J. Gen. Physiol., Volume 111, Number 4, April 1, 1998 565-581

Gating of Recombinant Small-Conductance Ca-activated K⁺ Channels by Calcium

Birgit Hirschberg,^* James Maylie, John P. Adelman,^* and Neil V. Marrion^*

From the ^* Vollum Institute, and   Department of Obstetrics and Gynecology, Oregon Health Sciences University, Portland, Oregon 97201

Small-conductance Ca-activated K⁺ channels play an important role in modulating excitability in many cell types. These channels are activated by submicromolar concentrations of intracellular Ca²⁺, but little is known about the gating kinetics upon activation by Ca²⁺. In this study, single channel currents were recorded from Xenopus oocytes expressing the apamin-sensitive clone rSK2. Channel activity was detectable in 0.2 µM Ca²⁺ and was maximal above 2 µM Ca²⁺. Analysis of stationary currents revealed two open times and three closed times, with only the longest closed time being Ca dependent, decreasing with increasing Ca²⁺ concentrations. In addition, elevated Ca²⁺ concentrations resulted in a larger percentage of long openings and short closures. Membrane voltage did not have significant effects on either open or closed times. The open probability was ~0.6 in 1 µM free Ca²⁺. A lower open probability of ~0.05 in 1 µM Ca²⁺ was also observed, and channels switched spontaneously between behaviors. The occurrence of these switches and the amount of time channels spent displaying high open probability behavior was Ca²⁺ dependent. The two behaviors shared many features including the open times and the short and intermediate closed times, but the low open probability behavior was characterized by a different, long Ca²⁺-dependent closed time in the range of hundreds of milliseconds to seconds. Small-conductance Ca- activated K⁺ channel gating was modeled by a gating scheme consisting of four closed and two open states. This model yielded a close representation of the single channel data and predicted a macroscopic activation time course similar to that observed upon fast application of Ca²⁺ to excised inside-out patches.

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