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Inward rectifying potassium channels facilitate cell-to-cell communication in hamster retractor muscle feed arteries

¹Smooth Muscle Research Group and the Department of Physiology and Biophysics, University of Calgary, Calgary, Alberta, Canada; ²Department of Pharmacology and Toxicology, Michigan State University, East Lansing, Michigan; and ³Department of Electrical and Computer Engineering, University of Calgary, Calgary, Alberta, Canada

Submitted 28 February 2006 ; accepted in final form 30 March 2006

This study examined whether inward rectifying K⁺ (K_IR) channels facilitate cell-to-cell communication along skeletal muscle resistance arteries. With the use of feed arteries from the hamster retractor muscle, experiments examined whether K_IR channels were functionally expressed and whether channel blockade attenuated the conduction of acetylcholine-induced vasodilation, an index of cell-to-cell communication. Consistent with K_IR channel expression, this study observed the following: 1) a sustained Ba²⁺-sensitive, K⁺-induced dilation in preconstricted arteries; 2) a Ba²⁺-sensitive inwardly rectifying K⁺ current in arterial smooth muscle cells; and 3) K_IR2.1 and K_IR2.2 expression in the smooth muscle layer of these arteries. It was subsequently shown that the discrete application of acetylcholine elicits a vasodilation that conducts with limited decay along the feed artery wall. In the presence of 100 µM Ba²⁺, the local and conducted response to acetylcholine was attenuated, a finding consistent with a role for K_IR in facilitating cell-to-cell communication. A computational model of vascular communication accurately predicted these observations. Control experiments revealed that in contrast to Ba²⁺, ATP-sensitive- and large-conductance Ca²⁺ activated-K⁺ channel inhibitors had no effect on the local or conducted vasodilatory response to acetylcholine. We conclude that smooth muscle K_IR channels play a key role in facilitating cell-to-cell communication along skeletal muscle resistance arteries. We attribute this facilitation to the intrinsic property of negative slope conductance, a biophysical feature common to K_IR2.1- and 2.2-containing channels, which enables them to increase their activity as a cell hyperpolarizes.

gap junctions; intercellular conduction; K⁺ channels; skeletal muscle arteries

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