Afferent neurotransmission mediated by hemichannels in mammalian taste cells.
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.
Romanov
Roman A
RA
Institute of Cell Biophysics, Russian Academy of Sciences, Pushchino, Moscow Region, Russia.
Rogachevskaja
Olga A
OA
Bystrova
Marina F
MF
Jiang
Peihua
P
Margolskee
Robert F
RF
Kolesnikov
Stanislav S
SS
D000255:Adenosine Triphosphate / Q000378:metabolism; D000344:Afferent Pathways / Q000502:physiology; D000818:Animals; D002118:Calcium / Q000378:metabolism; D002478:Cells, Cultured; D017630:Connexins / Q000378:metabolism; D004594:Electrophysiology; D007150:Immunohistochemistry; D007527:Isoenzymes / Q000378:metabolism; D008565:Membrane Proteins / Q000378:metabolism*; D051379:Mice; D008856:Microscopy, Fluorescence; D009419:Nerve Tissue Proteins / Q000378:metabolism; D054799:Phospholipase C beta; D018048:Receptors, Purinergic P2 / Q000378:metabolism*; D020133:Reverse Transcriptase Polymerase Chain Reaction; D015398:Signal Transduction / Q000502:physiology*; D050053:TRPM Cation Channels / Q000378:metabolism; D013650:Taste Buds / Q000502:physiology*; D015293:Transducin / Q000378:metabolism; D010738:Type C Phospholipases / Q000378:metabolism
D017630:Connexins; D007527:Isoenzymes; D008565:Membrane Proteins; D009419:Nerve Tissue Proteins; C503631:Panx1 protein, mouse; D018048:Receptors, Purinergic P2; D050053:TRPM Cation Channels; C498617:Trpm5 protein, mouse; C075192:gustducin; D000255:Adenosine Triphosphate; D010738:Type C Phospholipases; D054799:Phospholipase C beta; D015293:Transducin; D002118:Calcium