Afferent neurotransmission mediated by hemichannels in mammalian taste cells

Abstract

In mammalian taste buds, ionotropic P2X receptors operate in gustatory nerve endings to mediate afferent inputs. Thus, ATP secretion represents a key aspect of taste transduction. Here, we characterized individual vallate taste cells electrophysiologically and assayed their secretion of ATP with a biosensor. Among electrophysiologically distinguishable taste cells, a population was found that released ATP in a manner that was Ca²⁺ independent but voltage‐dependent. Data from physiological and pharmacological experiments suggested that ATP was released from taste cells via specific channels, likely to be connexin or pannexin hemichannels. A small fraction of ATP‐secreting taste cells responded to bitter compounds, indicating that they express taste receptors, their G‐protein‐coupled and downstream transduction elements. Single cell RT–PCR revealed that ATP‐secreting taste cells expressed gustducin, TRPM5, PLCβ2, multiple connexins and pannexin 1. Altogether, our data indicate that tastant‐responsive taste cells release the neurotransmitter ATP via a non‐exocytotic mechanism dependent upon the generation of an action potential.