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J. Biol. Chem., Vol. 280, Issue 16, 15794-15799, April 22, 2005

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Stable Golgi-Mitochondria Complexes and Formation of Golgi Ca²⁺ Gradients in Pancreatic Acinar Cells^*

Nick J. Dolman, Julia V. Gerasimenko, Oleg V. Gerasimenko, Svetlana G. Voronina, Ole H. Petersen, and Alexei V. Tepikin

From the Physiological Laboratory, University of Liverpool, Liverpool L69 3BX, England, United Kingdom

We have determined the localization of the Golgi with respect to other organelles in living pancreatic acinar cells and the importance of this localization to the establishment of Ca²⁺ gradients over the Golgi. Using confocal microscopy and the Golgi-specific fluorescent probe 6-((N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)amino)hexanoyl)sphingosine, we found Golgi structures localizing to the outer edge of the secretory granular region of individual acinar cells. We also assessed Golgi positioning in acinar cells located within intact pancreatic tissue using two-photon microscopy and found a similar localization. The mitochondria segregate the Golgi from lateral regions of the plasma membrane, the nucleus, and the basal part of the cytoplasm. The Golgi is therefore placed between the principal Ca²⁺ release sites in the apical region of the cell and the important Ca²⁺ sink formed by the peri-granular mitochondria. During acetylcholine-induced cytosolic Ca²⁺ signals in the apical region, large Ca²⁺ gradients form over the Golgi (decreasing from trans- to cis-Golgi). We further describe a novel, close interaction of the peri-granular mitochondria and the Golgi apparatus. The mitochondria and the Golgi structures form very close contacts, and these contacts remain stable over time. When the cell is forced to swell, the Golgi and mitochondria remain juxtaposed up to the point of cell lysis. The strategic position of the Golgi (closer to release sites than the bulk of the mitochondrial belt) makes this organelle receptive to local apical Ca²⁺ transients. In addition the Golgi is ideally placed to be preferentially supplied by ATP from adjacent mitochondria.

Received for publication, November 19, 2004 , and in revised form, January 12, 2005.

^* This work was supported by a Medical Research Council program grant (to O. H. P., A. V. T., and O. V. G.), a Medical Research Council research professorship (to O. H. P.), and the Wellcome Trust (to N. J. D.). 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. S1–S4 and supplemental Videos 1 and 2.

A Wellcome Trust Prize Ph.D. student. To whom correspondence may be addressed. Present address: Synaptic Physiology Unit, National Institutes of Health/National Institute of Neurological Disorders and Stroke, Bldg. 35, 35 Convent Dr., Bethesda, MD 20892. To whom correspondence may be addressed. Tel. 44-151-794-5351; Fax: 44-151-794-5327; E-mail: a.tepikin{at}liv.ac.uk.

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