The afferent and efferent arterioles regulate the inflow and outflow resistance of the glomerulus, acting in concert to control the glomerular capillary pressure and glomerular filtration rate. The myocytes of these two vessels are remarkably different, especially regarding electromechanical coupling. This study investigated the expression and function of inward rectifier K(+) channels in these two vessels using perfused hydronephrotic rat kidneys and arterioles and myocytes isolated from normal rat kidneys. In afferent arterioles pre-constricted with angiotensin II, elevating [K(+)](0) from 5 to 15 mmol/L induced hyperpolarization (-27 +/- 2 to 41 +/- 3 mV) and vasodilation (6.6 +/- 0.9 to 13.1 +/- 0.6 microm). This manipulation also attenuated angiotensin II-induced Ca(2+) signaling, an effect blocked by 100 micromol/LBa(2+). By contrast, elevating [K(+)](o) did not alter angiotensin II-induced Ca2(+) signaling or vasoconstriction in efferent arterioles, even though a significant hyperpolarization was observed (from -30 +/- 1 to 37 +/- 3 mV, P = 0.003). Both vessels expressed mRNA for Kir2.1 and exhibited anti-Kir2.1 antibody labeling.Patch-clamp measurements revealed prominent inwardly rectifying and Ba(2+)-sensitive currents in afferent and efferent arteriolar myocytes. Our findings indicate that both arterioles express an inward rectifier K(+) current, but that modulation of this current alters responsiveness of only the a different arteriole. The expression of Kir in the efferent arteriole, a resistance vessel whose tone is not affected by membrane potential, is intriguing and may suggest a novel function of this channel in the renal microcirculation.