Sensing of amino acids by the gut-expressed taste receptor T1R1-T1R3 stimulates CCK secretion

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 304, Issue 3, 2013, Pages

  Daly, Kristian ^a   Al Rammahi, Miran ^a   Moran, Andrew ^a   Marcello, Marco ^a   Ninomiya, Yuzo ^b   Shirazi Beechey, Soraya P ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

Amino acid; Cholecystokinin; Intestine; Sensing; T1R1 T1R3

Indexed keywords

2 CHLORO 6 [3 [1,1 DIMETHYL 2 (2 NAPHTHYL)ETHYLAMINO] 2 HYDROXYPROPOXY]BENZONITRILE; AMINO ACID; AMINO ACID RECEPTOR; CALCIUM ION; CHOLECYSTOKININ; CHOLECYSTOKININ RECEPTOR BLOCKING AGENT; GLUTAMIC ACID; GUANOSINE PHOSPHATE; GURMARIN; INOSINE PHOSPHATE; LEUCINE; PHENYLALANINE; SMALL INTERFERING RNA; T1R1 PROTEIN; T1R3 PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DRUG INHIBITION; ENTEROENDOCRINE CELL; FEMALE; INTESTINE; MALE; MOLECULAR SENSOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; SMALL INTESTINE; TASTE BUD;

AMINO ACIDS; ANIMALS; BLOTTING, WESTERN; CELL MEMBRANE; CELLS, CULTURED; CHOLECYSTOKININ; FEMALE; GASTROINTESTINAL TRACT; IMMUNOHISTOCHEMISTRY; INOSITOL PHOSPHATES; ISOMERISM; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; NAPHTHALENES; PEPTIDES; PLANT PROTEINS; PROTEIN HYDROLYSATES; RECEPTORS, G-PROTEIN-COUPLED; RNA INTERFERENCE; STIMULATION, CHEMICAL;

EID: 84873339870     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00074.2012     Document Type: Article

References (71)

1. Anika SM, Houpt TR, Houpt KA. Satiety elicited by cholecystokinin in intact and vagotomized rats. Physiol Behav 19: 761-766, 1977.
2. Backus RC, Howard KA, Rogers QR. The potency of dietary amino acids in elevating plasma cholecystokinin immunoreactivity in cats is related to amino acid hydrophobicity. Regul Pept 72: 31-40, 1997.
3. Batchelor DJ, Al-Rammahi M, Moran AW, Brand JG, Li X, Haskins M, German AJ, Shirazi-Beechey SP. Sodium/glucose cotransporter-1, sweet receptor, and disaccharidase expression in the intestine of the domestic dog and cat: two species of different dietary habit. Am J Physiol Regul Integr Comp Physiol 300: R67-R75, 2011.
4. Brown EM, MacLeod RJ. Extracellular calcium sensing and extracellular calcium signaling. Physiol Rev 81: 239-297, 2001.
5. Calebiro D, Nikolaev VO, Persani L, Lohse MJ. Signaling by internalized G-protein-coupled receptors. Trends Pharmacol Sci 31: 221-228, 2010.
6. Chandrashekar J, Hoon MA, Ryba NJ, Zuker CS. The receptors and cells for mammalian taste. Nature 444: 288-294, 2006.
7. Chang CH, Chey WY, Sun Q, Leiter A, Chang TM. Characterization of the release of cholecystokinin from a murine neuroendocrine tumor cell line, STC-1. Biochim Biophys Acta 1221: 339-347, 1994.
8. Choi S, Lee M, Shiu AL, Yo SJ, Halldén G, Aponte GW. GPR93 activation by protein hydrolysate induces CCK transcription and secretion in STC-1 cells. Am J Physiol Gastrointest Liver Physiol 292: G1366-G1375, 2007.
9. Conigrave AD, Brown EM. Taste receptors in the gastrointestinal tract. II. L-Amino acid sensing by calcium-sensing receptors: implications for GI physiology. Am J Physiol Gastrointest Liver Physiol 291: G753-G761, 2006.
10. 2+-sensing receptor. Proc Natl Acad Sci USA 97: 4814-4819, 2000.
11. Cuff M, Dyer J, Jones M, Shirazi-Beechey S. The human colonic monocarboxylate transporter isoform 1: its potential importance to colonic tissue homeostasis. Gastroenterology 128: 676-686, 2005.
12. Daly K, Al-Rammahi M, Arora DK, Moran AW, Proudman CJ, Ninomiya Y, Shirazi-Beechey SP. Expression of sweet receptor components in equine small intestine: relevance to intestinal glucose transport. Am J Physiol Regul Integr Comp Physiol 303: R199-R208, 2012.
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. Diepvens K, Häberer D, Westerterp-Plantenga M. Different proteins and biopeptides differently affect satiety and anorexigenic/orexigenic hormones in healthy humans. Int J Obes (Lond) 32: 510-518, 2008.
15. Dockray GJ. Cholecystokinin. Curr Opin Endocrinol Diabetes Obes 19: 8-12, 2012.
16. +/glucose co-transporter (SGLT1) to an increase in dietary soluble carbohydrate. Pflügers Arch 458: 419-430, 2009.
17. Dyer J, Daly K, Salmon KS, Arora DK, Kokrashvili Z, Margolskee RF, Shirazi-Beechey SP. Intestinal glucose sensing and regulation of intestinal glucose absorption. Biochem Soc Trans 35: 1191-1194, 2007.
18. Dyer J, Salmon KS, Zibrik L, Shirazi-Beechey SP. Expression of sweet taste receptors of the T1R family in the intestinal tract and enteroendocrine cells. Biochem Soc Trans 33: 302-305, 2005.
19. Dyer J, Vayro S, King TP, Shirazi-Beechey SP. Glucose sensing in the intestinal epithelium. Eur J Biochem 270: 3377-3388, 2003.
20. Faget L, Erbs E, Le Merrer J, Scherrer G, Matifas A, Benturquia N, Noble F, Decossas M, Koch M, Kessler P, Vonesch JL, Schwab Y, Kieffer BL, Massotte D. In vivo visualization of 8-opioid receptors upon physiological activation uncovers a distinct internalization profile. J Neu-rosci 32: 7301-7310, 2012.
21. Foltz M, Ansems P, Schwarz J, Tasker MC, Lourbakos A, Gerhardt CC. Protein hydrolysates induce CCK release from enteroendocrine cells and act as partial agonists of the CCK1 receptor. J Agric Food Chem 56: 837-843, 2008.
22. Fujita T. Taste cells in the gut and on the tongue. Their common, paraneuronal features. Physiol Behav 49: 883-885, 1991.
23. Guan D, Green GM. Significance of peptic digestion in rat pancreatic secretory response to dietary protein. Am J Physiol Gastrointest Liver Physiol 271: G42-G47, 1996.
24. He W, Yasumatsu K, Varadarajan V, Yamada A, Lem J, Ninomiya Y, Margolskee RF, Damak S. Umami taste responses are mediated by a-transducin and a-gustducin. J Neurosci 24: 7674-7680, 2004.
25. Hira T, Maekawa T, Asano K, Hara H. Cholecystokinin secretion induced by fj-conglycinin peptone depends on Gaq-mediated pathways in enteroendocrine cells. Eur J Nutr 48: 124-127, 2009.
26. Hira T, Nakajima S, Eto Y, Hara H. Calcium-sensing receptor mediates phenylalanine-induced cholecystokinin secretion in enteroendocrine STC-1 cells. FEBS J 275: 4620-4626, 2008.
27. Hirasawa A, Tsumaya K, Awaji T, Katsuma S, Adachi T, Yamada M, Sugimoto Y, Miyazaki S, Tsujimoto G. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med 11: 90-94, 2005.
28. Ikeda K. New seasonings. Chem Senses 27: 847-849, 2002.
29. Imoto T, Miyasaka A, Ishima R, Akasaka K. A novel peptide isolated from the leaves of Gymnema sylvestre. I. Characterization and its suppressive effect on the neural responses to sweet stimuli in the rat. Comp Biochem Physiol A 100: 309-314, 1991.
30. Ivy AC, Oldberg E. A hormone mechanism for gallbladder contraction and evacuation. Am J Physiol 86: 599-613, 1928.
31. Jalink K, Moolenaar WH. G protein-coupled receptors: the inside story. Bioessays 32: 13-16, 2010.
32. Jang HJ, Kokrashvili Z, Theodorakis MJ, Carlson OD, Kim BJ, Zhou J, Kim HH, Xu X, Chan SL, Juhaszova M, Bernier M, Mosinger B, Margolskee RF, Egan JM. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proc Natl Acad Sci USA 104: 15069-15074, 2007.
33. Kokrashvili Z, Mosinger B, Margolskee RF. Taste signaling elements expressed in gut enteroendocrine cells regulate nutrient-responsive secretion of gut hormones. Am J Clin Nutr 90: 822S-825S, 2009.
34. Koop I, Buchan AM. Cholecystokinin release from isolated canine epithelial cells in short-term culture. Gastroenterology 102: 28-34, 1992.
35. 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.
36. Liddle RA. Cholecystokinin. In: Gut Peptides: Biochemistry and Physiology, edited by Walsh JH, Dockray GJ. New York: Raven, 1994.
37. Liou AP, Chavez DI, Espero E, Hao S, Wank SA, Raybould HE. Protein hydrolysate-induced cholecystokinin secretion from enteroendocrine cells is indirectly mediated by the intestinal oligopeptide transporter PepT1. Am J Physiol Gastrointest Liver Physiol 300: G895-G902, 2011.
38. Liou AP, Lu X, Sei Y, Zhao X, Pechhold S, Carrero RJ, Raybould HE, Wank S. The G-protein-coupled receptor GPR40 directly mediates long-chain fatty acid-induced secretion of cholecystokinin. Gastroenterology 140: 903-912, 2011.
39. Liou AP, Sei Y, Zhao X, Feng J, Lu X, Thomas C, Pechhold S, Raybould HE, Wank SA. The extracellular calcium-sensing receptor is required for cholecystokinin secretion in response to L-phenylalanine in acutely isolated intestinal I cells. Am J Physiol Gastrointest Liver Physiol 300: G538-G546, 2011.
40. Magalhaes AC, Dunn H, Ferguson SS. Regulation of GPCR activity, trafficking and localization by GPCR-interacting proteins. Br J Pharmacol 165: 1717-1736, 2012.
41. Maillet EL, Pelletier L, Cardozo TJ, Quijada J, Silie P, Zhao B, Ninomiya Y, Max M, Margolskee RF. Gurmarin inhibits the sweet receptor by binding to the Venus fly trap module of T1R3 (Abstract). Chem Senses 34: A78, 2009.
42. +-glucose cotransporter 1. Proc Natl Acad Sci USA 104: 15075-15080, 2007.
43. McLaughlin SK, McKinnon PJ, Margolskee RF. Gustducin is a taste-cell-specific G protein closely related to the transducins. Nature 357: 563-569, 1992.
44. Meyer JH, Kelly GA, Spingola LJ, Jones RS. Canine gut receptors mediating pancreatic responses to luminal L-amino acids. Am J Physiol 231: 669-677, 1976.
45. +/glucose transporter 1 (SGLT1) is enhanced by supplementation of the diet of weaning piglets with artificial sweeteners. Br J Nutr 104: 637-646, 2010.
46. +/glucose co-transporter 1 (SGLT1) in the intestine of piglets weaned to different concentrations of dietary carbohydrate. Br J Nutr 104: 647-655, 2010.
47. Moran TH. Gut peptides in the control of food intake. Int J Obes (Lond) 33: S7-S10, 2009.
48. Nakajima S, Hira T, Eto Y, Asano K, Hara H. Soybean beta 51-63 peptide stimulates cholecystokinin secretion via a calcium-sensing receptor in enteroendocrine STC-1 cells. Regul Pept 159: 148-155, 2010.
49. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS. An amino-acid taste receptor. Nature 416: 199-202, 2002.
50. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS. Mammalian sweet taste receptors. Cell 106: 381-390, 2001.
51. 2+ receptor antagonists that stimulate secretion of parathyroid hormone. J Pharmacol Exp Ther 299: 323-331, 2001.
52. Némoz-Gaillard E, Bernard C, Abello J, Cordier-Bussat M, Chay-vialle JA, Cuber JC. Regulation of cholecystokinin secretion by peptones and peptidomimetic antibiotics in STC-1 cells. Endocrinology 139: 932-938, 1998.
53. Ninomiya Y, Imoto T. Gurmarin inhibition of sweet taste responses in mice. Am J Physiol Regul Integr Comp Physiol 268: R1019-R1025, 1995.
54. Ninomiya Y, Nakashima K, Fukuda A, Nishino H, Sugimura T, Hino A, Danilova V, Hellekant G. Responses to umami substances in taste bud cells innervated by the chorda tympani and glossopharyngeal nerves. J Nutr 130: 950S-953S, 2000.
55. Nishi T, Hara H, Hira T, Tomita F. Dietary protein peptic hydrolysates stimulate cholecystokinin release via direct sensing by rat intestinal mucosal cells. Exp Biol Med (Maywood) 226: 1031-1036, 2001.
56. Owyang C, May D, Louie DS. Trypsin suppression of pancreatic enzyme secretion. Differential effect on cholecystokinin release and the entero-pancreatic reflex. Gastroenterology 91: 637-643, 1986.
57. Rehfeld JF. Cholecystokinin. Clin Gastroenterol 9: 593-607, 1980.
58. Rindi G, Grant SG, Yiangou Y, Ghatei MA, Bloom SR, Bautch VL, Solcia E, Polak JM. Development of neuroendocrine tumors in the gastrointestinal tract of transgenic mice. Heterogeneity of hormone expression. Am J Pathol 136: 1349-1363, 1990.
59. Stearns AT, Balakrishnan A, Rhoads DB, Tavakkolizadeh A. Rapid upregulation of sodium-glucose transporter SGLT1 in response to intestinal sweet taste stimulation. Ann Surg 251: 865-871, 2010.
60. Sufian MK, Hira T, Asano K, Hara H. Peptides derived from dolicholin, a phaseolin-like protein in country beans (Dolichos lablab), potently stimulate cholecystokinin secretion from enteroendocrine STC-1 cells. J Agric Food Chem 55: 8980-8986, 2007.
61. 2+-sensing receptor. Am J Physiol Gastrointest Liver Physiol 300: G528-G537, 2011.
62. White WO, Schwartz GJ, Moran TH. Role of endogenous CCK in the inhibition of gastric emptying by peptone and Intralipid in rats. Regul Pept 88: 47-53, 2000.
63. Wu SV, Rozengurt N, Yang M, Young SH, Sinnett-Smith J, Rozen-gurt E. Expression of bitter taste receptors of the T2R family in the gastrointestinal tract and enteroendocrine STC-1 cells. Proc Natl Acad Sci USA 99: 2392-2397, 2002.
64. Yamaguchi S. The synergistic taste effect of monosodium glutamate and disodium 5'-inosinate. J Food Sci 32: 473-478, 1970.
65. Yamaguchi S. Basic properties of umami and effects on humans. Physiol Behav 49: 833-841, 1991.
66. 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 49: 919-925, 1991.
67. Yasumatsu K, Ogiwara Y, Takai S, Yoshida R, Iwatsuki K, Torii K, Margolskee RF, Ninomiya Y. Umami taste in mice uses multiple receptors and transduction pathways. J Physiol 590: 1155-1170, 2012.
68. Yasumatsu K, Ohkuri T, Sanematsu K, Shigemura N, Katsukawa H, Sako N, Ninomiya Y. Genetically-increased taste cell population with Gagustducin-coupled sweet receptors is associated with increase of gurmarin-sensitive taste nerve fibers in mice. BMC Neurosci 10: 152, 2009.
69. Yoshii K, Yokouchi C, Kurihara K. Synergistic effects of 5'-nucleotides on rat taste responses to various amino acids. Brain Res 367: 45-51, 1986.
70. Zhang F, Klebansky B, Fine RM, Xu H, Pronin A, Liu H, Tachdjian C, Li X. Molecular mechanism for the umami taste synergism. Proc Natl Acad Sci USA 105: 20930-20934, 2008.
71. 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.