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Endothelial cell signaling during conducted vasomotor responses

Department of Molecular Physiology and Biological Physics, University of Virginia Health Sciences Center, Charlottesville, Virginia 22906-0011

Submitted 24 July 2002 ; accepted in final form 12 March 2003

ACh and KCl stimulate vasomotor responses that spread rapidly and bidirectionally along arteriole walls, most likely via spread of electric current or Ca²⁺ through gap junctions. We examined these possibilities with isolated, cannulated, and perfused hamster cheek pouch arterioles (50- to 80-µm resting diameter). After intraluminal loading of 2 µM fluo 3 to measure Ca²⁺ or 1 µM di-8-ANEPPS to measure membrane potential, photometric techniques were used to selectively measure changes in intracellular Ca²⁺ concentration ([Ca²⁺]_i) or membrane potential in endothelial cells. Activation of the endothelium by micropipette application of ACh (10^-4 M, 1.0-s pulse) to a short segment of arteriole (100–200 µm) increased endothelial cell [Ca²⁺]_i and caused hyperpolarization at the site of stimulation. This response was followed rapidly by vasodilation of the entire arteriole (2-mm length). Change in membrane potential always preceded dilation, both at the site of stimulation and at distant sites along the arteriole. In contrast, an increase in endothelial cell [Ca²⁺]_i was observed only at the application site. Micropipette application of KCl, which can depolarize both smooth muscle and endothelial cells (250 mM, 2.5-s pulse), also caused a rapid, spreading response consisting of depolarization followed by vasoconstriction. With KCl stimulation, in addition to changes in membrane potential, increases in endothelial cell [Ca²⁺]_i were observed at distant sites not directly exposed to KCl. The rapid longitudinal spread of both hyperpolarizing and depolarizing responses support electrical coupling as the mode of signal transmission along the arteriolar length. In addition, the relatively short distance between heterologous cell types enables the superimposed radial Ca²⁺ signaling between smooth muscle and endothelial cells to modulate vasomotor responses.

gap junctions; acetylcholine; hyperpolarization; depolarization; intracellular calcium ion concentration

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