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J Physiol Volume 524, Number 3, 737-755, May 1, 2000
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The Journal of Physiology (2000), 524.3, pp. 737-755
© Copyright 2000 The Physiological Society

Slow modal gating of single G protein-activated K+ channels expressed in Xenopus oocytes

Daniel Yakubovich, Vassili Pastushenko *, Arkadi Bitler, Carmen W. Dessauer ¹ and Nathan Dascal

Department of Physiology and Pharmacology, Sackler School of Medicine, Tel Aviv University, Ramat Aviv 69978, Israel, * Institute of Biophysics, Johannes-Kepler University of Linz, A-4040 Linz, Austria and ¹ Department of Integrative Biology, Pharmacology and Physiology, Medical School, University of Texas, Houston, TX 77030, USA

  1. The slow kinetics of G protein-activated K+ (GIRK) channels expressed in Xenopus oocytes were studied in single-channel, inside-out membrane patches. Channels formed by GIRK1 plus GIRK4 subunits, which are known to form the cardiac acetylcholine (ACh)-activated GIRK channel (KACh), were activated by a near-saturating dose of G protein betagamma subunits (Gbetagamma; 20 nM).

  2. The kinetic parameters of the expressed GIRK1/4 channels were similar to those of cardiac KACh. GIRK1/4 channels differed significantly from channels formed by GIRK1 with the endogenous oocyte subunit GIRK5 (GIRK1/5) in some of their kinetic parameters and in a 3-fold lower open probability, Po. The unexpectedly low Po (0·025) of GIRK1/4 was due to the presence of closures of hundreds of milliseconds; the channel spent 90 % of the time in the long closed states.

  3. GIRK1/4 channels displayed a clear modal behaviour: on a time scale of tens of seconds, the Gbetagamma-activated channels cycled between a low-Po mode (Po of about 0·0034) and a bursting mode characterized by an 30-fold higher Po and a different set of kinetic constants (and, therefore, a different set of channel conformations). The available evidence indicates that the slow modal transitions are not driven by binding and unbinding of Gbetagamma.

  4. The GTPgammaS-activated Galphai1 subunit, previously shown to inhibit GIRK channels, substantially increased the time spent in closed states and apparently shifted the channel to a mode similar, but not identical, to the low-Po mode.

  5. This is the first demonstration of slow modal transitions in GIRK channels. The detailed description of the slow gating kinetics of GIRK1/4 may help in future analysis of mechanisms of GIRK gating.



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