Voltage sensitivity and gating charge in Shaker and Shab family potassium channels

The members of the voltage-dependent potassium channel family subserve a va riety of functions and are expected to have voltage sensors with different sensitivities. The Shaker channel of Drosophila, which underlies a transien t potassium current, has a high voltage sensitivity that is conferred by a large gating charge movement, similar to 13 elementary charges, A Shaker su bunit's primary voltage-sensing (S4) region has seven positively charged re sidues. The Shab channel and its homologue Kv2.1 both carry a delayed-recti fier current, and their subunits have only five positively charged residues in S4; they would be expected to have smaller gating-charge movements and voltage sensitivities. We have characterized the gating currents and single -channel behavior of Shab channels and have estimated the charge movement i n Shaker, Shab, and their rat homologues Kv1.1 and Kv2.1 by measuring the v oltage dependence of open probability at very negative voltages and compari ng this with the charge-voltage relationships. We find that Shab has a rela tively small grating charge, similar to 7.5 e(o). Surprisingly, the corresp onding mammalian delayed rectifier Kv2.1, which has the same complement of charged residues in the S2, S3, and S4 segments, has a gating charge of 12. 5 e(o), essentially equal to that of Shaker and Kv1.1. Evidence for very st rong coupling between charge movement and channel opening is seen in two ch annel types, with the probability of voltage-independent channel openings m easured to be below 10(-9) in Shaker and below 4 x 10(-8) in Kv2.1.