© 1995 American Heart Association, Inc.
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[Ca2+]i Inhibition of K+ Channels in Canine Renal Artery
Novel Mechanism for Agonist-Induced Membrane Depolarization
From the Department of Physiology, University of Nevada School of Medicine, Reno.
Correspondence to Dr Joseph R. Hume, Department of Physiology, University of Nevada School of Medicine, Reno, NV 89557-0004.
Abstract The patch-clamp technique was used to examine the inhibition of delayed rectifier K+ channels by agents that release intracellular Ca2+. During voltage-clamp experiments on isolated myocytes with 4-aminopyridine (4-AP, 10 mmol/L) and niflumic acid (100 µmol/L) present to inhibit delayed rectifier K+ current (IK(dr)) and Ca2+-activated Cl- current (ICl(Ca)), angiotensin II (Ang II) and caffeine increased Ca2+-activated K+ current (IK(Ca)) between -25 and 80 mV (n=5). Conversely, with charybdotoxin (ChTX, 100 nmol/L) and niflumic acid (100 µmol/L) present to inhibit IK(Ca) and ICl(Ca), Ang II and caffeine only caused inhibition of IK(dr). Block was achieved within 15 seconds of drug application and was reversible upon washout (n=5). The effects of Ang II on IK(Ca) and IK(dr) were inhibited by the specific Ang II receptor antagonist losartan (1 mmol/L, n=3). Intracellular BAPTA (10 mmol/L) also abolished the effects of Ang II and caffeine on both IK(Ca) and IK(dr). In current-clamp experiments, the application of ChTX (100 nmol/L) and niflumic acid (100 µmol/L) caused little change in resting membrane potential; however, subsequent application of caffeine (10 mmol/L) caused a 26±2.9 mV depolarization from -54±3.1 to -28±1.7 mV (n=6). 4-AP (10 mmol/L) blocked the caffeine-induced depolarization. When isolated cells were loaded with the Ca2+ indicator indo 1 (100 µmol/L), Ang II, caffeine, and 4-AP increased [Ca2+]i and depolarized the cells. Both Ang II and caffeine caused an increase in [Ca2+]i that preceded membrane depolarization, whereas 4-AP depolarized the cell first and then caused an increase in [Ca2+]i (n=4). In inside-out patches, with 200 nmol/L ChTX in the patch pipette to block large-conductance Ca2+-activated K+ channels, a 45±7-picosiemen 4-AP–sensitive K+ channel was identified that was sensitive to cytoplasmic Ca2+ (n=6). Increasing intracellular Ca2+ decreased channel opening probability [NxP(open), where N is the number of functional channels in a patch and P(open) is the opening probability] at all membrane potentials examined. At 0 mV, increasing Ca2+ from <5 to 200 and 600 nmol/L free Ca2+ decreased NxP(open) by 52±3% and 73±7%, respectively (n=6). The decrease in opening probability of the delayed rectifier K+ channel resulted from a concentration- and voltage-dependent decrease in mean open time. The decrease in mean open time reflected significant decreases and increases in open and closed time constants, respectively. These results suggest that agonist-induced changes in intracellular Ca2+ can alter vascular smooth muscle membrane potential through regulation of delayed rectifier K+ channels.
Key Words: renal artery • [Ca2+]i • K+ channels • membrane potential regulation
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