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TRP Channels as Targets for Modulation of Taste Transduction

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TRP Channels in Sensory Transduction

Abstract

The sense of taste endows organisms with the ability to distinguish nutritious from potentially harmful food components and to orchestrate adaptive attractive or aversive behaviors. Several members of the Transient Receptor Potential (TRP) family of cation channels have been implicated in the perception of canonical and non-canonical taste modalities, TRPM5 for sweet, bitter, umami and fat, TRPP3/PKD1L3 for sour and TRPV1 for salt and metallic tastes. However, TRPM5 is the only one for which there is consensus on its contribution to taste transduction. Here I review recent findings on the role of this channel in taste perception at the peripheral level. Emphasis is made on reported mechanisms of TRPM5 channel modulation that may have an impact on gustatory transduction. Understanding these mechanisms allows learning about basic taste signaling processes and their modulation (e.g. by temperature and taste-taste interactions), and is essential for the design of optimal therapeutic strategies targeting the gustatory system.

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References

  • Bartel DL, Sullivan SL, Lavoie EG, Sevigny J, Finger TE (2006) Nucleoside triphosphate diphosphohydrolase-2 is the ecto-ATPase of type I cells in taste buds. J Comp Neurol 497:1–12

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Boucher Y, Simons CT, Cuellar JM, Jung SW, Carstens MI, Carstens E (2003) Activation of brain stem neurons by irritant chemical stimulation of the throat assessed by c-fos immunohistochemistry. Exp Brain Res 148:211–218

    CAS  PubMed  Google Scholar 

  • Carstens E, Kuenzler N, Handwerker HO (1998) Activation of neurons in rat trigeminal subnucleus caudalis by different irritant chemicals applied to oral or ocular mucosa. J Neurophysiol 80:465–492

    CAS  PubMed  Google Scholar 

  • Chaudhari N, Roper SD (2010) The cell biology of taste. J Cell Biol 190:285–296

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cruz A, Green BG (2000) Thermal stimulation of taste. Nature 403:889–892

    Article  CAS  PubMed  Google Scholar 

  • Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Perez CA, Shigemura N, Yoshida R, Mosinger B Jr, Glendinning JI, Ninomiya Y, Margolskee RF (2006) Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses 31:253–264

    Article  CAS  PubMed  Google Scholar 

  • de Araujo IE, Oliveira-Maia AJ, Sotnikova TD, Gainetdinov RR, Caron MG, Nicolelis MA, Simon SA (2008) Food reward in the absence of taste receptor signaling. Neuron 57:930–941

    Article  PubMed  Google Scholar 

  • Devantier HR, Long DJ, Brennan FX, Carlucci SA, Hendrix C, Bryant RW, Salemme FR, Palmer RK (2008) Quantitative assessment of TRPM5-dependent oral aversiveness of pharmaceuticals using a mouse brief-access taste aversion assay. Behav Pharmacol 19:673–682

    Article  PubMed  Google Scholar 

  • Dotson CD, Roper SD, Spector AC (2005) PLCb2-independent behavioral avoidance of prototypical bitter-tasting ligands. Chem Senses 30:593–600

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dvoryanchikov G, Sinclair MS, Perea-Martinez I, Wang T, Chaudhari N (2009) Inward rectifier channel, ROMK, is localized to the apical tips of glial-like cells in mouse taste buds. J Comp Neurol 517:1–14

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Eddy MC, Eschle BK, Peterson D, Lauras N, Margolskee RF, Delay ER (2012) A conditioned aversion study of sucrose and SC45647 taste in TRPM5 knockout mice. Chem Senses 37:391–401

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Feng P, Huang L, Wang H (2012) Taste bud homeostasis in health, disease, and aging. Chem Senses 39:3–16

    Article  Google Scholar 

  • Formaker BK, Frank ME (1996) Responses of the hamster chorda tympani nerve to binary component taste stimuli: evidence for peripheral gustatory mixture interactions. Brain Res 727:79–90

    Article  CAS  PubMed  Google Scholar 

  • Gao N, Lu M, Echeverri F, Laita B, Kalabat D, Williams ME, Hevezi P, Zlotnik A, Moyer BD (2009) Voltage-gated sodium channels in taste bud cells. BMC Neurosci 10:20

    Article  PubMed Central  PubMed  Google Scholar 

  • Gees M, Alpizar YA, Luyten T, Parys JB, Nilius B, Bultynck G, Voets T, Talavera K (2014) Differential effects of bitter compounds on the taste transduction channels TRPM5 and IP3 receptor type 3. Chem Senses 39:295–311

    Article  CAS  PubMed  Google Scholar 

  • Glendinning JI, Bloom LD, Onishi M, Zheng KH, Damak S, Margolskee RF, Spector AC (2005) Contribution of alpha-gustducin to taste-guided licking responses of mice. Chem Senses 30:299–316

    Article  CAS  PubMed  Google Scholar 

  • Grunberg NE (1982) The effects of nicotine and cigarette smoking on food consumption and taste preferences. Addict Behav 7:317–331

    Article  CAS  PubMed  Google Scholar 

  • Grunberg NE (1985) Nicotine, cigarette smoking, and body weight. Br J Addict 80:369–377

    Article  CAS  PubMed  Google Scholar 

  • Hisatsune C, Yasumatsu K, Takahashi-Iwanaga H, Ogawa N, Kuroda Y, Yoshida R, Ninomiya Y, Mikoshiba K (2007) Abnormal taste perception in mice lacking the type 3 inositol 1,4,5-trisphosphate receptor. J Biol Chem 282:37225–37231

    Article  CAS  PubMed  Google Scholar 

  • Hofmann T, Chubanov V, Gudermann T, Montell C (2003) TRPM5 is a voltage-modulated and Ca2+-activated monovalent selective cation channel. Curr Biol 13:1153–1158

    Article  CAS  PubMed  Google Scholar 

  • Huang YA, Roper SD (2010) Intracellular Ca2+ and TRPM5-mediated membrane depolarization produce ATP secretion from taste receptor cells. J Physiol 588:2343–2350

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ishimaru Y, Matsunami H (2009) Transient receptor potential (TRP) channels and taste sensation. J Dent Res 88:212–218

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Katsumata T, Nakakuki H, Tokunaga C, Fujii N, Egi M, Phan TH, Mummalaneni S, Desimone JA, Lyall V (2008) Effect of Maillard reacted peptides on human salt taste and the amiloride-insensitive salt taste receptor (TRPV1t). Chem Senses 33:665–680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kinnamon SC (2012) Taste receptor signalling—from tongues to lungs. Acta Physiol (Oxf) 204:158–168

    Article  CAS  Google Scholar 

  • Kinnamon SC, Finger TE (2013) A taste for ATP: neurotransmission in taste buds. Front Cell Neurosci 7:264

    Article  PubMed Central  PubMed  Google Scholar 

  • Liman ER (2006) Thermal gating of TRP ion channels: food for thought? Sci STKE 2006, pe12

    Google Scholar 

  • Liman ER (2014) TRPM5. Handb Exp Pharmacol 222:489–502

    Article  CAS  PubMed  Google Scholar 

  • Liman ER, Zhang YV, Montell C (2014) Peripheral coding of taste. Neuron 81:984–1000

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu L, Zhu W, Zhang ZS, Yang T, Grant A, Oxford G, Simon SA (2004) Nicotine inhibits voltage-dependent sodium channels and sensitizes vanilloid receptors. J Neurophysiol 91:1482–1491

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Zhang Z, Liman ER (2005) Extracellular acid block and acid-enhanced inactivation of the Ca2+-activated cation channel TRPM5 involve residues in the S3-S4 and S5-S6 extracellular domains. J Biol Chem 280:20691–20699

    Article  CAS  PubMed  Google Scholar 

  • Liu P, Shah BP, Croasdell S, Gilbertson TA (2011) Transient receptor potential channel type M5 is essential for fat taste. J Neurosci 31:8634–8642

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lopez Jimenez 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

    Article  CAS  Google Scholar 

  • Lyall V, Heck GL, Vinnikova AK, Ghosh S, Phan TH, Alam RI, Russell OF, Malik SA, Bigbee JW, Desimone JA (2004) The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant. J Physiol 558:147–159

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lyall V, Phan TH, Mummalaneni S, Mansouri M, Heck GL, Kobal G, Desimone JA (2007) Effect of nicotine on chorda tympani responses to salty and sour stimuli. J Neurophysiol 98:1662–1674

    Article  CAS  PubMed  Google Scholar 

  • Lyall V, Phan TH, Mummalaneni S, Melone P, Mahavadi S, Murthy KS, Desimone JA (2009) Regulation of the benzamil-insensitive salt taste receptor by intracellular Ca2+, protein kinase C, and calcineurin. J Neurophysiol 102:1591–1605

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Meseguer VM, Denlinger BL, Talavera K (2011) Methodological considerations to understand the sensory function of TRP channels. Curr Pharm Biotechnol 12:3–11

    Article  CAS  PubMed  Google Scholar 

  • Mueller KL, Hoon MA, Erlenbach I, Chandrashekar J, Zuker CS, Ryba NJ (2005) The receptors and coding logic for bitter taste. Nature 434:225–229

    Article  CAS  PubMed  Google Scholar 

  • Nilius B, Appendino G (2013) Spices: the savory and beneficial science of pungency. Rev Physiol Biochem Pharmacol 164:1–76

    Article  CAS  PubMed  Google Scholar 

  • Nilius B, Talavera K, Owsianik G, Prenen J, Droogmans G, Voets T (2005) Gating of TRP channels: a voltage connection? J Physiol 567:35–44

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Öhrwall H (1891) Untersuchungen über den Geschmackssinn. Skand Arch Physiol 2:1–69

    Article  Google Scholar 

  • Oike H, Wakamori M, Mori Y, Nakanishi H, Taguchi R, Misaka T, Matsumoto I, Abe K (2006) Arachidonic acid can function as a signaling modulator by activating the TRPM5 cation channel in taste receptor cells. Biochim Biophys Acta 1761:1078–1084

    Article  CAS  PubMed  Google Scholar 

  • Oka Y, Butnaru M, von Buchholtz L, Ryba NJ, Zuker CS (2013) High salt recruits aversive taste pathways. Nature 494:472–475

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oliveira-Maia AJ, Stapleton-Kotloski JR, Lyall V, Phan TH, Mummalaneni S, Melone P, Desimone JA, Nicolelis MA, Simon SA (2009) Nicotine activates TRPM5-dependent and independent taste pathways. Proc Natl Acad Sci U S A 106:1596–1601

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Perez CA, Huang L, Rong M, Kozak JA, Preuss AK, Zhang H, Max M, Margolskee RF (2002) A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5:1169–1176

    Article  CAS  PubMed  Google Scholar 

  • Perez CA, Margolskee RF, Kinnamon SC, Ogura T (2003) Making sense with TRP channels: store-operated calcium entry and the ion channel TRPM5 in taste receptor cells. Cell Calcium 33:541–549

    Article  CAS  PubMed  Google Scholar 

  • Philippaert KP (2013) Screening for and characterization of pharmacological tools to target the Ca2+ activated non-selective cation channels TRPM4 and TRPM5. In 22nd Congress of the European-Chemoreception-Research-Organization (ECRO), vol 39. ed. Press, O. U., pp 106–107, Leuven

    Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pumplin DW, Yu C, Smith DV (1997) Light and dark cells of rat vallate taste buds are morphologically distinct cell types. J Comp Neurol 378:389–410

    Article  CAS  PubMed  Google Scholar 

  • Ren Z, Rhyu MR, Phan TH, Mummalaneni S, Murthy KS, Grider JR, Desimone JA, Lyall V (2013) TRPM5-dependent amiloride- and benzamil-insensitive NaCl chorda tympani taste nerve response. Am J Physiol Gastrointest Liver Physiol 305:G106–G117

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Riera CE, Vogel H, Simon SA, Damak S, Le Coutre J (2009) Sensory attributes of complex tasting divalent salts are mediated by TRPM5 and TRPV1 channels. J Neurosci 29:2654–2662

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roper SD (2014) TRPs in taste and chemesthesis. Handb Exp Pharmacol 223:827–871

    Article  CAS  PubMed  Google Scholar 

  • Simons CT, Boucher Y, Carstens MI, Carstens E (2006) Nicotine suppression of gustatory responses of neurons in the nucleus of the solitary tract. J Neurophysiol 96:1877–1886

    Article  CAS  PubMed  Google Scholar 

  • Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y, Margolskee RF, Nilius B (2005) Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438:1022–1025

    Article  CAS  PubMed  Google Scholar 

  • Talavera K, Ninomiya Y, Winkel C, Voets T, Nilius B (2007) Influence of temperature on taste perception. Cell Mol Life Sci 64:377–381

    Article  CAS  PubMed  Google Scholar 

  • Talavera K, Nilius B, Voets T (2008a) Neuronal TRP channels: thermometers, pathfinders and life-savers. Trends Neurosci 31:287–295

    Article  CAS  PubMed  Google Scholar 

  • Talavera K, Voets T, Nilius B (2008b) Mechanisms of thermosensation in TRP channels. In Martinac B (ed) Sensing with ion channels. Springer, pp 101–120

    Google Scholar 

  • Talavera K, Yasumatsu K, Yoshida R, Margolskee RF, Voets T, Ninomiya Y, Nilius B (2008c) The taste transduction channel TRPM5 is a locus for bitter-sweet taste interactions. FASEB J 22:1343–1355

    Article  CAS  PubMed  Google Scholar 

  • Talavera K, Gees M, Karashima Y, Meseguer VM, Vanoirbeek JA, Damann N, Everaerts W, Benoit M, Janssens A, Vennekens R, Viana F, Nemery B, Nilius B, Voets T (2009) Nicotine activates the chemosensory cation channel TRPA1. Nat Neurosci 12:1293–1299

    Article  CAS  PubMed  Google Scholar 

  • Taruno A, Matsumoto I, Ma Z, Marambaud P, Foskett JK (2013a) How do taste cells lacking synapses mediate neurotransmission? CALHM1, a voltage-gated ATP channel. Bioessays 35:1111–1118

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Taruno A, Vingtdeux V, Ohmoto M, Ma Z, Dvoryanchikov G, Li A, Adrien L, Zhao H, Leung S, Abernethy M, Koppel J, Davies P, Civan MM, Chaudhari N, Matsumoto I, Hellekant G, Tordoff MG, Marambaud P, Foskett JK (2013b) CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes. Nature 495:223–226

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tomassini S, Cuoghi V, Catalani E, Casini G, Bigiani A (2007) Long-term effects of nicotine on rat fungiform taste buds. Neuroscience 147:803–810

    Article  CAS  PubMed  Google Scholar 

  • Tordoff MG, Shao H, Alarcon LK, Margolskee RF, Mosinger B, Bachmanov AA, Reed DR, Mccaughey S (2008) Involvement of T1R3 in calcium-magnesium taste. Physiol Genomics 34:338–348

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tordoff MG, Alarcon LK, Valmeki S, Jiang P (2012) T1R3: a human calcium taste receptor. Sci Rep 2:496

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Uchida K, Tominaga M (2013) Extracellular zinc ion regulates transient receptor potential melastatin 5 (TRPM5) channel activation through its interaction with a pore loop domain. J Biol Chem 288:25950–25955

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Vandenbeuch A, Kinnamon SC (2009) Why do taste cells generate action potentials? J Biol 8:42

    Article  PubMed Central  PubMed  Google Scholar 

  • Vandenbeuch A, Clapp TR, Kinnamon SC (2008) Amiloride-sensitive channels in type I fungiform taste cells in mouse. BMC Neurosci 9:1

    Article  PubMed Central  PubMed  Google Scholar 

  • Vandenbeuch A, Anderson CB, Parnes J, Enjyoji K, Robson SC, Finger TE, Kinnamon SC (2013) Role of the ectonucleotidase NTPDase2 in taste bud function. Proc Natl Acad Sci U S A 110:14789–14794

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430:748–754

    Article  CAS  PubMed  Google Scholar 

  • Voets T, Owsianik G, Janssens A, Talavera K, Nilius B (2007) TRPM8 voltage sensor mutants reveal a mechanism for integrating thermal and chemical stimuli. Nat Chem Biol 3:174–182

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from the Research Council of the KU Leuven (EF/95/010 and PF-TRPLe).

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  1. Laboratory of Ion Channel Research, Department of Cellular and Molecular Medicine, KU Leuven, O&N I, Herestraat 49—box 802, 3000, Leuven, Belgium

    Karel Talavera

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  1. Karel Talavera
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Correspondence to Karel Talavera .

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  1. Faculty of Chemistry and Biology, University of Santiago de Chile, Santiago, Chile

    Rodolfo Madrid

  2. Faculty of Science, University of Chile, Santiago, Chile

    Juan Bacigalupo

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Talavera, K. (2015). TRP Channels as Targets for Modulation of Taste Transduction. In: Madrid, R., Bacigalupo, J. (eds) TRP Channels in Sensory Transduction. Springer, Cham. https://doi.org/10.1007/978-3-319-18705-1_6

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