Detecting sweet and umami tastes in the gastrointestinal tract

Acta Physiologica

Volumn 204, Issue 2, 2012, Pages 169-177

  Iwatsuki, K ^a   Ichikawa, R ^a   Uematsu, A ^a   Kitamura, A ^a   Uneyama, H ^a   Torii, K ^a  

^a AJINOMOTO CO INC   (Japan)

Author keywords

ATP; Enteroendocrine cell; Gastrointestinal tract; Sweet; Taste cells; Taste receptor; Umami

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINO ACID; PROTEIN;

CELL SHAPE; CELL TYPE; CHEMORECEPTOR; CHEMOSENSITIVITY; ENTEROENDOCRINE CELL; FOOD INTAKE; GASTROINTESTINAL TRACT; GUSTATORY SYSTEM; HUMAN; INTESTINE CELL; INTESTINE INNERVATION; MOUTH CAVITY; ORGANOLEPTIC PROPERTY; PRIORITY JOURNAL; REVIEW; SENSORY NERVE; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SMELL AND TASTE PARAMETERS; SWEETNESS; TASTE BUD; TASTE CELL; TASTE DISCRIMINATION; UMAMI TASTE; VAGUS NERVE; VAGUS NERVE STIMULATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CHEMORECEPTOR CELLS; ENTEROENDOCRINE CELLS; GASTROINTESTINAL TRACT; HUMANS; MICE; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; TASTE; TASTE BUDS;

EID: 84855344414     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2011.02353.x     Document Type: Review

References (90)

1. Ackroff, K., Lucas, F. & Sclafani, A. 2005. Flavor preference conditioning as a function of fat source. Physiol Behav85, 448-460.
2. Akiba, Y., Watanabe, C., Mizumori, M. & Kaunitz, J.D. 2009. Luminal L-glutamate enhances duodenal mucosal defense mechanisms via multiple glutamate receptors in rats. Am J Physiol Gastrointest Liver Physiol297, G781-G791.
3. Asano-Miyoshi, M., Abe, K. & Emori, Y. 2000. Co-expression of calcium signaling components in vertebrate taste bud cells. Neurosci Lett283, 61-64.
4. Baggio, L.L. & Drucker, D.J. 2007. Biology of incretins: GLP-1 and GIP. Gastroenterology132, 2131-2157.
5. Bartel, D.L., Sullivan, S.L., Lavoie, E.G., Sevigny, J. & Finger, T.E. 2006. Nucleoside triphosphate diphosphohydrolase-2 is the ecto-ATPase of type I cells in taste buds. J Comp Neurol497, 1-12.
6. Berthoud, H.R. 2008. Vagal and hormonal gut-brain communication: from satiation to satisfaction. Neurogastroenterol Motil20(Suppl. 1), 64-72.
7. Bezencon, C., le Coutre, J. & Damak, S. 2007. Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses32, 41-49.
8. Bezencon, C., Furholz, A., Raymond, F., Mansourian, R., Metairon, S., Le Coutre, J. & Damak, S. 2008. Murine intestinal cells expressing Trpm5 are mostly brush cells and express markers of neuronal and inflammatory cells. J Comp Neurol509, 514-525.
9. Blackshaw, L.A., Brookes, S.J., Grundy, D. & Schemann, M. 2007. Sensory transmission in the gastrointestinal tract. Neurogastroenterol Motil19, 1-19.
10. Burnstock, G. 1990. Overview. Purinergic mechanisms. Ann N Y Acad Sci603, 1-17.
11. Burnstock, G. 2001. Purine-mediated signalling in pain and visceral perception. Trends Pharmacol Sci22, 182-188.
12. Burnstock, G. 2007. Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev87, 659-797.
13. Chandrashekar, J., Mueller, K.L., Hoon, M.A., Adler, E., Feng, L., Guo, W., Zuker, C.S. & Ryba, N.J. 2000. T2Rs function as bitter taste receptors. Cell100, 703-711.
14. Chandrashekar, J., Hoon, M.A., Ryba, N.J. & Zuker, C.S. 2006. The receptors and cells for mammalian taste. Nature444, 288-294.
15. Chandrashekar, J., Kuhn, C., Oka, Y., Yarmolinsky, D.A., Hummler, E., Ryba, N.J. & Zuker, C.S. 2010. The cells and peripheral representation of sodium taste in mice. Nature464, 297-301.
16. Chaudhari, N., Landin, A.M. & Roper, S.D. 2000. A metabotropic glutamate receptor variant functions as a taste receptor. Nat Neurosci3, 113-119.
17. Clapp, T.R., Stone, L.M., Margolskee, R.F. & Kinnamon, S.C. 2001. Immunocytochemical evidence for co-expression of Type III IP3 receptor with signaling components of bitter taste transduction. BMC Neurosci2, 6.
18. Clapp, T.R., Yang, R., Stoick, C.L., Kinnamon, S.C. & Kinnamon, J.C. 2004. Morphologic characterization of rat taste receptor cells that express components of the phospholipase C signaling pathway. J Comp Neurol468, 311-321.
19. Conigrave, A.D. & Brown, E.M. 2006. Taste receptors in the gastrointestinal tract. II. L-amino acid sensing by calcium-sensing receptors: implications for GI physiology. Am J Physiol Gastrointest Liver Physiol291, G753-G761.
20. Conigrave, A.D. & Hampson, D.R. 2006. Broad-spectrum L-amino acid sensing by class 3G-protein-coupled receptors. Trends Endocrinol Metab17, 398-407.
21. Cooke, H.J., Wunderlich, J. & Christofi, F.L. 2003. "The force be with you": ATP in gut mechanosensory transduction. News Physiol Sci18, 43-49.
22. Cordier-Bussat, M., Bernard, C., Levenez, F., Klages, N., Laser-Ritz, B., Philippe, J., Chayvialle, J.A. & Cuber, J.C. 1998. Peptones stimulate both the secretion of the incretin hormone glucagon-like peptide 1 and the transcription of the proglucagon gene. Diabetes47, 1038-1045.
23. Cummings, D.E. & Overduin, J. 2007. Gastroinestinal regulation of food intake. J Clin Invest117, 13-23.
24. 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. Science301, 850-853.
25. 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 Senses31, 253-264.
26. Doolin, R.E. & Gilbertson, T.A. 1996. Distribution and characterization of functional amiloride-sensitive sodium channels in rat tongue. J Gen Physiol107, 545-554.
27. Dotson, C.D., Vigues, S., Steinle, N.I. & Munger, S.D. 2010. T1R and T2R receptors: the modulation of incretin hormones and potential targets for the treatment of type 2 diabetes mellitus. Curr Opin Investig Drugs11, 447-454.
28. Drucker, D.J., Jin, T., Asa, S.L., Young, T.A. & Brubaker, P.L. 1994. Activation of proglucagon gene transcription by protein kinase-A in a novel mouse enteroendocrine cell line. Mol Endocrinol8, 1646-1655.
29. Farbman, A.I. 1965. Fine structure of the taste bud. J Ultrastruct Res12, 328-350.
30. Finger, T.E., Danilova, V., Barrows, J., Bartel, D.L., Vigers, A.J., Stone, L., Hellekant, G. & Kinnamon, S.C. 2005. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science310, 1495-1499.
31. Fong, A.Y., Krstew, E.V., Barden, J. & Lawrence, A.J. 2002. Immunoreactive localisation of P2Y1 receptors within the rat and human nodose ganglia and rat brainstem: comparison with [alpha 33P]deoxyadenosine 5'-triphosphate autoradiography. Neuroscience113, 809-823.
32. Fujita, T. 1991. Taste cells in the gut and on the tongue. Their common, paraneuronal features. Physiol Behav49, 883-885.
33. Furuya, K., Sokabe, M. & Furuya, S. 2005. Characteristics of subepithelial fibroblasts as a mechano-sensor in the intestine: cell-shape-dependent ATP release and P2Y1 signaling. J Cell Sci118, 3289-3304.
34. Galligan, J.J. & Bertrand, P.P. 1994. ATP mediates fast synaptic potentials in enteric neurons. J Neurosci14, 7563-7571.
35. Herness, S. & Zhao, F.L. 2009. The neuropeptides CCK and NPY and the changing view of cell-to-cell communication in the taste bud. Physiol Behav97, 581-591.
36. Hisatsune, C., Yasumatsu, K., Takahashi-Iwanaga, H., Ogawa, N., Kuroda, Y., Yoshida, R., Ninomiya, Y. & Mikoshiba, K. 2007. Abnormal taste perception in mice lacking the type 3 inositol 1, 4, 5-trisphosphate receptor. J Biol Chem282, 37225-37231.
37. 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 USA93, 6631-6634.
38. Huang, A.L., Chen, X., Hoon, M.A., Chandrashekar, J., Guo, W., Trankner, D., Ryba, N.J. & Zuker, C.S. 2006. The cells and logic for mammalian sour taste detection. Nature442, 934-938.
39. Ishimaru, Y., Inada, H., Kubota, M., Zhuang, H., Tominaga, M. & Matsunami, H. 2006. Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc Natl Acad Sci USA103, 12569-12574.
40. Iwatsuki, K., Ichikawa, R., Hiasa, M., Moriyama, Y., Torii, K. & Uneyama, H. 2009. Identification of the vesicular nucleotide transporter (VNUT) in taste cells. Biochem Biophys Res Commun388, 1-5.
41. Iwatsuki, K., Nomura, M., Shibata, A., Ichikawa, R., Enciso, P.L., Wang, L., Takayanagi, R., Torii, K. & Uneyama, H. 2010. Generation and characterization of T1R2-LacZ knock-in mouse. Biochem Biophys Res Commun402, 495-499.
42. Iwatsuki, K., Ichikawa, R., Kitamura, A., Uematsu, A., Uneyama, H. & Torii, K. 2011. Purinergic signaling in the taste and gust system. In: E.J. Lynch & A.P. Petrov (eds) The Sense of Taste, (in press), Nova Science Publishers Inc., New York.
43. Jang, H.J., Kokrashvili, Z., Theodorakis, M.J., Carlson, O.D., Kim, B.J., Zhou, J., Kim, H.H., Xu, X., Chan, S.L., Juhaszova, M., Bernier, M., Mosinger, B., Margolskee, R.F. & Egan, J.M. 2007. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proc Natl Acad Sci USA104, 15069-15074.
44. Jeanningros, R. 1982. Vagal unitary responses to intestinal amino acid infusions in the anesthetized cat: a putative signal for protein induced satiety. Physiol Behav28, 9-21.
45. Kant, R. 2005. Sweet proteins - potential replacement for artificial low calorie sweeteners. Nutr J4, 5.
46. Kinnamon, J.C., Taylor, B.J., Delay, R.J. & Roper, S.D. 1985. Ultrastructure of mouse vallate taste buds. I. Taste cells and their associated synapses. J Comp Neurol235, 48-60.
47. Kirkup, A.J., Booth, C.E., Chessell, I.P., Humphrey, P.P. & Grundy, D. 1999. Excitatory effect of P2X receptor activation on mesenteric afferent nerves in the anaesthetised rat. J Physiol520(Pt 2), 551-563.
48. Kokrashvili, Z., Rodriguez, D., Yevshayeva, V., Zhou, H., Margolskee, R.F. & Mosinger, B. 2009. Release of endogenous opioids from duodenal enteroendocrine cells requires Trpm5. Gastroenterology137, 598-606.
49. Lal, S., Kirkup, A.J., Brunsden, A.M., Thompson, D.G. & Grundy, D. 2001. Vagal afferent responses to fatty acids of different chain length in the rat. Am J Physiol Gastrointest Liver Physiol281, G907-G915.
50. Li, Y. & Owyang, C. 1996. Peptone stimulates CCK-releasing peptide secretion by activating intestinal submucosal cholinergic neurons. J Clin Invest97, 1463-1470.
51. Lindemann, B. 1996. Taste reception. Physiol Rev76, 718-766.
52. Lyall, V., Heck, G.L., Vinnikova, A.K., Ghosh, S., Phan, T.H., Alam, R.I., Russell, O.F., Malik, S.A., Bigbee, J.W. & DeSimone, J.A. 2004. The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant. J Physiol558, 147-159.
53. Margolskee, R.F., Dyer, J., Kokrashvili, Z., Salmon, K.S., Ilegems, E., Daly, K., Maillet, E.L., Ninomiya, Y., Mosinger, B. & Shirazi-Beechey, S.P. 2007. T1R3 and gustducin in gut sense sugars to regulate expression of Na+-glucose cotransporter 1. Proc Natl Acad Sci USA104, 15075-15080.
54. Matsunami, H., Montmayeur, J.P. & Buck, L.B. 2000. A family of candidate taste receptors in human and mouse. Nature404, 601-604.
55. 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 Genet28, 58-63.
56. McIntyre, N., Holdsworth, C.D. & Turner, D.S. 1964. New interpretation of oral glucose tolerance. Lancet2, 20-21.
57. McLaughlin, S.K., McKinnon, P.J. & Margolskee, R.F. 1992. Gustducin is a taste-cell-specific G protein closely related to the transducins. Nature357, 563-569.
58. Meyerhof, W., Batram, C., Kuhn, C., Brockhoff, A., Chudoba, E., Bufe, B., Appendino, G. & Behrens, M. 2010. The molecular receptive ranges of human TAS2R bitter taste receptors. Chem Senses35, 157-170.
59. Nakagawa, Y., Nagasawa, M., Yamada, S., Hara, A., Mogami, H., Nikolaev, V.O., Lohse, M.J., Shigemura, N., Ninomiya, Y. & Kojima, I. 2009. Sweet taste receptor expressed in pancreatic beta-cells activates the calcium and cyclic AMP signaling systems and stimulates insulin secretion. PLoS ONE4, e5106.
60. Nelson, G., Hoon, M.A., Chandrashekar, J., Zhang, Y., Ryba, N.J. & Zuker, C.S. 2001. Mammalian sweet taste receptors. Cell106, 381-390.
61. Nelson, G., Chandrashekar, J., Hoon, M.A., Feng, L., Zhao, G., Ryba, N.J. & Zuker, C.S. 2002. An amino-acid taste receptor. Nature416, 199-202.
62. Newson, B., Ahlman, H., Dahlstrom, A. & Nyhus, L.M. 1982. Ultrastructural observations in the rat ileal mucosa of possible epithelial "taste cells" and submucosal sensory neurons. Acta Physiol Scand114, 161-164.
63. Niijima, A. 1991. Effects of oral and intestinal stimulation with umami substance on gastric vagus activity. Physiol Behav49, 1025-1028.
64. Ohsu, T., Amino, Y., Nagasaki, H., Yamanaka, T., Takeshita, S., Hatanaka, T., Mamyama, Y., Miyamura, N. & Eto, Y. 2010. Involvement of the calcium-sensing Receptor in Human Taste Percaption. J Biol Chem285, 1016-1022.
65. Perez, C.A., Huang, L., Rong, M., Kozak, J.A., Preuss, A.K., Zhang, H., Max, M. & Margolskee, R.F. 2002. A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci5, 1169-1176.
66. Raybould, H.E. 1998. Does your gut taste? sensory transduction in the gastrointestinal tractNews Physiol Sci13, 275-280.
67. Reimer, R.A., Darimont, C., Gremlich, S., Nicolas-Metral, V., Ruegg, U.T. & Mace, K. 2001. A human cellular model for studying the regulation of glucagon-like peptide-1 secretion. Endocrinology142, 4522-4528.
68. Rozengurt, E. 2006. Taste receptors in the gastrointestinal tract. I. Bitter taste receptors and alpha-gustducin in the mammalian gut. Am J Physiol Gastrointest Liver Physiol291, G171-G177.
69. Rozengurt, E. & Sternini, C. 2007. Taste receptor signaling in the mammalian gut. Curr Opin Pharmacol7, 557-562.
70. San Gabriel, A., Maekawa, T., Uneyama, H. & Torii, K. 2009. Metabotropic glutamate receptor type 1 in taste tissue. Am J Clin Nutr90, 743S-746S.
71. Sawada, K., Echigo, N., Juge, N., Miyaji, T., Otsuka, M., Omote, H., Yamamoto, A. & Moriyama, Y. 2008. Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci USA105, 5683-5686.
72. Schiffman, S.S., Sennewald, K. & Gagnon, J. 1981. Comparison of taste qualities and thresholds of D- and L-amino acids. Physiol Behav27, 51-59.
73. Schwartz, G.J. & Moran, T.H. 1998. Duodenal nutrient exposure elicits nutrient-specific gut motility and vagal afferent signals in rat. Am J Physiol274, R1236-R1242.
74. Sclafani, A. 1995. How food preferences are learned: laboratory animal models. Proc Nutr Soc54, 419-427.
75. Sclafani, A. 2004. Oral and postoral determinants of food reward. Physiol Behav81, 773-779.
76. Shin, Y.K., Martin, B., Golden, E., Dotson, C.D., Maudsley, S., Kim, W., Jang, H.J., Mattson, M.P., Drucker, D.J., Egan, J.M. & Munger, S.D. 2008. Modulation of taste sensitivity by GLP-1 signaling. J Neurochem106, 455-463.
77. Steinert, R.E., Gerspach, A.C., Gutmann, H., Asarian, L., Drewe, J. & Beglinger, C. 2011. The functional involvement of gut-expressed sweet taste receptors in glucose-stimulated secretion of glucagon-like peptide-1 (GLP-1) and peptide YY (PYY). Clin Nutr4, 524-532.
78. Sutherland, K., Young, R.L., Cooper, N.J., Horowitz, M. & Blackshaw, L.A. 2007. Phenotypic characterization of taste cells of the mouse small intestine. Am J Physiol Gastrointest Liver Physiol292, G1420-G1428.
79. Tordoff, M.G., Shao, H., Alarcon, L.K., Margolskee, R.F., Mosinger, B., Bachmanov, A.A., Reed, D.R. & McCaughey, S. 2008. Involvement of T1R3 in calcium-magnesium taste. Physiol Genomics34, 338-348.
80. Uneyama, H., Niijima, A., San Gabriel, A. & Torii, K. 2006. Luminal amino acid sensing in the rat gastric mucosa. Am J Physiol Gastrointest Liver Physiol291, G1163-G1170.
81. Vulchanova, L., Riedl, M.S., Shuster, S.J., Buell, G., Surprenant, A., North, R.A. & Elde, R. 1997. Immunohistochemical study of the P2X2 and P2X3 receptor subunits in rat and monkey sensory neurons and their central terminals. Neuropharmacology36, 1229-1242.
82. Wade, P.R. & Westfall, J.A. 1985. Ultrastructure of enterochromaffin cells and associated neural and vascular elements in the mouse duodenum. Cell Tissue Res241, 557-563.
83. Wong, G.T., Gannon, K.S. & Margolskee, R.F. 1996. Transduction of bitter and sweet taste by gustducin. Nature381, 796-800.
84. Wu, S.V., Rozengurt, N., Yong, M., Young, S.H., Sinettt-Smith, J. & Rozengurt, E. 2002. Expression of bitter taste receptors of the T2R family in the gastrointestinal tract and enteroendocrine STC-1 cells. Proc Natl Acad Sci USA99, 2392-2397.
85. Yarmolinsky, D.A., Zuker, C.S. & Ryba, N.J. 2009. Common sense about taste: from mammals to insects. Cell139, 234-244.
86. Yee, C.L., Yang, R., Bottger, B., Finger, T.E. & Kinnamon, J.C. 2001. "Type III" cells of rat taste buds: immunohistochemical and ultrastructural studies of neuron-specific enolase, protein gene product 9.5, and serotonin. J Comp Neurol440, 97-108.
87. 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. Cell112, 293-301.
88. Zhang, F., Klebansky, B., Fine, R.M., Xu, H., Pronin, A., Liu, H., Tachdjian, C. & Li, X. 2008. Molecular mechanism for the umami taste synergism. Proc Natl Acad Sci USA105, 20930-20934.
89. 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. Cell115, 255-266.
90. Zhu, J.X., Zhu, X.Y., Owyang, C. & Li, Y. 2001. Intestinal serotonin acts as a paracrine substance to mediate vagal signal transmission evoked by luminal factors in the rat. J Physiol530, 431-442.