The Journal of General Physiology
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Published online November 24, 2008
doi:10.1085/jgp.200810108
The Journal of General Physiology, Vol. 132, No. 6, 731-744
The Rockefeller University Press, 0022-1295 $30.00
© 2008 Romanov et al.
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ARTICLE

Voltage Dependence of ATP Secretion in Mammalian Taste Cells



Roman A. Romanov, Olga A. Rogachevskaja, Alexander A. Khokhlov, and Stanislav S. Kolesnikov

Institute of Cell Biophysics, Russian Academy of Sciences, Moscow 142290, Russia

Correspondence to Stanislav S. Kolesnikov: staskolesnikov{at}yahoo.com

Mammalian type II taste cells release the afferent neurotransmitter adenosine triphosphate (ATP) through ATP-permeable ion channels, most likely to be connexin (Cx) and/or pannexin hemichannels. Here, we show that ion channels responsible for voltage-gated (VG) outward currents in type II cells are ATP permeable and demonstrate a strong correlation between the magnitude of the VG current and the intensity of ATP release. These findings suggest that slowly deactivating ion channels transporting the VG outward currents can also mediate ATP secretion in type II cells. In line with this inference, we studied a dependence of ATP secretion on membrane voltage with a cellular ATP sensor using different pulse protocols. These were designed on the basis of predictions of a model of voltage-dependent transient ATP efflux. Consistently with curves that were simulated for ATP release mediated by ATP-permeable channels deactivating slowly, the bell-like and Langmuir isotherm–like potential dependencies were characteristic of ATP secretion obtained for prolonged and short electrical stimulations of taste cells, respectively. These observations strongly support the idea that ATP is primarily released via slowly deactivating channels. Depolarizing voltage pulses produced negligible Ca2+ transients in the cytoplasm of cells releasing ATP, suggesting that ATP secretion is mainly governed by membrane voltage under our recording conditions. With the proviso that natural connexons and pannexons are kinetically similar to exogenously expressed hemichannels, our findings suggest that VG ATP release in type II cells is primarily mediated by Cx hemichannels.


Abbreviations used in this paper: Cx, connexin; Px, pannexin; VG, voltage-gated; WC, whole cell.

© 2008 Romanov et al. This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.jgp.org/misc/terms.shtml). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).


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Am. J. Physiol. Cell Physiol.Home page
G. R. Dubyak
Both sides now: multiple interactions of ATP with pannexin-1 hemichannels. Focus on "A permeant regulating its permeation pore: inhibition of pannexin 1 channels by ATP"
Am J Physiol Cell Physiol, February 1, 2009; 296(2): C235 - C241.
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