The past decade has witnessed a consolidation and refinement of the extraordinary progress made in taste research. This Review describes recent advances in our understanding of taste receptors, taste buds, and the connections between taste buds and sensory afferent fibres. The article discusses new findings regarding the cellular mechanisms for detecting tastes, new data on the transmitters involved in taste processing and new studies that address longstanding arguments about taste coding.
At a glance
- Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112, 293–301 (2003).
This study demonstrates that sweet-taste and bitter-taste receptors signal via a common pathway that includes PLCβ2 and TRPM5. Mice lacking the genes that encode these signalling proteins are shown to lose taste sensitivity for sweet, bitter and umami.
- Morphologic characterization of rat taste receptor cells that express components of the phospholipase C signaling pathway. J. Comp. Neurol. 468, 311–321 (2004). , , , &
- Separate populations of receptor cells and presynaptic cells in mouse taste buds. J. Neurosci. 26, 3971–3980 (2006).
This study uses Ca2+ imaging and single-cell reverse transcription PCR to show that cells with taste GPCRs (T1Rs and T2Rs) and their downstream effectors are distinct from taste cells that express proteins for vesicular neurotransmitter release.
- The cells and logic for mammalian sour taste detection. Nature 442, 934–938 (2006). et al.
- Presynaptic (type III) cells in mouse taste buds sense sour (acid) taste. J. Physiol. 586, 2903–2912 (2008). , , &
- The K+ channel KIR2.1 functions in tandem with proton influx to mediate sour taste transduction. Proc. Natl Acad. Sci. USA 113, E229–E238 (2016).
This patch-clamp study shows that cytoplasmic acidification excites sour-sensing taste bud cells by blocking the inwardly rectifying K+ channel KIR2.1.
- The cells and peripheral representation of sodium taste in mice. Nature 464, 297–301 (2010). et al.
- Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell 96, 541–551 (1999). et al.
- Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat. Genet. 28, 58–63 (2001). et al.
- A candidate taste receptor gene near a sweet taste locus. Nat. Neurosci. 4, 492–498 (2001). , , &
- Identification of a novel member of the T1R family of putative taste receptors. J. Neurochem. 77, 896–903 (2001). , , &
- Mammalian sweet taste receptors. Cell 106, 381–390 (2001).
This study shows that the heterologous expression of T1R2 and T1R3 confers sensitivity to sugars and synthetic sweeteners.
- An amino-acid taste receptor. Nature 416, 199–202 (2002).
This study shows that the heterologous expression of taste GPCRs T1R1 and T1R3 confers sensitivity to many amino acids, including glutamate.
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- Distinct contributions of T1R2 and T1R3 taste receptor subunits to the detection of sweet stimuli. Curr. Biol. 15, 1948–1952 (2005). , , , &
- Different functional roles of T1R subunits in the heteromeric taste receptors. Proc. Natl Acad. Sci. USA 101, 14258–14263 (2004). et al.
- The heterodimeric sweet taste receptor has multiple potential ligand binding sites. Curr. Pharm. Des. 12, 4591–4600 (2006). et al.
- Characterization of the modes of binding between human sweet taste receptor and low-molecular-weight sweet compounds. PLoS ONE 7, e35380 (2012). et al.
- Key amino acid residues involved in multi-point binding interactions between brazzein, a sweet protein, and the T1R2–T1R3 human sweet receptor. J. Mol. Biol. 398, 584–599 (2010). et al.
- The cysteine-rich region of T1R3 determines responses to intensely sweet proteins. J. Biol. Chem. 279, 45068–45075 (2004). et al.
- The receptors for mammalian sweet and umami taste. Cell 115, 255–266 (2003).
This study involves the genetic ablation of the taste receptors T1R1, T1R2 or T1R3, and the results suggested that these receptors are necessary and sufficient for behavioural responses to sweet and umami tastes in mice (but see reference 22).
- Detection of sweet and umami taste in the absence of taste receptor T1r3. Science 301, 850–853 (2003).
This study shows that knockout of the gene that encodes T1R3 results in a selective loss of taste sensitivity to artificial sweeteners but does not abolish responses to sugars and umami (but see reference 21).
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- Glucose transporters and ATP-gated K+ (KATP) metabolic sensors are present in type 1 taste receptor 3 (T1r3)-expressing taste cells. Proc. Natl Acad. Sci. USA 108, 5431–5436 (2011). , , , &
- Taste cell-expressed α-glucosidase enzymes contribute to gustatory responses to disaccharides. Proc. Natl Acad. Sci. USA 113, 6035–6040 (2016). et al.
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- Oral glucose is the prime elicitor of preabsorptive insulin secretion. Am. J. Physiol. 246, R88–R95 (1984). , &
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- Endocrine taste cells. Br. J. Nutr. 111 (Suppl. 1), S23–S29 (2014). et al.
- Glucagon-like peptide-1 is specifically involved in sweet taste transmission. FASEB J. 29, 2268–2280 (2015). et al.
- Sugar-induced cephalic-phase insulin release is mediated by a T1r2+T1r3- independent taste transduction pathway in mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 309, R552–R560 (2015). et al.
- Glucose elicits cephalic-phase insulin release in mice by activating KATP channels in taste cells. Am. J. Physiol. Regul. Integr. Comp. Physiol. 312, R597–R610 (2017).
References 32 and 33 demonstrate the involvement of taste buds in stimulating insulin release immediately following sugar ingestion. The mechanism is independent of the sweet-taste receptors T1R2 and T1R3, and instead uses a transduction pathway similar to that used in pancreatic islet β cells.
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- T1R3 taste receptor is critical for sucrose but not Polycose taste. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R866–R876 (2009). , , &
- Orosensory detection of sucrose, maltose, and glucose is severely impaired in mice lacking T1R2 or T1R3, but Polycose sensitivity remains relatively normal. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303, R218–R235 (2012). &
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- Taste responses in mice lacking taste receptor subunit T1R1. J. Physiol. 591, 1967–1985 (2013). et al.
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- Taste receptors for umami: the case for multiple receptors. Am. J. Clin. Nutr. 90, 738S–742S (2009). , &
- Metabotropic glutamate receptor type 1 in taste tissue. Am. J. Clin. Nutr. 90, 743S–746S (2009). , , &
- Involvement of multiple taste receptors in umami taste: analysis of gustatory nerve responses in metabotropic glutamate receptor 4 knockout mice. J. Physiol. 593, 1021–1034 (2015). et al.
- Bitter taste receptor research comes of age: from characterization to modulation of TAS2Rs. Semin. Cell Dev. Biol. 24, 215–221 (2013). &
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- A family of candidate taste receptors in human and mouse. Nature 404, 601–604 (2000). , &
- Gustatory expression pattern of the human TAS2R bitter receptor gene family reveals a heterogenous population of bitter responsive taste receptor cells. J. Neurosci. 27, 12630–12640 (2007). , , , &
- A novel family of mammalian taste receptors. Cell 100, 693–702 (2000). et al.
- The molecular receptive ranges of human TAS2R bitter taste receptors. Chem. Senses 35, 157–170 (2010).
This study comprehensively expresses human bitter-taste receptors in heterologous cells to de-orphan them and catalogue the compounds that active them.
- Bitter taste receptors for saccharin and acesulfame K. J. Neurosci. 24, 10260–10265 (2004). et al.
- Functional characterization of human bitter taste receptors. Biochem. J. 403, 537–543 (2007). et al.
- Comprehensive analysis of mouse bitter taste receptors reveals different molecular receptive ranges for orthologous receptors in mice and humans. J. Biol. Chem. 291, 15358–15377 (2016). et al.
- Genetic variation in taste receptor pseudogenes provides evidence for a dynamic role in human evolution. BMC Evol. Biol. 14, 198 (2014). , , , &
- The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. Curr. Biol. 15, 322–327 (2005). et al.
- Variation in the gene TAS2R38 is associated with the eating behavior disinhibition in Old Order Amish women. Appetite 54, 93–99 (2010). , , , &
- Gγ13 colocalizes with gustducin in taste receptor cells and mediates IP3 responses to bitter denatonium. Nat. Neurosci. 2, 1055–1062 (1999). et al.
- Gustducin is a taste-cell-specific G protein closely related to the transducins. Nature 357, 563–569 (1992). , &
- Expression of Gα14 in sweet-transducing taste cells of the posterior tongue. BMC Neurosci. 9, 110 (2008). et al.
- Transduction of bitter and sweet taste by gustducin. Nature 381, 796–800 (1996). , &
- Tonic activity of Gα-gustducin regulates taste cell responsivity. FEBS Lett. 582, 3783–3787 (2008). et al.
- A transient receptor potential channel expressed in taste receptor cells. Nat. Neurosci. 5, 1169–1176 (2002). et al.
- The transduction channel TRPM5 is gated by intracellular calcium in taste cells. J. Neurosci. 27, 5777–5786 (2007). , , &
- Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc. Natl Acad. Sci. USA 100, 15160–15165 (2003). &
- Decrease in rat taste receptor cell intracellular pH is the proximate stimulus in sour taste transduction. Am. J. Physiol. Cell Physiol. 281, C1005–C1013 (2001).
This study shows that cytosolic acidification is a prerequisite for the sour taste-induced stimulation of taste bud cells.
- Sour taste stimuli evoke Ca2+ and pH responses in mouse taste cells. J. Physiol. 547, 475–483 (2003). , &
- A proton current drives action potentials in genetically identified sour taste cells. Proc. Natl Acad. Sci. USA 107, 22320–22325 (2010). , &
- Proton currents through amiloride-sensitive Na channels in hamster taste cells. Role in acid transduction. J. Gen. Physiol. 100, 803–824 (1992). , , &
- Hyperpolarization-activated channels HCN1 and HCN4 mediate responses to sour stimuli. Nature 413, 631–635 (2001). et al.
- Amiloride-insensitive currents of the acid-sensing ion channel-2a (ASIC2a)/ASIC2b heteromeric sour-taste receptor channel. J. Neurosci. 23, 3616–3622 (2003). et al.
- Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc. Natl Acad. Sci. USA 103, 12569–12574 (2006). et al.
- Acid-sensing ion channel-2 is not necessary for sour taste in mice. J. Neurosci. 24, 4088–4091 (2004). , , &
- Sour taste responses in mice lacking PKD channels. PLoS ONE 6, e20007 (2011). et al.
- Acid-sensitive two-pore domain potassium (K2P) channels in mouse taste buds. J. Neurophysiol. 92, 1928–1936 (2004). , , &
- Salt taste transduction occurs through an amiloride-sensitive sodium transport pathway. Science 223, 403–405 (1984). , &
- Amiloride and vertebrate gustatory responses to NaCl. Neurosci. Biobehav. Rev. 23, 5–47 (1998).
- Amiloride suppresses the sourness of NaCl and LiCl. Physiol. Behav. 60, 1317–1322 (1996). &
- High salt recruits aversive taste pathways. Nature 494, 472–475 (2013). , , , &
- Differential expression of RNA and protein of the three pore-forming subunits of the amiloride-sensitive epithelial sodium channel in taste buds of the rat. J. Histochem. Cytochem. 47, 51–64 (1999). , &
- Breadth of tuning in taste afferent neurons varies with stimulus strength. Nat. Commun. 6, 8171 (2015).
This study uses Ca2+ imaging in anaesthetized mice to show that gustatory afferent neurons respond to single or multiple taste quality stimuli depending on their concentration; this finding provides support for combinatorial taste coding (but see reference 141).
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- Amiloride-sensitive channels in type I fungiform taste cells in mouse. BMC Neurosci. 9, 1 (2008). , &
- Localization of amiloride-sensitive sodium current and voltage-gated calcium currents in rat fungiform taste cells. J. Neurophysiol. 98, 2483–2487 (2007). &
- Amiloride-insensitive salt taste is mediated by two populations of type III taste cells with distinct transduction mechanisms. J. Neurosci. 36, 1942–1953 (2016). , , &
- Chorda tympani nerve transection alters linoleic acid taste discrimination by male and female rats. Physiol. Behav. 89, 311–319 (2006). , &
- Importance of lipolysis in oral cavity for orosensory detection of fat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R447–R454 (2003). &
- The role of lipolysis in human orosensory fat perception. J. Lipid Res. 55, 870–882 (2014). et al.
- Lingual lipase activity in the orosensory detection of fat by humans. Am. J. Physiol. Regul. Integr. Comp. Physiol. 306, R879–R885 (2014). &
- G protein-coupled receptors in human fat taste perception. Chem. Senses 37, 123–139 (2012). et al.
- Fatty acid modulation of K+ channels in taste receptor cells: gustatory cues for dietary fat. Am. J. Physiol. 272, C1203–C1210 (1997). , , , &
- Expression of the putative membrane fatty acid transporter (FAT) in taste buds of the circumvallate papillae in rats. FEBS Lett. 414, 461–464 (1997). et al.
- CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J. Clin. Invest. 115, 3177–3184 (2005). et al.
- Colocalization of GPR120 with phospholipase-Cβ2 and α-gustducin in the taste bud cells in mice. Neurosci. Lett. 450, 186–190 (2009). et al.
- Taste preference for fatty acids is mediated by GPR40 and GPR120. J. Neurosci. 30, 8376–8382 (2010). et al.
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- The gustatory pathway is involved in CD36-mediated orosensory perception of long-chain fatty acids in the mouse. FASEB J. 22, 1458–1468 (2008). et al.
- Behavioral palatability of dietary fatty acids correlates with the intracellular calcium ion levels induced by the fatty acids in GPR120-expressing cells. Biomed. Res. 35, 357–367 (2014). et al.
- The endocrinology of taste receptors. Nat. Rev. Endocrinol. 11, 213–227 (2015). &
- Localization of ATP-gated P2X2 and P2X3 receptor immunoreactive nerves in rat taste buds. Neuroreport 10, 1107–1111 (1999). et al.
- ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 310, 1495–1499 (2005).
The authors of this study identify ATP as a taste neurotransmitter that acts on P2X2 and P2X3 receptors expressed by sensory afferent fibres that innervate taste buds.
- Knocking out P2X receptors reduces transmitter secretion in taste buds. J. Neurosci. 31, 13654–13661 (2011). et al.
- 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 (2007). et al.
- Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J. 26, 657–667 (2007). et al.
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- CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes. Nature 495, 223–226 (2013).
In this paper, patch clamp, molecular biological and genetic knockout studies demonstrate that ATP is released from taste bud cells during gustatory stimulation through CALHM1 channels.
- Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett. 580, 239–244 (2006). , &
- Calcium homeostasis modulator (CALHM) ion channels. Pflugers Arch. 468, 395–403 (2016). , , &
- Normal taste acceptance and preference of PANX1 knockout mice. Chem. Senses 40, 453–459 (2015). et al.
- Mice lacking pannexin 1 release ATP and respond normally to all taste qualities. Chem. Senses 40, 461–467 (2015). , &
- Salty taste deficits in CALHM1 knockout mice. Chem. Senses 39, 515–528 (2014). et al.
- Immunocytochemical analysis of P2X2 in rat circumvallate taste buds. BMC Neurosci. 13, 51 (2012). , , , &
- Nucleoside triphosphate diphosphohydrolase-2 is the ecto-ATPase of type I cells in taste buds. J. Comp. Neurol. 497, 1–12 (2006). , , , &
- Role of the ectonucleotidase NTPDase2 in taste bud function. Proc. Natl Acad. Sci. USA 110, 14789–14794 (2013). et al.
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- A physiologic role for serotonergic transmission in adult rat taste buds. PLoS ONE 9, e112152 (2014). , , &
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- Acetylcholine is released from taste cells, enhancing taste signalling. J. Physiol. 590, 3009–3017 (2012). &
- Norepinephrine is coreleased with serotonin in mouse taste buds. J. Neurosci. 28, 13088–13093 (2008). , &
- Breadth of tuning and taste coding in mammalian taste buds. J. Neurosci. 27, 10840–10848 (2007).
This study uses Ca2+ imaging in lingual slice preparations to show that GPCR-expressing type II taste bud cells are tuned to single taste qualities, whereas type III cells respond to and integrate signals from multiple cells in the taste bud.
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This study uses retrograde labelling to show that mouse taste buds are innervated by only three, four or five sensory afferent neurons. Conversely, the authors estimate that a sensory afferent neuron in mice innervates only a single taste bud.
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This study uses Ca2+ imaging in anaesthetized mice to show that taste-detecting afferent neurons respond predominantly to single taste quality stimuli, which supports the idea of labelled-line taste coding (but see reference 80).
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This is an early compilation of high-resolution electron micrographs that support current interpretations of the structure and function of the different types of taste cell that are described in this Review.
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- Localization of the glutamate–aspartate transporter, GLAST, in rat taste buds. Eur. J. Neurosci. 12, 3163–3171 (2000). , , &
- Inward rectifier channel, ROMK, is localized to the apical tips of glial-like cells in mouse taste buds. J. Comp. Neurol. 517, 1–14 (2009). , , , &
- Taste cells with synapses in rat circumvallate papillae display SNAP-25-like immunoreactivity. J. Comp. Neurol. 424, 205–215 (2000). , , &
- Synaptobrevin-2-like immunoreactivity is associated with vesicles at synapses in rat circumvallate taste buds. J. Comp. Neurol. 471, 59–71 (2004). , &
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- Claudin-based permeability barriers in taste buds. J. Comp. Neurol. 502, 1003–1011 (2007). , &
- A permeability barrier surrounds taste buds in lingual epithelia. Am. J. Physiol. Cell Physiol. 308, C21–C32 (2015). et al.
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- Nicotine activates TRPM5-dependent and independent taste pathways. Proc. Natl Acad. Sci. USA 106, 1596–1601 (2009). et al.
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- Positional cloning of the human quantitative trait locus underlying taste sensitivity to phenylthiocarbamide. Science 299, 1221–1225 (2003).
This genetic study identifies the human locus responsible for the inheritance of the taster and non-taster phenotypes for the bitter compound PTC.
- Natural selection and molecular evolution in PTC, a bitter-taste receptor gene. Am. J. Hum. Genet. 74, 637–646 (2004). et al.
- Positive selection on a high-sensitivity allele of the human bitter-taste receptor TAS2R16. Curr. Biol. 15, 1257–1265 (2005). et al.
- Limited evidence for adaptive evolution and functional effect of allelic variation at rs702424 in the promoter of the TAS2R16 bitter taste receptor gene in Africa. J. Hum. Genet. 59, 349–352 (2014). et al.
- A gene-wide investigation on polymorphisms in the taste receptor 2R14 (TAS2R14) and susceptibility to colorectal cancer. BMC Med. Genet. 11, 88 (2010). et al.
- Differential bitterness in capsaicin, piperine, and ethanol associates with polymorphisms in multiple bitter taste receptor genes. Physiol Behav. 156, 117–127 (2016). , &
- Variations in bitter-taste receptor genes, dietary intake, and colorectal adenoma risk. Nutr. Cancer 65, 982–990 (2013). , , , &
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- Allelic polymorphism within the TAS1R3 promoter is associated with human taste sensitivity to sucrose. Curr. Biol. 19, 1288–1293 (2009).
The human psychophysics and signal detection analyses carried out in this study indicate that a TAS1R3 allele is associated with an increased sensitivity to sucrose.
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- Genetic variation in TAS1R2 (Ile191Val) is associated with consumption of sugars in overweight and obese individuals in 2 distinct populations. Am. J. Clin. Nutr. 92, 1501–1510 (2010). , , &
- Sweet taste receptor TAS1R2 polymorphism (Val191Val) is associated with a higher carbohydrate intake and hypertriglyceridemia among the population of West Mexico. Nutrients 8, 101 (2016). , , &
- Association of sweet taste receptor gene polymorphisms with dental caries experience in school children. Caries Res. 49, 275–281 (2015). et al.
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- Mouse nasal epithelial innate immune responses to Pseudomonas aeruginosa quorum-sensing molecules require taste signaling components. Innate Immun. 20, 606–617 (2014). , , , &
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