Signaling mechanisms controlling taste cell function

Critical Reviews in Eukaryotic Gene Expression

Volumn 18, Issue 2, 2008, Pages 125-137

  Medler, Kathryn ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Signal transduction; Tastants; Taste receptors

Indexed keywords

AMINO ACID; CANNABINOID 2 RECEPTOR; CYCLIC AMP; GLUTAMIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; METABOTROPIC RECEPTOR 4; PHOSPHOLIPASE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; VANILLOID RECEPTOR 1;

BEHAVIOR; BITTER TASTE; CELL FUNCTION; CHEMICAL STRUCTURE; MATE CHOICE; NONHUMAN; PERCEPTION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SKIN EXAMINATION; SMELLING; SWEETNESS; TASTE DISCRIMINATION;

EID: 41149173254     PISSN: 10454403     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevEukarGeneExpr.v18.i2.20     Document Type: Review

References (98)

1. Farbman AI. Renewal of taste bud cells in rat circumvallate papillae. Cell Tissue Kinet. 1980;13(4):349-57.
2. Finger TE, Simon SA. Cell biology of taste epithelium. In: Finger TE, Silver WL, Restrepo D, editor. The neurobiology of taste and smell. New York: Wiley-Liss; 2000. p. 287-314.
3. Lindemann B. Taste reception. Physiol Rev. 1996;76(3):718-66.
4. Lindemann B. Receptors and transduction in taste. Nature. 2001;413(6852):219-25.
5. Kinnamon SC, Margolskee RF. Mechanisms of taste transduction. Curr Opin Neurobiol. 1996;6(4):506-13.
6. Medler KF, Margolskee RF, Kinnamon SC. Electrophysiological characterization of voltage-gated currents in defined taste cell types of mice. J Neurosci. 2003;23(7):2608-17.
7. DeFazio RA, Dvoryanchikov G, Maruyama Y, Kim JW, Pereira E, Roper SD, Chaudhari N. Separate populations of receptor cells and presynaptic cells in mouse taste buds. J Neurosci. 2006;26(15):3971-80.
8. Clapp TR, Medler KF, Damak S, Margolskee RF, Kinnamon SC. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biol. 2006;4:7.
9. Clapp TR, Yang R, Stoick CL, Kinnamon SC, Kinnamon JC. Morphologic characterization of rat taste receptor cells that express components of the phospholipase C signaling pathway. J Comp Neurol. 2004;468(3):311-21.
10. Romanov RA, Rogachevskaja OA, Bystrova MF, Jiang P, Margolskee RF, Kolesnikov SS. Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J. 2007;26(3):657-67.
11. Avenet P, Lindemann B. Noninvasive recording of receptor cell action potentials and sustained currents from single taste buds maintained in the tongue: the response to mucosal NaCl and amiloride. J Membr Biol. 1991;124(1):33-41.
12. + channel subunits in rat taste cells: localization and regulation by aldosterone. J Comp Neurol. 1999;405(3):406-20.
13. Doolin RE, Gilbertson TA. Distribution and characterization of functional amiloride-sensitive sodium channels in rat tongue. J Gen Physiol. 1996;107(4):545-54.
14. + receptor mechanisms. Chem Senses. 1995;20(1):37-46.
15. Smith DV, Ossebaard CA. Amiloride suppression of the taste intensity of sodium chloride: evidence from direct magnitude scaling. Physiol Behav. 1995;57(4):773-7.
16. + channel is made of three homologous subunits. Nature. 1994;367(6462):463-7.
17. Lyall V, Heck GL, Vinnikova AK, Ghosh S, Phan TH, Alam RI, Russell OF, Malik SA, Bigbee JW, DeSimone JA. The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant. J Physiol. 2004;558(Pt 1):147-59.
18. Lyall V, Heck GL, Phan TH, Mummalaneni S, Malik SA, Vinnikova AK, Desimone JA. Ethanol modulates the VR-1 variant amiloride-insensitive salt taste receptor. II. Effect on chorda tympani salt responses. J Gen Physiol. 2005;125(6):587-600.
19. Gunthorpe MJ, Benham CD, Randall A, Davis JB. The diversity in the vanilloid (TRPV) receptor family of ion channels. Trends Pharmacol Sci. 2002;23(4):183-91.
20. Ruiz C, Gutknecht S, Delay E, Kinnamon S. Detection of NaCl and KCl in TRPV1 knockout mice. Chem Senses. 2006;31(9):813-20.
21. Treesukosol Y, Lyall V, Heck GL, Desimone JA, Spector AC. A psychophysical and electrophysiological analysis of salt taste in Trpv1 null mice. Am J Physiol Regul Integr Comp Physiol. 2007;292(5):R1799-809.
22. Garty H, Palmer LG. Epithelial sodium channels: function, structure, and regulation. Physiol Rev. 1997;77(2):359-96.
23. Lin W, Ogura T, Kinnamon SC. Acid-activated cation currents in rat vallate taste receptor cells. J Neurophysiol. 2002;88(1):133-41.
24. Lyall V, Alam RI, Phan DQ, Ereso GL, Phan TH, Malik SA, Montrose MH, Chu S, Heck GL, Feldman GM, DeSimone JA. Decrease in rat taste receptor cell intracellular pH is the proximate stimulus in sour taste transduction. Am J Physiol Cell Physiol. 2001;281(3):C1005-13.
25. Richter TA, Caicedo A, Roper SD. Sour taste stimuli evoke Ca2+ and pH responses in mouse taste cells. J Physiol. 2003;547(Pt 2):475-83.
26. Sowalsky RA, Noble AC. Comparison of the effects of concentration, pH and anion species on astringency and sourness of organic acids. Chem Senses. 1998;23(3):343-9.
27. Stevens DR, Seifert R, Bufe B, Muller F, Kremmer E, Gauss R, Meyerhof W, Kaupp UB, Lindemann B. Hyperpolarization-activated channels HCN1 and HCN4 mediate responses to sour stimuli. Nature. 2001;413(6856):631-5.
28. Ugawa S, Minami Y, Guo W, Saishin Y, Takatsuji K, Yamamoto T, et al. Receptor that leaves a sour taste in the mouth. Nature. 1998;395(6702):555-6.
29. Ugawa S, Ueda T, Ishida Y, Nishigaki M, Shibata Y, Shimada S. Amiloride-blockable acid-sensing ion channels are leading acid sensors expressed in human nociceptors. J Clin Invest. 2002;110(8):1185-90.
30. Ugawa S, Yamamoto T, Ueda T, Ishida Y, Inagaki A, Nishigaki M, Tohyama M, Shimada S. Amiloride-insensitive currents of the acid-sensing ion channel-2a (ASIC2a)/ASIC2b heteromeric sour-taste receptor channel. J Neurosci. 2003;23(9):3616-22.
31. + channels. J Neurophysiol. 2004;92(5):2909-19.
32. Richter TA, Dvoryanchikov GA, Chaudhari N, Roper SD. Acid-sensitive two-pore domain potassium (K2P) channels in mouse taste buds. J Neurophysiol. 2004;92(3):1928-36.
33. Ishimaru Y, Inada H, Kubota M, Zhuang H, Tominaga M, Matsunami H. Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc Natl Acad Sci U S A. 2006;103(33):12569-74.
34. LopezJimenez ND, Cavenagh MM, Sainz E, Cruz-Ithier MA, Battey JF, Sullivan SL. Two members of the TRPP family of ion channels, Pkd1l3 and Pkd2l1, are co-expressed in a subset of taste receptor cells. J Neurochem. 2006;98(1):68-77.
35. Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, Kinnamon SC. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science. 2005;310(5753):1495-9.
36. Ruiz-Avila L, Wong GT, Damak S, Margolskee RF. Dominant loss of responsiveness to sweet and bitter compounds caused by a single mutation in α-gustducin. Proc Natl Acad Sci U S A. 2001;98(15):8868-73.
37. Wong GT, Gannon KS, Margolskee RF. Transduction of bitter and sweet taste by gustducin. Nature. 1996;381(6585):796-800.
38. Wong GT, Ruiz-Avila L, Ming D, Gannon KS, Margolskee RF. Biochemical and transgenic analysis of gustducin's role in bitter and sweet transduction. Cold Spring Harb Symp Quant Biol. 1996;61:173-84.
39. 2+ influx via store-operated channels. J Neurophysiol. 2002;87(6):3152-5.
40. Ming D, Ruiz-Avila L, Margolskee RF. Characterization and solubilization of bitter-responsive receptors that couple to gustducin. Proc Natl Acad Sci U S A. 1998;95(15):8933-8.
41. Ming D, Ninomiya Y, Margolskee RF. Blocking taste receptor activation of gustducin inhibits gustatory responses to bitter compounds. Proc Natl Acad Sci U S A. 1999;96(17):9903-8.
42. McLaughlin SK, McKinnon PJ, Margolskee RF. Gustducin is a taste-cell-specific G protein closely related to the transducins. Nature. 1992;357(6379):563-9.
43. McLaughlin SK, McKinnon PJ, Robichon A, Spickofsky N, Margolskee RF. Gustducin and transducin: a tale of two G proteins. Ciba Found Symp. 1993;179:186-200.
44. Hoon MA, Northup JK, Margolskee RF, Ryba NJ. Functional expression of the taste specific G-protein, α-gustducin. Biochem J. 1995;309(Pt 2):629-36.
45. Danilova V, Damak S, Margolskee RF, Hellekant G. Taste responses to sweet stimuli in α-gustducin knockout and wild-type mice. Chem Senses. 2006;31(6):573-80.
46. Caicedo A, Pereira E, Margolskee RF, Roper SD. Role of the G-protein subunit α-gustducin in taste cell responses to bitter stimuli. J Neurosci. 2003;23(30): 9947-52.
47. Glendinning JI, Bloom LD, Onishi M, Zheng KH, Damak S, Margolskee RF, Spector AC. Contribution of α-gustducin to taste-guided licking responses of mice. Chem Senses. 2005;30(4):299-316.
48. He W, Yasumatsu K, Varadarajan V, Yamada A, Lem J, Ninomiya Y, Margolskee RF, Damak S. Umami taste responses are mediated by α-transducin and α-gustducin. J Neurosci. 2004;24(35):7674-80.
49. Ruiz CJ, Wray K, Delay E, Margolskee RF, Kinnamon SC. Behavioral evidence for a role of α-gustducin in glutamate taste. Chem Senses. 2003;28(7):573-9.
50. He W, Danilova V, Zou S, Hellekant G, Max M, Margolskee RF, Damak S. Partial rescue of taste responses of α-gustducin null mice by transgenic expression of α-transducin. Chem Senses. 2002;27(8):719-27.
51. Spickofsky N, Robichon A, Danho W, Fry D, Greeley D, Graves B, Madison V, Margolskee RF. Biochemical analysis of the transducin-phosphodiesterase interaction. Nat Struct Biol. 1994;1(11):771-81.
52. McLaughlin SK, McKinnon PJ, Spickofsky N, Danho W, Margolskee RF. Molecular cloning of G proteins and phosphodiesterases from rat taste cells. Physiol Behav. 1994;56(6):1157-64.
53. Ruiz-Avila L, McLaughlin SK, Wildman D, McKinnon PJ, Robichon A, Spickofsky N, Margolskee RF. Coupling of bitter receptor to phosphodiesterase through transducin in taste receptor cells. Nature. 1995;376(6535):80-5.
54. 3 responses to bitter denatonium. Nat Neurosci. 1999;2(12):1055-62.
55. 3 and α-gustducin-dependent fall in cyclic nucleotides. Am J Physiol Cell Physiol. 2001;280(4):C742-51.
56. Rossler P, Boekhoff I, Tareilus E, Beck S, Breer H, Freitag J. G protein βγ complexes in circumvallate taste cells involved in bitter transduction. Chem Senses. 2000;25(4):413-21.
57. Rossler P, Kroner C, Freitag J, Noe J, Breer H. Identification of a phospholipase C β subtype in rat taste cells. Eur J Cell Biol. 1998;77(3):253-61.
58. 3 receptor with signaling components of bitter taste transduction. BMC Neurosci. 2001;2:6.
59. 3 receptor type 3 and PLCβ2 are co-expressed with taste receptors T1R and T2R in rat taste bud cells. Chem Senses. 2001;26(3):259-65.
60. Perez CA, Huang L, Rong M, Kozak JA, Preuss AK, Zhang H, Max M, Margolskee RF. A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci. 2002;5(11):1169-76.
61. Perez CA, Margolskee RF, Kinnamon SC, Ogura T. Making sense with TRP channels: store-operated calcium entry and the ion channel Trpm5 in taste receptor cells. Cell Calcium. 2003;33(5-6):541-9.
62. i. Proc Natl Acad Sci U S A. 2003;100(25):15166-71.
63. 2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci U S A. 2003;100(25):15160-5.
64. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, Zuker CS, Ryba NJ. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell. 2003;112(3):293-301.
65. Dotson CD, Roper SD, Spector AC. PLCβ2-independent behavioral avoidance of prototypical bittertasting ligands. Chem Senses. 2005;30(7):593-600.
66. Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Perez CA, Shigemura N, Yoshida R, Mosinger B Jr, Glendinning JI, Ninomiya Y, Margolskee RF. Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses. 2006;31(3):253-64.
67. 2+-activated monovalent selective cation channel. Curr Biol. 2003;13(13):1153-8.
68. Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJ, Zuker CS. A novel family of mammalian taste receptors. Cell. 2000;100(6):693-702.
69. Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zuker CS, Ryba NJ. T2Rs function as bitter taste receptors. Cell. 2000;100(6):703-11.
70. Caicedo A, Roper SD. Taste receptor cells that discriminate between bitter stimuli. Science. 2001;291(5508):1557-60.
71. Sawano S, Seto E, Mori T, Hayashi Y. G-prote-independent and -independent pathways in denatonium signal transduction. Biosci Biotechnol Biochem. 2005;69(9):1643-51.
72. 2+ from intracellular stores: a novel mechanism for transduction of bitter stimuli. J Neurophysiol. 1999;82(5):2657-66.
73. 2+ in response to sugars and non-sugar sweeteners in transduction of sweet taste in the rat. J Physiol. 1996;490 (Pt 2):325-36.
74. Naim M, Ronen T, Striem BJ, Levinson M, Zehavi U. Adenylate cyclase responses to sucrose stimulation in membranes of pig circumvallate taste papillae. Comp Biochem Physiol B. 1991;100(3):455-8.
75. Zubare-Samuelov M, Peri I, Tal M, Tarshish M, Spielman AI, Naim M. Some sweet and bitter tastants stimulate inhibitory pathway of adenylyl cyclase via melatonin and α 2-adrenergic receptors in Xenopus laevis melanophores. Am J Physiol Cell Physiol. 2003;285(5):C1255-62.
76. Striem BJ, Pace U, Zehavi U, Naim M, Lancet D. Sweet tastants stimulate adenylate cyclase coupled to GTP-binding protein in rat tongue membranes. Biochem J. 1989;260(1):121-6.
77. Krizhanovsky V, Agamy O, Naim M. Sucrose-stimulated subsecond transient increase in cGMP level in rat intact circumvallate taste bud cells. Am J Physiol Cell Physiol. 2000;279(1):C120-5.
78. Montmayeur JP, Matsunami H. Receptors for bitter and sweet taste. Curr Opin Neurobiol. 2002;12(4):366-71.
79. Montmayeur JP, Liberles SD, Matsunami H, Buck LB. A candidate taste receptor gene near a sweet taste locus. Nat Neurosci. 2001;4(5):492-8.
80. Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS. The receptors for mammalian sweet and umami taste. Cell. 2003;115(3):255-66.
81. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS. Mammalian sweet taste receptors. Cell. 2001;106(3):381-90.
82. Hoon MA, Adler E, Lindemeier J, Battey JF, Ryba NJ, Zuker CS. Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell. 1999;96(4):541-51.
83. 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. 2001;28(1):58-63.
84. Sainz E, Korley JN, Battey JF, Sullivan SL. Identification of a novel member of the T1R family of putative taste receptors. J Neurochem. 2001;77(3):896-903.
85. Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E. Human receptors for sweet and umami taste. Proc Natl Acad Sci U S A. 2002;99(7):4692-6.
86. Stone LM, Barrows J, Finger TE, Kinnamon SC. Expression of T1Rs and gustducin in palatal taste buds of mice. Chem Senses. 2007;32(3):255-62.
87. Nakashima K, Ninomiya Y. Increase in inositol 1,4,5-triphosphate levels of the fungiform papilla in response to saccharin and bitter substances in mice. Cell Physiol Biochem. 1998;8(4):224-30.
88. Nakashima K, Ninomiya Y. Transduction for sweet taste of saccharin may involve both inositol 1,4,5-triphosphate and cAMP pathways in the fungiform taste buds in C57BL mice. Cell Physiol Biochem. 1999;9(2):90-8.
89. Cummings TA, Powell J, Kinnamon SC. Sweet taste transduction in hamster taste cells: evidence for the role of cyclic nucleotides. J Neurophysiol. 1993;70(6):2326-36.
90. + current. J Neurophysiol. 1996;75(3):1256-63.
91. Trubey KR, Culpepper S, Maruyama Y, Kinnamon SC, Chaudhari N. Tastants evoke cAMP signal in taste buds that is independent of calcium signaling. Am J Physiol Cell Physiol. 2006;291(2):C237-44.
92. Abaffy T, Trubey KR, Chaudhari N. Adenylyl cyclase expression and modulation of cAMP in rat taste cells. Am J Physiol Cell Physiol. 2003;284(6):C1420-8.
93. Varkevisser B, Kinnamon SC. Sweet taste transduction in hamster: role of protein kinases. J Neurophysiol. 2000;83(5):2526-32.
94. Chaudhari N, Yang H, Lamp C, Delay E, Cartford C, Than T, Roper S. The taste of monosodium glutamate: membrane receptors in taste buds. J Neurosci. 1996;16(12):3817-26.
95. Purves D. Neuroscience. 3rd ed. Sunderland (MA): Sinauer Associates, Inc.; 2004.
96. Chaudhari N, Landin AM, Roper SD. A metabotropic glutamate receptor variant functions as a taste receptor. Nat Neurosci. 2000;3(2):113-9.
97. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS. An amino-acid taste receptor. Nature. 2002;416(6877):199-202.
98. 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. 2003;301(5634):850-3.