Calcium signaling in taste cells: Regulation required

Chemical Senses

Volumn 35, Issue 9, 2010, Pages 753-765

  Medler, Kathryn F ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

Calcium clearance mechanisms; Calcium signaling; Mitochondria; Sodium calcium exchangers; Taste

Indexed keywords

CALCIUM; VOLTAGE GATED CALCIUM CHANNEL;

CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; EVOKED RESPONSE; HUMAN; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SENSORY NERVE CONDUCTION; SENSORY STIMULATION; SIGNAL TRANSDUCTION; SODIUM CALCIUM EXCHANGE; SYNAPSE; TASTE BUD;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; HUMANS; MITOCHONDRIA; SIGNAL TRANSDUCTION; SODIUM-CALCIUM EXCHANGER; TASTE; TASTE BUDS;

EID: 78649347881     PISSN: 0379864X     EISSN: 14643553     Source Type: Journal    
DOI: 10.1093/chemse/bjq082     Document Type: Review

References (125)

1. Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJ, Zuker CS. 2000. A novel family of mammalian taste receptors. Cell. 100:693-702.
2. Akabas MH, Dodd J, Al-Awqati Q. 1988. A bitter substance induces a rise in intracellular calcium in a subpopulation of rat taste cells. Science. 242: 1047-1050.
3. Arnaudeau S, Kelley WL, Walsh JV Jr, Demaurex N. 2001. Mitochondria recycle Ca(2+) to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J Biol Chem. 276: 29430-29439.
4. Augustine GJ, Santamaria F, Tanaka K. 2003. Local calcium signaling in neurons. Neuron. 40:331-346.
5. Barlow LA, Chien CB, Northcutt RG. 1996. Embryonic taste buds develop in the absence of innervation. Development. 122:1103-1111.
6. Barreiro-Iglesias A, Villar-Cervino V, Villar-Cheda B, Anadon R, Rodicio MC. 2008. Neurochemical characterization of sea lamprey taste buds and afferent gustatory fibers: presence of serotonin, calretinin, and CGRP immunoreactivity in taste bud bi-ciliated cells of the earliest vertebrates. J Comp Neurol. 511:438-453.
7. Baryshnikov SG, Rogachevskaja OA, Kolesnikov SS. 2003. Calcium signaling mediated by P2Y receptors in mouse taste cells. J Neurophysiol. 90: 3283-3294.
8. Behe P, DeSimone JA, Avenet P, Lindemann B. 1990. Membrane currents in taste cells of the rat fungiform papilla. Evidence for two types of Ca currents and inhibition of K currents by saccharin. J Gen Physiol. 96: 1061-1084.
9. Berridge M, Bootman M. 1996. Calcium signaling. London: Chapman and Hall.
10. Berridge MJ, Bootman MD, Lipp P. 1998. Calcium-a life and death signal. Nature. 395:645-648.
11. Blaustein MP. 1988. Calcium transport and buffering in neurons. Trends Neurosci. 11:438-443.
12. Blaustein MP, Juhaszova M, Golovina VA, Church PJ, Stanley EF. 2002. Na/Ca exchanger and PMCA localization in neurons and astrocytes: functional implications. Ann N Y Acad Sci. 976:356-366.
13. Blaustein MP, Santiago EM. 1977. Effects of internal and external cations and of ATP on sodium-calcium and calcium-calcium exchange in squid axons. Biophys J. 20:79-111.
14. Boitier E, Rea R, Duchen MR. 1999. Mitochondria exert a negative feedback on the propagation of intracellular Ca2+ waves in rat cortical astrocytes. J Cell Biol. 145:795-808.
15. Bootman MD, Berridge MJ, Roderick HL. 2002. Calcium signalling: more messengers, more channels, more complexity. Curr Biol. 12: R563-R565.
16. Braunewell KH, Klein-Szanto AJ. 2009. Visinin-like proteins (VSNLs): interaction partners and emerging functions in signal transduction of a subfamily of neuronal Ca2+ -sensor proteins. Cell Tissue Res. 335: 301-316.
17. Budd SL, Nicholls DG. 1996. A reevaluation of the role of mitochondria in neuronal Ca2+ homeostasis. J Neurochem. 66:403-411.
18. Budd SL, Nicholls DG. 1998. Mitochondria in the life and death of neurons. Essays Biochem. 33:43-52.
19. Burgoyne RD. 2007. Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci. 8:182-193.
20. Burgoyne RD, Weiss JL. 2001. The neuronal calcium sensor family of Ca2+ -binding proteins. Biochem J. 353:1-12.
21. Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zuker CS, Ryba NJ. 2000. T2Rs function as bitter taste receptors. Cell. 100: 703-711.
22. Chaudhari N, Landin AM, Roper SD. 2000. A metabotropic glutamate receptor variant functions as a taste receptor. Nat Neurosci. 3:113-119.
23. Clapp TR, Medler KF, Damak S, Margolskee RF, Kinnamon SC. 2006. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biol. 4:7.
24. Clapp TR, Stone LM, Margolskee RF, Kinnamon SC. 2001. Immunocyto-chemical evidence for co-expression of Type III IP3 receptor with signaling components of bitter taste transduction. BMC Neurosci. 2:6.
25. Clapp TR, Yang R, Stoick CL, Kinnamon SC, Kinnamon JC. 2004. Morphologic characterization of rat taste receptor cells that express components of the phospholipase C signaling pathway. J Comp Neurol. 468:311-321.
26. Contreras L, Drago I, Zampese E, Pozzan T. 2010. Mitochondria: the calcium connection. Biochim Biophys Acta. 1797(6-7):607-618.
27. Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Perez CA, Shigemura N, Yoshida R, Mosinger B Jr, Glendinning JI, Ninomiya Y, et al. 2006. Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses. 31:253-264.
28. Dando R, Roper SD. 2009. Cell-to-cell communication in intact taste buds through ATP signalling from pannexin 1 gap junction hemichannels. J Physiol. 587:5899-5906.
29. DeFazio RA, Dvoryanchikov G, Maruyama Y, Kim JW, Pereira E, Roper SD, Chaudhari N. 2006. Separate populations of receptor cells and presynaptic cells in mouse taste buds. J Neurosci. 26:3971-3980.
30. Diaz-Regueira SM, Lamas I, Anadon R. 2005. Calretinin immunoreactivity in taste buds and afferent fibers of the grey mullet Chelon labrosus. Brain Res. 1031:297-301.
31. Duszynski J, Koziel R, Brutkowski W, Szczepanowska J, Zablocki K. 2006. The regulatory role of mitochondria in capacitative calcium entry. Biochim Biophys Acta. 1757:380-387.
32. Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, Kinnamon SC. 2005. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science. 310:1495-1499.
33. Friel DD. 2000. Mitochondria as regulators of stimulus-evoked calcium signals in neurons. Cell Calcium. 28:307-316.
34. Germana A, Paruta S, Germana GP, Ochoa-Erena FJ, Montalbano G, Cobo J, Vega JA. 2007. Differential distribution of S100 protein and calretinin in mechanosensory and chemosensory cells of adult zebrafish (Danio rerio). Brain Res. 1162:48-55.
35. Gilabert JA, Bakowski D, Parekh AB. 2001. Energized mitochondria increase the dynamic range over which inositol 1,4,5-trisphosphate activates store-operated calcium influx. EMBO J. 20:2672-2679.
36. Gunter TE, Pfeiffer DR. 1990. Mechanisms by which mitochondria transport calcium. Am J Physiol. 258:C755-C786.
37. Hacker K, Laskowski A, Feng L, Restrepo D, Medler K. 2008. Evidence for two populations of bitter responsive taste cells in mice. J Neurophysiol. 99:1503-1514.
38. Hacker K, Medler KF. 2008. Mitochondrial calcium buffering contributes to the maintenance of basal calcium levels in mouse taste cells. J Neurophysiol. 100:2177-2191.
39. Haeseleer F, Imanishi Y, Sokal I, Filipek S, Palczewski K. 2002. Calciumbinding proteins: intracellular sensors from the calmodulin superfamily. Biochem Biophys Res Commun. 290:615-623.
40. Hajnoczky G, Hager R, Thomas AP. 1999. Mitochondria suppress local feedback activation of inositol 1,4, 5-trisphosphate receptors by Ca2+. J Biol Chem. 274:14157-14162.
41. Halaszovich CR, Zitt C, Jungling E, Luckhoff A. 2000. Inhibition of TRP3 channels by lanthanides. Block from the cytosolic side of the plasma membrane. J Biol Chem. 275:37423-37428.
42. Hille B. 2001. Ion channels of excitable membranes. Sunderland (MA): Sinauer Associates, Inc.
43. Hofmann T, Chubanov V, Gudermann T, Montell C. 2003. TRPM5 is a voltage-modulated and Ca(2+)-activated monovalent selective cation channel. Curr Biol. 13:1153-1158.
44. Huang L, Shanker YG, Dubauskaite J, Zheng JZ, Yan W, Rosenzweig S, Spielman AI, Max M, Margolskee RF. 1999. Ggamma13 colocalizes with gustducin in taste receptor cells and mediates IP3 responses to bitter denatonium. Nat Neurosci. 2:1055-1062.
45. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD. 2007. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci U S A. 104: 6436-6441.
46. Ichikawa H, Helke CJ. 1997. Coexistence of calcium-binding proteins in vagal and glossopharyngeal sensory neurons of the rat. Brain Res. 768: 349-353.
47. Ichikawa H, Jacobowitz DM, Sugimoto T. 1992. Calretinin-immunoreactivity in the oro-facial and pharyngeal regions of the rat. Neurosci Lett. 146: 155-158.
48. Ishii S, Misaka T, Kishi M, Kaga T, Ishimaru Y, Abe K. 2009. Acetic acid activates PKD1L3-PKD2L1 channel-a candidate sour taste receptor. Biochem Biophys Res Commun. 385:346-350.
49. 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 U S A. 103: 12569-12574.
50. Jackson JG, Thayer SA. 2006. Mitochondrial modulation of Ca2+ -induced Ca2+ -release in rat sensory neurons. J Neurophysiol. 96: 1093-1104.
51. Johnson EW, Eller PM, Jafek BW, Norman AW. 1992. Calbindin-like immunoreactivity in two peripheral chemosensory tissues of the rat: taste buds and the vomeronasal organ. Brain Res. 572: 319-324.
52. Jung S, Muhle A, Schaefer M, Strotmann R, Schultz G, Plant TD. 2003. Lanthanides potentiate TRPC5 currents by an action at extracellular sites close to the pore mouth. J Biol Chem. 278:3562-3571.
53. Kaske S, Krasteva G, Konig P, Kummer W, Hofmann T, Gudermann T, Chubanov V. 2007. TRPM5, a taste-signaling transient receptor potential ion-channel, is a ubiquitous signaling component in chemosensory cells. BMC Neurosci. 8:49.
54. Kataoka S, Yang R, Ishimaru Y, Matsunami H, Sevigny J, Kinnamon JC, Finger TE. 2008. The candidate sour taste receptor, PKD2L1, is expressed by type III taste cells in the mouse. Chem Senses. 33: 243-254.
55. Kim MH, Korogod N, Schneggenburger R, Ho WK, Lee SH. 2005. Interplay between Na+/Ca2+ exchangers and mitochondria in Ca2+ clearance at the calyx of Held. J Neurosci. 25:6057-6065.
56. Kits KS, Dreijer AM, Lodder JC, Borgdorff A, Wadman WJ. 1997. High intracellular calcium levels during and after electrical discharges in molluscan peptidergic neurons. Neuroscience. 79: 275-284.
57. Kleene SJ. 2009. Limits of calcium clearance by plasma membrane calcium ATPase in olfactory cilia. PLoS One. 4:e5266.
58. Landolfi B, Curci S, Debellis L, Pozzan T, Hofer AM. 1998. Ca2+ homeostasis in the agonist-sensitive internal store: functional interactions between mitochondria and the ER measured In situ in intact cells. J Cell Biol. 142:1235-1243.
59. Laskowski AI, Medler KF. 2009. Sodium/calcium exchangers contribute to the regulation of cytosolic calcium levels in mouse taste cells. J Physiol. 587(Pt 16):4077-4089.
60. Lawrie AM, Rizzuto R, Pozzan T, Simpson AWM. 1996. A role for calcium influx in the regulation of mitochondrial calcium in endothelial cells. J Biol Chem. 271:10753-10759.
61. Liman ER. 2007. TRPM5 and taste transduction. Handb Exp Pharmacol. 179:287-298.
62. Liu D, Liman ER. 2003. Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci U S A. 100: 15160-15165.
63. LopezJimenez ND, Cavenagh MM, Sainz E, Cruz-Ithier MA, Battey JF, Sullivan SL. 2006. Two members of the TRPP family of ion channels, Pkd1l3 and Pkd2l1, are co-expressed in a subset of taste receptor cells. J Neurochem. 98:68-77.
64. Lyall V, Heck GL, Phan TH, Mummalaneni S, Malik SA, Vinnikova AK, Desimone JA. 2005. Ethanol modulates the VR-1 variant amilorideinsensitive salt taste receptor. II. Effect on chorda tympani salt responses. J Gen Physiol. 125:587-600.
65. Lyall V, Heck GL, Vinnikova AK, Ghosh S, Phan TH, Alam RI, Russell OF, Malik SA, Bigbee JW, DeSimone JA. 2004. The mammalian amilorideinsensitive non-specific salt taste receptor is a vanilloid receptor-1 variant. J Physiol. 558:147-159.
66. Lyall V, Heck GL, Vinnikova AK, Ghosh S, Phan TH, Desimone JA. 2005. A novel vanilloid receptor-1 (VR-1) variant mammalian salt taste receptor. Chem Senses. (30 Suppl)1: i42-i43.
67. Malamud D. 1993. Guidelines for saliva nomenclature and collection. Ann N Y Acad Sci. 694:xi-xii.
68. Malli R, Frieden M, Trenker M, Graier WF. 2005. The role of mitochondria for Ca2+ refilling of the endoplasmic reticulum. J Biol Chem. 280: 12114-12122.
69. Mandel ID. 1993. Salivary diagnosis: promises, promises. Ann N Y Acad Sci. 694:1-10.
70. Matsuda T, Takuma K, Baba A. 1997. Na(+)-Ca2+ exchanger: physiology and pharmacology. Jpn J Pharmacol. 74:1-20.
71. Matsunami H, Montmayeur JP, Buck LB. 2000. A family of candidate taste receptors in human and mouse. Nature. 404:601-604.
72. Max M, Shanker YG, Huang L, Rong M, Liu Z, Campagne F, Weinstein H, Damak S, Margolskee RF. 2001. Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet. 28:58-63.
73. Medler K, Gleason EL. 2002. Mitochondrial Ca(2+) buffering regulates synaptic transmission between retinal amacrine cells. J Neurophysiol. 87: 1426-1439.
74. Medler KF. 2005. Regulating calcium in taste cells: expression of calcium ATPases. Sarasota (FL): Achems XXVII. pp. #240.
75. Medler KF, Margolskee RF, Kinnamon SC. 2003. Electrophysiological characterization of voltage-gated currents in defined taste cell types of mice. J Neurosci. 23:2608-2617.
76. Ming D, Ninomiya Y, Margolskee RF. 1999. Blocking taste receptor activation of gustducin inhibits gustatory responses to bitter compounds. Proc Natl Acad Sci U S A. 96:9903-9908.
77. Mironov SL, Ivannikov MV, Johansson M. 2005. [Ca2+]i signaling between mitochondria and endoplasmic reticulum in neurons is regulated by microtubules. From mitochondrial permeability transition pore to Ca2+-induced Ca2+ release. J Biol Chem. 280: 715-721.
78. Miyawaki Y, Morisaki I, Tabata MJ, Kurisu K, Wakisaka S. 1996. Calbindin D28k-like immunoreactivity in the gustatory epithelium in the rat. Neurosci Lett. 214:29-32.
79. Miyawaki Y, Morisaki I, Tabata MJ, Maeda T, Kurisu K, Wakisaka S. 1998. Calbindin D28k-like immunoreactivity in the developing and regenerating circumvallate papilla of the rat. Cell Tissue Res. 291:81-90.
80. Miyoshi MA, Abe K, Emori Y. 2001. IP(3) receptor type 3 and PLCbeta2 are co-expressed with taste receptors T1R and T2R in rat taste bud cells. Chem Senses. 26:259-265.
81. Monteith GR, Roufogalis BD. 1995. The plasma membrane calcium pump-a physiological perspective on its regulation. Cell Calcium. 18: 459-470.
82. Montero M, Alonso MT, Albillos A, Cuchillo-Ibanez I, Olivares R, AGG, Garcia-Sancho J, Alvarez J. 2001. Control of secretion by mitochondria depends on the size of the local [Ca2+] after chromaffin cell stimulation. Eur J Neurosci. 13:2247-2254.
83. Montero M, Alonso MT, Albillos A, Garcia-Sancho J, Alvarez J. 2001. Mitochondrial Ca(2+)-induced Ca(2+) release mediated by the Ca(2+) uniporter. Mol Biol Cell. 12:63-71.
84. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, Zuker CS. 2002. An amino-acid taste receptor. Nature. 416:199-202.
85. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS. 2001. Mammalian sweet taste receptors. Cell. 106:381-390.
86. Nicholls DG. 2005. Mitochondria and calcium signaling. Cell Calcium. 38: 311-317.
87. Nicholls DG, Budd SL. 2000. Mitochondria and neuronal survival. Physiol Rev. 80:315-360.
88. Northcutt RG. 2005. Taste bud development in the channel catfish. J Comp Neurol. 482:1-16.
89. Ogura T, Mackay-Sim A, Kinnamon SC. 1997. Bitter taste transduction of denatonium in the mudpuppy Necturus maculosus. J Neurosci. 17: 3580-3587.
90. Ogura T, Margolskee RF, Kinnamon SC. 2002. Taste receptor cell responses to the bitter stimulus denatonium involve Ca2+ influx via store-operated channels. J Neurophysiol. 87:3152-3155.
91. Ohkubo Y, Yokosuka H, Kumakura M, Yoshie S. 2007. Existence of subtypes of gustducin-immunoreactive cells in the vallate taste bud of guinea pigs. Arch Histol Cytol. 70:291-296.
92. Pacher P, Csordas P, Schneider T, Hajnoczky G. 2000. Quantification of calcium signal transmission from sarco-endoplasmic reticulum to the mitochondria. J Physiol. 529(Pt 3):553-564.
93. Parekh AB. 2003. Store-operated Ca2+ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane. J Physiol. 547:333-348.
94. Parys JB, Vanlingen S, Raeymaekers L, De Smedt H, Missiaen L. 2000. Subcellular fractionation and intracellular calcium stores. In: Putney J, editor. Calcium signaling. Boca Raton (FL): CRC Press. p. 71-110.
95. Prawitt D, Monteilh-Zoller MK, Brixel L, Spangenberg C, Zabel B, Fleig A, Penner R. 2003. TRPM5 is a transient Ca2+-activated cation channel responding to rapid changes in [Ca2+]i. Proc Natl Acad Sci U S A. 100: 15166-15171.
96. Purves D. 2007. Neuroscience. Sunderland (MA): Sinauer Associates, Inc.
97. Ricken S, Leipziger J, Greger R, Nitschke R. 1998. Simultaneous measurements of cytosolic and mitochondrial Ca2+ transients in HT29 cells. J Biol Chem. 273:34961-34969.
98. Rizzuto R, Brini M, Murgia M, Pozzan T. 1993. Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science. 262:744-747.
99. Rizzuto R, Pinton P, Brini M, Chiesa A, Filippin L, Pozzan T. 1999. Mitochondria as biosensors of calcium microdomains. Cell Calcium. 26:193-199.
100. Roberts CD, Dvoryanchikov G, Roper SD, Chaudhari N. 2009. Interaction between the second messengers cAMP and Ca2+ in mouse presynaptic taste cells. J Physiol. 587:1657-1668.
101. Rogers J, Khan M, Ellis J. 1990. Calretinin and other CaBPs in the nervous system. Adv Exp Med Biol. 269:195-203.
102. Romanov RA, Rogachevskaja OA, Bystrova MF, Jiang P, Margolskee RF, Kolesnikov SS. 2007. Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J. 26:657-667.
103. Romanov RA, Rogachevskaja OA, Khokhlov AA, Kolesnikov SS. 2008. Voltage dependence of ATP secretion in mammalian taste cells. J Gen Physiol. 132:731-744.
104. Rossler P, Kroner C, Freitag J, Noe J, Breer H. 1998. Identification of a phospholipase C beta subtype in rat taste cells. Eur J Cell Biol. 77:253-261.
105. Royer SM, Kinnamon JC. 1988. Ultrastructure of mouse foliate taste buds: synaptic and nonsynaptic interactions between taste cells and nerve fibers. J Comp Neurol. 270:11-24. 58-59.
106. Ruiz C, Gutknecht S, Delay E, Kinnamon S. 2006. Detection of NaCl and KCl in TRPV1 knockout mice. Chem Senses. 31:813-820.
107. Saidu SP, Weeraratne SD, Valentine M, Delay R, Van Houten JL. 2009. Role of plasma membrane calcium ATPases in calcium clearance from olfactory sensory neurons. Chem Senses. 34:349-358.
108. Schramm W, Smith RH, Craig PA. 1993. Methods of simplified saliva collection for the measurement of drugs of abuse, therapeutic drugs, and other molecules. Ann N Y Acad Sci. 694:311-313.
109. Sedova M, Blatter LA. 1999. Dynamic regulation of [Ca2+]i by plasma membrane Ca(2+)-ATPase and Na+/Ca2+ exchange during capacitative Ca2+ entry in bovine vascular endothelial cells. Cell Calcium. 25: 333-343.
110. Szebenyi SA, Laskowski AI, Medler KF. 2010. Sodium/calcium exchangers selectively regulate calcium signaling in mouse taste receptor cells. J Neurophysiol. 104(1):529-538.
111. Treesukosol Y, Lyall V, Heck GL, Desimone JA, Spector AC. 2007. A psychophysical and electrophysiological analysis of salt taste in Trpv1 null mice. Am J Physiol Regul Integr Comp Physiol. 292:R1799-R1809.
112. Ullrich ND, Voets T, Prenen J, Vennekens R, Talavera K, Droogmans G, Nilius B. 2005. Comparison of functional properties of the Ca2+- activated cation channels TRPM4 and TRPM5 from mice. Cell Calcium. 37:267-278.
113. Verkhratsky AJ, Petersen OH. 1998. Neuronal calcium stores. Cell Calcium. 24:333-343.
114. Weeraratne SD, Valentine M, Cusick M, Delay R, Van Houten JL. 2006. Plasma membrane calcium pumps in mouse olfactory sensory neurons. Chem Senses. 31:725-730.
115. White RJ, Reynolds IJ. 1995. Mitochondria and Na+/Ca2+ exchange buffer glutamate-induced calcium loads in cultured cortical neurons. J Neurosci. 15:1318-1328.
116. White RJ, Reynolds IJ. 1997. Mitochondria accumulate Ca2+ following intense glutamate stimulation of cultured rat forebrain neurones. J Physiol. 498(Pt 1):31-47.
117. Yamagishi M, Ishizuka Y, Fujiwara M, Nakamura H, Igarashi S, Nakano Y, Kuwano R. 1993. Distribution of calcium binding proteins in sensory organs of the ear, nose and throat. Acta Otolaryngol Suppl. 506:85-89.
118. Yamamoto Y, Atoji Y, Suzuki Y. 2000. Calbindin D28k-immunoreactive afferent nerve endings in the laryngeal mucosa. Anat Rec. 259:237-247.
119. Yan W, Sunavala G, Rosenzweig S, Dasso M, Brand JG, Spielman AI. 2001. Bitter taste transduced by PLC-beta(2)-dependent rise in IP(3) and alphagustducin-dependent fall in cyclic nucleotides. Am J Physiol Cell Physiol. 280:C742-C751.
120. Yang R, Crowley HH, Rock ME, Kinnamon JC. 2000. Taste cells with synapses in rat circumvallate papillae display SNAP-25-like immunoreactivity. J Comp Neurol. 424:205-215.
121. Yang R, Tabata S, Crowley HH, Margolskee RF, Kinnamon JC. 2000. Ultrastructural localization of gustducin immunoreactivity in microvilli of type II taste cells in the rat. J Comp Neurol. 425:139-151.
122. Yee CL, Yang R, Bottger B, Finger TE, Kinnamon JC. 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 Neurol. 440:97-108.
123. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, Zuker CS, Ryba NJ. 2003. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell. 112:293-301.
124. Zhang Z, Zhao Z, Margolskee R, Liman E. 2007. The transduction channel TRPM5 is gated by intracellular calcium in taste cells. J Neurosci. 27: 5777-5786.
125. Zhu X, Jiang M, Peyton M, Boulay G, Hurst R, Stefani E, Birnbaumer L. 1996. trp, a novel mammalian gene family essential for agonist-activated capacitative Ca2+ entry. Cell. 85:661-671.