Peptide regulators of peripheral taste function

Seminars in Cell and Developmental Biology

Volumn 24, Issue 3, 2013, Pages 232-239

  Dotson, Cedrick D ^a   Geraedts, Maartje C P ^b   Munger, Steven D ^b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Cholecystokinin; Glucagon; Glucagon like peptide 1; Gustatory; Neuropeptide; Sweet

Indexed keywords

CHOLECYSTOKININ; GALANIN; GHRELIN; GLUCAGON; GLUCAGON LIKE PEPTIDE 1; NEUROPEPTIDE Y; PEPTIDE; PEPTIDE YY; VASOACTIVE INTESTINAL POLYPEPTIDE;

APPETITE; BRAIN; GUSTATORY SYSTEM; HUMAN; METABOLISM; PANCREAS; PROTEIN EXPRESSION; REVIEW; SATIETY; SENSORY NERVE CELL; TASTE; TASTE BUD;

EID: 84875610335     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2013.01.004     Document Type: Review

References (109)

1. Field G.D., Chichilnisky E.J. Information processing in the primate retina: circuitry and coding. Annual Review of Neuroscience 2007, 30:1-30.
2. Tranchina D., Gordon J., Shapley R., Toyoda J. Linear information processing in the retina: a study of horizontal cell responses. Proceedings of the National Academy of Sciences of the United States of America 1981, 78:6540-6542.
3. Schiller P.H. Parallel information processing channels created in the retina. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:17087-17094.
4. Leinwand S.G., Chalasani S.H. Olfactory networks: from sensation to perception. Current Opinion in Genetics and Development 2011, 21:806-811.
5. Savigner A., Duchamp-Viret P., Grosmaitre X., Chaput M., Garcia S., Ma M., et al. Modulation of spontaneous and odorant-evoked activity of rat olfactory sensory neurons by two anorectic peptides, insulin and leptin. Journal of Neurophysiology 2009, 101:2898-2906.
6. Hall R.A. Autonomic modulation of olfactory signaling. Sci Signaling 2011, 4:pe1.
7. Levine J.D., Fields H.L., Basbaum A.I. Peptides and the primary afferent nociceptor. Journal of Neuroscience 1993, 13:2273-2286.
8. Kurt S., Sausbier M., Ruttiger L., Brandt N., Moeller C.K., Kindler J., et al. Critical role for cochlear hair cell BK channels for coding the temporal structure and dynamic range of auditory information for central auditory processing. FASEB Journal 2012, 26:3834-3843.
9. Meyer A.C., Moser T. Structure and function of cochlear afferent innervation. Current Opinion in Otolaryngology & Head and Neck Surgery 2010, 18:441-446.
10. Ross M.D., Donovan K. Gravity receptors: an ultrastructural basis for peripheral sensory processing. Physiologist 1984, 27:S85-S86.
11. Davies S.N. Evidence for peripheral, but not central modulation of trigeminal cold receptive cells in the rat. Brain Research 1984, 301:299-305.
12. Yarmolinsky D.A., Zuker C.S., Ryba N.J. Common sense about taste: from mammals to insects. Cell 2009, 139:234-244.
13. Chaudhari N., Roper S.D. The cell biology of taste. Journal of Cell Biology 2010, 190:285-296.
14. Bartel D.L., Sullivan S.L., Lavoie E.G., Sevigny J., Finger T.E. Nucleoside triphosphate diphosphohydrolase-2 is the ecto-ATPase of type I cells in taste buds. Journal of Comparative Neurology 2006, 497:1-12.
15. Yoshida R., Horio N., Murata Y., Yasumatsu K., Shigemura N., Ninomiya Y. NaCl responsive taste cells in the mouse fungiform taste buds. Neuroscience 2009, 159:795-803.
16. Vandenbeuch A., Clapp T.R., Kinnamon S.C. Amiloride-sensitive channels in type I fungiform taste cells in mouse. BMC Neuroscience 2008, 9:1.
17. Chandrashekar J., Kuhn C., Oka Y., Yarmolinsky D.A., Hummler E., Ryba N.J., et al. The cells and peripheral representation of sodium taste in mice. Nature 2010, 464:297-301.
18. Nelson G., Hoon M.A., Chandrashekar J., Zhang Y., Ryba N.J., Zuker C.S. Mammalian sweet taste receptors. Cell 2001, 106:381-390.
19. Adler E., Hoon M.A., Mueller K.L., Chandrashekar J., Ryba N.J., Zuker C.S. A novel family of mammalian taste receptors. Cell 2000, 100:693-702.
20. DeFazio R.A., Dvoryanchikov G., Maruyama Y., Kim J.W., Pereira E., Roper S.D., et al. Separate populations of receptor cells and presynaptic cells in mouse taste buds. Journal of Neuroscience 2006, 26:3971-3980.
21. Clapp T.R., Medler K.F., Damak S., Margolskee R.F., Kinnamon S.C. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biology 2006, 4:7.
22. Huang A., Chen X., Hoon M., Chandrashekar J., Guo W., Tränkner D., et al. The cells and logic for mammalian sour taste detection. Nature 2006, 442:934-938.
23. Kataoka S., Yang R., Ishimaru Y., Matsunami H., Sévigny J., Kinnamon J., et al. The candidate sour taste receptor, PKD2L1, is expressed by type III taste cells in the mouse. Chemical Senses 2008, 33:243-254.
24. Sullivan J.M., Borecki A.A., Oleskevich S. Stem and progenitor cell compartments within adult mouse taste buds. European Journal of Neuroscience 2010, 31:1549-1560.
25. Finger T.E., Danilova V., Barrows J., Bartel D.L., Vigers A.J., Stone L., et al. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 2005, 310:1495-1499.
26. Huang Y.J., Maruyama Y., Dvoryanchikov G., Pereira E., Chaudhari N., Roper S.D.C.P. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:6436-6441.
27. Dando R., Roper S.D. Cell-to-cell communication in intact taste buds through ATP signalling from pannexin 1 gap junction hemichannels. Journal of Physiology 2009, 587:5899-5906.
28. Romanov R.A., Rogachevskaja O.A., Bystrova M.F., Jiang P., Margolskee R.F., Kolesnikov S.S. Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO Journal 2007, 26:657-667.
29. Bo X., Alavi A., Xiang Z., Oglesby I., Ford A., Burnstock G. Localization of ATP-gated P2X2 and P2X3 receptor immunoreactive nerves in rat taste buds. Neuroreport 1999, 10:1107-1111.
30. Yang R., Montoya A., Bond A., Walton J., Kinnamon J.C. Immunocytochemical analysis of P2X2 in rat circumvallate taste buds. BMC Neuroscience 2012, 13:51.
31. Dando R., Roper S.D. Acetylcholine is released from taste cells, enhancing taste signalling. Journal of Physiology 2012, 590:3009-3017.
32. 2+ in taste cells via activation of muscarinic receptors. Journal of Neurophysiology 2002, 87:2643-2649.
33. Dvoryanchikov G., Huang Y.A., Barro-Soria R., Chaudhari N., Roper S.D. GABA, its receptors, and GABAergic inhibition in mouse taste buds. Journal of Neuroscience 2011, 31:5782-5791.
34. Huang Y.A., Maruyama Y., Roper S.D. Norepinephrine is coreleased with serotonin in mouse taste buds. Journal of Neuroscience 2008, 28:13088-13093.
35. Huang Y.A., Maruyama Y., Stimac R., Roper S.D. Presynaptic (Type III) cells in mouse taste buds sense sour (acid) taste. Journal of Physiology 2008, 586:2903-2912.
36. Huang Y.A., Dando R., Roper S.D. Autocrine and paracrine roles for ATP and serotonin in mouse taste buds. Journal of Neuroscience 2009, 29:13909-13918.
37. Huang Y.A., Pereira E., Roper S.D. Acid stimulation (sour taste) elicits GABA and serotonin release from mouse taste cells. PLoS ONE 2011, 6:e25471.
38. Obata H., Shimada K., Sakai N., Saito N. GABAergic neurotransmission in rat taste buds: immunocytochemical study for GABA and GABA transporter subtypes. Brain Research: Molecular Brain Research 1997, 49:29-36.
39. Cao Y., Zhao F.L., Kolli T., Hivley R., Herness S.G.A.B.A. expression in the mammalian taste bud functions as a route of inhibitory cell-to-cell communication. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:4006-4011.
40. Shin Y.K., Martin B., Golden E., Dotson C.D., Maudsley S., Kim W., et al. Modulation of taste sensitivity by GLP-1 signaling. Journal of Neurochemistry 2008, 106:455-463.
41. Elson A.E., Dotson C.D., Egan J.M., Munger S.D. Glucagon signaling modulates sweet taste responsiveness. FASEB Journal 2010, 24:3960-3969.
42. Feng X.H., Liu X.M., Zhou L.H., Wang J., Liu G.D. Expression of glucagon-like peptide-1 in the taste buds of rat circumvallate papillae. Acta Histochemica 2008, 110:151-154.
43. Shen T., Kaya N., Zhao F.L., Lu S.G., Cao Y., Herness S. Co-expression patterns of the neuropeptides vasoactive intestinal peptide and cholecystokinin with the transduction molecules alpha-gustducin and T1R2 in rat taste receptor cells. Neuroscience 2005, 130:229-238.
44. Herness S., Zhao F.L., Lu S.G., Kaya N., Shen T. Expression and physiological actions of cholecystokinin in rat taste receptor cells. Journal of Neuroscience 2002, 22:10018-10029.
45. Zhao F.L., Shen T., Kaya N., Lu S.G., Cao Y., Herness S.C. Expression, physiological action, and coexpression patterns of neuropeptide Y in rat taste-bud cells. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:11100-11105.
46. Acosta A., Hurtado M.D., Gorbatyuk O., La Sala M., Duncan D., Aslanidi G., et al. Salivary PYY: a putative bypass to satiety. PLoS ONE 2011, 6:e26137.
47. Herness M.S. Vasoactive intestinal peptide-like immunoreactivity in rodent taste cells. Neuroscience 1989, 33:411-419.
48. Martin B., Shin Y.K., White C.M., Ji S., Kim W., Carlson O.D., et al. Vasoactive intestinal peptide-null mice demonstrate enhanced sweet taste preference, dysglycemia, and reduced taste bud leptin receptor expression. Diabetes 2010, 59:1143-1152.
49. Shin Y.K., Martin B., Kim W., White C.M., Ji S., Sun Y., et al. Ghrelin is produced in taste cells and ghrelin receptor null mice show reduced taste responsivity to salty (NaCl) and sour (citric acid) tastants. PLoS ONE 2010, 5:e12729.
50. Seta Y., Kataoka S., Toyono T., Toyoshima K. Expression of galanin and the galanin receptor in rat taste buds. Archives of Histology and Cytology 2006, 69:273-280.
51. Herness S., Zhao F.L. The neuropeptides CCK and NPY and the changing view of cell-to-cell communication in the taste bud. Physiology and Behavior 2009, 97:581-591.
52. Shin A.C., Townsend R.L., Patterson L.M., Berthoud H.R. "Liking" and "wanting" of sweet and oily food stimuli as affected by high-fat diet-induced obesity, weight loss, leptin, and genetic predisposition. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 2011, 301:R1267-R1280.
53. Le Roux C.W., Bueter M., Theis N., Werling M., Ashrafian H., Lowenstein C., et al. Gastric bypass reduces fat intake and preference. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 2011, 301:R1057-R1066.
54. Tichansky D.S., Glatt A.R., Madan A.K., Harper J., Tokita K., Boughter J.D. Decrease in sweet taste in rats after gastric bypass surgery. Surgical Endoscopy 2011, 25:1176-1181.
55. Hajnal A., Kovacs P., Ahmed T., Meirelles K., Lynch C.J., Cooney R.N. Gastric bypass surgery alters behavioral and neural taste functions for sweet taste in obese rats. American Journal of Physiology: Gastrointestinal and Liver Physiology 2010, 299:G967-G979.
56. Olbers T., Bjorkman S., Lindroos A., Maleckas A., Lonn L., Sjostrom L., et al. Body composition, dietary intake, and energy expenditure after laparoscopic Roux-en-Y gastric bypass and laparoscopic vertical banded gastroplasty: a randomized clinical trial. Annals of Surgery 2006, 244:715-722.
57. Chen K., Yan J., Suo Y., Li J., Wang Q., Lv B. Nutritional status alters saccharin intake and sweet receptor mRNA expression in rat taste buds. Brain Research 2010, 1325:53-62.
58. Umabiki M., Tsuzaki K., Kotani K., Nagai N., Sano Y., Matsuoka Y., et al. The improvement of sweet taste sensitivity with decrease in serum leptin levels during weight loss in obese females. Tohoku Journal of Experimental Medicine 2010, 220:267-271.
59. Nakamura Y., Sanematsu K., Ohta R., Shirosaki S., Koyano K., Nonaka K., et al. Diurnal variation of human sweet taste recognition thresholds is correlated with plasma leptin levels. Diabetes 2008, 57:2661-2665.
60. Shigemura N., Ohta R., Kusakabe Y., Miura H., Hino A., Koyano K., et al. Leptin modulates behavioral responses to sweet substances by influencing peripheral taste structures. Endocrinology 2004, 145:839-847.
61. Kawai K., Sugimoto K., Nakashima K., Miura H., Ninomiya Y.C. Leptin as a modulator of sweet taste sensitivities in mice. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:11044-11049.
62. Baggio L.L., Drucker D.J. Biology of incretins: GLP-1 and GIP. Gastroenterology 2007, 132:2131-2157.
63. Brubaker P.L. The glucagon-like peptides: pleiotropic regulators of nutrient homeostasis. Annals of the New York Academy of Sciences 2006, 1070:10-26.
64. Holst J.J., Orskov C., Nielsen O.V., Schwartz T.W. Truncated glucagon-like peptide I, an insulin-releasing hormone from the distal gut. FEBS Letters 1987, 211:169-174.
65. Maljaars P.W., Peters H.P., Mela D.J., Masclee A.A. Ileal brake: a sensible food target for appetite control. A review. Physiology and Behavior 2008, 95:271-281.
66. Williams D.L. Minireview: finding the sweet spot: peripheral versus central glucagon-like peptide 1 action in feeding and glucose homeostasis. Endocrinology 2009, 150:2997-3001.
67. Scrocchi L.A., Brown T.J., MaClusky N., Brubaker P.L., Auerbach A.B., Joyner A.L., et al. Glucose intolerance but normal satiety in mice with a null mutation in the glucagon-like peptide 1 receptor gene. Nature Medicine 1996, 2:1254-1258.
68. Martin B., Dotson C.D., Shin Y.K., Ji S., Drucker D.J., Maudsley S., et al. Modulation of taste sensitivity by GLP-1 signaling in taste buds. Annals of the New York Academy of Sciences 2009, 1170:98-101.
69. Martin C., Passilly-Degrace P., Chevrot M., Ancel D., Sparks S.M., Drucker D.J., et al. Lipid-mediated release of GLP-1 by mouse taste buds from circumvallate papillae: putative involvement of GPR120 and impact on taste sensitivity. Journal of Lipid Research 2012, 53:2256-2265.
70. Mathes C.M., Bueter M., Smith K.R., Lutz T.A., le Roux C.W., Spector A.C. Roux-en-Y gastric bypass in rats increases sucrose taste-related motivated behavior independent of pharmacological GLP-1-receptor modulation. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 2012, 302:R751-R767.
71. Unger R.H., Cherrington A.D. Glucagonocentric restructuring of diabetes: a pathophysiologic and therapeutic makeover. Journal of Clinical Investigation 2012, 122:4-12.
72. Gelling R.W., Vuguin P.M., Du X.Q., Cui L., Romer J., Pederson R.A., et al. Pancreatic beta-cell overexpression of the glucagon receptor gene results in enhanced beta-cell function and mass. American Journal of Physiology: Endocrinology and Metabolism 2009, 297:E695-E707.
73. Kieffer T.J., Heller R.S., Unson C.G., Weir G.C., Habener J.F. Distribution of glucagon receptors on hormone-specific endocrine cells of rat pancreatic islets. Endocrinology 1996, 137:5119-5125.
74. Ma X., Zhang Y., Gromada J., Sewing S., Berggren P.O., Buschard K., et al. Glucagon stimulates exocytosis in mouse and rat pancreatic alpha-cells by binding to glucagon receptors. Molecular Endocrinology 2005, 19:198-212.
75. Brubaker P.L., Drucker D.J. Structure-function of the glucagon receptor family of G protein-coupled receptors: the glucagon, GIP, GLP-1, and GLP-2 receptors. Receptors and Channels 2002, 8:179-188.
76. Moran T.H., Kinzig K.P. Gastrointestinal satiety signals II. Cholecystokinin. American Journal of Physiology: Gastrointestinal and Liver Physiology 2004, 286:G183-G188.
77. Staljanssens D., Azari E.K., Christiaens O., Beaufays J., Lins L., Van Camp J., et al. The CCK(-like) receptor in the animal kingdom: functions, evolution and structures. Peptides 2011, 32:607-619.
78. Hajnal A., Covasa M., Bello N.T. Altered taste sensitivity in obese, prediabetic OLETF rats lacking CCK-1 receptors. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 2005, 289:R1675-R1686.
79. Said S.I., Mutt V. Polypeptide with broad biological activity: isolation from small intestine. Science 1970, 169:1217-1218.
80. Moody T.W., Ito T., Osefo N., Jensen R.T.V.I.P PACAP: recent insights into their functions/roles in physiology and disease from molecular and genetic studies. Current Opinion in Endocrinology, Diabetes and Obesity 2011, 18:61-67.
81. Fahrenkrug J. Transmitter role of vasoactive intestinal peptide. Pharmacology and Toxicology 1993, 72:354-363.
82. Dickson L., Finlayson K.V.P.A.C PAC receptors: from ligands to function. Pharmacology and Therapeutics 2009, 121:294-316.
83. Kusakabe T., Matsuda H., Gono Y., Furukawa M., Hiruma H., Kawakami T., et al. Immunohistochemical localisation of regulatory neuropeptides in human circumvallate papillae. Journal of Anatomy 1998, 192(Pt 4):557-564.
84. Nguyen A.D., Herzog H., Sainsbury A. Neuropeptide Y and peptide YY: important regulators of energy metabolism. Current Opinion in Endocrinology, Diabetes and Obesity 2011, 18:56-60.
85. Zhang L., Bijker M.S., Herzog H. The neuropeptide Y system: pathophysiological and therapeutic implications in obesity and cancer. Pharmacology and Therapeutics 2011, 131:91-113.
86. Michel M.C., Beck-Sickinger A., Cox H., Doods H.N., Herzog H., Larhammar D., et al. XVI. International Union of Pharmacology recommendations for the nomenclature of neuropeptide Y, peptide YY, and pancreatic polypeptide receptors. Pharmacological Reviews 1998, 50:143-150.
87. Tatemoto K., Carlquist M., Mutt V. Neuropeptide Y - a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 1982, 296:659-660.
88. Chen C.H., Stephens R.L., Rogers R.C. PYY and NPY: control of gastric motility via action on Y1 and Y2 receptors in the DVC. Neurogastroenterology and Motility 1997, 9:109-116.
89. Hastings J.A., McClure-Sharp J.M., Morris M.J. NPY Y1 receptors exert opposite effects on corticotropin releasing factor and noradrenaline overflow from the rat hypothalamus in vitro. Brain Research 2001, 890:32-37.
90. Leibowitz S.F., Alexander J.T. Analysis of neuropeptide Y-induced feeding: dissociation of Y1 and Y2 receptor effects on natural meal patterns. Peptides 1991, 12:1251-1260.
91. Hurtado M.D., Acosta A., Riveros P.P., Baum B.J., Ukhanov K., Brown A.R., et al. Distribution of y-receptors in murine lingual epithelia. PLoS ONE 2012, 7:e46358.
92. Hansel D.E., Eipper B.A., Ronnett G.V. Neuropeptide Y functions as a neuroproliferative factor. Nature 2001, 410:940-944.
93. Michel M.C., Fliers E., Van Noorden C.J. Dipeptidyl peptidase IV inhibitors in diabetes: more than inhibition of glucagon-like peptide-1 metabolism. Naunyn-Schmiedebergs Archives of Pharmacology 2008, 377:205-207.
94. Hartel S., Gossrau R., Hanski C., Reutter W. Dipeptidyl peptidase (DPP) IV in rat organs. Comparison of immunohistochemistry and activity histochemistry. Histochemistry 1988, 89:151-161.
95. Kojima M., Hosoda H., Date Y., Nakazato M., Matsuo H., Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1999, 402:656-660.
96. Inui A., Asakawa A., Bowers C.Y., Mantovani G., Laviano A., Meguid M.M., et al. Ghrelin, appetite, and gastric motility: the emerging role of the stomach as an endocrine organ. FASEB Journal 2004, 18:439-456.
97. Sato T., Nakamura Y., Shiimura Y., Ohgusu H., Kangawa K., Kojima M. Structure, regulation and function of ghrelin. Journal of Biochemistry 2012, 151:119-128.
98. Tatemoto K., Rokaeus A., Jornvall H., McDonald T.J., Mutt V. Galanin - a novel biologically active peptide from porcine intestine. FEBS Letters 1983, 164:124-128.
99. Branchek T.A., Smith K.E., Gerald C., Walker M.W. Galanin receptor subtypes. Trends in Pharmacological Sciences 2000, 21:109-117.
100. Waters S.M., Krause J.E. Distribution of galanin-1, -2 and -3 receptor messenger RNAs in central and peripheral rat tissues. Neuroscience 2000, 95:265-271.
101. Kaplan L.M., Spindel E.R., Isselbacher K.J., Chin W.W. Tissue-specific expression of the rat galanin gene. Proceedings of the National Academy of Sciences of the United States of America 1988, 85:1065-1069.
102. Koegler F.H., Ritter S. Galanin injection into the nucleus of the solitary tract stimulates feeding in rats with lesions of the paraventricular nucleus of the hypothalamus. Physiology and Behavior 1998, 63:521-527.
103. Wang S., Ghibaudi L., Hashemi T., He C., Strader C., Bayne M., et al. The GalR2 galanin receptor mediates galanin-induced jejunal contraction, but not feeding behavior, in the rat: differentiation of central and peripheral effects of receptor subtype activation. FEBS Letters 1998, 434:277-282.
104. Branchek T., Smith K.E., Walker M.W. Molecular biology and pharmacology of galanin receptors. Annals of the New York Academy of Sciences 1998, 863:94-107.
105. + channels. Journal of Biological Chemistry 1998, 273:23321-23326.
106. Mahoney S.A., Hosking R., Farrant S., Holmes F.E., Jacoby A.S., Shine J., et al. The second galanin receptor GalR2 plays a key role in neurite outgrowth from adult sensory neurons. Journal of Neuroscience 2003, 23:416-421.
107. Bueter M., Miras A.D., Chichger H., Fenske W., Ghatei M.A., Bloom S.R., et al. Alterations of sucrose preference after Roux-en-Y gastric bypass. Physiology and Behavior 2011, 104:709-721.
108. Miras A.D., le Roux C.W. Bariatric surgery and taste: novel mechanisms of weight loss. Current Opinion in Gastroenterology 2010, 26:140-145.
109. Sinclair M.S., Perea-Martinez I., Dvoryanchikov G., Yoshida M., Nishimori K., Roper S.D., et al. Oxytocin signaling in mouse taste buds. PLoS ONE 2010, 5:e11980.