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J. Biol. Chem., Vol. 279, Issue 8, 7234-7240, February 20, 2004

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Organelle Selection Determines Agonist-specific Ca²⁺ Signals in Pancreatic Acinar and Cells^*

Michiko Yamasaki, Roser Masgrau¶, Anthony J. Morgan, Grant C. Churchill, Sandip Patel||, Stephen J. H. Ashcroft**, and Antony Galione

From the Department of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3QT, the ^||Department of Physiology, University College London, Gower Street, London WC1E 6BT, and ^**Oxford Centre for Diabetes, Endocrinology and Metabolism, Churchill Hospital, Oxford OX3 7LJ, United Kingdom

How different extracellular stimuli can evoke different spatiotemporal Ca²⁺ signals is uncertain. We have elucidated a novel paradigm whereby different agonists use different Ca²⁺-storing organelles ("organelle selection") to evoke unique responses. Some agonists select the endoplasmic reticulum (ER), and others select lysosome-related (acidic) organelles, evoking spatial Ca²⁺ responses that mirror the organellar distribution. In pancreatic acinar cells, acetylcholine and bombesin exclusively select the ER Ca²⁺ store, whereas cholecystokinin additionally recruits a lysosome-related organelle. Similarly, in a pancreatic cell line MIN6, acetylcholine selects only the ER, whereas glucose mobilizes Ca²⁺ from a lysosome-related organelle. We also show that the key to organelle selection is the agonist-specific coupling messenger(s) such that the ER is selected by recruitment of inositol 1,4,5-trisphosphate (or cADP-ribose), whereas lysosome-related organelles are selected by NAADP.

Received for publication, October 8, 2003 , and in revised form, November 19, 2003.

^* This work was supported by The Wellcome Trust through a senior fellowship (to A. G.), a Research Career Development fellowship (to S. P.), a Prize Studentship (to M. Y.), and a project grant (to A. G. and S. J. H. A.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Both authors contributed equally to this work.

^¶ To whom correspondence should be addressed: Dept. of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3QT, UK. Tel.: 44 01865 271 606; Fax: 44 01865 271 853; E-mail: roser.masgrau-juanola{at}pharmacology.oxford.ac.uk.

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