Active Ion Transport in Dog Tongue: A Possible Role in Taste

Abstract

An in vitro preparation of the dorsal epithelium of the dog tongue actively transports ions, producing a transepithelial potential difference characteristic of the ions and their concentration. Hypertonic sodium chloride solutions generally cause increased potentials and short-circuit currents and reduced resistances when placed on the mucosal surface. This hypertonic flux is eliminated by ouabain and is not found in ventral lingual epithelia. When either sodium acetate or tetramethylammonium chloride is substituted for sodium chloride in the mucosal medium, the currents are diminished but their sum at a given concentration approximates that for sodium chloride at the same concentration. This result suggests a current composed of inward sodium ion movement and outward chloride ion movement. Actively regulated potentials and currents, whether generated in the taste buds or in supporting cells, may be important in both normal chemotransduction and in taste responses evoked by currents passing through the tongue.

Salt-Evoked Lingual Surface Potential in Humans

“…In contrast to affecting the lingual potential in some humans only, amiloride affects electrical activity in almost all animals (Halpern 1998;Heck et al 1984Heck et al , 1989Herness 1987;Ninomiya et al 1989;Schiffman et al 1990;Simon et al 1993). In the individuals who exhibit amiloride sensitivity, the amiloride inhibitable portion of saltevoked hyperpolarization appears to be smaller than that observed in animals (Avenet and Lindemann 1988;DeSimone et al 1981DeSimone et al , 2001Gilbertson et al 1993;Simon and Garvin 1985). However, when amiloride does block, the human IC 50 approximates the value observed in rodents, suggesting that there are quantitative, but not qualitative, differences between ENaC activity in humans and ENaC activity in animals (Avenet and Lindemann 1991;Doolin and Gilbertson 1996;Miyamoto et al 2001).…”

“…In these models, anterior lingual short circuit current and transepithelial potential or translingual potential (lingual surface potential) as well as the more proximal chorda tympani integrated response are attributed to the transepithelial movement of sodium (or other ions) through trans-and para-cellular pathways (Kloub et al 1997(Kloub et al , 1998Ye et al 1993Ye et al , 1994. The electrophysiological responses evoked by Na-salts in animals are positively correlated to the concentration of the salt and are decreased by amiloride (Avenet and Lindemann 1988;DeSimone et al 1981;Gilbertson et al 1993;Simon and Garvin 1985;Ye et al 1991). Importantly, in animal studies, the salt-evoked lingual surface potential correlates well with the chorda tympani response and taste sensory activation (DeSimone and Ferrell 1985).…”

Expression and localization of amiloride-sensitivesodium channel indicate a role for non-taste cells in tasteperception.

“…5). First, DeSimone and collaborators (8,22) have shown that transepithelial sodium currents are sensitive both to amiloride and ouabain. Since the great majority of cells in these preparations are non-taste cells, this establishes that non-taste cells in the tongue possess amiloride-sensitive sodium channels, indicating that the ASSC that we have visualized in non-taste cells are functional.…”

TRPM5-dependent amiloride- and benzamil-insensitive NaCl chorda tympani taste nerve response

“…Several studies suggest that in the anterior tongue Na ϩ from a Na ϩ salt taste stimulus enters a subset of taste bud cells by at least two types of cation channels located in taste cell apical membranes. One channel type is the Na ϩ -specific epithelial Na ϩ channel (ENaC), in which Na ϩ transport is inhibited by amiloride and benzamil (Bz) (1,3,8). The second involves Na ϩ transport through a putative transient receptor potential (TRP) vanilloid subfamily member 1 (TRPV1t)-nonspecific cation channel (26,27).…”