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Volume 272, Number 44, Issue of October 31, 1997 pp. 27764-27770
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.

The Endoplasmic Reticulum Can Act as a Functional Ca²⁺ Store in All Subcellular Regions of the Pancreatic Acinar Cell

(Received for publication, June 13, 1997, and in revised form, August 14, 1997)

From the Cell Physiology Group, School of Biological Sciences, University of Manchester, G.38 Stopford Building, Oxford Road, Manchester M13 9PT, United Kingdom

Stimulation of pancreatic acinar cells raises [Ca²⁺]_i via Ca²⁺ release from inositol-1,4,5-trisphosphate (InsP₃)-sensitive intracellular Ca²⁺ stores, generally considered to reside within the endoplasmic reticulum (ER). However, with physiological doses of cholinergic agonists, the [Ca²⁺]_i increase is localized to the apical (secretory) pole of the cell, leading to suggestions that zymogen (secretory) granules themselves may constitute an InsP₃-sensitive Ca²⁺ store responsible for localized Ca²⁺ release. We have therefore re-investigated whether the ER in pancreatic acinar cells is capable of acting as a functional Ca²⁺ store in all, or only some, cellular regions. In streptolysin O-permeabilized cells, the ER accumulated up to 25 mmol of ⁴⁵Ca²⁺ per liter ER volume by an ATP-dependent, thapsigargin-sensitive, process. This tracer Ca²⁺ uptake was dependent on ambient (loading) [Ca²⁺], as was the intra-ER free [Ca²⁺], assessed by imaging the fluorescence of Magfura-2 within the Ca²⁺ stores. Comparison of free and total intra-ER [Ca²⁺] indicated that 200-300 Ca²⁺ ions are bound within the ER lumen for every Ca²⁺ ion remaining free. Subcellular analysis showed that ER stores in all regions of the permeabilized cell took up Ca²⁺ at loading [Ca²⁺] between 60 nM and 1 µM. Thapsigargin released Ca²⁺ from stores in all cellular regions, as did InsP₃. Immunofluorescence with antibodies against sarco(endo)plasmic reticulum-2b type Ca²⁺,Mg²⁺-ATPase or calreticulin confirmed that ER Ca²⁺ stores were present throughout the cytoplasm. In summary, these results clearly show that the endoplasmic reticulum can act as a functional Ca²⁺ store in all regions of the acinar cell, including the apical pole.

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