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J. Biol. Chem., Vol. 276, Issue 47, 44146-44156, November 23, 2001

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Polarized Expression of G Protein-coupled Receptors and an All-or-None Discharge of Ca²⁺ Pools at Initiation Sites of [Ca²⁺]_i Waves in Polarized Exocrine Cells^*

Dong Min Shin, Xiang Luo, Thomas M. Wilkie^§, Laurence J. Miller^¶, Ammon B. Peck, Michael G. Humphreys-Beher^**, and Shmuel Muallem

From the Departments of  Physiology and ^§ Pharmacology, University of Texas Southwestern Medical Center, Dallas, Texas 75390, the ^¶ Center for Basic Research in Digestive Diseases, Mayo Clinic and Foundation, Rochester, Minnesota 55905, the  Department of Pathology and Laboratory Medicine and the ^** Departments of Oral Biology and Pharmacology and Therapeutics, University of Florida, Gainesville, Florida 32610

In the present work we examined localization and behavior of G protein-coupled receptors (GPCR) in polarized exocrine cells to address the questions of how luminal to basal Ca²⁺ waves can be generated in a receptor-specific manner and whether quantal Ca²⁺ release reflects partial release from a continuous pool or an all-or-none release from a compartmentalized pool. Immunolocalization revealed that expression of GPCRs in polarized cells is not uniform, with high levels of GPCR expression at or near the tight junctions. Measurement of phospholipase C activity and receptor-dependent recruitment and trapping of the box domain of RGS4 in GPCRs complexes indicated autonomous functioning of G_q-coupled receptors in acinar cells. These findings explain the generation of receptor-specific Ca²⁺ waves and why the waves are always initiated at the apical pole. The initiation site of Ca²⁺ wave at the apical pole and the pattern of wave propagation were independent of inositol 1,4,5-trisphosphate concentration. Furthermore, a second Ca²⁺ wave with the same initiation site and pattern was launched by inhibition of sarco/endoplasmic reticulum Ca²⁺-ATPase pumps of cells continuously stimulated with sub-maximal agonist concentration. By contrast, rapid sequential application of sub-maximal and maximal agonist concentrations to the same cell triggered Ca²⁺ waves with different initiation sites. These findings indicate that signaling specificity in pancreatic acinar cells is aided by polarized expression and autonomous functioning of GPCRs and that quantal Ca²⁺ release is not due to a partial Ca²⁺ release from a continuous pool, but rather, it is due to an all-or-none Ca²⁺ release from a compartmentalized Ca²⁺ pool.

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