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Biophysical Journal 85:2988-3006 (2003)
© 2003 The Biophysical Society

Thermodynamics of Heat Activation of Single Capsaicin Ion Channels VR1

Beiying Liu *, Kwokyin Hui {dagger} and Feng Qin *

* Department of Physiology and Biophysical Sciences, State University of New York at Buffalo, Buffalo, New York; and {dagger} Department of Physiology, University of Toronto, Toronto, Ontario, Canada

Correspondence: Address reprint requests to F. Qin, 125 Sherman Hall, Dept. of Physiology & Biophysics, SUNY at Buffalo, Buffalo, NY 14214. Tel.: 716-829-2764; Fax: 716-829-2569; E-mail: qin{at}acsu.buffalo.edu.

Temperature affects functions of all ion channels, but few of them can be gated directly. The vanilloid receptor VR1 provides one exception. As a pain receptor, it is activated by heat >42°C in addition to other noxious stimuli, e.g. acids and vanilloids. Although it is understood how ligand- and voltage-gated channels might detect their stimuli, little is known on how heat could be sensed and activate a channel. In this study, we characterized the heat-induced single-channel activity of VR1, in an attempt to localize the temperature-dependent components involved in the activation of the channel. At <42°C, openings were few and brief. Raising the ambient temperature rapidly increased the frequency of openings. Despite the large temperature coefficient of the apparent activity (Q10 {approx} 27), the unitary current, the open dwell-times, and the intraburst closures were all only weakly temperature dependent (Q10 < 2). Instead, heat had a localized effect on the reduction of long closures between bursts (Q10 {approx} 7) and the elongation of burst durations (Q10 {approx} 32). Both membrane lipids and solution ionic strength affected the temperature threshold of the activation, but neither diminished the response. The thermodynamic basis of heat activation is discussed, to elucidate what makes a thermal-sensitive channel unique.




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