Abstract
TRP channels are expressed in taste buds, nerve fibers, and keratinocytes in the oronasal cavity. These channels play integral roles in transducing chemical stimuli, giving rise to sensations of taste, irritation, warmth, coolness, and pungency. Specifically, TRPM5 acts downstream of taste receptors in the taste transduction pathway. TRPM5 channels convert taste-evoked intracellular Ca2+ release into membrane depolarization to trigger taste transmitter secretion. PKD2L1 is expressed in acid-sensitive (sour) taste bud cells but is unlikely to be the transducer for sour taste. TRPV1 is a receptor for pungent chemical stimuli such as capsaicin and for several irritants (chemesthesis). It is controversial whether TRPV1 is present in the taste buds and plays a direct role in taste. Instead, TRPV1 is expressed in non-gustatory sensory afferent fibers and in keratinocytes of the oronasal cavity. In many sensory fibers and epithelial cells lining the oronasal cavity, TRPA1 is also co-expressed with TRPV1. As with TRPV1, TRPA1 transduces a wide variety of irritants and, in combination with TRPV1, assures that there is a broad response to noxious chemical stimuli. Other TRP channels, including TRPM8, TRPV3, and TRPV4, play less prominent roles in chemesthesis and no known role in taste, per se. The pungency of foods and beverages is likely highly influenced by the temperature at which they are consumed, their acidity, and, for beverages, their carbonation. All these factors modulate the activity of TRP channels in taste buds and in the oronasal mucosa.
Keywords
- TRPM5
- TRPV1
- TRPA1
- Gustation
- Chemesthesis
- Sour
- Salty
- Irritants
- Spices
- Carbonated sodas
- Oronasal cavity
- Trigeminal
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- 1.
The proportions of types I, II, and III cells stated here are based on taste tissues from mice and rats, immunostained for cell markers that characterize these types (Ma et al. 2007). These proportions vary markedly depending on the location of the taste buds within the oral cavity.
- 2.
It remains arguable whether fatty acids or fats in general stimulate a primary taste quality in humans, as opposed to the sensations of olfaction and texture that fats elicit (Tucker and Mattes 2012).
- 3.
- 4.
TRPM5 channels are also found in chemical-sensing cells that express “taste” GPCRs but that are located outside the taste buds. For instance, solitary chemosensory cells in the upper air tract express taste receptors and TRPM5 channels (Kaske et al. 2007; Lin et al. 2008). These cells are discussed in greater detail later in this chapter. Also, isolated receptor cells in the lower respiratory tract that are innervated by vagal sensory fibers (“brush cells”) express bitter taste receptors and other components of the taste receptor transduction pathway, including TRPM5 (Kaske et al. 2007; Tizzano et al. 2010; Krasteva et al. 2011). In the intestinal tract, nutrient-sensing cells express taste GPCRs as well as TRPM5 channels (Wu et al. 2002; Fonfria et al. 2006; Bezencon et al. 2007; Jang et al. 2007; Kidd et al. 2008; Kokrashvili et al. 2009; Young et al. 2009; Janssen et al. 2011). These gut chemoreceptor cells may employ TRPM5 in a similar transduction pathway as do taste cells. Also, TRPM5 and taste receptors are expressed in the pancreas (Taniguchi 2004; Fonfria et al. 2006; Reimann et al. 2008; Nakagawa et al. 2009; Colsoul et al. 2010). TRPM5 channels are required for normal glucose-stimulated insulin secretion from the pancreas (Uchida and Tominaga 2011); Trpm5 knockout mice have impaired glucose tolerance, and pancreatic islets from these mice show defective glucose-induced insulin release (Colsoul et al. 2010). Nakagawa et al. (2009) showed that the insulin-secreting pancreatic β cell line, MIN6, that had previously been shown to express TRPM5 channels (Prawitt et al. 2003) expresses sweet taste receptors. They reported that artificial sweeteners and glucose promoted insulin secretion from these cells. These data reinforce the notion that there may be a transduction pathway in pancreatic β cells resembling that in taste Receptor (Type II) cells. [Curiously, without referring to the earlier study showing TRPM5 expression in MIN6 cells (Prawitt et al. 2003), Nakagawa et al. (2009) reported that TRPM5 was not present in their MIN6 cells.] Finally, taste receptors and TRPM5 are co-expressed in spermatids (Iwatsuki et al. 2010; Li and Zhou 2012; Meyer et al. 2012; Mosinger et al. 2013). The function of this chemoreceptor transduction pathway remains to be elucidated, though it appears to be involved in spermatid differentiation and maturation (Mosinger et al. 2013).
As a generality, one might argue that many chemosensory cells throughout the body that express “taste” GPCRs also express TRPM5 and likely mobilize intracellular Ca2+ in a manner similar to the canonical taste transduction pathway (Fig. 4). Perhaps the nomenclature for “taste” receptor genes, “TASRs,” should be reconsidered and renamed to apply more broadly to chemical sensors situated far distant from the end organs of taste in the oral cavity.
- 5.
However, using patch-clamp recordings, Nakamura and Bradley (2011) reported that geniculate ganglion neurons with axons in the posterior auricular nerve specifically were insensitive to capsaicin, a TRPV1 agonist. This finding argues against a population of geniculate ganglion nociceptive neurons dedicated to the posterior auricular nerve.
- 6.
Nakamura and Bradley (2011) also noted that geniculate ganglion neurons with axons in the chorda tympani nerve were insensitive to capsaicin, complementing the findings of Hiura et al. (1990). The only capsaicin-responsive geniculate ganglion neurons were those innervating the soft palate and having axons in the greater petrosal nerve (Nakamura and Bradley 2011).
- 7.
These are reasonable concentrations of capsaicin. Five to 100 μM capsaicin, when applied to the tongue, elicits a mild to moderate burning sensation (Simons et al. 2002).
- 8.
Parenthetically, other gustatory-related sensations attributed to TRPV1 channels include metallic taste (Riera et al. 2009) and aversive off-tastes of artificial sweeteners (Riera et al. 2008). These conclusions were reached by investigations using heterologous expression systems and taste behavioral assays. The conclusions from the behavioral studies were verified using Trpv1 knockout mice. How or whether those findings specifically implicate TRPV1 in taste bud cells or gustatory afferents remains to be examined in greater detail. TRPV1 also appears to play some role in the consumption of ethanol, though whether this involves taste per se is unlikely. Specifically, Trpv1 knockout mice have a higher preference for and consumption of ethanol solutions. Moreover, Trpv1 knockout mice have greater tolerance for the inebriating action of ethanol (Blednov and Harris 2009).
- 9.
Organic (“weak”) acids such as acetic acid exist as a mixture of protonated and dissociated acid molecules at levels of pH that are sharply sour tasting. Mineral (“strong”) acids such as HCl that are fully dissociated in aqueous solution do not readily cross the plasma membrane (i.e., the plasma membrane is tolerably impermeable to protons). Mineral acids are not as sour tasting as organic acids at equivalent pH values. Protons can only gain access to the cytosol via H+-permeable ion channels and transporters, neither of which are features of the PKD2L1/PKD1L3 dimer. Parenthetically, one such H+-permeable channel has been identified in Presynaptic (type III) taste bud cells. This channel may contribute to the sour taste of mineral acids (Chang et al. 2010).
- 10.
An interesting aside is that TRPV1 in birds lacks the molecular binding domain for capsaicin. Consequently, birds are indifferent to the irritation of capsaicin. This allows birds to consume and disperse seeds of plants such as chili peppers that otherwise repel animals (Jordt and Julius 2002).
- 11.
This is a simplification. By definition, at equi-pH, citric and acetic acid solutions contribute the same [H+]o. However, at a given pH, fully protonated acetic acid molecules will more readily cross the cell membrane and contribute to intracellular acidification more effectively than will partially protonated citric acid. For example, given their dissociation constants for the fully protonated, neutral moieties (presumably the molecule that is most membrane-permeant), a 10 mM solution of citric acid (pKa1 = 3.13) at pH = 3.13 will contribute 0.75 mM H+ and 4.9 mM triprotonated (neutral, membrane-permeant) acid molecules (H3Citrate). The remaining 5.1 mM consists of H2Citrate-, H1Citrate2-, and Citrate3-. By contrast, the same concentration of acetic acid (10 mM, pKa = 4.75) at this same pH will also contribute 0.75 mM H+ but a twofold higher concentration (9.8 mM) of the uncharged, membrane-permeant molecule, Hacetate.
- 12.
Parenthetically, altering the physical properties of the plasma membrane is how menthol might be modulating TRPM8 channel activity (Morenilla-Palao et al. 2009).
- 13.
Humans do not possess a comparable anatomical structure and the existence of human pheromones is debatable.
- 14.
As an aside, this low pH contributes little sourness to colas because protons do not readily cross the plasma membrane and stimulate sour taste. To put this pH into perspective, vinegar is ~700 mM acetic acid, pH 2.3 to 2.6 (see discussion in Roper 2007).
References
Abe J, Hosokawa H, Okazawa M, Kandachi M, Sawada Y, Yamanaka K, Matsumura K, Kobayashi S (2005) TRPM8 protein localization in trigeminal ganglion and taste papillae. Brain Res Mol Brain Res 136:91–98
Adachi R, Sasaki Y, Morita H, Komai M, Shirakawa H, Goto T, Furuyama A, Isono K (2012) Behavioral analysis of Drosophila transformants expressing human taste receptor genes in the gustatory receptor neurons. J Neurogenet 26:198–205
Adcock JJ (2009) TRPV1 receptors in sensitisation of cough and pain reflexes. Pulm Pharmacol Ther 22:65–70
Akopian AN (2011) Regulation of nociceptive transmission at the periphery via TRPA1-TRPV1 interactions. Curr Pharm Biotechnol 12:89–94
Akopian AN, Ruparel NB, Patwardhan A, Hargreaves KM (2008) Cannabinoids desensitize capsaicin and mustard oil responses in sensory neurons via TRPA1 activation. J Neurosci 28:1064–1075
Amato V, Vina E, Calavia MG, Guerrera MC, Laura R, Navarro M, De Carlos F, Cobo J, Germana A, Vega JA (2012) TRPV4 in the sensory organs of adult zebrafish. Microsc Res Techniq 75:89–96
Anand U, Otto WR, Facer P, Zebda N, Selmer I, Gunthorpe MJ, Chessell IP, Sinisi M, Birch R, Anand P (2008) TRPA1 receptor localisation in the human peripheral nervous system and functional studies in cultured human and rat sensory neurons. Neurosci Lett 438:221–227
Andersson DA, Gentry C, Bevan S (2012) TRPA1 has a key role in the somatic pro-nociceptive actions of hydrogen sulfide. PLoS One 7:e46917
Arai T, Ohkuri T, Yasumatsu K, Kaga T, Ninomiya Y (2010) The role of transient receptor potential vanilloid-1 on neural responses to acids by the chorda tympani, glossopharyngeal and superior laryngeal nerves in mice. Neuroscience 165:1476–1489
Atoyan R, Shander D, Botchkareva NV (2009) Non-neuronal expression of transient receptor potential type A1 (TRPA1) in human skin. J Invest Dermatol 129:2312–2315
Bae YC, Oh JM, Hwang SJ, Shigenaga Y, Valtschanoff JG (2004) Expression of vanilloid receptor TRPV1 in the rat trigeminal sensory nuclei. J Comp Neurol 478:62–71
Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849–857
Bandell M, Macpherson LJ, Patapoutian A (2007) From chills to chilis: mechanisms for thermosensation and chemesthesis via thermoTRPs. Curr Opin Neurobiol 17:490–497
Barham HP, Cooper SE, Anderson CB, Tizzano M, Kingdom TT, Finger TE, Kinnamon SC, Ramakrishnan VR (2013) Solitary chemosensory cells and bitter taste receptor signaling in human sinonasal mucosa. Int Forum Allergy Rhinol 3:450–457
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
Bautista DM, Movahed P, Hinman A, Axelsson HE, Sterner O, Hogestatt ED, Julius D, Jordt SE, Zygmunt PM (2005) Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci USA 102:12248–12252
Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204–208
Becker D, Blase C, Bereiter-Hahn J, Jendrach M (2005) TRPV4 exhibits a functional role in cell-volume regulation. J Cell Sci 118:2435–2440
Bezencon C, le CJ, Damak S (2007) Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses 32:41–49
Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, Watkins S, Caterina MJ (2002) Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 5:856–860
Blednov YA, Harris RA (2009) Deletion of vanilloid receptor (TRPV1) in mice alters behavioral effects of ethanol. Neuropharmacology 56:814–820
Bo X, Alavi A, Xiang Z, Oglesby I, Ford A, Burnstock G (1999) Localization of ATP-gated P2X2 and P2X3 receptor immunoreactive nerves in rat taste buds. Neuroreport 10(5):1107–1111
Boulais N, Pennec JP, Lebonvallet N, Pereira U, Rougier N, Dorange G, Chesne C, Misery L (2009) Rat Merkel cells are mechanoreceptors and osmoreceptors. PLoS One 4:e7759
Bradley RM (2000) Sensory receptors of the larynx. Am J Med 108:47S–50S
Cain WS, Murphy CL (1980) Interaction between chemoreceptive modalities of odour and irritation. Nature 284:255–257
Carstens E, Iodi Carstens M, Dessirier J-M, O’Mahony M, Simons CT, Sudo M, Sudo S (2002) It hurts so good: oral irritation by spices and carbonated drinks and the underlying neural mechanisms. Food Qual Pref 13:431–443
Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824
Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436–441
Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306–313
Chang RB, Waters H, Liman ER (2010) A proton current drives action potentials in genetically identified sour taste cells. Proc Natl Acad Sci USA 107:22320–22325
Chaudhari N, Roper SD (2010) The cell biology of taste. J Cell Biol 190:285–296
Chung MK, Lee H, Caterina MJ (2003) Warm temperatures activate TRPV4 in mouse 308 keratinocytes. J Biol Chem 278:32037–32046
Chung S, Kim YH, Koh JY, Nam TS, Ahn DS (2011) Intracellular acidification evoked by moderate extracellular acidosis attenuates transient receptor potential V1 (TRPV1) channel activity in rat dorsal root ganglion neurons. Exp Physiol 96:1270–1281
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
Colburn RW, Lubin ML, Stone DJ Jr, Wang Y, Lawrence D, D’Andrea MR, Brandt MR, Liu Y, Flores CM, Qin N (2007) Attenuated cold sensitivity in TRPM8 null mice. Neuron 54:379–386
Collier JG, Fuller RW (1984) Capsaicin inhalation in man and the effects of sodium cromoglycate. Br J Pharmacol 81:113–117
Colsoul B, Schraenen A, Lemaire K, Quintens R, Van Lommel L, Segal A, Owsianik G, Talavera K, Voets T, Margolskee RF, Kokrashvili Z, Gilon P, Nilius B, Schuit FC, Vennekens R (2010) Loss of high-frequency glucose-induced Ca2+ oscillations in pancreatic islets correlates with impaired glucose tolerance in Trpm5-/- mice. Proc Natl Acad Sci USA 107:5208–5213
Cortright DN, Szallasi A (2009) TRP channels and pain. Curr Pharm Des 15:1736–1749
Costa RM, Liu L, Nicolelis MA, Simon SA (2005) Gustatory effects of capsaicin that are independent of TRPV1 receptors. Chem Senses 30:i198–200
Cruz A, Green BG (2000) Thermal stimulation of taste. Nature 403:889–892
Dahl M, Erickson RP, Simon SA (1997) Neural responses to bitter compounds in rats. Brain Res 756:22–34
Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Perez CA, Shigemura N, Yoshida R, Mosinger B, Glendinning JI, Ninomiya Y, Margolskee RF (2006) Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses 31:253–264
Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183–187
de la Roche J, Eberhardt MJ, Klinger AB, Stanslowksy N, Wegner F, Koppert W, Reeh PW, Lampert A, Fischer MJ, Leffler A (2013) The molecular basis for species-specific activation of human TRPA1 by protons involves poorly conserved residues within transmembrane domains 5 and 6. J Biol Chem 288:20280–20292
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
Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A (2007) TRPM8 is required for cold sensation in mice. Neuron 54:371–378
Dhaka A, Earley TJ, Watson J, Patapoutian A (2008) Visualizing cold spots: TRPM8-expressing sensory neurons and their projections. J Neurosci 28:566–575
Dhaka A, Uzzell V, Dubin AE, Mathur J, Petrus M, Bandell M, Patapoutian A (2009) TRPV1 is activated by both acidic and basic pH. J Neurosci 29:153–158
Diogenes A, Akopian AN, Hargreaves KM (2007) NGF up-regulates TRPA1: implications for orofacial pain. J Dent Res 86:550–555
Dixon CJ, Bowler WB, Littlewood-Evans A, Dillon JP, Bilbe G, Sharpe GR, Gallagher JA (1999) Regulation of epidermal homeostasis through P2Y2 receptors. Br J Pharmacol 127:1680–1686
Dussor GO, Leong AS, Gracia NB, Kilo S, Price TJ, Hargreaves KM, Flores CM (2003) Potentiation of evoked calcitonin gene-related peptide release from oral mucosa: a potential basis for the pro-inflammatory effects of nicotine. Eur J Neurosci 18:2515–2526
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
Everaerts W, Sepulveda MR, Gevaert T, Roskams T, Nilius B, De Ridder D (2009) Where is TRPV1 expressed in the bladder, do we see the real channel? Naunyn Schmiedebergs Arch Pharmacol 379:421–425
Fernandes ES, Fernandes MA, Keeble JE (2012) The functions of TRPA1 and TRPV1: moving away from sensory nerves. Br J Pharmacol 166:510–521
Finger TE (1986) Peptide immunohistochemistry demonstrates multiple classes of perigemmal nerve fibers in the circumvallate papilla of the rat. Chem Senses 11:135–144
Finger TE, Bottger B, Hansen A, Anderson KT, Alimohammadi H, Silver WL (2003) Solitary chemoreceptor cells in the nasal cavity serve as sentinels of respiration. Proc Natl Acad Sci USA 100:8981–8986
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
Fonfria E, Murdock PR, Cusdin FS, Benham CD, Kelsell RE, McNulty S (2006) Tissue distribution profiles of the human TRPM cation channel family. J Recept Signal Transduct Res 26:159–178
Frank ME, Formaker BK, Hettinger TP (2005) Peripheral gustatory processing of sweet stimuli by golden hamsters. Brain Res Bull 66:70–84
Frasnelli J, Schuster B, Hummel T (2007) Interactions between olfaction and the trigeminal system: what can be learned from olfactory loss. Cereb Cortex 17:2268–2275
Gerhold KA, Bautista DM (2009) Molecular and cellular mechanisms of trigeminal chemosensation. Ann N Y Acad Sci 1170:184–189
Green BG (1986) Sensory interactions between capsaicin and temperature in the oral cavity. Chem Senses 11:371–382
Green BG (2000) Measurement of sensory irritation of the skin. Am J Contact Dermat 11:170–180
Green BG (2012) Chemesthesis and the chemical senses as components of a “chemofensor complex”. Chem Senses 37:201–206
Green BG, Macon JR, Kare MR (1990) Chemical senses volume 2: irritation. Marcel Dekker, New York, NY
Green BG, Lim J, Osterhoff F, Blacher K, Nachtigal D (2010) Taste mixture interactions: suppression, additivity, and the predominance of sweetness. Physiol Behav 101:731–737
Gu XF, Lee JH, Yoo SB, Moon YW, Jahng JW (2009) Intra-oral pre-treatment with capsaicin increases consumption of sweet solutions in rats. Nutr Neurosci 12:149–154
Hansson L, Choudry NB, Karlsson JA, Fuller RW (1994) Inhaled nicotine in humans: effect on the respiratory and cardiovascular systems. J Appl Physiol 76:2420–2427
Harvey RB (1920) The relation between the total acidity, the concentration of the hydrogen ion, and the taste of acid solutions. J Am Chem Soc 42:712–714
Hewson L, Hollowood T, Chandra S, Hort J (2009) Gustatory, olfactory and trigeminal interactions in a model carbonated beverage. Chem Percept 2:94–107
Hiura A, Ishizuka H, Sakamoto Y (1990) Electron microscopic study of the effect of capsaicin on the mouse chorda tympani nerves. Arch Oral Biol 35:913–916
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
Holzer P (1988) Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24:739–768
Horio N, Yoshida R, Yasumatsu K, Yanagawa Y, Ishimaru Y, Matsunami H, Ninomiya Y (2011) Sour taste responses in mice lacking PKD channels. PLoS One 6:e20007
Huang YA, Roper SD (2010) Intracellular Ca2+ and TRPM5-mediated membrane depolarization produce ATP secretion from taste receptor cells. J Physiol 588:2343–2350
Huang AL, Chen X, Hoon MA, Chandrashekar J, Guo W, Trankner D, Ryba NJ, Zuker CS (2006) The cells and logic for mammalian sour taste detection. Nature 442:934–938
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 USA 104:6436–6441
Huang SM, Lee H, Chung MK, Park U, Yu YY, Bradshaw HB, Coulombe PA, Walker JM, Caterina MJ (2008a) Overexpressed transient receptor potential vanilloid 3 ion channels in skin keratinocytes modulate pain sensitivity via prostaglandin E2. J Neurosci 28:13727–13737
Huang YA, Maruyama Y, Stimac R, Roper SD (2008b) Presynaptic (Type III) cells in mouse taste buds sense sour (acid) taste. J Physiol 586:2903–2912
Huang SM, Li X, Yu Y, Wang J, Caterina MJ (2011) TRPV3 and TRPV4 ion channels are not major contributors to mouse heat sensation. Mol Pain 7:37
Huque T, Cowart BJ, Dankulich-Nagrudny L, Pribitkin EA, Bayley DL, Spielman AI, Feldman RS, Mackler SA, Brand JG (2009) Sour ageusia in two individuals implicates ion channels of the ASIC and PKD families in human sour taste perception at the anterior tongue. PLoS One 4:e7347
Ichikawa H, Sugimoto T (2001) VR1-immunoreactive primary sensory neurons in the rat trigeminal ganglion. Brain Res 890:184–188
Inada H, Kawabata F, Ishimaru Y, Fushiki T, Matsunami H, Tominaga M (2008) Off-response property of an acid-activated cation channel complex PKD1L3-PKD2L1. EMBO Rep 9:690–697
Ishida Y, Ugawa S, Ueda T, Murakami S, Shimada S (2002) Vanilloid receptor subtype-1 (VR1) is specifically localized to taste papillae. Brain Res Mol Brain Res 107:17–22
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
Ishii S, Kishi M, Yamagami K, Okada S, Abe K, Misaka T (2012) The use of mammalian cultured cells loaded with a fluorescent dye shows specific membrane penetration of undissociated acetic acid. Biosci Biotechnol Biochem 76:523–529
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 USA 103:12569–12574
Iwatsuki K, Nomura M, Shibata A, Ichikawa R, Enciso PL, Wang L, Takayanagi R, Torii K, Uneyama H (2010) Generation and characterization of T1R2-LacZ knock-in mouse. Biochem Biophys Res Commun 402:495–499
Jain P, Nihill P, Sobkowski J, Agustin MZ (2007) Commercial soft drinks: pH and in vitro dissolution of enamel. Gen Dent 55:150–154
Jang HJ, Kokrashvili Z, Theodorakis MJ, Carlson OD, Kim BJ, Zhou J, Kim HH, Xu X, Chan SL, Juhaszova M, Bernier M, Mosinger B, Margolskee RF, Egan JM (2007) Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proc Natl Acad Sci USA 104:15069–15074
Janssen S, Laermans J, Verhulst PJ, Thijs T, Tack J, Depoortere I (2011) Bitter taste receptors and alpha-gustducin regulate the secretion of ghrelin with functional effects on food intake and gastric emptying. Proc Natl Acad Sci USA 108:2094–2099
Jeftinija S, Jeftinija K, Liu F, Skilling SR, Smullin DH, Larson AA (1991) Excitatory amino acids are released from rat primary afferent neurons in vitro. Neurosci Lett 125:191–194
Jordt SE, Julius D (2002) Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108:421–430
Jordt SE, Tominaga M, Julius D (2000) Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc Natl Acad Sci USA 97:8134–8139
Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260–265
Karashima Y, Damann N, Prenen J, Talavera K, Segal A, Voets T, Nilius B (2007) Bimodal action of menthol on the transient receptor potential channel TRPA1. J Neurosci 27:9874–9884
Kashiwayanagi M, Suenaga A, Enomoto S, Kurihara K (1990) Membrane fluidity changes of liposomes in response to various odorants. Complexity of membrane composition and variety of adsorption sites for odorants. Biophys J 58:887–895
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
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
Katsura H, Tsuzuki K, Noguchi K, Sakagami M (2006) Differential expression of capsaicin-, menthol-, and mustard oil-sensitive receptors in naive rat geniculate ganglion neurons. Chem Senses 31:681–688
Kawaguchi H, Yamanaka A, Uchida K, Shibasaki K, Sokabe T, Maruyama Y, Yanagawa Y, Murakami S, Tominaga M (2010) Activation of polycystic kidney disease-2-like 1 (PKD2L1)-PKD1L3 complex by acid in mouse taste cells. J Biol Chem 285:17277–17281
Kawashima M, Imura K, Sato I (2012) Topographical organization of TRPV1-immunoreactive epithelium and CGRP-immunoreactive nerve terminals in rodent tongue. Eur J Histochem 56:e21
Keast RSJ, Breslin PAS (2003) An overview of binary taste–taste interactions. Food Qual Prefer 14:111–124
Kichko TI, Reeh PW (2009) TRPV1 controls acid- and heat-induced calcitonin gene-related peptide release and sensitization by bradykinin in the isolated mouse trachea. Eur J Neurosci 29:1896–1904
Kida N, Sokabe T, Kashio M, Haruna K, Mizuno Y, Suga Y, Nishikawa K, Kanamaru A, Hongo M, Oba A, Tominaga M (2012) Importance of transient receptor potential vanilloid 4 (TRPV4) in epidermal barrier function in human skin keratinocytes. Pflugers Arch 463:715–725
Kidd M, Modlin IM, Gustafsson BI, Drozdov I, Hauso O, Pfragner R (2008) Luminal regulation of normal and neoplastic human EC cell serotonin release is mediated by bile salts, amines, tastants, and olfactants. Am J Physiol Gastrointest Liver Physiol 295:G260–272
Kido MA, Muroya H, Yamaza T, Terada Y, Tanaka T (2003) Vanilloid receptor expression in the rat tongue and palate. J Dent Res 82:393–397
Kim HY, Chung G, Jo HJ, Kim YS, Bae YC, Jung SJ, Kim JS, Oh SB (2011) Characterization of dental nociceptive neurons. J Dent Res 90:771–776
Knowlton WM, Palkar R, Lippoldt EK, McCoy DD, Baluch F, Chen J, McKemy DD (2013) A sensory-labeled line for cold: TRPM8-expressing sensory neurons define the cellular basis for cold, cold pain, and cooling-mediated analgesia. J Neurosci 33:2837–2848
Kobayashi K, Fukuoka T, Obata K, Yamanaka H, Dai Y, Tokunaga A, Noguchi K (2005) Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors. J Comp Neurol 493:596–606
Koizumi S, Fujishita K, Inoue K, Shigemoto-Mogami Y, Tsuda M, Inoue K (2004) Ca2+ waves in keratinocytes are transmitted to sensory neurons: the involvement of extracellular ATP and P2Y2 receptor activation. Biochem J 380:329–338
Kokrashvili Z, Rodriguez D, Yevshayeva V, Zhou H, Margolskee RF, Mosinger B (2009) Release of endogenous opioids from duodenal enteroendocrine cells requires Trpm5. Gastroenterology 137:598–606
Krasteva G, Canning BJ, Hartmann P, Veres TZ, Papadakis T, Muhlfeld C, Schliecker K, Tallini YN, Braun A, Hackstein H, Baal N, Weihe E, Schutz B, Kotlikoff M, Ibanez-Tallon I, Kummer W (2011) Cholinergic chemosensory cells in the trachea regulate breathing. Proc Natl Acad Sci USA 108:9478–9483
Kroeze JH, Bartoshuk LM (1985) Bitterness suppression as revealed by split-tongue taste stimulation in humans. Physiol Behav 35:779–783
Kun J, Helyes Z, Perkecz A, Ban A, Polgar B, Szolcsanyi J, Pinter E (2012) Effect of surgical and chemical sensory denervation on non-neural expression of the transient receptor potential vanilloid 1 (TRPV1) receptors in the rat. J Mol Neurosci 48:795–803
Kusuhara Y, Yoshida R, Ohkuri T, Yasumatsu K, Voigt A, Hubner S, Maeda K, Boehm U, Meyerhof W, Ninomiya Y (2013) Taste responses in mice lacking taste receptor subunit T1R1. J Physiol 591:1967–1985
Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277–289
Lanosa MJ, Willis DN, Jordt S, Morris JB (2010) Role of metabolic activation and the TRPA1 receptor in the sensory irritation response to styrene and naphthalene. Toxicol Sci 115:589–595
Laska M, Distel H, Hudson R (1997) Trigeminal perception of odorant quality in congenitally Anosmic subjects. Chem Senses 22:447–456
Lawless HT (1979) Evidence for neural inhibition in bittersweet taste mixtures. J Comp Physiol Psychol 93:538–547
Lawless H, Rozin P, Shenker J (1985) Effects of oral capsaicin on gustatory, olfactory and irritant sensations and flavor identification in humans who regularly or rarely consume chili pepper. Chemi Senses 10:579–589
Lee H, Caterina MJ (2005) TRPV channels as thermosensory receptors in epithelial cells. Pflugers Arch 451:160–167
Li F, Zhou M (2012) Depletion of bitter taste transduction leads to massive spermatid loss in transgenic mice. Mol Hum Reprod 18:289–297
Liman ER (2007) TRPM5 and taste transduction. Handb Exp Pharmacol 179:287–298
Lin W, Ogura T, Margolskee RF, Finger TE, Restrepo D (2008) TRPM5-expressing solitary chemosensory cells respond to odorous irritants. J Neurophysiol 99:1451–1460
Liu D, Liman ER (2003) Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci USA 100:15160–15165
Liu L, Simon SA (2000) Capsaicin, acid and heat-evoked currents in rat trigeminal ganglion neurons: relationship to functional VR1 receptors. Physiol Behav 69:363–378
Liu L, Simon SA (2001) Acidic stimuli activates two distinct pathways in taste receptor cells from rat fungiform papillae. Brain Res 923:58–70
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
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
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
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
Lumpkin EA, Caterina MJ (2007) Mechanisms of sensory transduction in the skin. Nature 445:858–865
Lundberg JM, Saria A (1983) Capsaicin-induced desensitization of airway mucosa to cigarette smoke, mechanical and chemical irritants. Nature 302:251–253
Lyall V, Alam RI, Phan DQ, Ereso GL, Phan TH, Malik SA, Montrose MH, Chu S, Heck GL, Feldman GM, DeSimone JA (2001) Decrease in rat taste receptor cell intracellular pH is the proximate stimulus in sour taste transduction. Am J Physiol Cell Physiol 281:C1005–C1013
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
Ma H, Yang R, Thomas SM, Kinnamon JC (2007) Qualitative and quantitative differences between taste buds of the rat and mouse. BMC Neurosci 8:5
Macpherson LJ, Geierstanger BH, Viswanath V, Bandell M, Eid SR, Hwang S, Patapoutian A (2005) The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin. Curr Biol 15:929–934
Malkia A, Morenilla-Palao C, Viana F (2011) The emerging pharmacology of TRPM8 channels: hidden therapeutic potential underneath a cold surface. Curr Pharm Biotechnol 12:54–67
Marincsak R, Toth BI, Czifra G, Marton I, Redl P, Tar I, Toth L, Kovacs L, Biro T (2009) Increased expression of TRPV1 in squamous cell carcinoma of the human tongue. Oral Dis 15:328–335
Martenson ME, Ingram SL, Baumann TK (1994) Potentiation of rabbit trigeminal responses to capsaicin in a low pH environment. Brain Res 651:143–147
Matsumoto I, Emori Y, Ninomiya Y, Abe K (2001) A comparative study of three cranial sensory ganglia projecting into the oral cavity: in situ hybridization analyses of neurotrophin receptors and thermosensitive cation channels. Brain Res Mol Brain Res 93:105–112
McKemy DD (2007) Temperature sensing across species. Pflugers Arch 454:777–791
McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52–58
McNamara FN, Randall A, Gunthorpe MJ (2005) Effects of piperine, the pungent component of black pepper, at the human vanilloid receptor (TRPV1). Br J Pharmacol 144:781–790
Meyer D, Voigt A, Widmayer P, Borth H, Huebner S, Breit A, Marschall S, de Angelis MH, Boehm U, Meyerhof W, Gudermann T, Boekhoff I (2012) Expression of Tas1 taste receptors in mammalian spermatozoa: functional role of Tas1r1 in regulating basal Ca(2)(+) and cAMP concentrations in spermatozoa. PLoS One 7:e32354
Mihara H, Boudaka A, Sugiyama T, Moriyama Y, Tominaga M (2011) Transient receptor potential vanilloid 4 (TRPV4)-dependent calcium influx and ATP release in mouse oesophageal keratinocytes. J Physiol 589:3471–3482
Moon YW, Lee JH, Yoo SB, Jahng JW (2010) Capsaicin receptors are colocalized with sweet/bitter receptors in the taste sensing cells of circumvallate papillae. Genes Nutr 5:251–255
Moore C, Cevikbas F, Pasolli HA, Chen Y, Kong W, Kempkes C, Parekh P, Lee SH, Kontchou NA, Yeh I, Jokerst NM, Fuchs E, Steinhoff M, Liedtke WB (2013) UVB radiation generates sunburn pain and affects skin by activating epidermal TRPV4 ion channels and triggering endothelin-1 signaling. Proc Natl Acad Sci USA 110:E3225–E3234
Moqrich A, Hwang SW, Earley TJ, Petrus MJ, Murray AN, Spencer KS, Andahazy M, Story GM, Patapoutian A (2005) Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307:1468–1472
Morales-Lazaro SL, Simon SA, Rosenbaum T (2013) The role of endogenous molecules in modulating pain through TRPV1. J Physiol 591:3109–3121
Morenilla-Palao C, Pertusa M, Meseguer V, Cabedo H, Viana F (2009) Lipid raft segregation modulates TRPM8 channel activity. J Biol Chem 284:9215–9224
Mosinger B, Redding KM, Parker MR, Yevshayeva V, Yee KK, Dyomina K, Li Y, Margolskee RF (2013) Genetic loss or pharmacological blockade of testes-expressed taste genes causes male sterility. Proc Natl Acad Sci USA 110:12319–12324
Moussaieff A, Rimmerman N, Bregman T, Straiker A, Felder CC, Shoham S, Kashman Y, Huang SM, Lee H, Shohami E, Mackie K, Caterina MJ, Walker JM, Fride E, Mechoulam R (2008) Incensole acetate, an incense component, elicits psychoactivity by activating TRPV3 channels in the brain. FASEB J 22:3024–3034
Nagy JI, Goedert M, Hunt SP, Bond A (1982) The nature of the substance P-containing nerve fibres in taste papillae of the rat tongue. Neuroscience 7:3137–3151
Nakagawa Y, Nagasawa M, Yamada S, Hara A, Mogami H, Nikolaev VO, Lohse MJ, Shigemura N, Ninomiya Y, Kojima I (2009) Sweet taste receptor expressed in pancreatic beta-cells activates the calcium and cyclic AMP signaling systems and stimulates insulin secretion. PLoS One 4:e5106
Nakamura S, Bradley RM (2011) Characteristics of sodium currents in rat geniculate ganglion neurons. J Neurophysiol 106:2982–2991
Nakashimo Y, Takumida M, Fukuiri T, Anniko M, Hirakawa K (2010) Expression of transient receptor potential channel vanilloid (TRPV) 1–4, melastin (TRPM) 5 and 8, and ankyrin (TRPA1) in the normal and methimazole-treated mouse olfactory epithelium. Acta Otolaryngol 130:1278–1286
Nakatsuka M, Iwai Y (2009) Expression of TRPV4 in the stimulated rat oral mucous membrane–nociceptive mechanisms of lingual conical papillae. Okajimas Folia Anat Jpn 86:45–54
Nassini R, Pedretti P, Moretto N, Fusi C, Carnini C, Facchinetti F, Viscomi AR, Pisano AR, Stokesberry S, Brunmark C, Svitacheva N, McGarvey L, Patacchini R, Damholt AB, Geppetti P, Materazzi S (2012) Transient receptor potential ankyrin 1 channel localized to non-neuronal airway cells promotes non-neurogenic inflammation. PLoS One 7:e42454
Nealen ML, Gold MS, Thut PD, Caterina MJ (2003) TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J Neurophysiol 90:515–520
Neeper MP, Liu Y, Hutchinson TL, Wang Y, Flores CM, Qin N (2007) Activation properties of heterologously expressed mammalian TRPV2: evidence for species dependence. J Biol Chem 282:15894–15902
Nelson TM, Lopezjimenez ND, Tessarollo L, Inoue M, Bachmanov AA, Sullivan SL (2010) Taste function in mice with a targeted mutation of the pkd1l3 gene. Chem Senses 35:565–577
Nilius B, Appendino G (2011) Tasty and healthy TR(i)Ps. The human quest for culinary pungency. EMBO Rep 12:1094–1101
Nilius B, Appendino G (2013) Spices: the savory and beneficial science of pungency. Rev Physiol Biochem Pharmacol 164:1–76
Nilius B, Appendino G, Owsianik G (2012) The transient receptor potential channel TRPA1: from gene to pathophysiology. Pflugers Arch 464:425–458
Ogura T, Krosnowski K, Zhang L, Bekkerman M, Lin W (2010) Chemoreception regulates chemical access to mouse vomeronasal organ: role of solitary chemosensory cells. PLoS One 5:e11924
O'Hanlon S, Facer P, Simpson KD, Sandhu G, Saleh HA, Anand P (2007) Neuronal markers in allergic rhinitis: expression and correlation with sensory testing. Laryngoscope 117:1519–1527
Ohta T, Imagawa T, Ito S (2007) Novel agonistic action of mustard oil on recombinant and endogenous porcine transient receptor potential V1 (pTRPV1) channels. Biochem Pharmacol 73:1646–1656
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
Oka Y, Butnaru M, von Buchholtz L, Ryba NJ, Zuker CS (2013) High salt recruits aversive taste pathways. Nature 494:472–475
Okada Y, Reinach PS, Shirai K, Kitano A, Kao WW, Flanders KC, Miyajima M, Liu H, Zhang J, Saika S (2011) TRPV1 involvement in inflammatory tissue fibrosis in mice. Am J Pathol 178:2654–2664
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 USA 106:1596–1601
Omote K, Kawamata T, Kawamata M, Namiki A (1998) Formalin-induced release of excitatory amino acids in the skin of the rat hindpaw. Brain Res 787:161–164
Osada K, Komai M, Bryant BP, Suzuki H, Goto A, Tsunoda K, Kimura S, Furukawa Y (1997) Capsaicin modifies responses of rat chorda tympani nerve fibers to NaCl. Chem Senses 22:249–255
Palmer RK, Atwal K, Bakaj I, Carlucci-Derbyshire S, Buber MT, Cerne R, Cortes RY, Devantier HR, Jorgensen V, Pawlyk A, Lee SP, Sprous DG, Zhang Z, Bryant R (2010) Triphenylphosphine oxide is a potent and selective inhibitor of the transient receptor potential melastatin-5 ion channel. Assay Drug Dev Technol 8:703–713
Park K, Brown PD, Kim YB, Kim JS (2003) Capsaicin modulates K + currents from dissociated rat taste receptor cells. Brain Res 962:135–143
Park U, Vastani N, Guan Y, Raja SN, Koltzenburg M, Caterina MJ (2011) TRP vanilloid 2 knock-out mice are susceptible to perinatal lethality but display normal thermal and mechanical nociception. J Neurosci 31:11425–11436
Parker GH (1912) The relations of smell, taste, and the common chemical sense in vertebrates. J Acad Natl Sci Phila 15:221–234
Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A (2002a) A TRP channel that senses cold stimuli and menthol. Cell 108:705–715
Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, Story GM, Colley S, Hogenesch JB, McIntyre P, Bevan S, Patapoutian A (2002b) A heat-sensitive TRP channel expressed in keratinocytes. Science 296:2046–2049
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
Petersen M, LaMotte RH (1993) Effect of protons on the inward current evoked by capsaicin in isolated dorsal root ganglion cells. Pain 54:37–42
Peyrot des Gachons C, Uchida K, Bryant B, Shima A, Sperry JB, Dankulich-Nagrudny L, Tominaga M, Smith AB, Beauchamp GK, Breslin PA (2011) Unusual pungency from extra-virgin olive oil is attributable to restricted spatial expression of the receptor of oleocanthal. J Neurosci 31:999–1009
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 USA 100:15166–15171
Prescott J, Allen S, Stephens L (1993) Interactions between oral chemical irritation, taste and temperature. Chem Senses 18:389–404
Qin N, Neeper MP, Liu Y, Hutchinson TL, Lubin ML, Flores CM (2008) TRPV2 is activated by cannabidiol and mediates CGRP release in cultured rat dorsal root ganglion neurons. J Neurosci 28:6231–6238
Reimann F, Habib AM, Tolhurst G, Parker HE, Rogers GJ, Gribble FM (2008) Glucose sensing in L cells: a primary cell study. Cell Metab 8:532–539
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:G106–117
Rentmeister-Bryant H, Green BG (1997) Perceived irritation during ingestion of capsaicin or piperine: comparison of trigeminal and non-trigeminal areas. Chem Senses 22:257–266
Richter TA, Caicedo A, Roper SD (2003) Sour taste stimuli evoke Ca2+ and pH responses in mouse taste cells. J Physiol 547:475–483
Riera CE, Vogel H, Simon SA, Damak S, le Coutre J (2008) The capsaicin receptor participates in artificial sweetener aversion. Biochem Biophys Res Commun 376:653–657
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
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
Rong W, Burnstock G, Spyer KM (2000) P2X purinoceptor-mediated excitation of trigeminal lingual nerve terminals in an in vitro intra-arterially perfused rat tongue preparation. J Physiol 524(Pt 3):891–902
Roper SD (2007) Signal transduction and information processing in mammalian taste buds. Pflugers Arch 454:759–776
Roper SD (2013) Taste buds as peripheral chemosensory processors. Semin Cell Dev Biol 2013(24):71–79
Rozin P, Mark M, Schiller D (1981) The role of desensitization to capsaicin in chili pepper ingestion and preference. Chem Senses 6:23–31
Ruiz C, Gutknecht S, Delay E, Kinnamon S (2006) Detection of NaCl and KCl in TRPV1 Knockout Mice. Chem Senses 31:813–820
Salas MM, Hargreaves KM, Akopian AN (2009) TRPA1-mediated responses in trigeminal sensory neurons: interaction between TRPA1 and TRPV1. Eur J Neurosci 29:1568–1578
Sasaki R, Sato T, Yajima T, Kano M, Suzuki T, Ichikawa H (2013) The distribution of TRPV1 and TRPV2 in the rat pharynx. Cell Mol Neurobiol 33(5):707–714
Sato M, Ogawa H, Yamashita S (1975) Response properties of macaque monkey chorda tympani fibers. J Gen Physiol 66:781–810
Sato T, Fujita M, Kano M, Hosokawa H, Kondo T, Suzuki T, Kasahara E, Shoji N, Sasano T, Ichikawa H (2013) The distribution of transient receptor potential melastatin-8 in the rat soft palate, epiglottis, and pharynx. Cell Mol Neurobiol 33:161–165
Saunders CJ, Winston YL, Patel TD, Muday JA, Silver WL (2013) Dissecting the role of TRPV1 in detecting multiple trigeminal irritants in three behavioral assays for sensory irritation. F1000Res 2:74
Savant L, McDaniel M (2004) Suppression of sourness: A comparative study involving mixtures of organic acids and sugars. Percept Psychophys 66:642–650
Sbarbati A, Osculati F (2005) The taste cell-related diffuse chemosensory system. Prog Neurobiol 75:295–307
Schiffman SS, Sattely-Miller EA, Graham BG, Bennett JL, Booth BJ, Desai N, Bishay I (2000) Effect of temperature, pH, and ions on sweet taste. Physiol Behav 68:469–481
Seki N, Shirasaki H, Kikuchi M, Sakamoto T, Watanabe N, Himi T (2006) Expression and localization of TRPV1 in human nasal mucosa. Rhinology 44:128–134
Sherkheli MA, Gisselmann G, Hatt H (2012) Supercooling agent icilin blocks a warmth-sensing ion channel TRPV3. Scientific World J 2012:982725
Shimohira D, Kido MA, Danjo A, Takao T, Wang B, Zhang JQ, Yamaza T, Masuko S, Goto M, Tanaka T (2009) TRPV2 expression in rat oral mucosa. Histochem Cell Biol 132:423–433
Shin Y-C, Shin S-Y, So I, Kwon D, Jeon J-H (2011) TRIP Database: a manually curated database of protein–protein interactions for mammalian TRP channels. Nucleic Acids Res 39:D356–D361
Silver WL, Clapp TR, Stone LM, Kinnamon SC (2006) TRPV1 receptors and nasal trigeminal chemesthesis. Chem Senses 31:807–812
Simons CT, O'Mahony M, Carstens E (2002) Taste suppression following lingual capsaicin pre-treatment in humans. Chem Senses 27:353–365
Sizer F, Harris N (1985) The influence of common food additives and temperature on threshold perception of capsaicin. Chem Senses 10:279–286
Smith PL, Maloney KN, Pothen RG, Clardy J, Clapham DE (2006) Bisandrographolide from Andrographis paniculata activates TRPV4 channels. J Biol Chem 281:29897–29904
Smith KR, Treesukosol Y, Paedae AB, Contreras RJ, Spector AC (2012) Contribution of the TRPV1 channel to salt taste quality in mice as assessed by conditioned taste aversion generalization and chorda tympani nerve responses. Am J Physiol Regul Integr Comp Physiol 303:R1195–1205
Sokabe T, Fukumi-Tominaga T, Yonemura S, Mizuno A, Tominaga M (2010) The TRPV4 channel contributes to intercellular junction formation in keratinocytes. J Biol Chem 285:18749–18758
Sprague J, Harrison C, Rowbotham DJ, Smart D, Lambert DG (2001) Temperature-dependent activation of recombinant rat vanilloid VR1 receptors expressed in HEK293 cells by capsaicin and anandamide. Eur J Pharmacol 423:121–125
Stander S, Moormann C, Schumacher M, Buddenkotte J, Artuc M, Shpacovitch V, Brzoska T, Lippert U, Henz BM, Luger TA, Metze D, Steinhoff M (2004) Expression of vanilloid receptor subtype 1 in cutaneous sensory nerve fibers, mast cells, and epithelial cells of appendage structures. Exp Dermatol 13:129–139
Staruschenko A, Jeske NA, Akopian AN (2010) Contribution of TRPV1-TRPA1 interaction to the single channel properties of the TRPA1 channel. J Biol Chem 285:15167–15177
Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–829
Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD (2000) OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2:695–702
Sugiura T, Tominaga M, Katsuya H, Mizumura K (2002) Bradykinin lowers the threshold temperature for heat activation of vanilloid receptor 1. J Neurophysiol 88:544–548
Suzuki M, Watanabe Y, Oyama Y, Mizuno A, Kusano E, Hirao A, Ookawara S (2003) Localization of mechanosensitive channel TRPV4 in mouse skin. Neurosci Lett 353:189–192
Symanowicz PT, Gianutsos G, Morris JB (2004) Lack of role for the vanilloid receptor in response to several inspired irritant air pollutants in the C57Bl/6J mouse. Neurosci Lett 362:150–153
Szolcsanyi J (1977) A pharmacological approach to elucidation of the role of different nerve fibres and receptor endings in mediation of pain. J Physiol (Paris) 73:251–259
Ta LE, Bieber AJ, Carlton SM, Loprinzi CL, Low PA, Windebank AJ (2010) Transient Receptor Potential Vanilloid 1 is essential for cisplatin-induced heat hyperalgesia in mice. Mol Pain 6:15
Takashima Y, Daniels RL, Knowlton W, Teng J, Liman ER, McKemy DD (2007) Diversity in the neural circuitry of cold sensing revealed by genetic axonal labeling of transient receptor potential melastatin 8 neurons. J Neurosci 27:14147–14157
Talavera K, Alpizar YA, Startek J (2013) Interaction of lipopolysaccharides with plasma membranes as possible trigger of TRP channel activation. In: Paper presented at ECRO 2013, Leuven, Belgium, 26–29 Aug 2013
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
Talavera K, Yasumatsu K, Yoshida R, Margolskee RF, Voets T, Ninomiya Y, Nilius B (2008) The taste transduction channel TRPM5 is a locus for bitter-sweet taste interactions. FASEB J 22:1343–1355
Taniguchi K (2004) Expression of the sweet receptor protein, T1R3, in the human liver and pancreas. J Vet Med Sci 66:1311–1314
Tanimoto T, Takeda M, Nasu M, Kadoi J, Matsumoto S (2005) Immunohistochemical co-expression of carbonic anhydrase II with Kv1.4 and TRPV1 in rat small-diameter trigeminal ganglion neurons. Brain Res 1044:262–265
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 (2013) CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes. Nature 495:223–226
Taylor-Clark TE, Undem BJ (2010) Ozone activates airway nerves via the selective stimulation of TRPA1 ion channels. J Physiol 588:423–433
Tizzano M, Gulbransen BD, Vandenbeuch A, Clapp TR, Herman JP, Sibhatu HM, Churchill ME, Silver WL, Kinnamon SC, Finger TE (2010) Nasal chemosensory cells use bitter taste signaling to detect irritants and bacterial signals. Proc Natl Acad Sci USA 107:3210–3215
Tohda C, Sasaki M, Konemura T, Sasamura T, Itoh M, Kuraishi Y (2001) Axonal transport of VR1 capsaicin receptor mRNA in primary afferents and its participation in inflammation-induced increase in capsaicin sensitivity. J Neurochem 76:1628–1635
Tokita K, Boughter JD Jr (2012) Sweet-bitter and umami-bitter taste interactions in single parabrachial neurons in C57BL/6J mice. J Neurophysiol 108:2179–2190
Tomchik SM, Berg S, Kim JW, Chaudhari N, Roper SD (2007) Breadth of tuning and taste coding in mammalian taste buds. J Neurosci 27:10840–10848
Tominaga M, Tominaga T (2005) Structure and function of TRPV1. Pflugers Arch 451:143–150
Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21:531–543
Toyoshima K (1989) Chemoreceptive and mechanoreceptive paraneurons in the tongue. Arch Histol Cytol 52(Suppl):383–388
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:R1799–1809
Trevisani M, Milan A, Gatti R, Zanasi A, Harrison S, Fontana G, Morice AH, Geppetti P (2004) Antitussive activity of iodo-resiniferatoxin in guinea pigs. Thorax 59:769–772
Trevisani M, Siemens J, Materazzi S, Bautista DM, Nassini R, Campi B, Imamachi N, Andre E, Patacchini R, Cottrell GS, Gatti R, Basbaum AI, Bunnett NW, Julius D, Geppetti P (2007) 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc Natl Acad Sci USA 104:13519–13524
Tsavaler L, Shapero MH, Morkowski S, Laus R (2001) Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res 61:3760–3769
Tucker RM, Mattes RD (2012) Are free fatty acids effective taste stimuli in humans? J Food Sci 77:S148–151
Uchida K, Tominaga M (2011) The role of thermosensitive TRP (transient receptor potential) channels in insulin secretion. Endocr J 58:1021–1028
Vandenbeuch A, Clapp TR, Kinnamon SC (2008) Amiloride-sensitive channels in type I fungiform taste cells in mouse. BMC Neurosci 9:1
Vandewauw I, Owsianik G, Voets T (2013) Systematic and quantitative mRNA expression analysis of TRP channel genes at the single trigeminal and dorsal root ganglion level in mouse. BMC Neurosci 14:21
Vay L, Gu C, McNaughton PA (2010) Current perspectives on the modulation of thermo-TRP channels: new advances and therapeutic implications. Expert Rev Clin Pharmacol 3:687–704
Veronesi B, Oortgiesen M (2006) The TRPV1 receptor: target of toxicants and therapeutics. Toxicol Sci 89:1–3
Vetter I, Lewis RJ (2011) Natural product ligands of TRP channels. Adv Exp Med Biol 704:41–85
Viana F (2011) Chemosensory properties of the trigeminal system. ACS Chem Neurosci 2:38–50
Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B (2004) Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci USA 101:396–401
Wang Y, Erickson RP, Simon SA (1995) Modulation of rat chorda tympani nerve activity by lingual nerve stimulation. J Neurophysiol 73:1468–1483
Wang YY, Chang RB, Liman ER (2010) TRPA1 is a component of the nociceptive response to CO2. J Neurosci 30:12958–12963
Wang YY, Chang RB, Allgood SD, Silver WL, Liman ER (2011) A TRPA1-dependent mechanism for the pungent sensation of weak acids. J Gen Physiol 137:493–505
Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, Nilius B (2002) Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem 277:47044–47051
Whitear M (1989) Merkel cells in lower vertebrates. Arch Histol Cytol 52(Suppl):415–422
Whitehead MC, Ganchrow JR, Ganchrow D, Yao B (1999) Organization of geniculate and trigeminal ganglion cells innervating single fungiform taste papillae: a study with tetramethylrhodamine dextran amine labeling. Neuroscience 93:931–941
Wilson DM, Lemon CH (2013) Modulation of central gustatory coding by temperature. J Neurophysiol 110:1117–1129
Wu SV, Rozengurt N, Yang M, Young SH, Sinnett-Smith J, Rozengurt E (2002) Expression of bitter taste receptors of the T2R family in the gastrointestinal tract and enteroendocrine STC-1 cells. Proc Natl Acad Sci USA 99:2392–2397
Xu H, Ramsey IS, Kotecha SA, Moran MM, Chong JA, Lawson D, Ge P, Lilly J, Silos-Santiago I, Xie Y, DiStefano PS, Curtis R, Clapham DE (2002) TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418:181–186
Xu H, Delling M, Jun JC, Clapham DE (2006) Oregano, thyme and clove-derived flavors and skin sensitizers activate specific TRP channels. Nat Neurosci 9:628–635
Yilmaz Z, Renton T, Yiangou Y, Zakrzewska J, Chessell IP, Bountra C, Anand P (2007) Burning mouth syndrome as a trigeminal small fibre neuropathy: Increased heat and capsaicin receptor TRPV1 in nerve fibres correlates with pain score. J Clin Neurosci 14:864–871
Young RL, Sutherland K, Pezos N, Brierley SM, Horowitz M, Rayner CK, Blackshaw LA (2009) Expression of taste molecules in the upper gastrointestinal tract in humans with and without type 2 diabetes. Gut 58:337–346
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
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
Acknowledgments
I would like to thank Drs. Sidney A Simon (Duke University), Thomas Finger (University of Colorado School of Medicine), and Emily R Liman (University of Southern California) for their detailed reading of and perceptive remarks on this manuscript during its writing and editing.
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Roper, S.D. (2014). TRPs in Taste and Chemesthesis. In: Nilius, B., Flockerzi, V. (eds) Mammalian Transient Receptor Potential (TRP) Cation Channels. Handbook of Experimental Pharmacology, vol 223. Springer, Cham. https://doi.org/10.1007/978-3-319-05161-1_5
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