Evidence for a novel mechanism of binding and release of stimuli in the primate taste bud

Abstract

In previous work, we showed that thaumatin, an intensely sweet protein, binds to certain formed elements in taste pores of Rhesus monkey foliate papillae, namely, microvilli and small vesicles shed from microvilli, in addition to amorphous secretions (Farbman et al., 1987). We suggested that the taste bud responds to a thaumatin stimulus by shedding the small vesicles containing fragments of microvillar membrane bearing the stimulus-binding site complex. To examine this hypothesis further, we used electron microscopy to examine taste pores of both vallate and foliate papillae from Rhesus monkeys before or after stimulation with thaumatin or sucrose. We also recorded the neural activity from the glossopharyngeal nerve during stimulation with thaumatin, sucrose, citric acid, and NaCl. The results indicate (1) with no stimulation, vesicles are found in pores of foliate papilla taste buds much more frequently than in pores of vallate papilla buds, (2) in both types of papillae, stimulation with sucrose has no apparent effect on the number of pores containing vesicles, (3) stimulation with thaumatin elicits release of vesicles into pores of both foliate and vallate buds, (4) repeated stimulation of taste buds with thaumatin results in a declining neural response, not seen after repeated stimulation with sucrose, citric acid, or NaCl, and (5) stimulation with thaumatin suppresses the neural response to sucrose, but the reverse does not occur. The combined morphological and physiological data support our original hypothesis that, in response to thaumatin stimulation, binding sites on taste microvillar membranes may be shed as a stimulus-receptor complex into the pore. Alternatively, the binding sites may in some way be altered by the shedding of part of the membrane. The data suggest further that the binding site for sucrose may be close to that for thaumatin because it too is lost or altered after thaumatin stimulation. The reduced neural response after repeated thaumatin stimulation indicates that cells may have suffered a net loss of functional receptors or at least a loss in functional capacity of the receptors. The data indicate that the cellular mechanism for handling the protein sweetener, thaumatin, is strikingly different from the adsorption-desorption response to saccharide sweeteners.