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NEUROREGULATION AND MOTILITY

Characterization of intracellular Ca²⁺ stores in gallbladder smooth muscle

¹Department of Physiology, Nursing School, University of Extremadura, Cáceres, Spain; ²Department of Anatomy and Neurobiology, University of Vermont, Burlington, Vermont

Submitted 25 August 2004 ; accepted in final form 21 October 2004

The existence of functionally distinct intracellular Ca²⁺ stores has been proposed in some types of smooth muscle. In this study, we sought to examine Ca²⁺ stores in the gallbladder by measuring intracellular Ca²⁺ concentration ([Ca²⁺]_i) in fura 2-loaded isolated myocytes, membrane potential in intact smooth muscle, and isometric contractions in whole mount preparations. Exposure of isolated myocytes to 10 nM CCK caused a transient elevation in [Ca²⁺]_i that persisted in Ca²⁺-free medium and was inhibited by 2-aminoethoxydiphenylborane (2-APB). Application of caffeine induced a rapid spike-like elevation in [Ca²⁺]_i that was insensitive to 2-APB but was abolished by pretreatment with 10 µM ryanodine. These data support the idea that both inositol trisphosphate (IP₃) receptors (IP₃R) and ryanodine receptors (RyR) are present in this tissue. When caffeine was applied in Ca²⁺-free solution, the [Ca²⁺]_i transients decreased as the interval between Ca²⁺ removal and caffeine application was increased, indicating a possible leakage of Ca²⁺ in these stores. The refilling of caffeine-sensitive stores involved sarcoendoplasmic reticulum Ca²⁺-ATPase activation, similar to IP₃-sensitive stores. The moderate Ca²⁺ elevation caused by CCK was associated with a gallbladder contraction, but caffeine or ryanodine failed to induce gallbladder contraction. Nevertheless, caffeine caused a concentration-dependent relaxation in gallbladder strips either under resting tone conditions or precontracted with 1 µM CCK. Taken together, these results suggest that, in gallbladder smooth muscle, multiple pharmacologically distinct Ca²⁺ pools do not exist, but IP₃R and RyR must be spatially separated because Ca²⁺ release via these pathways leads to opposite responses.

inositol trisphosphate receptor; ryanodine receptor; refilling; caffeine; thapsigargin

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