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Department of Medicine, Washington University School of Medicine, St. Louis, Missouri, USA
1Correspondence: Washington University School of Medicine, Department of Medicine, Campus Box 8113, 4566 Scott Ave., St. Louis, MO 63110, USA. E-mail: jhollosz{at}im.wustl.edu
Endurance exercise induces increases in mitochondria and the GLUT4 isoform of the glucose transporter in muscle. Although little is known about the mechanisms underlying these adaptations, new information has accumulated regarding how mitochondrial biogenesis and GLUT4 expression are regulated. This includes the findings that the transcriptional coactivator PGC-1 promotes mitochondrial biogenesis and that NRF-1 and NRF-2 act as transcriptional activators of genes encoding mitochondrial enzymes. We tested the hypothesis that increases in PGC-1, NRF-1, and NRF-2 are involved in the initial adaptive response of muscle to exercise. Five daily bouts of swimming induced increases in mitochondrial enzymes and GLUT4 in skeletal muscle in rats. One exercise bout resulted in 
twofold increases in full-length muscle PGC-1 mRNA and PGC-1 protein, which were evident 18 h after exercise. A smaller form of PGC-1 increased after exercise. The exercise induced increases in muscle NRF-1 and NRF-2 that were evident 12 to 18 h after one exercise bout. These findings suggest that increases in PGC-1, NRF-1, and NRF-2 represent key regulatory components of the stimulation of mitochondrial biogenesis by exercise and that PGC-1 mediates the coordinated increases in GLUT4 and mitochondria.—Baar, K., Wende, A. R., Jones, T. E., Marison, M., Nolte, L. A., Chen, M., Kelly, D. P., Holloszy, J. O. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1.
Key Words: GLUT4 • mitochondrial biogenesis • NRF-1 • NRF-2
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K. E. Padfield, L. G. Astrakas, Q. Zhang, S. Gopalan, G. Dai, M. N. Mindrinos, R. G. Tompkins, L. G. Rahme, and A. A. Tzika Burn injury causes mitochondrial dysfunction in skeletal muscle PNAS, April 12, 2005; 102(15): 5368 - 5373. [Abstract] [Full Text] [PDF]
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P. M. Garcia-Roves, T. E. Jones, K. Otani, D.-H. Han, and J. O. Holloszy Calcineurin Does Not Mediate Exercise-Induced Increase in Muscle GLUT4 Diabetes, March 1, 2005; 54(3): 624 - 628. [Abstract] [Full Text] [PDF]
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A. Garnier, D. Fortin, J. Zoll, B. N'Guessan, B. Mettauer, E. Lampert, V. Veksler, and R. Ventura-Clapier Coordinated changes in mitochondrial function and biogenesis in healthy and diseased human skeletal muscle FASEB J, January 1, 2005; 19(1): 43 - 52. [Abstract] [Full Text] [PDF]
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T. Akimoto, T. J. Ribar, R. S. Williams, and Z. Yan Skeletal muscle adaptation in response to voluntary running in Ca2+/calmodulin-dependent protein kinase IV-deficient mice Am J Physiol Cell Physiol, November 1, 2004; 287(5): C1311 - C1319. [Abstract] [Full Text] [PDF]
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M. Sano and M. D. Schneider Cyclin-Dependent Kinase-9: An RNAPII Kinase at the Nexus of Cardiac Growth and Death Cascades Circ. Res., October 29, 2004; 95(9): 867 - 876. [Abstract] [Full Text] [PDF]
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M J Watt, R J Southgate, A G Holmes, and M A Febbraio Suppression of plasma free fatty acids upregulates peroxisome proliferator-activated receptor (PPAR) {alpha} and {delta} and PPAR coactivator 1{alpha} in human skeletal muscle, but not lipid regulatory genes J. Mol. Endocrinol., October 1, 2004; 33(2): 533 - 544. [Abstract] [Full Text] [PDF]
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R. L. G. S. Oliveira, M. Ueno, C. T. de Souza, M. Pereira-da-Silva, A. L. Gasparetti, R. M. N. Bezzera, L. C. Alberici, A. E. Vercesi, M. J. A. Saad, and L. A. Velloso Cold-induced PGC-1{alpha} expression modulates muscle glucose uptake through an insulin receptor/Akt-independent, AMPK-dependent pathway Am J Physiol Endocrinol Metab, October 1, 2004; 287(4): E686 - E695. [Abstract] [Full Text] [PDF]
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J. M. Huss and D. P. Kelly Nuclear Receptor Signaling and Cardiac Energetics Circ. Res., September 17, 2004; 95(6): 568 - 578. [Abstract] [Full Text] [PDF]
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T. Akimoto, B. S. Sorg, and Z. Yan Real-time imaging of peroxisome proliferator-activated receptor-{gamma} coactivator-1{alpha} promoter activity in skeletal muscles of living mice Am J Physiol Cell Physiol, September 1, 2004; 287(3): C790 - C796. [Abstract] [Full Text] [PDF]
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P. J. Willy, I. R. Murray, J. Qian, B. B. Busch, W. C. Stevens Jr., R. Martin, R. Mohan, S. Zhou, P. Ordentlich, P. Wei, et al. Regulation of PPAR{gamma} coactivator 1{alpha} (PGC-1{alpha}) signaling by an estrogen-related receptor {alpha} (ERR{alpha}) ligand PNAS, June 15, 2004; 101(24): 8912 - 8917. [Abstract] [Full Text] [PDF]
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S. L. McGee and M. Hargreaves Exercise and Myocyte Enhancer Factor 2 Regulation in Human Skeletal Muscle Diabetes, May 1, 2004; 53(5): 1208 - 1214. [Abstract] [Full Text] [PDF]
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H. Oberkofler, V. Linnemayr, R. Weitgasser, K. Klein, M. Xie, B. Iglseder, F. Krempler, B. Paulweber, and W. Patsch Complex Haplotypes of the PGC-1{alpha} Gene Are Associated With Carbohydrate Metabolism and Type 2 Diabetes Diabetes, May 1, 2004; 53(5): 1385 - 1393. [Abstract] [Full Text] [PDF]
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S. N. Schreiber, R. Emter, M. B. Hock, D. Knutti, J. Cardenas, M. Podvinec, E. J. Oakeley, and A. Kralli The estrogen-related receptor {alpha} (ERR{alpha}) functions in PPAR{gamma} coactivator 1{alpha} (PGC-1{alpha})-induced mitochondrial biogenesis PNAS, April 27, 2004; 101(17): 6472 - 6477. [Abstract] [Full Text] [PDF]
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L. K. Russell, C. M. Mansfield, J. J. Lehman, A. Kovacs, M. Courtois, J. E. Saffitz, D. M. Medeiros, M. L. Valencik, J. A. McDonald, and D. P. Kelly Cardiac-Specific Induction of the Transcriptional Coactivator Peroxisome Proliferator-Activated Receptor {gamma} Coactivator-1{alpha} Promotes Mitochondrial Biogenesis and Reversible Cardiomyopathy in a Developmental Stage-Dependent Manner Circ. Res., March 5, 2004; 94(4): 525 - 533. [Abstract] [Full Text] [PDF]
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 D. P. Kelly and R. C. Scarpulla Transcriptional regulatory circuits controlling mitochondrial biogenesis and function Genes & Dev., February 15, 2004; 18(4): 357 - 368. [Full Text] [PDF]
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S. Terada and I. Tabata Effects of acute bouts of running and swimming exercise on PGC-1{alpha} protein expression in rat epitrochlearis and soleus muscle Am J Physiol Endocrinol Metab, February 1, 2004; 286(2): E208 - E216. [Abstract] [Full Text] [PDF]
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 M. P. Czubryt and E. N. Olson Balancing Contractility and Energy Production: The Role of Myocyte Enhancer Factor 2 (MEF2) in Cardiac Hypertrophy Recent Prog. Horm. Res., January 1, 2004; 59(1): 105 - 124. [Abstract] [Full Text]
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J. Norrbom, C. J. Sundberg, H. Ameln, W. E. Kraus, E. Jansson, and T. Gustafsson PGC-1{alpha} mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle J Appl Physiol, January 1, 2004; 96(1): 189 - 194. [Abstract] [Full Text] [PDF]
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U. Dressel, T. L. Allen, J. B. Pippal, P. R. Rohde, P. Lau, and G. E. O. Muscat The Peroxisome Proliferator-Activated Receptor {beta}/{delta} Agonist, GW501516, Regulates the Expression of Genes Involved in Lipid Catabolism and Energy Uncoupling in Skeletal Muscle Cells Mol. Endocrinol., December 1, 2003; 17(12): 2477 - 2493. [Abstract] [Full Text] [PDF]
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A. P. Russell, J. Feilchenfeldt, S. Schreiber, M. Praz, A. Crettenand, C. Gobelet, C. A. Meier, D. R. Bell, A. Kralli, J.-P. Giacobino, et al. Endurance Training in Humans Leads to Fiber Type-Specific Increases in Levels of Peroxisome Proliferator-Activated Receptor-{gamma} Coactivator-1 and Peroxisome Proliferator-Activated Receptor-{alpha} in Skeletal Muscle Diabetes, December 1, 2003; 52(12): 2874 - 2881. [Abstract] [Full Text] [PDF]
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 A.M.W.J. Schols Nutritional and metabolic modulation in chronic obstructive pulmonary disease management Eur. Respir. J., November 2, 2003; 22(46_suppl): 81s - 86s. [Abstract] [Full Text] [PDF]
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P. M. Garcia-Roves, D.-H. Han, Z. Song, T. E. Jones, K. A. Hucker, and J. O. Holloszy Prevention of glycogen supercompensation prolongs the increase in muscle GLUT4 after exercise Am J Physiol Endocrinol Metab, October 1, 2003; 285(4): E729 - E736. [Abstract] [Full Text] [PDF]
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S. C. Leary, C. N. Lyons, A. G. Rosenberger, J. S. Ballantyne, J. Stillman, and C. D. Moyes Fiber-type differences in muscle mitochondrial profiles Am J Physiol Regulatory Integrative Comp Physiol, October 1, 2003; 285(4): R817 - R826. [Abstract] [Full Text] [PDF]
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M. Suwa, H. Nakano, and S. Kumagai Effects of chronic AICAR treatment on fiber composition, enzyme activity, UCP3, and PGC-1 in rat muscles J Appl Physiol, September 1, 2003; 95(3): 960 - 968. [Abstract] [Full Text] [PDF]
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K. BAAR, Z. SONG, C. F. SEMENKOVICH, T. E. JONES, D.-H. HAN, L. A. NOLTE, E. O. OJUKA, M. CHEN, and J. O. HOLLOSZY Skeletal muscle overexpression of nuclear respiratory factor 1 increases glucose transport capacity FASEB J, September 1, 2003; 17(12): 1666 - 1673. [Abstract] [Full Text] [PDF]
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S. Miura, Y. Kai, M. Ono, and O. Ezaki Overexpression of Peroxisome Proliferator-activated Receptor {gamma} Coactivator-1{alpha} Down-regulates GLUT4 mRNA in Skeletal Muscles J. Biol. Chem., August 15, 2003; 278(33): 31385 - 31390. [Abstract] [Full Text] [PDF]
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C. Handschin, J. Rhee, J. Lin, P. T. Tarr, and B. M. Spiegelman An autoregulatory loop controls peroxisome proliferator-activated receptor {gamma} coactivator 1{alpha} expression in muscle PNAS, June 10, 2003; 100(12): 7111 - 7116. [Abstract] [Full Text] [PDF]
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I. Irrcher, P. J. Adhihetty, T. Sheehan, A.-M. Joseph, and D. A. Hood PPARgamma coactivator-1alpha expression during thyroid hormone- and contractile activity-induced mitochondrial adaptations Am J Physiol Cell Physiol, June 1, 2003; 284(6): C1669 - C1677. [Abstract] [Full Text] [PDF]
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E. O. OJUKA, T. E. JONES, D.-H. HAN, M. CHEN, and J. O. HOLLOSZY Raising Ca2+ in L6 myotubes mimics effects of exercise on mitochondrial biogenesis in muscle FASEB J, April 1, 2003; 17(6): 675 - 681. [Abstract] [Full Text] [PDF]
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J. O. Holloszy A forty-year memoir of research on the regulation of glucose transport into muscle Am J Physiol Endocrinol Metab, March 1, 2003; 284(3): E453 - E467. [Abstract] [Full Text] [PDF]
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