweet taste transduction. J Biol Chem 277, 1 4.
50. Matsunami, H., Montmayeur, J.P. Buck, L.B 2000) A family of candidate taste receptors in human and mouse. Nature 404, 601 604.
51. Mattes, R.D. DiMeglio, D 2001) Ethanol perception and ingestion. Physiol Behav 72, 217 229.
52. Max, M., Shanker, Y.G., Huang, L., Rong, M., Liu, Z., Campagne, F., Weinstein, H., Damak, S. Margolskee, R.F 2001) Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet 28, 58 63.
53. McLaughlin, S.K., McKinnon, P.J. Margolskee, R.F 1992) Gustducin is a taste-cell-specific G protein closely related to the transducins. Nature 357, 563 569.
54. Metten, P., Phillips, T.J., Crabbe, J.C., Tarantino, L.M., McClearn, G.E., Plomin, R., Erwin, V.G. Belknap, J.K 1998) High genetic susceptibility to ethanol withdrawal predicts low ethanol consumption. Mamm Genome 9, 983 990.
55. Ming, D., Ruiz-Avila, L. Margolskee, R.F 1998) Characterization and solubilization of bitter-responsive receptors that couple to gustducin. Proc Natl Acad Sci USA 95, 8933 8938
56. Mombaerts, P 2004) Genes and ligands for odorant, vomeronasal and taste receptors. Nat Rev Neurosci 5, 263 278.
57. Montmayeur, J.P. Matsunami, H 2002) Receptors for bitter and sweet taste. Curr Opin Neurobiol 12, 366 371.
58. Nurnberger, J.I. Jr., Foroud, T., Flury, L., Su, J., Meyer, E.T., Hu, K., Crowe, R., Edenberg, H., Goate, A. Bierut, L 2001) Evidence for a locus on chromosome 1 that influences vulnerability to alcoholism and affective disorder. Am. J. Psychiatry 158, 718 724.
59. Ogura, T., Margolskee, R.F. Kinnamon, S.C 2002) Taste receptor cell responses to the bitter stimulus denatonium involve Ca2+ influx via store-operated channels. J Neurophysiol 87, 3152 3155.
60. Ramirez, I. Sprott, R.L 1978) Genetic mechanisms of drinking and feeding. Neurosci Biobehav Rev 2, 15 26.
61. Reed, D.R., Li, S., Li, X., Huang, L., Tordoff, M.G., Starling-Roney, R., Taniguchi, K., West, D.B., Ohmen, J.D., Beauchamp, G.K. Bachmanov, A.A 2004) Polymorphisms in the taste receptor gene (Tas1r3) region are associated with saccharin preference in 30 mouse strains. J Neurosci 24, 938 946.
62. Risinger, F.O. Cunningham, C.L 1995) Genetic differences in ethanol-induced conditioned taste aversion after ethanol preexposure. Alcohol 12, 535 539.
63. Rodgers, D.A. McClearn, G.E 1962) Mouse strain differences in preference for various concentrations of alcohol. Q J Stud Alcohol 23, 26 33.
64. Rodgers, D.A., McClearn, G.E., Bennett, E.L. Hebert, M 1963) Alcohol preference as a function of its caloric utility in mice. J Comp Physiol Psychol 56, 666 672.
65. Ruiz-Avila, L., Wong, G.T., Damak, S. Margolskee, R.F 2001) Dominant loss of responsiveness to sweet and bitter compounds caused by a single mutation in alpha-gustducin. Proc Natl Acad Sci USA 98, 8868 8873.
66. Scinska, A., Bogucka-Bonikowska, A., Koros, E., Polanowska, E., Habrat, B., Kukwa, A., Kostowski, W. Bienkowski, P 2001) Taste responses in sons of alcoholics. Alcohol Alcohol 36, 79 84.
67. Scott, K 2004) The sweet and the bitter of mammalian taste. Curr Opin Neurobiol 14, 423 427.
68. Sinclair, J.D., Kampov-Polevoy, A., Stewart, E. Li, T.K 1992) Taste preferences in rat lines selected for high and low ethanol consumption. Alcohol 9, 155 160.
69. Smith, M.E., Norgren, R. Grigson, P.S 2004) A mixed design reveals that glucose moieties facilitate extinction of a conditioned taste aversion in rats. Learn Behav 32, 454 462.
70. Spanagel, R., Siegmund, S., Cowen, M., Schroff, K.C., Schumann, G., Fiserova, M., Sillaber, I., Wellek, S., Singer, M. Putzke, J 2002) The neuronal nitric oxide synthase gene is critically involved in neurobehavioral effects of alcohol. J Neurosci 22, 8676 8683.
71. Stewart, R.B., Russell, R.N., Lumeng, L., Li, T.K. Murphy, J.M 1994) Consumption of sweet, salty, sour, and bitter solutions by selectively bred alcohol-preferring and alcohol-nonpreferring lines of rats. Alcohol Clin Exp Res 18, 375 381.
72. Sugita, M 2006) Taste perception and coding in the periphery. Cell Mol Life Sci 63, 2000 2015.
73. Thiele, T.E., Marsh, D.J., Ste, M.L., Bernstein, I.L. Palmiter, R.D 1998) Ethanol consumption and resistance are inversely related to neuropeptide Y levels. Nature 396, 366 369.
74. 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.
75. Wong, G.T., Gannon, K.S. Margolskee, R.F 1996) Transduction of bitter and sweet taste by gustducin. Nature 381, 796 800.
76. Zhang, Y., Hoon, M.A., Chandrashekar, J., Mueller, K.L., Cook, B., Wu, D., Zuker, C.S. Ryba, N.J 2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112, 293 301.
77. Zhao, G.Q., Zhang, Y., Hoon, M.A., Chandrashekar, J., Erlenbach, I., Ryba, N.J. Zuker, C.S 2003) The receptors for mammalian sweet and umami taste. Cell 115, 255 266.