Making sense with TRP channels: Store-operated calcium entry and the ion channel Trpm5 in taste receptor cells

Cell Calcium

Volumn 33, Issue 5-6, 2003, Pages 541-549

  Pérez, Cristian A ^a   Margolskee, Robert F ^a   Kinnamon, Sue C ^b,c   Ogura, Tatsuya ^b,c  

^a NEW YORK UNIVERSITY   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

Taste receptor cell; TRP channels; Trpm5

Indexed keywords

CALCIUM ION; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; ION CHANNEL; MEMBRANE PROTEIN; PHOSPHOLIPASE C; PROTEIN G; RECEPTOR PROTEIN; RECEPTOR SUBTYPE; TRANSIENT RECEPTOR POTENTIAL M5 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOPHYSICS; BITTER TASTE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; NONHUMAN; NUTRITIONAL STATUS; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TASTE BUD; TASTE DISCRIMINATION; XENOPUS;

MAMMALIA;

EID: 0038650737     PISSN: 01434160     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0143-4160(03)00059-9     Document Type: Article

References (86)

1. B. Lindemann, Taste reception, Physiol. Rev. 76 (1996) 718-766.
2. B. Lindemann, Receptors and transduction in taste, Nature 413 (2001) 219-225.
3. T.A. Gilbertson, S. Damak, R.F. Margolskee, The molecular physiology of taste transduction, Curt. Opin. Neurobiol. 10 (2000) 519-527.
4. T.A. Gilbertson, Role of the taste system in ingestive behavior. Studies in NaCl and fatty acid transduction, Ann. NY Acad. Sci. 855 (1998) 860-867.
5. J.I. Glendinning, S. Domdom, E. Long, Selective adaptation to noxious foods by a herbivorous insect, J. Exp. Biol. 204 (2001) 3355-3367.
6. J.A. DeSimone, V. Lyall, G.L. Heck, G.M. Feldman, Acid detection by taste receptor cells, Respir. Physiol. 129 (2001) 231-245.
7. C. Saper, T. Chou, J. Elmquist, The need to feed. Homeostatic and hedonic control of eating, Neuron 36 (2002) 199.
8. K. Nakamura, R. Norgren, Gustatory responses of neurons in the nucleus of the solitary tract of behaving rats, J. Neurophysiol. 66 (1991) 1232-1248.
9. F.H. Netter, 1989. Atlas of human anatomy. Icon Learning Systems, Summit, NJ.
10. D.B. Katz, M.A. Nicolelis, S.A. Simon, Gustatory processing is dynamic and distributed, Curr. Opin. Neurobiol. 12 (2002) 448-454.
11. R. Waldmann, G. Champigny, F. Bassilana, C. Heurteaux, M. Lazdunski, A proton-gated cation channel involved in acid-sensing, Nature 386 (1997) 173-177.
12. C.C. Askwith, C.J. Benson, M.J. Welsh, P.M. Snyder, DEG/ENaC ion channels involved in sensory transduction are modulated by cold temperature, Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 6459-6463.
13. S. Kellenberger, L. Schild, Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure, Physiol. Rev. 82 (2002) 735-767.
14. W. Lin, T.E. Finger, B.C. Rossier, S.C. Kinnamon, Epithelial Na+ channel subunits in rat taste cells: localization and regulation by aldosterone, J. Comp. Neurol. 405 (1999) 406-420.
15. W. Lin, T. Ogura, S.C. Kinnamon Acid-activated cation currents in rat vallate taste receptor cells, J. Neurophysiol. 88 (2002) 133-141.
16. D.R. Stevens, R. Seifert, B. Bufe, E Muller, E. Kremmer, R. Gauss, W. Meyerhof, U.B. Kaupp, B. Lindemann, Hyperpolarization activated channels HCN1 and HCN4 mediate responses to sour stimuli, Nature 413 (2001) 631-635.
17. R.F. Margolskee, Molecular mechanisms of bitter and sweet taste transduction, J. Biol. Chem. 277 (2002) 1-4.
18. J.P. Montmayeur, H. Matsunami, Receptors for bitter and sweet taste, Curr. Opin. Neurobiol. 12 (2002) 366-371.
19. E. Adler, M.A. Hoon, K.L. Mueller, J. Chandrashekar, N.J. Ryba, C.S. Zuker, A novel family of mammalian taste receptors, Cell 100 (2000) 693-702.
20. B. Bufe, T. Hofmann, D. Krautwurst, J.D. Raguse, W. Meyerhof, The human TAS2R16 receptor mediates bitter taste in response to beta glucopyranosides, Nat. Genet. 32 (2002) 397-401.
21. H. Matsunami, J.P. Montmayeur, L.B. Buck, A family of candidate taste receptors in human and mouse, Nature 404 (2000) 601-604.
22. M.A. Hoon, E. Adler, J. Lindemeier, J.F. Battey, N.J. Ryba, C.S. Zuker, Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity, Cell 96 (1999) 541-551.
23. A.A. Bachmanov, X. Li, D.R. Reed, J.D. Ohmen, S. Li, Z. Chen, M.G. Tordoff, P.J. de Jong, C. Wu, D.B. West, A. Chatterjee, D.A. Ross, G.K. Beauchamp, Positional cloning of the mouse saccharin preference (Sac) locus, Chem. Senses 26 (2001) 925-933.
24. M. Kitagawa, Y. Kusakabe, H. Miura, Y. Ninomiya, A. Hino, Molecular genetic identification of a candidate receptor gene for sweet taste, Biochem. Biophys. Res. Commum. 283 (2001) 236-242.
25. M. Max, Y.G. Shanker, L. Huang, M. Rong, Z. Liu, E Campagne, H. Weinstein, S. Damak, R.F. Margolskee, Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac, Nat. Genet. 28 (2001) 58-63.
26. J.P. Montmayeur, S.D. Liberles, H. Matsunami, L.B. Buck, A candidate taste receptor gene near a sweet taste locus, Nat. Neurosci. 4 (2001) 492-498.
27. E. Sainz, J.N. Korley, J.F. Battey, S.L. Sullivan, Identification of a novel member of the T1R family of putative taste receptors, J. Neurochem. 77 (2001) 896-903.
28. G. Nelson, J. Chandrashekar, M.A. Hoon, L. Feng, G. Zhao, N.J. Ryba, C.S. Zuker, An amino-acid taste receptor, Nature 416 (2002) 199-202.
29. G. Nelson, M.A. Hoon, J. Chandrashekar, Y. Zhang, N.J. Ryba, C.S. Zuker, Mammalian sweet taste receptors, Cell 106 (2001) 381-390.
30. X. Li, L. Staszewski, H. Xu, K. Durick, M. Zoller, E. Adler, Human receptors for sweet and umami taste, Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 4692-4696.
31. N. Chaudhari, A.M. Landin, S.D. Roper, A metabotropic glutamate receptor variant functions as a taste receptor, Nat. Neurosci. 3 (2000) 113-119.
32. S.K. McLaughlin, P.J. McKinnon, R.F. Margolskee, Gustducin is a taste-cell-specific G protein closely related to the transducins, Nature 357 (1992) 563-569.
33. G.T. Wong, L. Ruiz-Avila, D. Ming, K.S. Gannon, R.F. Margolskee, Biochemical and transgenic analysis of gustducin's role in bitter and sweet transduction, Cold Spring Harb. Symp. Quant. Biol. 61 (1996) 173-184.
34. L. Huang, Y.G. Shanker, J. Dubauskaite, J.Z. Zheng, W. Yan, S. Rosenzweig, A.I. Spielman, M. Max, R.F. Margolskee, Ggamma13 colocalizes with gustducin in taste receptor cells and mediates IP3 responses to bitter denatonium, Nat. Neurosci. 2 (1999) 1055-1062.
35. P. Rossler, I. Boekhoff, E. Tareilus, S. Beck, H. Breer, J. Freitag, G protein betagamma complexes in circumvallate taste cells involved in bitter transduction, Chem. Senses 25 (2000) 413-421.
36. P. Rossler, C. Kroner, J. Freitag, J. Noe, H. Breer, Identification of a phospholipase C beta subtype in rat taste cells, Eur. J. Cell Biol. 77 (1998) 253-261.
37. T.R. Clapp, L.M. Stone, R.F. Margolskee, S.C. Kinnamon, Immunocytochemical evidence for co-expression of Type III IP3 receptor with signaling components of bitter taste transduction, BMC Neurosci. 2 (2001) 6.
38. M.A. Miyoshi, K. Abe, Y. Emori, IP(3) receptor type 3 and PLCbeta2 are co-expressed with taste receptors T1R and T2R in rat taste bud cells, Chem. Senses 26 (2001) 259-265.
39. S.S. Kolesnikov, R.F. Margolskee, A cyclic-nucleotide-suppressible conductance activated by transducin in taste cells, Nature 376 (1995) 85-88.
40. T. Misaka, Y. Kusakabe, Y. Emori, S. Arai, K. Abe, Molecular cloning and taste bud-specific expression of a novel cyclic nucleotide-gated channel, Ann. NY Acad. Sci. 855 (1998) 150-159.
41. T. Misaka, Y. Kusakabe, Y. Emori, T. Gonoi, S. Arai, K. Abe, Taste buds have a cyclic nucleotide-activated channel, CNGgust. J. Biol. Chem. 272 (1997) 22623-22629.
42. M. Berridge, P. Lipp, M. Bootman, Calcium signalling, Curr. Biol. 9 (1999) R157-R159.
43. S.J. Bernhardt, M. Naim, U. Zehavi, B. Lindemann, Changes in IP3 and cytosolic Ca2+ in response to sugars and non-sugar sweeteners in transduction of sweet taste in the rat, J. Physiol. 490 (1996) 325-336.
44. T. Ogura, A. Mackay-Sim, S.C. Kinnamon, Bitter taste transduction of denatonium in the mudpuppy Necturus maculosus, J. Neurosci. 17 (1997) 3580-3587.
45. T. Ogura, Acetylcholine increases intracellular Ca2+ in taste cells via activation of muscarinic receptors, J. Neurophysiol. 87 (2002) 2643-2649.
46. Y.V. Kim, Y.V. Bobkov, S.S. Kolesnikov, Adenosine triphosphate mobilizes cytosolic calcium and modulates ionic currents in mouse taste receptor cells, Neurosci. Lett. 290 (2000) 165-168.
47. S. Herness, F.L. Zhao, S.G. Lu, N. Kaya, T. Shen, Expression and physiological actions of cholecystokinin in rat taste receptor cells, J. Neurosci. 22 (2002) 10018-10029.
48. A. Caicedo, M.S. Jafri, S.D. Roper, In situ Ca2+ imaging reveals neurotransmitter receptors for glutamate in taste receptor cells, J. Neurosci. 20 (2000) 7978-7985.
49. Y. Hayashi, M.M. Zviman, J.G. Brand, J.H. Teeter, D. Restrepo, Measurement of membrane potential and [Ca2+]i in cell ensembles: application to the study of glutamate taste in mice, Biophys. J. 71 (1996) 1057-1070.
50. W. Lin, T. Ogura, S.C. Kinnamon, Responses to di-sodium guanosine 5′-monophosphate and monosodium L-glutamate in taste receptor cells of rat fungiform papillae, J. Neurophysiol. 00994.2002 (2002).
51. R. Hayato, T. Kitabori, Y. Katayama, K. Takeuchi, T. Kumazawa, S. Endo, K. Yoshii, Oscillating currents and [Ca2+]in increase in response to 5-HT applied to the basolateral membranes of mouse taste bud cells. In: Proceedings of the Society for Neuroscience 32nd Annual Meeting, Orlando, FL, 2002.
52. S. Herness, F.L. Zhao, N. Kaya, S.G. Lu, T. Shen, X.D. Sun, Adrenergic signalling between rat taste receptor cells, J. Physiol. 543 (2002) 601-614.
53. T. Ogura, S.C. Kinnamon, IP(3)-Independent release of Ca(2+) from intracellular stores: a novel mechanism for transduction of bitter stimuli, J. Neurophysiol. 82 (1999) 2657-2666.
54. J. Chandrashekar, K.L. Mueller, M.A. Hoon, E. Adler, L. Feng, W. Guo, C.S. Zuker, N.J. Ryba, T2Rs function as bitter taste receptors, Cell 100 (2000) 703-711.
55. D. Ming, L. Ruiz-Avila, R.F. Margolskee, Characterization and solubilization of bitter-responsive receptors that couple to gustducin, Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 8933-8938.
56. A.I. Spielman, T. Huque, H. Nagai, G. Whitney, J.G. Brand, Generation of inositol phosphates in bitter taste transduction, Physiol. Behav. 56 (1994) 1149-1155.
57. W. Yan, S. Rosenzweig, J.G. Brand, A.I. Spielman, Bitter taste transduction uses two second messenger systems, in: AChems, Sarasota, FL, 2000, p. 81.
58. W. Yan, G. Sunavala, S. Rosenzweig, M. Dasso, J.G. Brand, A.I. Spielman, Bitter taste transduced by PLC-beta(2)-dependent rise in IP(3) and alpha-gustducin-dependent fall in cyclic nucleotides, Am. J. Physiol. Cell Physiol. 280 (2001) C742-C751.
59. M.S. Herness, X.D. Sun, Y. Chen, cAMP and forskolin inhibit potassium currents in rat taste receptor cells by different mechanisms, Am. J. Physiol. 272 (1997) C2005-C2018.
60. M.A. Miyoshi, K. Abe, Y. Emori, Co-expression of calcium signaling components in vertebrate taste bud cells, Neurosci. Lett. 283 (2000) 61-64.
61. T. Ogura, R.F. Margolskee, S.C. Kinnamon, Taste receptor cell responses to the bitter stimulus denatonium involve Ca2+ influx via store-operated channels, J. Neurophysiol. 87 (2002) 3152-3155.
62. K. Venkatachalam, D.B. Van Rossum, R.L. Patterson, H.T. Ma, D.L. Gill, The cellular and molecular basis of store-operated calcium entry, Nat. Cell Biol. 4 (2002) E263-E272.
63. J.W. Putney Jr., R.R. McKay, Capacitative calcium entry channels, Bioessays 21 (1999) 38-46.
64. I. McFadzean, A. Gibson, The developing relationship between receptor-operated and store-operated calcium channels in smooth muscle, Br. J. Pharmacol. 135 (2002) 1-13.
65. R.L. Patterson, D.B. van Rossum, D.L. Ford, K.J. Hurt, S.S. Bae, P.G. Sub, T. Kurosaki, S.H. Snyder, D.L. Gill, Phospholipase C-gamma is required for agonist-induced Ca(2+) entry, Cell 111 (2002) 529-541.
66. R.C. Hardie, B. Minke, The up gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors, Neuron 8 (1992) 643-651.
67. D.E. Clapham, L.W. Runnels, C. Strubing, The TRP ion channel family, Nat. Rev. Neurosci. 2 (2001) 387-396.
68. X. Zhu, M. Jiang, M. Peyton, G. Boulay, R. Hurst, E. Stefani, L. Birnbaumer, trp, a novel mammalian gene family essential for agonist-activated capacitative Ca2+ entry, Cell 85 (1996) 661-671.
69. C.A. Pérez, L. Huang, M. Rong, J.A. Kozak, A.K. Preuss, H. Zhang, M. Max, R.F. Margolskee, A transient receptor potential channel expressed in taste receptor cells, Nat. Neurosci. 5 (2002) 1169-1176.
70. P. Csutora, Z. Su, H.Y. Kim, A. Bugrim, K.W. Cunningham, R. Nuccitelli, J.E. Keizer, M.R. Hanley, J.E. Blalock, R.B. Marchase, Calcium influx factor is synthesized by yeast and mammalian cells depleted of organellar calcium stores, Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 121-126.
71. D. Thomas, M.R. Hanley, Evaluation of calcium influx factors from stimulated Jurkat T- lymphocytes by microinjection into Xenopus oocytes, J. Biol. Chem. 270 (1995) 6429-6432.
72. G. Boulay, D.M. Brown, N. Qin, M. Jiang, A. Dietrich, M.X. Zhu, Z. Chen, M. Birnbaumer, K. Mikoshiba, L. Birnbaumer, Modulation of Ca(2+) entry by polypeptides of the inositol 1,4, 5-trisphosphate receptor (IP3R) that bind transient receptor potential (TRP): evidence for roles of TRP and IP3R in store depletion-activated Ca(2+) entry, Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 14955-14960.
73. K. Kiselyov, G.A. Mignery, MX Zhu, S. Muallem, The N-terminal domain of the IP3 receptor gates store-operated hTrp3 channels, Mol. Cell 4 (1999) 423-429.
74. K. Kiselyov, X. Xu, G. Mozhayeva, T. Kuo, I. Pessah, G. Mignery, X. Zhu, L. Birnbaumer, S. Muallem, Functional interaction between InsP3 receptors and store-operated Htrp3 channels, Nature 396 (1998) 478-482.
75. H.T. Ma, R.L. Patterson, D.B. van Rossum, L. Birnbaumer, K. Mikoshiba, D.L. Gill, Requirement of the mositol trisphosphate receptor for activation of store-operated Ca2+ channels, Science 287 (2000) 1647-1651.
76. H.T. Ma, K. Venkatachalam, H.S. Li, C. Montell, T. Kurosaki, R.L. Patterson, D.L. Gill, Assessment of the role of the inositol 1,4,5-trisphosphate receptor in the activation of transient receptor potential channels and store-operated Ca2+ entry channels, J. Biol. Chem. 276 (2001) 18888-18896.
77. Y. Yao, A.V. Ferrer-Montiel, M. Montal, R.Y. Tsien, Activation of store-operated Ca2+ current in Xenopus oocytes requires SNAP-25 but not a diffusible messenger, Cell 98 (1999) 475-485.
78. R.L. Patterson, D.B. van Rossum, D.L. Gill, Store-operated Ca2+ entry: evidence for a secretion-like coupling model, Cell 98 (1999) 487-499.
79. T. Hofmann, A.G. Obukhov, M. Schaefer, C. Harteneck, T. Gudermann, G. Schultz, Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol, Nature 397 (1999) 259-263.
80. S. Chyb, P. Raghu, R.C. Hardie, Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL, Nature 397 (1999) 255-259.
81. G.T. Wong, L. Ruiz-Avila, R.F. Margolskee, Directing gene expression to gustducin-positive taste receptor cells, J. Neurosci. 19 (1999) 5802-5809.
82. K.F. Stortkuhl, B.T. Hovemann, J.R. Carlson, Olfactory adaptation depends on the Trp Ca2+ channel in Drosophila, J. Neurosci. 19 (1999) 4839-4846.
83. E.R. Liman, D.P. Corey, C. Dulac, TRP2: a candidate transduction channel for mammalian pheromone sensory signaling, Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 5791-5796.
84. L. Stowers, T.E. Holy, M. Meister, C. Dulac, G. Koentges, Loss of sex discrimination and male-male aggression in mice deficient for TRP2, Science 295 (2002) 1493-1500.
85. W. Liedtke, Y. Choe, M.A. Marti-Renom, A.M. Bell, C.S. Denis, A. Sali, A.J. Hudspeth, J.M. Friedman, S. Heller, Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor, Cell 103 (2000) 525-535.
86. M.J. Caterina, A. Leffler, A.B. Malmberg, W.J. Martin, J. Trafton, K.R. Petersen-Zeitz, M. Koltzenburg, A.I. Basbaum, D. Julius, Impaired nociception and pain sensation in mice lacking the capsaicin receptor, Science 288 (2000) 306-313.