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Originally published In Press as doi:10.1074/jbc.M106609200 on November 1, 2001

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. BruceDagger , 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.

* This work was supported by National Institutes of Health Grants DEO 13539 (to T. J. S. and D. I. Y.), GM 40457 (to T. J. S.), and DK54568 (to D. I. Y.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger To whom correspondence should be addressed: Dept. of Pharmacology & Physiology, School of Medicine and Dentistry, University of Rochester Medical Center, 601 Elmwood Ave., Rochester, NY 14642. Tel.: 716-275-6128; Fax: 716-273-2652; E-mail: jason_bruce@urmc.rochester.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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