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.
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Notes
- 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).
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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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