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J Biol Chem, Vol. 275, Issue 20, 15305-15313, May 19, 2000

Calcium Signal Transmission between Ryanodine Receptors and Mitochondria*

Gábor SzalaiDagger , György CsordásDagger , Basil M. Hantash§, Andrew P. ThomasDagger §, and György HajnóczkyDagger ||

From the Dagger  Department of Pathology, Anatomy and Cell Biology, Thomas Jefferson University, Philadelphia, Pennsylvania 19107 and the § Department of Pharmacology and Physiology, University of Medicine and Dentistry of New Jersey, New Jersey Medical School, Newark, New Jersey 07103

Control of energy metabolism by increases of mitochondrial matrix [Ca2+] ([Ca2+]m) may represent a fundamental mechanism to meet the ATP demand imposed by heart contractions, but the machinery underlying propagation of [Ca2+] signals from ryanodine receptor Ca2+ release channels (RyR) to the mitochondria remains elusive. Using permeabilized cardiac (H9c2) cells we investigated the cytosolic [Ca2+] ([Ca2+]c) and [Ca2+]m signals elicited by activation of RyR. Caffeine, Ca2+, and ryanodine evoked [Ca2+]c spikes that often appeared as frequency-modulated [Ca2+]c oscillations in these permeabilized cells. Rapid increases in [Ca2+]m and activation of the Ca2+-sensitive mitochondrial dehydrogenases were synchronized to the rising phase of the [Ca2+]c spikes. The RyR-mediated elevations of global [Ca2+]c were in the submicromolar range, but the rate of [Ca2+]m increases was as large as it was in the presence of 30 µM global [Ca2+]c. Furthermore, RyR-dependent increases of [Ca2+]m were relatively insensitive to buffering of [Ca2+]c by EGTA. Therefore, RyR-driven rises of [Ca2+]m appear to result from large and rapid increases of perimitochondrial [Ca2+]. The falling phase of [Ca2+]c spikes was followed by a rapid decay of [Ca2+]m. CGP37157 slowed down relaxation of [Ca2+]m spikes, whereas cyclosporin A had no effect, suggesting that activation of the mitochondrial Ca2+ exchangers accounts for rapid reversal of the [Ca2+]m response with little contribution from the permeability transition pore. Thus, rapid activation of Ca2+ uptake sites and Ca2+ exchangers evoked by RyR-mediated local [Ca2+]c signals allow mitochondria to respond rapidly to single [Ca2+]c spikes in cardiac cells.

* This work was supported by a grant-in-aid (to G. H.) from the American Heart Association and Grants DK51526 (to G. H.) and DK38422 (to A. P. T.) from the National Institutes of Health.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.

Recipient of an American Heart Association Predoctoral fellowship.

|| Recipient of a Burroughs Wellcome Fund Career Award in the Biomedical Sciences. To whom correspondence should be addressed: Dept. of Pathology, Anatomy and Cell Biology, Rm. 253 JAH, Thomas Jefferson University, Philadelphia, PA 19107. Tel.: (215) 503-1427; Fax: (215) 923-2218; E-mail: Gyorgy.Hajnoczky@mail.tju.edu.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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