Behavioral responses to glutamate receptor agonists and antagonists implicate the involvement of brain-expressed mGluR4 and mGluR1 in taste transduction for umami in mice

Physiology and Behavior

Volumn 105, Issue 3, 2012, Pages 709-719

  Nakashima, Kiyohito ^a   Eddy, Meghan C ^b   Katsukawa, Hideo ^a   Delay, Eugene R ^b   Ninomiya, Yuzo ^c  

^a ASAHI UNIVERSITY   (Japan)

^b UNIVERSITY OF VERMONT   (United States)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

Behavioral response; MGluR agonist; MGluR antagonist; Taste transduction; Umami

Indexed keywords

1 AMINO 1,5 INDANDICARBOXYLIC ACID; 2 AMINO 4 PHOSPHONOBUTYRIC ACID; ALPHA CYCLOPROPYL 4 PHOSPHONOPHENYLGLYCINE; AMILORIDE; GLUTAMATE RECEPTOR AGONIST; GLUTAMATE RECEPTOR ANTAGONIST;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; BRAIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; MALE; MICE; MICE, INBRED C57BL; PROPIONIC ACIDS; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; SODIUM GLUTAMATE; TASTE; TASTE THRESHOLD;

EID: 80155214052     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2011.09.028     Document Type: Article

References (51)

1. Bartoshuk L.M. The psychophysics of taste. Am J Clin Nutr 1978, 31:1068-1077.
2. Bouton M.E. Learning and behavior: a contemporary synthesis 2007, Sinauer Associates, Inc., Sunderland, MA.
3. Brosvic G.M., Slotnick B.M. Absolute and intensity-difference taste thresholds in the rat: evaluation of an automated multi-channel gustometer. Physiol Behav 1986, 38:711-717.
4. Chaudhari N., Yang H., Lamp C., Delay E., Cartford C., Than T., et al. The taste of monosodium glutamate: membrane receptors in taste buds. J Neurosci 1996, 16:3817-3826.
5. Chaudhari N., Roper S.D. Molecular and physiological evidence for glutamate (umami) taste transduction via a G protein-coupled receptor. Ann N Y Acad Sci 1998, 855:398-406.
6. Chaudhari N., Landin A.M., Roper S.D. A metabotropic glutamate receptor variant functions as a taste receptor. Nat Neurosci 2000, 3:113-119.
7. Conn P.J., Pin J.P. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 1997, 37:205-237.
8. Damak S., Rong M., Yasumatsu K., Kokrashvili Z., Varadarajan V., Zou S., et al. Detection of sweet and umami taste in the absence of taste receptor T1r3. Science 2003, 301:850-853.
9. Damak S., Rong M., Yasumatsu K., Kokrashvili Z., Pérez C.A., Shigemura N., et al. Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses 2006, 31:253-264.
10. Delay E.R., Sewczak G.M., Stapleton J.R., Roper S.D. Glutamate taste: discrimination between the tastes of glutamate agonists and monosodium glutamate in rats. Chem Senses 2004, 29:291-299.
11. Delay E.R., Hernandez N.P., Bromley K., Margolskee R.F. Sucrose and monosodium glutamate taste thresholds and discrimination ability of T1R3 knockout mice. Chem Senses 2006, 31:351-357.
12. Eylam S., Spector A.C. Oral amiloride treatment decreases taste sensitivity to sodium salts in C57BL/6 J and DBA/2 J mice. Chem Senses 2003, 28(5):447-458.
13. Gabriel A.S., Uneyama H., Yoshie Y., Torii K. Cloning and characterization of a novel mGluR1 variant from vallate papillae that functions as a receptor for l-glutamate stimuli. Chem Senses 2005, 30(supple 1):i25-i26.
14. Glendinning J.I., Bloom L.D., Onishi M., Zheng K.H., Damak S., Margolskee R.F., et al. Contribution of alpha-gustducin to taste-guided licking responses of mice. Chem Senses 2005, 30:299-316.
15. Halpern B.P., Darlington R.B. Effects of amiloride on gustatory quality descriptions and temporal patterns produced by NaCl. Chem Senses 1998, 23:501-511.
16. Harada S., Yamaguchi K., Kasahara Y. Gustatory responses to amino acids in the chorda tympani nerve of C3H mice. Chem Senses 1998, 23:699-707.
17. He W., Yasumatsu K., Varadarajan V., Yamada A., Lem J., Ninomiya Y., et al. Umami taste responses are mediated by alpha-transducin and alpha-gustducin. J Neurosci 2004, 24:7674-7680.
18. Hisatsune C., Yasumatsu K., Takahashi-Iwanaga H., Ogawa N., Kuroda Y., Yoshida R., et al. Abnormal taste perception in mice lacking the type 3 inositol 1,4,5-trisphosphate receptor. J Biol Chem 2007, 282:37225-37231.
19. Inoue M., Beauchamp G.K., Bachmanov A.A. Gustatory neural responses to umami taste stimuli in C57BL/6ByJ and 129P3/J mice. Chem Senses 2004, 29:789-795.
20. Li X., Staszewski L., Xu H., Durick K., Zoller M., Adler E. Human receptors for sweet and umami taste. Proc Natl Acad Sci USA 2002, 99:4692-4696.
21. Lin W., Kinnamon S.C. Physiological evidence for ionotropic and metabotropic glutamate receptors in rat taste cells. J Neurophysiol 1999, 82:2061-2069.
22. Maruyama Y., Pereira E., Margolskee R.F., Chaudhari N., Roper S.D. Umami responses in mouse taste cells indicate more than one receptor. J Neurosci 2006, 26:2227-2234.
23. Monastyrskaia K., Lundstrom K., Plahl D., Acuna G., Schweitzer C., Malherbe P., et al. Effect of the umami peptides on the ligand binding and function of rat mGlu4a receptor might implicate this receptor in the monosodium glutamate taste transduction. Br J Pharmacol 1999, 128:1027-1034.
24. Moroni F., Lombardi G., Thomsen C., Leonardi P., Attucci S., Peruginelli F., et al. Pharmacological characterization of 1-aminoindan-1,5-dicarboxylic acid, a potent mGluR1 antagonist. J Pharmacol Exp Ther 1997, 281:721-729.
25. Nakashima K., Katsukawa H., Sasamoto K., Ninomiya Y. Behavioral taste similarities and differences among monosodium l-glutamate and glutamate receptor agonists in C57BL mice. J Nutr Sci Vitaminol (Tokyo) 2001, 47:161-166.
26. Nelson G., Chandrashekar J., Hoon M.A., Feng L., Zhao G., Ryba N.J., et al. An amino-acid taste receptor. Nature 2002, 416:199-202.
27. Ninomiya Y., Funakoshi M. Behavioral discrimination between glutamate and the four basic taste substances in mice. Comp Biochem Physiol A 1989, 92:365-370.
28. Ninomiya Y., Funakoshi M. Peripheral neural basis for behavioural discrimination between glutamate and the four basic taste substances in mice. Comp Biochem Physiol A 1989, 92:371-376.
29. Ninomiya Y., Tanimukai T., Yoshida S., Funakoshi M. Gustatory neural responses in preweanling mice. Physiol Behav 1991, 49:913-918.
30. Ninomiya Y., Kajiura H., Naito Y., Mochizuki K., Katsukawa H., Torii K. Glossopharyngeal denervation alters responses to nutrients and toxic substances. Physiol Behav 1994, 56:1179-1184.
31. Ninomiya Y., Kajiura H., Ishibashi T., Imai Y. Different responsiveness of the chorda tympani and glossopharyngeal nerves to L-lysine in mice. Chem Senses 1994, 19:617-626.
32. Ninomiya Y., Nakashima K., Fukuda A., Nishino H., Sugimura T., Hino A., et al. Responses to umami substances in taste bud cells innervated by the chorda tympani and glossopharyngeal nerves. J Nutr 2000, 130:950S-953S.
33. Roper S.D. Signal transduction and information processing in mammalian taste buds. Pflugers Arch 2007, 454:759-776.
34. Ruiz C., Gutknecht S., Delay E., Kinnamon S. Detection of NaCl and KCl in TRPV1 knockout mice. Chem Senses 2006, 31:813-820.
35. Spector A.C. Psychophysical evaluation of taste function n nonhuman mammals. Handbook of Olfaction and Gustation 2003, Marcel Dekker, Inc., New York, NY. 2nd ed. R.L. Doty (Ed.).
36. Spector A.C., Grill H.J. Differences in the taste quality of maltose and sucrose in rats: issues involving the generalization of conditioned taste aversions. Chem Senses 1988, 13:95-113.
37. Spielman A.I. Interaction of saliva and taste. J Dent Res 1990, 69:838-843.
38. Stapleton J.R., Luellig M., Roper S.D., Delay E.R. Discrimination between the tastes of sucrose and monosodium glutamate in rats. Chem Senses 2002, 27:375-382.
39. Stapleton J.R., Roper S.D., Delay E.R. The taste of monosodium glutamate (MSG): membrane receptors in taste buds. J Neurosci 1996, 16:3817-3826.
40. Stebbins W.C. Principles of animal psychophysics. Animal Psychophysics: the design and conduct of sensory experiments 1970, 1-19. Appleton-Century-Crofts, New York, NY. W.C. Stebbins (Ed.).
41. Tanabe Y., Nomura A., Masu M., Shigemoto R., Mizuno N., Nakanishi S. Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. J Neurosci 1993, 13:1372-1378.
42. Toms N.J., Jane D.E., Kemp M.C., Bedingfield J.S., Roberts P.J. The effects of (RS)-alpha-cyclopropyl-4-phosphonophenylglycine ((RS)-CPPG), a potent and selective metabotropic glutamate receptor antagonist. Br J Pharmacol 1996, 119:851-854.
43. Toyono T., Seta Y., Kataoka S., Harada H., Morotomi T., Kawano S., et al. Expression of the metabotropic glutamate receptor, mGluR4a, in the taste hairs of taste buds in rat gustatory papillae. Arch Histol Cytol 2002, 65:91-96.
44. Toyono T., Seta Y., Kataoka S., Kawano S., Shigemoto R., Toyoshima K. Expression of metabotropic glutamate receptor group I in rat gustatory papillae. Cell Tissue Res 2003, 313:29-35.
45. Vandenbeuch A., Clapp T.R., Kinnamon S.C. Amiloride-sensitive channels in type I fungiform taste cells in mouse. BMC Neurosci 2008, 9:1.
46. Yamaguchi S. The synergistic taste effect of monosodium glutamate and disodium 5'-inosinate. J Food Sci 1967, 32:473-478.
47. Yamaguchi S. Basic properties of umami and effects on humans. Physiol Behav 1991, 49:833-841.
48. Yamamoto T., Matsuo R., Fujimoto Y., Fukunaga I., Miyasaka A., Imoto T. Electrophysiological and behavioral studies on the taste of umami substances in the rat. Physiol Behav 1991, 49:919-925.
49. Yang H., Wanner I.B., Roper S.D., Chaudhari N. An optimized method for in situ hybridization with signal amplification that allows the detection of rare mRNAs. J Histochem Cytochem 1999, 47:431-446.
50. Yasumatsu K., Katsukawa H., Sasamoto K., Ninomiya Y. Recovery of amiloride-sensitive neural coding during regeneration of the gustatory nerve: behavioral-neural correlation of salt taste discrimination. J Neurosci 2003, 23:4362-4368.
51. Zhao G.Q., Zhang Y., Hoon M.A., Chandrashekar J., Erlenbach I., Ryba N.J., et al. The receptors for mammalian sweet and umami taste. Cell 2003, 115:255-266.