Action potential-enhanced ATP release from taste cells through hemichannels

Yoshihiro Murata, Toshiaki Yasuo, Ryusuke Yoshida, Kunihiko Obata, Yuchio Yanagawa, Robert F. Margolskee, Yuzo Ninomiya

Research output: Contribution to journalArticle

60 Citations (Scopus)

Abstract

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 α-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.

Original languageEnglish
Pages (from-to)896-901
Number of pages6
JournalJournal of Neurophysiology
Volume104
Issue number2
DOIs
Publication statusPublished - Aug 1 2010
Externally publishedYes

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Action Potentials
Adenosine Triphosphate
Electrodes
Fluorescence
Carbenoxolone
Saccharin
Connexins
Quinine
Tetrodotoxin
Luciferases
Transgenes
Synapses
Limit of Detection
Glutamic Acid
Proteins
gustducin
Membranes

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

Cite this

Murata, Y., Yasuo, T., Yoshida, R., Obata, K., Yanagawa, Y., Margolskee, R. F., & Ninomiya, Y. (2010). Action potential-enhanced ATP release from taste cells through hemichannels. Journal of Neurophysiology, 104(2), 896-901. https://doi.org/10.1152/jn.00414.2010

Action potential-enhanced ATP release from taste cells through hemichannels. / Murata, Yoshihiro; Yasuo, Toshiaki; Yoshida, Ryusuke; Obata, Kunihiko; Yanagawa, Yuchio; Margolskee, Robert F.; Ninomiya, Yuzo.

In: Journal of Neurophysiology, Vol. 104, No. 2, 01.08.2010, p. 896-901.

Research output: Contribution to journalArticle

Murata, Y, Yasuo, T, Yoshida, R, Obata, K, Yanagawa, Y, Margolskee, RF & Ninomiya, Y 2010, 'Action potential-enhanced ATP release from taste cells through hemichannels', Journal of Neurophysiology, vol. 104, no. 2, pp. 896-901. https://doi.org/10.1152/jn.00414.2010
Murata, Yoshihiro ; Yasuo, Toshiaki ; Yoshida, Ryusuke ; Obata, Kunihiko ; Yanagawa, Yuchio ; Margolskee, Robert F. ; Ninomiya, Yuzo. / Action potential-enhanced ATP release from taste cells through hemichannels. In: Journal of Neurophysiology. 2010 ; Vol. 104, No. 2. pp. 896-901.
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