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J. Biol. Chem., Vol. 276, Issue 39, 36411-36418, September 28, 2001

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Functionally Separate Intracellular Ca²⁺ Stores in Smooth Muscle^*

Elaine R. M. Flynn, Karen N. Bradley, Thomas C. Muir, and John G. McCarron^§

From Neuroscience and Biomedical Systems, Institute of Biomedical and Life Sciences, West Medical Bldg., University of Glasgow, Glasgow G12 8QQ, United Kingdom

In smooth muscle, release via the inositol 1,4,5-trisphosphate (Ins(1,4,5)P₃R) and ryanodine receptors (RyR) on the sarcoplasmic reticulum (SR) controls oscillatory and steady-state cytosolic Ca²⁺ concentrations ([Ca²⁺]_c). The interplay between the two receptors, itself determined by their organization on the SR, establishes the time course and spatial arrangement of the Ca²⁺ signal. Whether or not the receptors are co-localized or distanced from each other on the same store or whether they exist on separate stores will significantly affect the Ca²⁺ signal produced by the SR. To date these matters remain unresolved. The functional arrangement of the RyR and Ins(1,4,5)P₃R on the SR has now been examined in isolated single voltage-clamped colonic myocytes. Depletion of the ryanodine-sensitive store, by repeated application of caffeine, in the presence of ryanodine, abolished the response to Ins(1,4,5)P₃, suggesting that Ins(1,4,5)P₃R and RyR share a common Ca²⁺ store. Ca²⁺ release from the Ins(1,4,5)P₃R did not activate Ca²⁺-induced Ca²⁺ release at the RyR. Depletion of the Ins(1,4,5)P₃-sensitive store, by the removal of external Ca²⁺, on the other hand, caused only a small decrease (~26%) in caffeine-evoked Ca²⁺ transients, suggesting that not all RyR exist on the common store shared with Ins(1,4,5)P₃R. Dependence of the stores on external Ca²⁺ for replenishment also differed; removal of external Ca²⁺ depleted the Ins(1,4,5)P₃-sensitive store but caused only a slight reduction in caffeine-evoked transients mediated at RyR. Different mechanisms are presumably responsible for the refilling of each store. Refilling of both Ins(1,4,5)P₃-sensitive and caffeine-sensitive Ca²⁺ stores was inhibited by each of the SR Ca²⁺ ATPase inhibitors thapsigargin and cyclopiazonic acid. These results may be explained by the existence of two functionally distinct Ca²⁺ stores; the first expressing only RyR and refilled from [Ca²⁺]_c, the second expressing both Ins(1,4,5)P₃R and RyR and dependent upon external Ca²⁺ for refilling.

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