Amino Acid-Activated Channels in the Catfish Taste System

Membrane vesicles derived from external taste epithelia of channel catfish (Ictalurus punctatus) were incorporated into lipid bilayers on the tips of patch pipettes. Consistent with previous experiments (Teeter, J. H., J. G. Brand, and T. Kumazawa. 1990. Biophys. J. 58:253–259), micromolar (0.5–200 μM) concentrations of l-arginine (l-Arg), a potent taste stimulus for catfish, activated a nonselective cation conductance in some bilayers, which was antagonized by d-Arg. Two classes of l-Arg-gated receptor/channels were observed in reconstituted taste epithelial membranes: one with a unitary conductance of 40–60 pS, and the other with a conductance of 75–100 pS. A separate class of nonselective cation channels, with a conductance of 50–65 pS, was activated by high concentrations of l-proline (l-Pro) (0.1–3 mM), which is the range necessary to elicit neural responses in catfish taste fibers. The l-Pro-activated channels were not affected by either l- or d-Arg, but were blocked by millimolar concentrations of d-Pro. Conversely, neither l- nor d-Pro altered the activity of either class of l-Arg-activated channels, which were blocked by micromolar concentrations of d-Arg. These results are consistent with biochemical, neurophysiological, and behavioral studies indicating that taste responses of channel catfish to l-Arg are mediated by high-affinity receptors that are part of or closely coupled to nonselective cation channels directly gated by low concentrations of l-Arg, while responses to l-Pro are mediated by distinct, low-affinity receptors also associated with nonselective cation channels.