Afferent neurotransmission mediated by hemichannels in mammalian taste cells

• DOI: 10.1038/sj.emboj.7601526
• Publication Date: 2007-01-18T14:14:35Z
• Authors: Roman A Romanov; Olga A Rogachevskaja; Marina F Bystrova; Peihua Jiang; Robert F Margolskee; Stanislav S Koles...
• Keywords: Afferent Pathways; 0303 health sciences; Receptors, Purinergic P2; Reverse Transcriptase Polymerase Chain Reaction; Phospholipase C beta; Membrane Proteins; TRPM Cation Channels; Nerve Tissue Proteins; Taste Buds; Immunohistochemistry; Connexins; Electrophysiology; Isoenzymes; Mice; 03 medical and health sciences; Adenosine Triphosphate; Microscopy, Fluorescence; Animals; Calcium; Transducin; Cells, Cultured; Signal Transduction

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 Ca(2+) 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, PLCbeta2, 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.