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J. Biol. Chem., Vol. 281, Issue 3, 1547-1554, January 20, 2006

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Transfer and Tunneling of Ca²⁺ from Sarcoplasmic Reticulum to Mitochondria in Skeletal Muscle^*

From the Department of Pharmacology and Physiology, University of Medicine and Dentistry of New Jersey (UMDNJ), New Jersey Medical School, Newark, New Jersey 07103

The role of mitochondrial Ca²⁺ transport in regulating intracellular Ca²⁺ signaling and mitochondrial enzymes involved in energy metabolism is widely recognized in many tissues. However, the ability of skeletal muscle mitochondria to sequester Ca²⁺ released from the sarcoplasmic reticulum (SR) during the muscle contraction-relaxation cycle is still disputed. To assess the functional cross-talk of Ca²⁺ between SR and mitochondria, we examined the mutual relationship connecting cytosolic and mitochondrial Ca²⁺ dynamics in permeabilized skeletal muscle fibers. Cytosolic and mitochondrial Ca²⁺ transients were recorded with digital photometry and confocal microscopy using fura-2 and mag-rhod-2, respectively. In the presence of 0.5 mM slow Ca²⁺ buffer (EGTA (ethylene glycolbis(2-aminoethylether)-N,N,N',N'-tetraacetic acid)), application of caffeine induced a synchronized increase in both cytosolic and mitochondrial [Ca²⁺]. 5 mM fast Ca²⁺ buffer (BAPTA (1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid)) nearly eliminated caffeine-induced increases in [Ca²⁺]_c but only partially decreased the amplitude of mitochondrial Ca²⁺ transients. Confocal imaging revealed that in EGTA, almost all mitochondria picked up Ca²⁺ released from the SR by caffeine, whereas only about 70% of mitochondria did so in BAPTA. Taken together, these results indicated that a subpopulation of mitochondria is in close functional and presumably structural proximity to the SR, giving rise to subcellular microdomains in which Ca²⁺ has preferential access to the juxtaposed organelles.

Received for publication, May 6, 2005 , and in revised form, September 6, 2005.

^* This work was supported by grants from the Muscular Dystrophy Association and NIAMS National Institutes of Health (Grant R01 AR45690). 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.

¹ Present address: A. A. Bogomoletz Institute of Physiology, Ukrainian National Academy of Sciences, Bogomoletz Street 4, Kiev, 01024, Ukraine.

² To whom correspondence should be addressed: Dept. of Pharmacology and Physiology, UMDNJ, New Jersey Medical School, 185 South Orange Ave., Newark, NJ 07103. Tel.: 973-972-8877; Fax: 973-972-7950; E-mail: nshiroko{at}umdnj.edu.

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