Abstract
Taste plays an important role for organisms in determining the properties of ingested substances by conveying important information on five basic taste modalities—sweet, salty, sour, bitter, and umami. Sweet, salty, and umami taste modalities convey the carbohydrate, electrolyte, and glutamate content of food, indicating its desirability and stimulating appetitive responses. Sour and bitter modalities, on the other hand, convey the presence of acidity and potential toxins, respectively, stimulating aversive responses to such tastes. In recent years, the receptors mediating sweet, bitter, and umami tastes have been identified as members of the T1R and T2R G-protein-coupled receptor (GPCR) families, while the molecular mechanisms underlying sour taste have yet to be clearly elucidated. We review aspects of perception and anatomy of acid taste, and explore the various molecules and mechanisms proposed to mediate the detection of sour stimuli.
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Abbreviations
- ASIC:
-
Acid-sensing ion channel
- Car4:
-
Carbonic anhydrase 4
- CN:
-
Cranial nerve
- CT:
-
Chorda tympani
- CvP:
-
Circumvallate papillae
- DEG/ENaC:
-
Caenorhabditis elegans degenerin/human epithelium amiloride-sensitive Na+ channel
- DTA:
-
Diphtheria toxin A fragment
- FoP:
-
Foliate papillae
- FuP:
-
Fungiform papillae
- GAD:
-
Glutamate decarboxylase
- GG:
-
Geniculate ganglion
- GN:
-
Glossopharyngeal
- GPCR:
-
G protein-coupled receptors
- GSP:
-
Greater superficial petrosal
- HCN:
-
Hyperpolarization-activated cyclic nucleotide-gated channel
- K2P:
-
Two-pore domain K + channels
- NPG:
-
Nodose/petrosal ganglion
- NST:
-
Nucleus of the solitary tract
- PbN:
-
Parabrachial nucleus
- Pkd1l3:
-
Polycystic kidney disease 1-like 3
- Pkd2l1:
-
Polycystic kidney disease 2-like 1
- SP:
-
Substance P
- TRC:
-
Taste receptor cell
- TRPV1:
-
Transient receptor potential, vanilloid receptor subtype-1
- WGA:
-
Wheat germ agglutinin
References
Baeyens F, Vansteenwegen D, De Houwer J, Crombez G (1996) Observational conditioning of food valence in humans. Appetite 27(3):235–250. doi:10.1006/appe.1996.0049
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 Â497(1):1–12. doi:10.1002/cne.20954
Ben-Shahar Y (2011) Sensory functions for degenerin/epithelial sodium channels (DEG/ENaC). Adv Genet 76:1–26. doi:10.1016/B978–0-12–386481-9.00001–8
Bianchi L, Driscoll M (2002) Protons at the gate: DEG/ENaC ion channels help us feel and remember. Neuron 34(3):337–340
Biel M, Wahl-Schott C, Michalakis S, Zong X (2009) Hyperpolarization-activated Âcation channels: from genes to function. Physiol Rev 89(3):847–885. doi:10.1152/physrev.00029.2008
Chandrashekar J, Yarmolinsky D, von Buchholtz L, Oka Y, Sly W, Ryba NJ, Zuker CS (2009) The taste of carbonation. Science 326(5951):443–445. doi:10.1126/science.1174601
Chang RB, Waters H, Liman ER (2010) A proton current drives action potentials in genetically identified sour taste cells. Proc Natl Acad Sci U S A 107(51):22320–22325. doi:10.1073/pnas.1013664107
Chaudhari N, Roper SD (2010) The cell biology of taste. J Cell Biol 190(3):285–296. doi:10.1083/jcb.201003144
Chavez RA, Gray AT, Zhao BB, Kindler CH, Mazurek MJ, Mehta Y, Forsayeth JR, Yost CS (1999) TWIK-2, a new weak inward rectifying member of the tandem pore domain Âpotassium channel family. J Biol Chem 274(12):7887–7892
Clapp TR, Yang R, Stoick CL, Kinnamon SC, Kinnamon JC (2004) Morphologic Âcharacterization of rat taste receptor cells that express components of the phospholipase C signaling pathway. J Comp Neurol 468(3):311–321. doi:10.1002/cne.10963
Damak S, Mosinger B, Margolskee RF (2008) Transsynaptic transport of wheat germ Âagglutinin expressed in a subset of type II taste cells of transgenic mice. BMC Neurosci 9:96. doi:10.1186/1471–2202-9–96
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(15):3971–3980. doi:10.1523/JNEUROSCI.0515–06.2006
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(5753):1495–1499. doi:10.1126/science.1118435
Ganzevles PG, Kroeze JH (1987a) Effects of adaptation and cross-adaptation to common ions on sourness intensity. Physiol Behav 40(5):641–646
Ganzevles PGJ, Kroeze JHA (1987b) The sour taste of acids. The hydrogen ion and the undissociated acid as sour agents. Chem Senses 12(4):563–576. doi:10.1093/chemse/12.4.563
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(4):712–714. doi:10.1021/ja01449a005
Hayato R, Ohtubo Y, Yoshii K (2007) Functional expression of ionotropic purinergic receptors on mouse taste bud cells. J Physiol 584(Pt 2):473–488. doi:10.1113/jphysiol.2007.138370
Hirata K, Miyahara H, Kanaseki T (1988) Substance-P-containing fibers in the incisive papillae of the rat hard palate. Light- and electron-microscopic immunohistochemical study. Acta Anat (Basel) 132(3):197–204
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(5):e20007. doi:10.1371/journal.pone.0020007
Hu J, Zhong C, Ding C, Chi Q, Walz A, Mombaerts P, Matsunami H, Luo M (2007) Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science 317(5840):953–957. doi:10.1126/science.1144233
Huang YJ, Maruyama Y, Lu KS, Pereira E, Plonsky I, Baur JE, Wu D, Roper SD (2005) Mouse taste buds use serotonin as a neurotransmitter. J Neurosci 25(4):843–847. doi:10.1523/JNEUROSCI.4446–04.2005
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(7105):934–938. doi:10.1038/nature05084
Huang YA, Maruyama Y, Stimac R, Roper SD (2008) Presynaptic (Type III) cells in mouse taste buds sense sour (acid) taste. J Physiol 586(Pt 12):2903–2912. doi:10.1113/jphysiol.2008.151233
Huang YA, Dando R, Roper SD (2009) Autocrine and paracrine roles for ATP and serotonin in mouse taste buds. J Neurosci 29(44):13909–13918. doi:10.1523/JNEUROSCI.2351–09.2009
Huque T, Cowart BJ, Dankulich-Nagrudny L, Pribitkin EA, Bayley DL, Spielman AI, ÂFeldman 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(10):e7347. doi:10.1371/journal.pone.0007347
Inada H, Kawabata F, Ishimaru Y, Fushiki T, Matsunami H, Tominaga M (2008) ÂOff-response property of an acid-activated cation channel complex PKD1L3-PKD2L1. EMBO Rep 9(7):690–697. doi:10.1038/embor.2008.89
Ishimaru Y (2009) Molecular mechanisms of taste transduction in vertebrates. Odontology 97(1):1–7. doi:10.1007/s10266–008-0095-y
Ishimaru Y, Matsunami H (2009) Transient receptor potential (TRP) channels and taste Âsensation. J Dent Res 88(3):212–218. doi:10.1177/0022034508330212
Ishimaru Y, Inada H, Kubota M, Zhuang H, Tominaga M, Matsunami H (2006) Transient Âreceptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste Âreceptor. Proc Natl Acad Sci U S A 103(33):12569–12574. doi:10.1073/pnas.0602702103
Ishimaru Y, Katano Y, Yamamoto K, Akiba M, Misaka T, Roberts RW, Asakura T, Matsunami H, Abe K (2010) Interaction between PKD1L3 and PKD2L1 through their transmembrane domains is required for localization of PKD2L1 at taste pores in taste cells of circumvallate and foliate papillae. FASEB J 24(10):4058–4067. doi:10.1096/fj.10–162925
Johanningsmeiner SD, McFeeters RF, Drake M (2005) A hypothesis for the chemical Âbasis for perception of sour taste. J Food Sci 70(2):R44–R48. doi:10.1111/j.1365–2621.2005.tb07111.x
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(23):17277–17281. doi:10.1074/jbc.C110.132944
Kinnamon SC (2012) Taste receptor signalling—from tongues to lungs. Acta Physiol (Oxf) 204(2):158–168. doi:10.1111/j.1748–1716.2011.02308.x
Lesage F, Guillemare E, Fink M, Duprat F, Lazdunski M, Romey G, Barhanin J (1996) TWIK-1, a ubiquitous human weakly inward rectifying K+ channel with a novel structure. EMBO J 15(5):1004–1011
Lesage F, Lazdunski M (2000) Molecular and functional properties of two-pore-domain Âpotassium channels. Am J Physiol Renal Physiol 279(5):F793–F801
Lin W, Burks CA, Hansen DR, Kinnamon SC, Gilbertson TA (2004) Taste receptor cells express pH-sensitive leak K+ channels. J Neurophysiol 92(5):2909–2919. doi:10.1152/jn.01198.2003
Lingueglia E (2007) Acid-sensing ion channels in sensory perception. J Biol Chem 282(24):17325–17329. doi:10.1074/jbc.R700011200
Lu Y, Ma X, Sabharwal R, Snitsarev V, Morgan D, Rahmouni K, Drummond HA, Whiteis CA, Costa V, Price M, Benson C, Welsh MJ, Chapleau MW, Abboud FM (2009) The ion channel ASIC2 is required for baroreceptor and autonomic control of the circulation. Neuron 64(6):885–897. doi:10.1016/j.neuron.2009.11.007
Ludwig MG, Vanek M, Guerini D, Gasser JA, Jones CE, Junker U, Hofstetter H, Wolf RM, Seuwen K (2003) Proton-sensing G-protein-coupled receptors. Nature 425(6953):93–98. doi:10.1038/nature01905
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 Âintracellular pH is the proximate stimulus in sour taste transduction. Am J Physiol Cell Physiol 281(3):C1005–C1013
Maingret F, Patel AJ, Lesage F, Lazdunski M, Honore E (1999) Mechano- or acid stimulation, two interactive modes of activation of the TREK-1 potassium channel. J Biol Chem 274(38):26691–26696
Makhlouf GBA (1972) Kinetics of the taste response to chemical stimulation: a theory of acid taste in man. Gastroenterology 63(1):67–75
Mantyh PW, Rogers SD, Honore P, Allen BJ, Ghilardi JR, Li J, Daughters RS, Lappi DA, ÂWiley RG, Simone DA (1997) Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science 278(5336):275–279
Medler KF, Margolskee RF, Kinnamon SC (2003) Electrophysiological characterization of voltage-gated currents in defined taste cell types of mice. J Neurosci 23(7):2608–2617
Munsch T, Pape HC (1999) Modulation of the hyperpolarization-activated cation current of rat thalamic relay neurones by intracellular pH. J Physiol 519(Pt 2):493–504
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(12):3137–3151
Nakamura K, Norgren R (1995) Sodium-deficient diet reduces gustatory activity in the Ânucleus of the solitary tract of behaving rats. Am J Physiol 269(3 Pt 2):R647–R661
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(7):565–577. doi:10.1093/chemse/bjq070
Ninomiya Y, Funakoshi M (1988) Amiloride inhibition of responses of rat single chorda tympani fibers to chemical and electrical tongue stimulations. Brain Res 451(1–2):319–325
Ohmoto M, Matsumoto I, Yasuoka A, Yoshihara Y, Abe K (2008) Genetic tracing of the gustatory and trigeminal neural pathways originating from T1R3-expressing taste receptor cells and solitary chemoreceptor cells. Mol Cell Neurosci 38(4):505–517. doi:10.1016/j.mcn.2008.04.011
Ohmoto M, Maeda N, Abe K, Yoshihara Y, Matsumoto I (2010) Genetic tracing of the Âneural pathway for bitter taste in t2r5-WGA transgenic mice. Biochem Biophys Res Commun 400(4):734–738. doi:10.1016/j.bbrc.2010.08.139
Oka Y, Butnaru M, von Buchholtz L, Ryba NJ, Zuker CS (2013) High salt recruits aversive taste pathways. Nature 494(7438):472–475. doi:10.1038/nature11905
Pan Z, Yang H, Reinach PS (2011) Transient receptor potential (TRP) gene superfamily encoding cation channels. Hum Genom 5(2):108–116
Price MP, McIlwrath SL, Xie J, Cheng C, Qiao J, Tarr DE, Sluka KA, Brennan TJ, Lewin GR, Welsh MJ (2001) The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 32(6):1071–1083
Richter TA, Caicedo A, Roper SD (2003) Sour taste stimuli evoke Ca2+ and pH responses in mouse taste cells. J Physiol 547(Pt 2):475–483. doi:10.1113/jphysiol.2002.033811
Richter TA, Dvoryanchikov GA, Chaudhari N, Roper SD (2004a) Acid-sensitive two-pore domain potassium (K2P) channels in mouse taste buds. J Neurophysiol 92(3):1928–1936. doi:10.1152/jn.00273.2004
Richter TA, Dvoryanchikov GA, Roper SD, Chaudhari N (2004b) Acid-sensing ion channel-2 is not necessary for sour taste in mice. J Neurosci 24(16):4088–4091. doi:10.1523/JNEUROSCI.0653–04.2004
Roper SD (2007) Signal transduction and information processing in mammalian taste buds. Pflugers Arch 454(5):759–776. doi:10.1007/s00424–007-0247-x
Saper CB (2000) Hypothalamic connections with the cerebral cortex. Prog Brain Res 126:39–48. doi:10.1016/S0079–6123(00)26005–6
Scalera G, Spector AC, Norgren R (1995) Excitotoxic lesions of the parabrachial Ânuclei Âprevent conditioned taste aversions and sodium appetite in rats. Behav Neurosci 109(5):997–1008
Sowalsky RA, Noble AC (1998) Comparison of the effects of concentration, pH and anion species on astringency and sourness of organic acids. Chem Senses 23(3):343–349
Spector AC, Scalera G, Grill HJ, Norgren R (1995) Gustatory detection thresholds after Âparabrachial nuclei lesions in rats. Behav Neurosci 109(5):939–954
Stevens DR, Seifert R, Bufe B, Muller F, Kremmer E, Gauss R, Meyerhof W, Kaupp UB, Lindemann B (2001) Hyperpolarization-activated channels HCN1 and HCN4 mediate Âresponses to sour stimuli. Nature 413(6856):631–635. doi:10.1038/35098087
Sun X, Yang LV, Tiegs BC, Arend LJ, McGraw DW, Penn RB, Petrovic S (2010) Deletion of the pH sensor GPR4 decreases renal acid excretion. J Am Soc Nephrol 21(10):1745–1755. doi:10.1681/ASN.2009050477
Sutherland SP, Benson CJ, Adelman JP, McCleskey EW (2001) Acid-sensing ion channel 3 matches the acid-gated current in cardiac ischemia-sensing neurons. Proc Natl Acad Sci U S A 98(2):711–716. doi:10.1073/pnas.011404498
Talley EM, Sirois JE, Lei Q, Bayliss DA (2003) Two-pore-Domain (KCNK) potassium Âchannels: dynamic roles in neuronal function. Neuroscientist 9(1):46–56
Travers SP, Norgren R (1995) Organization of orosensory responses in the nucleus of the solitary tract of rat. J Neurophysiol 73(6):2144–2162
Ugawa S (2003) Identification of sour-taste receptor genes. Anat Sci Int 78(4):205–210. doi:10.1046/j.0022–7722.2003.00062.x
Ugawa S, Ueda T, Ishida Y, Nishigaki M, Shibata Y, Shimada S (2002) Amiloride-blockable acid-sensing ion channels are leading acid sensors expressed in human nociceptors. J Clin Invest 110(8):1185–1190. doi:10.1172/JCI15709
Ugawa S, Ueda T, Yamamura H, Nagao M, Shimada S (2005) Coexpression of vanilloid receptor subtype-1 and acid-sensing ion channel genes in the human trigeminal ganglion neurons. Chem Senses 30(Suppl 1):i195. doi:10.1093/chemse/bjh181
Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M (1997) A proton-gated cation channel involved in acid-sensing. Nature 386(6621):173–177. doi:10.1038/386173a0
Xie J, Price MP, Berger AL, Welsh MJ (2002) DRASIC contributes to pH-gated currents in large dorsal root ganglion sensory neurons by forming heteromultimeric channels. J Neurophysiol 87(6):2835–2843
Yamamoto K, Ishimaru Y, Ohmoto M, Matsumoto I, Asakura T, Abe K (2011) Genetic tracing of the gustatory neural pathway originating from Pkd1l3-expressing type III taste cells in circumvallate and foliate papillae. J Neurochem 119(3):497–506. doi:10.1111/j.1471–4159.2011.07443.x
Yamamoto T, Kawamura Y (1975) Dual innervation of the foliate papillae of the rat: an Âelectrophysiological study. Chem Senses 1(3):241–244. doi:10.1093/chemse/1.3.241
Yang LV, Radu CG, Roy M, Lee S, McLaughlin J, Teitell MA, Iruela-Arispe ML, Witte ON (2007) Vascular abnormalities in mice deficient for the G protein-coupled receptor GPR4 that functions as a pH sensor. Mol Cell Biol 27(4):1334–1347. doi:10.1128/MCB.01909–06
Yang R, Montoya A, Bond A, Walton J, Kinnamon JC (2012) Immunocytochemical analysis of P2X2 in rat circumvallate taste buds. BMC Neurosci 13:51. doi:10.1186/1471–2202-13–51
Yarmolinsky DA, Zuker CS, Ryba NJ (2009) Common sense about taste: from mammals to insects. Cell 139(2):234–244. doi:10.1016/j.cell.2009.10.001
Yoshihara Y (2002) Visualizing selective neural pathways with WGA transgene: combination of neuroanatomy with gene technology. Neurosci Res 44(2):133–140
Yoshihara Y, Mizuno T, Nakahira M, Kawasaki M, Watanabe Y, Kagamiyama H, Jishage K, Ueda O, Suzuki H, Tabuchi K, Sawamoto K, Okano H, Noda T, Mori K (1999) A genetic approach to visualization of multisynaptic neural pathways using plant lectin transgene. Neuron 22(1):33–41
Yu FH, Yarov-Yarovoy V, Gutman GA, Catterall WA (2005) Overview of molecular relationships in the voltage-gated ion channel superfamily. Pharmacol Rev 57(4):387–395. doi:10.1124/pr.57.4.13
Zong X, Stieber J, Ludwig A, Hofmann F, Biel M (2001) A single histidine residue determines the pH sensitivity of the pacemaker channel HCN2. J Biol Chem 276(9):6313–6319. doi:10.1074/jbc.M010326200
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Ho, J., Matsunami, H., Ishimaru, Y. (2014). The Molecular Basis of Sour Sensing in Mammals. In: Chi, JT. (eds) Molecular Genetics of Dysregulated pH Homeostasis. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1683-2_3
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