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Cellular Mechanisms in Taste Buds

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Cellular Mechanisms in Taste Buds Bull Tokyo Dent Coll (2007) 48(4): 151–161 151 Review Article Cellular Mechanisms in Taste Buds Takashi Suzuki Professor (retired), Department of Physiology, Tokyo Dental College, 1-2-2 Masago, Mihama-ku, Chiba 261-8502, Japan Received 23 May, 2007/Accepted for publication 10 October, 2007 Abstract In the soft palate, tongue, pharynx and larynx surrounding the oral region, taste buds are present, allowing the sensation of taste. On the tongue surface, 3 kinds of papillae are present: fungiform, foliate, and circumvallate. Approximately 5,000 taste buds cover the surface of the human tongue, with about 30% fungiform, 30% foliate and 40% circumvallate papillae. Each taste bud comprises 4 kinds of cells, namely high dark (type I), low light (type II), and intermediate (type III) cells in electron density and Merkel-like taste basal cells (type IV) located at a distance from taste pores. Type II cells sense taste stimuli and type III cells transmit taste signals to sensory afferent nerve fibers. However, type I and type IV cells are not considered to possess obvious taste functions. Synaptic interactions that mediate communication in taste cells provide signal outputs to primary afferent fibers. In the study of taste bud cells, molecular functional techniques using single cells have recently been applied. Serotonin (5-HT) plays a role in cell-to-cell transmission of taste signals. ATP fills the criterion of a neurotransmitter that activates receptors of taste nerve fibers. Findings on 5-HT and ATP suggest that various different transmitters and receptors are present in taste buds. However, no firm evidence for taste- evoked release from type III cells has been identified, except for 5-HT and ATP. These results suggest that different transmitters and receptors may not be present in taste buds. Accordingly, an understanding of how transmitters might function remains elusive. Key words: Taste bud cells—Cell communication—Second messenger— Serotonin—ATP Introduction fied into 4 types: type I, type II, type III and type IV (Merkel-like basal). Type IV cells are Taste buds are peripheral sensory organs that progenitor cells that appear during the nor- respond to various taste stimuli. Signals from mal course of cell turnover. Bigiani 4) noted taste are transmitted via synaptic pathways that these cells possess properties of glial-like between gustatory cells and afferent nerves, cells. Properties of type I and type IV cells are using these gustatory end organs. Afferent not well known, because receptive functions nerve fibers send signals to the central nervous for carrying signals are currently unknown. system (CNS) via 3 kinds of neurons. Morpho- On the other hand, type II and III cells seem logically, mammalian taste cells can be classi- to function as taste receptor cells and synaptic 151 152 Suzuki T outputs for taste signaling, respectively. Accord- hamster superior laryngeal nerve, which inner- ing to a recent classification based on cytology, vates taste buds of the epiglottis, respond well ultrastructure, and expression of certain mol- to water 53,55), but little to sweet- or bitter-tasting ecules, the functions of conventional taste bud compounds. cells have been lost 1,4,65). At present, a historical Although taste bud populations possess dif- nomenclature based on electron microgra- ferent sensitivities, the morphology of taste phy, molecular and functional features based buds is similar throughout the oral cavity. on electron micrography, molecular and func- Taste buds contain at least two morphological tional features based on immunostaining, cell types, dark (type I), and low light (type and in situ hybridization and RT-PCR in single II)17,37,38,52). Light cells are larger than dark cells, cells are suitable for these taste bud cells. have electron-lucent cytoplasm, and are circu- lar or oval in cross-section, with apical pro- cesses extending toward the taste pore. Dark General Characterization of Taste cells display electron-dense cytoplasm and an Receptive Mechanism irregular outline, with sheet-like cytoplasmic projections separating adjacent light cells50). The transduction of both sweet- and bitter- The relationship among these cell types and tasting substances is thought to involve mem- the mechanism of gustatory transduction is brane-bound receptors coupled to second- unknown. messenger systems38). Gustducin is an ␣-subunit If ␣-gustducin is present in cells that trans- of a G protein closely related to these trans- duce bitter and sweet stimuli, the number of ductions that is expressed in taste tissue42). rat taste cells expressing gustducin should be Studies with gustducin-knockout mice have greater in both palatal and posterior tongue implicated gustducin in the detection of both taste buds than in those of the anterior tongue. sweet- and bitter-tasting compounds. Taste Fungiform taste buds of hamsters should buds are specialized epithelial structures con- likewise contain more gustducin-expressing taining gustatory receptor cells. Taste buds in cells than those of rats. Boughter et al.6) used rat are grouped into several populations: immunofluorescence to quantify the distribu- fungiform papillae on the anterior portion of tion of gustducin-immunoreactive cells among the tongue, and foliate and circumvallate taste buds of various regions in both rats and papillae on the posterior tongue, in the epi- hamsters. thelia of the nasoincisor ducts and geschmacks- streifen of the palate, and on the laryngeal surface of the epiglottis19,43,56,58). These popula- Function of Type I Cell on Taste Buds tions differ in gustatory sensitivities, as shown by electrophysiological studies on peripheral Type I cells are believed to be supporting, taste fibers. In rat, chorda tympani nerve fibers glial-like cells controlling extracellular ion innervating the fungiform papillae are the concentrations. Using the patch-clamp tech- most sensitive to salts and acids20,21). The greater nique, Bigiani4) identified a new cell type in superficial petrosal nerve, which innervates the taste buds of the mouse circumvallate taste buds on the palate, is most responsive papilla. These cells represented about 30% of to sweet-tasting stimuli 48,59). Glossopharyngeal total cells and were characterized by a large nerve fibers innervating the foliate and cir- leakage current. The leakage current was car- Other .םand was blocked by Ba2 ,םcumvallate taste buds respond well to acids and ried by K bitter-tasting stimuli 22,23). In contrast, fungi- taste cells, such as those possessing voltage- -currents and thought to be chemo םform taste buds of the hamster are much gated Na more sensitive to sugars than those of the rat, sensory in function, did not express any but like the rat are relatively insensitive to sizeable leakage current. Consistent with the bitter stimuli 19,21). Single fibers in the rat and presence of a leakage conductance, leaky cells Mechanisms in Taste Buds 153 had a low input resistance (ϳ25 G⍀). Resting NaCl, 3.2 mM HCl, and 3.2 mM quinine hydro- potentials were close to the equilibrium poten- chloride (QHCl). When the cells were held at tial for potassium ions. Electrophysiological resting potentials, taste stimulation resulted analysis of membrane currents remaining in conductance changes. Sucrose and QHCl revealed produced a decrease in outward current and םafter pharmacological block by Ba2 ,conduct- membrane conductance, whereas NaCl, KCl מthat leaky cells also possessed Cl ance. In resting conditions, the membrane of NH4Cl, and HCl elicited inward currents these cells was about 60-fold more permeable accompanied by increased conductance. -Resting potassium conduc .מthan to Cl םto K tance in leaky cells could be involved in rap- 1. Serotonin receptors idly dissipating the increase in extracellular Taste receptor protein (TR) and G protein during action potential discharge in (gustducin) form a coupled unit. RT-PCR םK chemosensory cells. Leaky cells might thus was performed on RNA extracted from rat represent glial-like elements in taste buds. posterior taste buds with 14 primer sets rep- These findings support a model in which spe- resenting 5-HT1 through 5-HT7 receptor sub- cific cells control the chemical composition type families. Data suggest that 5-HT1A and of intracellular fluid in taste buds. Guanylyl 5-HT3 receptors are expressed in taste buds. cyclase activity has been associated with type I Immunocytochemistry with a 5-HT1A-specific cells2). Accordingly, the concept that type I cells antibody demonstrated that subsets of TRCs 35) represent supporting cells remains unchanged. were immunopositive for 5-HT1A. Kaya et al. Type I cells are not involved in signal process- hypothesized that 5-HT released from TRCs ing for taste sensation. activates postsynaptic 5-HT3 receptors on afferent nerve fibers and, via a paracrine route, inhibits neighboring TRCs via 5-HT1A Function of Type II and Type III Cells receptors. of Taste Buds In mammals, the transmitter of most taste cells making synapse with the gustatory nerve Synaptic interactions, both electrical and is 5-HT. These taste cells uptake 5-HT pre- chemical, are produced in taste cells. Type II cursor, and are immunopositive for 5-HT. cells seem to represent the primary sensory RT-PCR data indicate that 5-HT1A and 5-HT3 receptive cells. Type II cells are probably sen- receptors are present in the terminals of pri- sory receptive cells for taste stimuli trans- mary afferent fibers12,35). duced by G-protein coupled-receptors and Huang et al.32) used Chinese hamster ovary down-stream effectors, which are expressed cells stably expressing 5-HT2C receptors as bio- primarily in type II cells1,4,6). Although type II detectors to monitor 5-HT release from taste cells and the sensory afferent nerve are in buds. When taste buds were depolarized with closely contact with type III cells, no ultra- KCl or stimulated with bitter, sweet or sour and מstructural specializations indicate a synaptic (acid) tastants, 5-HT was released. KCl presence between type II cells and gustatory acid-induced 5-HT release, but no release afferents11).
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