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Different roles of ryanodine receptors and inositol (1,4,5)-trisphosphate receptors in adrenergically stimulated contractions of small arteries

Department of Physiology, School of Medicine, University of Maryland, Baltimore, Maryland 21201

Submitted 22 July 2003 ; accepted in final form 4 March 2004

The functions of ryanodine receptors (RyRs) and inositol (1,4,5)-trisphosphate receptors [Ins(1,4,5)P₃Rs] in adrenergically activated contractions of pressurized rat mesenteric small arteries were investigated. Caffeine (20 mM) but not phenylephrine (PE; 10 µM) facilitated the depletion of smooth muscle sarcoplasmic reticulum (SR) Ca²⁺ stores by ryanodine (40 µM). In ryanodine-treated SR-depleted arteries, 1) Ca²⁺ sparks were absent, 2) low concentrations of PE failed to elicit either vasoconstriction or normal asynchronous propagating Ca²⁺ waves, and 3) high [PE] induced abnormally slow oscillatory contractions (vasomotion) and synchronous Ca²⁺ oscillations. In ryanodine-treated SR-depleted arteries denuded of endothelium, high [PE] induced steady contraction and steady elevation of intracellular [Ca²⁺]. In contrast, 2-aminoethyl diphenylborate (2-APB), a putative blocker of Ins(1,4,5)P₃Rs, produced opposite effects to ryanodine: 1) Ca²⁺ sparks were present; 2) Ca²⁺ waves were absent; 3) caffeine-releasable Ca²⁺ stores were intact; and 4) PE, even at high concentrations on endothelial-denuded arteries, failed to elicit contraction, asynchronous Ca²⁺ waves, or synchronous Ca²⁺ oscillations or maintained elevated [Ca²⁺]. We conclude that 1) Ins(1,4,5)P₃Rs are essential for adrenergically induced asynchronous Ca²⁺ waves and the associated steady vasoconstriction, 2) RyRs are not appreciably opened during adrenergic activation (because PE did not facilitate the development of the effects of ryanodine), and 3) Ins(1,4,5)P₃Rs are not essential for Ca²⁺ sparks. This provides an explanation of the fact that adrenergic stimulation decreases the frequency of Ca²⁺ sparks (previously reported) while simultaneously increasing the frequency of asynchronous propagating Ca²⁺ waves; different SR Ca²⁺-release channels are involved.

ryanodine; 2-aminoethyl diphenylborate; vasomotion; smooth muscle; confocal microscopy

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