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Originally published In Press as doi:10.1074/jbc.M110917200 on July 8, 2002

J. Biol. Chem., Vol. 277, Issue 38, 35496-35502, September 20, 2002
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Identification of Annexin VI as a Ca2+-sensitive CRHSP-28-binding Protein in Pancreatic Acinar Cells*

Diana D. H. Thomas, Kala M. Kaspar, William B. Taft, Ning Weng, Lance A. Rodenkirch, and Guy E. GroblewskiDagger

From the Department of Nutritional Sciences, University of Wisconsin, Madison, Wisconsin 53706

CRHSP-28 is a member of the tumor protein D52 protein family that was recently shown to regulate Ca2+-stimulated secretory activity in streptolysin-O-permeabilized acinar cells (Thomas, D. H., Taft, W. B., Kaspar, K. M., and Groblewski, G. E. (2001) J. Biol. Chem. 276, 28866-28872). In the present study, the Ca2+-sensitive phospholipid-binding protein annexin VI was purified from rat pancreas as a CRHSP-28-binding protein. The interaction between CRHSP-28 and annexin VI was demonstrated by coimmunoprecipitation and gel-overlay assays and was shown to require low micromolar levels of free Ca2+, indicating these molecules likely interact under physiological conditions. Immunofluorescence microscopy confirmed a dual localization of CRHSP-28 and annexin VI, which appeared in a punctate pattern in the supranuclear and apical cytoplasm of acini. Stimulation of cells for 5 min with the secretagogue cholecystokinin enhanced the colocalization of CRHSP-28 and annexin VI within regions of acini immediately below the apical plasma membrane. Tissue fractionation revealed that CRHSP-28 is a peripheral membrane protein that is highly enriched in smooth microsomal fractions of pancreas. Further, the content of CRHSP-28 in microsomes was significantly reduced in pancreatic tissue obtained from rats that had been infused with a secretory dose of cholecystokinin for 40 min, demonstrating that secretagogue stimulation transiently alters the association of CRHSP-28 with membranes in cells. Collectively, the Ca2+-dependent binding of CRHSP-28 and annexin VI, together with their colocalization in the apical cytoplasm, is consistent with a role for these molecules in acinar cell membrane trafficking events that are essential for digestive enzyme secretion.

* This work was supported by Grants WISO4221 and WIS04444 from the United States Department of Agriculture Cooperative State Research Education and Extension Service Program, by American Cancer Society Institutional Research Grant IRG-58-011-42-2, and by National Science Foundation Award MCB-0094154 (to G. E. G.).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 Nutritional Sciences, University of Wisconsin, 1415 Linden Dr., Madison, WI 53706. Tel.: 608-262-0884; Fax: 608-262-5860; E-mail: groby@ nutrisci.wisc.edu.

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