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Am J Physiol Cell Physiol 288: C1074-C1082, 2005. First published January 12, 2005; doi:10.1152/ajpcell.00391.2004
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CELLULAR METABOLISM

Subsarcolemmal and intermyofibrillar mitochondria play distinct roles in regulating skeletal muscle fatty acid metabolism

Timothy R. Koves,1,3,5 Robert C. Noland,1 Andrew L. Bates,2 Sarah T. Henes,2 Deborah M. Muoio,3,4,5 and Ronald N. Cortright1,2

1Department of Physiology, Brody School of Medicine, and 2Department of Exercise and Sport Science, College of Health and Human Performance, East Carolina University, Greenville; and 3Department of Medicine, 4Department of Pharmacology and Cancer Biology, and 5Sarah W. Stedman Nutrition and Metabolism Center, Duke University, Durham, North Carolina

Submitted 9 August 2004 ; accepted in final form 4 January 2005

Skeletal muscle contains two populations of mitochondria that appear to be differentially affected by disease and exercise training. It remains unclear how these mitochondrial subpopulations contribute to fiber type-related and/or training-induced changes in fatty acid oxidation and regulation of carnitine palmitoyltransferase-1{beta} (CPT1{beta}), the enzyme that controls mitochondrial fatty acid uptake in skeletal muscle. To this end, we found that fatty acid oxidation rates were 8.9-fold higher in subsarcolemmal mitochondria (SS) and 5.3-fold higher in intermyofibrillar mitochondria (IMF) that were isolated from red gastrocnemius (RG) compared with white gastrocnemius (WG) muscle, respectively. Malonyl-CoA (10 µM), a potent inhibitor of CPT1{beta}, completely abolished fatty acid oxidation in SS and IMF mitochondria from WG, whereas oxidation rates in the corresponding fractions from RG were inhibited only 89% and 60%, respectively. Endurance training also elicited mitochondrial adaptations that resulted in enhanced fatty acid oxidation capacity. Ten weeks of treadmill running differentially increased palmitate oxidation rates 100% and 46% in SS and IMF mitochondria, respectively. In SS mitochondria, elevated fatty acid oxidation rates were accompanied by a 48% increase in citrate synthase activity but no change in CPT1 activity. Nonlinear regression analyses of mitochondrial fatty acid oxidation rates in the presence of 0–100 µM malonyl-CoA indicated that IC50 values were neither dependent on mitochondrial subpopulation nor affected by exercise training. However, in IMF mitochondria, training reduced the Hill coefficient (P < 0.05), suggesting altered CPT1{beta} kinetics. These results demonstrate that endurance exercise provokes subpopulation-specific changes in mitochondrial function that are characterized by enhanced fatty acid oxidation and modified CPT1{beta}-malonyl-CoA dynamics.

endurance exercise training; CPT-1; fiber type; rat; mitochondrial subpopulations


Address for correspondence and reprint requests: R. N. Cortright, 363 Ward Sports Medicine Bldg., East Carolina Univ., Greenville, NC 27858 (E-mail: cortrightr{at}mail.ecu.edu). Address for correspondence: D. M. Muoio, 4321 Medical Park Dr., Suite 200, Duke Univ. Medical Center, Durham, NC 27704 (E-mail: muoio{at}duke.edu)




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