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J. Biol. Chem., Vol. 277, Issue 2, 1340-1348, January 11, 2002

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Phosphorylation of Inositol 1,4,5-Trisphosphate Receptors in Parotid Acinar Cells
A MECHANISM FOR THE SYNERGISTIC EFFECTS OF cAMP ON Ca²⁺ SIGNALING^*

Jason I. E. Bruce, Trevor J. Shuttleworth, David R. Giovannucci, and David I. Yule

From the Department of Pharmacology & Physiology, School of Medicine and Dentistry, University of Rochester Medical Center, Rochester, New York 14642

Acetylcholine-evoked secretion from the parotid gland is substantially potentiated by cAMP-raising agonists. A potential locus for the action of cAMP is the intracellular signaling pathway resulting in elevated cytosolic calcium levels ([Ca²⁺]_i). This hypothesis was tested in mouse parotid acinar cells. Forskolin dramatically potentiated the carbachol-evoked increase in [Ca²⁺]_i, converted oscillatory [Ca²⁺]_i changes into a sustained [Ca²⁺]_i increase, and caused subthreshold concentrations of carbachol to increase [Ca²⁺]_i measurably. This potentiation was found to be independent of Ca²⁺ entry and inositol 1,4,5-trisphosphate (InsP₃) production, suggesting that cAMP-mediated effects on Ca²⁺ release was the major underlying mechanism. Consistent with this hypothesis, dibutyryl cAMP dramatically potentiated InsP₃-evoked Ca²⁺ release from streptolysin-O-permeabilized cells. Furthermore, type II InsP₃ receptors (InsP₃R) were shown to be directly phosphorylated by a protein kinase A (PKA)-mediated mechanism after treatment with forskolin. In contrast, no evidence was obtained to support direct PKA-mediated activation of ryanodine receptors (RyRs). However, inhibition of RyRs in intact cells, demonstrated a role for RyRs in propagating Ca²⁺ oscillations and amplifying potentiated Ca²⁺ release from InsP₃Rs. These data indicate that potentiation of Ca²⁺ release is primarily the result of PKA-mediated phosphorylation of InsP₃Rs, and may largely explain the synergistic relationship between cAMP-raising agonists and acetylcholine-evoked secretion in the parotid. In addition, this report supports the emerging consensus that phosphorylation at the level of the Ca²⁺ release machinery is a broadly important mechanism by which cells can regulate Ca²⁺-mediated processes.

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