The Journal of Neurophysiology Vol. 82 No. 4 October 1999, pp. 1655-1661
Copyright ©1999 by the American Physiological Society

Fast BK-Type Channel Mediates the Ca²⁺-Activated K⁺ Current in Crayfish Muscle

Instituto Cajal, Consejo Superior de Investigaciones, E-28002 Madrid, Spain

Araque, Alfonso and Washington Buño. Fast BK-Type Channel Mediates the Ca²⁺-Activated K⁺ Current in Crayfish Muscle. J. Neurophysiol. 82: 1655-1661, 1999. The role of the Ca²⁺-activated K⁺ current (I_K(Ca)) in crayfish opener muscle fibers is functionally important because it regulates the graded electrical activity that is characteristic of these fibers. Using the cell-attached and inside-out configurations of the patch-clamp technique, we found three different classes of channels with properties that matched those expected of the three different ionic channels mediating the depolarization-activated macroscopic currents previously described (Ca²⁺, K⁺, and Ca²⁺-dependent K⁺ currents). We investigated the properties of the ionic channels mediating the extremely fast activating and persistent I_K(Ca). These voltage- and Ca²⁺-activated channels had a mean single-channel conductance of ~ 70 pS and showed a very fast activation. Both the single-channel open probability and the speed of activation increased with depolarization. Both parameters also increased in inside-out patches, i.e., in high Ca²⁺ concentration. Intracellular loading with the Ca²⁺ chelator bis(2-aminophenoxy) ethane-N, N,N',N'-tetraacetic acid gradually reduced and eventually prevented channel openings. The channels opened at very brief delays after the pulse depolarization onset (<5 ms), and the time-dependent open probability was constant during sustained depolarization (560 ms), matching both the extremely fast activation kinetics and the persistent nature of the macroscopic I_K(Ca). However, the intrinsic properties of these single channels do not account for the partial apparent inactivation of the macroscopic I_K(Ca), which probably reflects temporal Ca²⁺ variations in the whole muscle fiber. We conclude that the channels mediating I_K(Ca) in crayfish muscle are voltage- and Ca²⁺-gated BK channels with relatively small conductance. The intrinsic properties of these channels allow them to act as precise Ca²⁺ sensors that supply the exact feedback current needed to control the graded electrical activity and therefore the contraction of opener muscle fibers.