Allelic variation of the Tas1r3 taste receptor gene selectively affects taste responses to sweeteners: Evidence from 129.B6-Tas1r3 congenic mice

Physiological Genomics

Volumn 32, Issue 1, 2007, Pages 82-94

  Inoue, Masashi ^a,b   Glendinning, John I ^c   Theodorides, Maria L ^b   Harkness, Sarah ^c   Li, Xia ^b   Bosak, Natalia ^b   Beauchamp, Gary K ^b,d   Bachmanov, Alexander A ^b  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^b MONELL CHEMICAL SENSES CENTER   (United States)

^c Barnard College of Columbia University   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Chorda tympani nerve; Electrophysiology; Genetics; Lick responses; Preference; Sweet taste

Indexed keywords

ACESULFAME; ALANINE; DEXTRO PHENYLALANINE; ERYTHRITOL; FRUCTOSE; GLUCOSE; GLUCOSE POLYMER; GLUTAMATE SODIUM; GLUTAMINE; GLYCINE; INOSINE PHOSPHATE; MALTOSE; PROLINE; QUININE; SACCHARIN; SODIUM CHLORIDE; SORBITOL; SUCRALOSE; SUCROSE; SUGAR ALCOHOL; SWEETENING AGENT; THREONINE; TRYPTOPHAN;

ALLELE; ANIMAL BEHAVIOR; ARTICLE; CHORDA TYMPANI; CONGENIC STRAIN; CONTROLLED STUDY; FEMALE; GENE; GENETIC VARIABILITY; GENOTYPE; LICKING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SWEETNESS; TAS1R3 GENE; TASTE BUD;

ANIMAL FEED; ANIMALS; CHROMOSOME MAPPING; CROSSES, GENETIC; FOOD PREFERENCES; GENOTYPE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; POLYMORPHISM, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, CELL SURFACE; TASTE; TOLL-LIKE RECEPTOR 3; VARIATION (GENETICS);

CHORDA; MUS;

EID: 37449024693     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00161.2007     Document Type: Article

References (67)

1. Bachmanov AA, Beauchamp GK. Amino acid and carbohydrate preferences in C57BL/6ByJ and 129P3/J mice. Physiol Behav (August 8, 2007). doi:10.1016/j.physbeh.2007.07.016.
2. Bachmanov AA, Inoue M, Tordoff MG, Ninomiya Y, Beauchamp GK. Modification of behavioral and neural taste responses to NaCl in C57BL/6 mice: effects of NaCl exposure and DOCA treatment. Physiol Behav 65: 817-822, 1999.
3. Bachmanov AA, Li X, Reed DR, Ohmen JD, Li S, Chen Z, Tordoff MG, de Jong PJ, Wu C, West DB, Chatterjee A, Ross DA, Beauchamp GK. Positional cloning of the mouse saccharin preference (Sac) locus. Chem Senses 26: 925-933, 2001.
4. Bachmanov AA, Reed DR, Beauchamp GK, Tordoff MG. Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet 32: 435-443, 2002.
5. Bachmanov AA, Reed DR, Ninomiya Y, Inoue M, Tordoff MG, Price RA, Beauchamp GK. Sucrose consumption in mice: major influence of two genetic loci affecting peripheral sensory responses. Mamm Genome 8: 545-548, 1997.
6. Bachmanov AA, Reed DR, Tordoff MG, Price RA, Beauchamp GK. Intake of ethanol, sodium chloride, sucrose, citric acid, and quinine hydrochloride solutions by mice: a genetic analysis. Behav Genet 26: 563-573, 1996.
7. Bachmanov AA, Reed DR, Tordoff MG, Price RA, Beauchamp GK. Nutrient preference and diet-induced adiposity in C57BL/6ByJ and 129P3/J mice. Physiol Behav 72: 603-613, 2001.
8. Bachmanov AA, Tordoff MG, Beauchamp GK. Ethanol consumption and taste preferences in C57BL/6ByJ and 129/J mice. Alcohol Clin Exp Res 20: 201-206, 1996.
9. Bachmanov AA, Tordoff MG, Beauchamp GK. Intake of umamitasting solutions by mice: a genetic analysis. J Nutr 130: 935S-941S, 2000.
10. Bachmanov AA, Tordoff MG, Beauchamp GK. Sweetener preference of C57BL/6ByJ and 129P3/J mice. Chem Senses 26: 905-913, 2001.
11. Bufe B, Breslin PA, Kuhn C, Reed DR, Tharp CD, Slack JP, Kim UK, Drayna D, Meyerhof W. The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. Curr Biol 15: 322-327, 2005.
12. Capeless CG, Whitney G. The genetic basis of preference for sweet substances among inbred strains of mice: preference ratio phenotypes and the alleles of the Sac and dpa loci. Chem Senses 20: 291-298, 1995.
13. Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Varadarajan V, Zou S, Jiang P, Ninomiya Y, Margolskee RF. Detection of sweet and umami taste in the absence of taste receptor T1r3. Science 301: 850-853, 2003.
14. Danilova V, Hellekant G. Comparison of the responses of the chorda tympani and glossopharyngeal nerves to taste stimuli in C57BL/6J mice. BMC Neurosci 4: 5, 2003.
15. Davis JD. The effectiveness of some sugars in stimulating licking behavior in the rat. Physiol Behav 11: 39-45, 1973.
16. Davis JD. Some new developments in the understanding of oropharyngeal and postingestional controls of meal size. Nutrition 15: 32-39, 1999.
17. Davis JD, Collins BJ, Levine MW. Peripheral control of drinking: gastrointestinal filling as a negative feedback signal, a theoretical and experimental analysis. J Comp Physiol Psychol 89: 985-1002, 1975.
18. Davis JD, Levine MW. A model for the control of ingestion. Psychol Rev 84: 379-412, 1977.
19. Dotson CD, Spector AC. The relative affective potency of glycine, L-serine and sucrose as assessed by a brief-access taste test in inbred strains of mice. Chem Senses 29: 489-498, 2004.
20. Eylam S, Spector AC. Stimulus processing of glycine is dissociable from that of sucrose and glucose based on behaviorally measured taste signal detection in Sac "taster" and "non-taster" mice. Chem Senses 29: 639-649, 2004.
21. Frank ME, Blizard DA. Chorda tympani responses in two inbred strains of mice with different taste preferences. Physiol Behav 67: 287-297, 1999.
22. Fuller JL. Single-locus control of saccharin preference in mice. J Hered 65: 33-36, 1974.
23. Glendinning JI, Bloom LD, Onishi M, Zheng KH, Damak S, Margolskee RF, Spector AC. Contribution of alpha-gustducin to taste-guided licking responses of mice. Chem Senses 30: 299-316, 2005.
24. Glendinning JI, Chyou S, Lin I, Onishi M, Patel P, Zheng KH. Initial licking responses of mice to sweeteners: effects of Tas1r3 polymorphisms. Chem Senses 30: 601-614, 2005.
25. Glendinning JI, Gresack J, Spector AC. A high-throughput screening procedure for identifying mice with aberrant taste and oromotor function. Chem Senses 27: 461-474, 2002.
26. Inoue M, Beauchamp GK, Bachmanov AA. Gustatory neural responses to umami taste stimuli in C57BL/6ByJ and 129P3/J mice. Chem Senses 29: 789-795, 2004.
27. Inoue M, Li X, McCaughey SA, Beauchamp GK, Bachmanov AA. Soa genotype selectively affects mouse gustatory neural responses to sucrose octaacetate. Physiol Genomics 5: 181-186, 2001.
28. Inoue M, McCaughey SA, Bachmanov AA, Beauchamp GK. Whole nerve chorda tympani responses to sweeteners in C57BL/6ByJ and 129P3/J mice. Chem Senses 26: 915-923, 2001.
29. Inoue M, Reed DR, Li X, Tordoff MG, Beauchamp GK, Bachmanov AA. Allelic variation of the Tas1r3 taste receptor gene selectively affects behavioral and neural taste responses to sweeteners in the F2 hybrids between C57BL/6ByJ and 129P3/J mice. J Neurosci 24: 2296-2303, 2004.
30. Inoue M, Tordoff MG. Calcium deficiency alters chorda tympani nerve responses to oral calcium chloride. Physiol Behav 63: 297-303, 1998.
31. Kitagawa M, Kusakabe Y, Miura H, Ninomiya Y, Hino A. Molecular genetic identification of a candidate receptor gene for sweet taste. Biochem Biophys Res Commun 283: 236-242, 2001.
32. Levine AS, Billington CJ. Why do we eat? A neural systems approach. Annu Rev Nutr 17: 597-619, 1997.
33. Levine AS, Kotz CM, Gosnell BA. Sugars: hedonic aspects, neuroregulation, and energy balance. Am J Clin Nutr 78: 834S-842S, 2003.
34. Lewis SR, Ahmed S, Dym C, Khaimova E, Kest B, Bodnar RJ. Inbred mouse strain survey of sucrose intake. Physiol Behav 85: 546-556, 2005.
35. Li X, Bachmanov AA, Li S, Chen Z, Tordoff MG, Beauchamp GK, de Jong PJ, Wu C, Chen L, West DB, Ross DA, Ohmen JD, Reed DR. Genetic, physical and comparative map of the subtelomeric region of mouse chromosome 4. Mamm Genome 13: 5-19, 2002.
36. Li X, Inoue M, Reed DR, Huque T, Puchalski RB, Tordoff MG, Ninomiya Y, Beauchamp GK, Bachmanov AA. High-resolution genetic mapping of the saccharin preference locus (Sac) and the putative sweet taste receptor (T1R1) gene (Gpr70) to mouse distal Chromosome 4. Mamm Genome 12: 13-16, 2001.
37. Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E. Human receptors for sweet and umami taste. Proc Natl Acad Sci USA 99: 4692-4696, 2002.
38. Lush IE. The genetics of tasting in mice. VI. Saccharin, acesulfame, dulcin and sucrose. Genet Res 53: 95-99, 1989.
39. Lush IE, Hornigold N, King P, Stoye JP. The genetics of tasting in mice. VII. Glycine revisited, and the chromosomal location of Sac and Soa. Genet Res 66: 167-174, 1995.
40. Max M, Shanker YG, Huang L, Rong M, Liu Z, Campagne F, Weinstein H, Damak S, Margolskee RF. Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet 28: 58-63., 2001.
41. Miyasaka A, Imoto T. Electrophysiological characterization of the inhibitory effect of a novel peptide gurmarin on the sweet taste response in rats. Brain Res 676: 63-68, 1995.
42. Montmayeur JP, Liberles SD, Matsunami H, Buck LB. A candidate taste receptor gene near a sweet taste locus. Nat Neurosci 4: 492-498, 2001.
43. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS. An amino-acid taste receptor. Nature 416: 199-202, 2002.
44. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS. Mammalian sweet taste receptors. Cell 106: 381-390, 2001.
45. Nie Y, Vigues S, Hobbs JR, Conn GL, Munger SD. Distinct contributions of T1R2 and T1R3 taste receptor subunits to the detection of sweet stimuli. Curr Biol 15: 1948-1952, 2005.
46. Ninomiya Y, Bachmanov AA, Yatabe A, Beauchamp GK. NaCl-preferring NZB/B1NJ mice and NaCl-avoiding CBA/J mice have similar amiloride inhibition of chorda tympani responses to NaCl. Chem Senses 23: 411-415, 1998.
47. Ninomiya Y, Funakoshi M. Peripheral neural basis for behavioural discrimination between glutamate and the four basic taste substances in mice. Comp Biochem Physiol A 92: 371-376, 1989.
48. Ninomiya Y, Kajiura H, Mochizuki K. Differential taste responses of mouse chorda tympani and glossopharyngeal nerves to sugars and amino acids. Neurosci Lett 163: 197-200, 1993.
49. Phillips TJ, Crabbe JC, Metten P, Belknap JK. Localization of genes affecting alcohol drinking in mice. Alcohol Clin Exp Res 18: 931-941, 1994.
50. Ramirez I. Why do sugars taste good? Neurosci Biobehav Rev 14: 125-134, 1990.
51. Ramirez I, Fuller JL. Genetic influence on water and sweetened water consumption in mice. Physiol Behav 16: 163-168, 1976.
52. Reed DR, Li S, Li X, Huang L, Tordoff MG, Starling-Roney R, Taniguchi K, West DB, Ohmen JD, Beauchamp GK, Bachmanov AA. Polymorphisms in the taste receptor gene (Tas1r3) region are associated with saccharin preference in 30 mouse strains. J Neurosci 24: 938-946, 2004.
53. Sainz E, Korley JN, Battey JF, Sullivan SL. Identification of a novel member of the T1R family of putative taste receptors. J Neurochem 77: 896-903, 2001.
54. Sclafani A. Enhanced sucrose and Polycose preference in sweet "sensitive" (C57BL/6J) and "subsensitive" (129P3/J) mice after experience with these saccharides. Physiol Behav 87: 745-756, 2006.
55. Sclafani A. Fat and sugar flavor preference and acceptance in C57BL/6J and 129 mice: experience attenuates strain differences. Physiol Behav 90: 602-611, 2007.
56. Sclafani A. Oral and postoral determinants of food reward. Physiol Behav 81: 773-779, 2004.
57. Sclafani A. Post-ingestive positive controls of ingestive behavior. Appetite 36: 79-83, 2001.
58. Sclafani A. The sixth taste? Appetite 43: 1-3, 2004.
59. Sclafani A. Sucrose motivation in sweet "sensitive" (C57BL/6J) and "subsensitive" (129P3/J) mice measured by progressive ratio licking. Physiol Behav 87: 734-744, 2006.
60. Sclafani A, Glendinning JI. Sugar and fat conditioned flavor preferences in C57BL/6J and 129 mice: oral and postoral interactions. Am J Physiol Regul Integr Comp Physiol 289: R712-R720, 2005.
61. Shingai T, Beidler LM. Response characteristics of three taste nerves in mice. Brain Res 335: 245-249, 1985.
62. Smith JC, Davis JD. Lack of an order effect in brief contact taste tests with closely spaced test trials. Physiol Behav 52: 1107-1111, 1992.
63. Spector AC. Psychophysical evaluation of taste function in nonhuman mammals. In: Handbook of Olfaction and Gustation, edited by Doty RL. New York: Dekker, 2003, p. 861-879.
64. Swithers-Mulvey SE, Miller GL, Hall WG. Habituation of oromotor responding to oral infusions in rat pups. Appetite 17: 55-67, 1991.
65. Xu H, Staszewski L, Tang H, Adler E, Zoller M, Li X. Different functional roles of T1R subunits in the heteromeric taste receptors. Proc Natl Acad Sci USA 101: 14258-14263, 2004.
66. Young P, Trafton C. Activity contour maps as related to preference in four gustatory stimulus areas of the rat. J Comp Physiol Psychol 58: 68-75, 1964.
67. Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS. The receptors for mammalian sweet and umami taste. Cell 115: 255-266, 2003.