Action potential-enhanced ATP release from taste cells through hemichannels.
Only some taste cells fire action potentials in response to sapid stimuli. Type II taste cells express many taste transduction molecules but lack well-elaborated synapses, bringing into question the functional significance of action potentials in these cells. We examined the dependence of adenosine triphosphate (ATP) transmitter release from taste cells on action potentials. To identify type II taste cells we used mice expressing a green fluorescence protein (GFP) transgene from the alpha-gustducin promoter. Action potentials were recorded by an electrode basolaterally attached to a single GFP-positive taste cell. We monitored ATP release from gustducin-expressing taste cells by collecting the electrode solution immediately after tastant-stimulated action potentials and using a luciferase assay to quantify ATP. Stimulation of gustducin-expressing taste cells with saccharin, quinine, or glutamate on the apical membrane increased ATP levels in the electrode solution; the amount of ATP depended on the firing rate. Increased spontaneous firing rates also induced ATP release from gustducin-expressing taste cells. ATP release from gustducin-expressing taste cells was depressed by tetrodotoxin and inhibited below the detection limit by carbenoxolone. Our data support the hypothesis that action potentials in taste cells responsive to sweet, bitter, or umami tastants enhance ATP release through pannexin 1, not connexin-based hemichannels.
Murata
Yoshihiro
Y
Section of Oral Neuroscience, Graduate School of Dental Science, Kyushu University, Higashi-ku, Fukuoka, Japan.
Yasuo
Toshiaki
T
Yoshida
Ryusuke
R
Obata
Kunihiko
K
Yanagawa
Yuchio
Y
Margolskee
Robert F
RF
Ninomiya
Yuzo
Y
D000200:Action Potentials / Q000187:drug effects; D000255:Adenosine Triphosphate / Q000378:metabolism*; D000818:Animals; D001550:Benzamidines / Q000494:pharmacology; D002229:Carbenoxolone / Q000494:pharmacology; D004305:Dose-Response Relationship, Drug; D005968:Glutamate Decarboxylase / Q000235:genetics; D049452:Green Fluorescent Proteins / Q000235:genetics; D051379:Mice; D008822:Mice, Transgenic; D011803:Quinine / Q000494:pharmacology; D026941:Sodium Channel Blockers / Q000494:pharmacology; D012970:Sodium Glutamate / Q000494:pharmacology; D013549:Sweetening Agents / Q000494:pharmacology; D013649:Taste / Q000187:drug effects / Q000502:physiology*; D013650:Taste Buds / Q000166:cytology* / Q000187:drug effects / Q000502:physiology*; D013779:Tetrodotoxin / Q000494:pharmacology; D015293:Transducin / Q000235:genetics / Q000502:physiology*
D001550:Benzamidines; D026941:Sodium Channel Blockers; D013549:Sweetening Agents; D049452:Green Fluorescent Proteins; C075192:gustducin; C018961:hexamidine; D013779:Tetrodotoxin; D000255:Adenosine Triphosphate; D011803:Quinine; D015293:Transducin; D005968:Glutamate Decarboxylase; C402565:glutamate decarboxylase 1; D002229:Carbenoxolone; D012970:Sodium Glutamate