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Rapidly inactivating and non-inactivating calcium-activated potassium currents in frog saccular hair cells

Cecilia E. Armstrong and William M. Roberts

1. Using a semi-intact epithelial preparation we examined the Ca²⁺-activated K⁺ (K_Ca) currents of frog (Rana pipiens) saccular hair cells. After blocking voltage-dependent K⁺ (K_V) currents with 4-aminopyridine (4-AP) an outward current containing inactivating (I_transient) and non-inactivating (I_steady) components remained.
2. The contribution of each varied greatly from cell to cell, with I_transient contributing from 14 to 90 % of the total outward current. Inactivation of I_transient was rapid ( 2-3 ms) and occurred within the physiological range of membrane potentials (V_1/2 = -63 mV). Recovery from inactivation was also rapid ( 10 ms).
3. Suppression of both I_transient and I_steady by depolarizations that approached the Ca²⁺ equilibrium potential and by treatments that blocked Ca²⁺ influx (application Ca²⁺-free saline or Cd²⁺), suggest both are Ca²⁺ dependent. Both were blocked by iberiotoxin, a specific blocker of large-conductance K_Ca channels (BK), but not by apamin, a specific blocker of small-conductance K_Ca channels.
4. Ensemble-variance analysis showed that I_transient and I_steady flow through two distinct populations of channels, both of which have a large single-channel conductance (~100 pS in non-symmetrical conditions). Together, these data indicate that both I_transient and I_steady are carried through BK channels, one of which undergoes rapid inactivation while the other does not.
5. Inactivation of I_transient could be removed by extracellular papain and could later be restored by intracellular application of the 'ball' domain of the auxiliary subunit (2) thought to mediate BK channel inactivation in rat chromaffin cells. We hypothesize that I_transient results from the association of a similar subunit with some of the BK channels and that papain removes inactivation by cleaving extracellular sites required for this association.

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