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(The FASEB Journal. 2002;16:1879-1886.)
© 2002 FASEB

Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1

KEITH BAAR, ADAM R. WENDE, TERRY E. JONES, MATTHEW MARISON, LORRAINE A. NOLTE, MAY CHEN, DANIEL P. KELLY and JOHN O. HOLLOSZY1

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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J Appl Physiol, October 1, 2005; 99(4): 1359 - 1363.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Heart Circ. Physiol.Home page
C. Ojaimi, W. Li, S. Kinugawa, H. Post, A. Csiszar, P. Pacher, G. Kaley, and T. H. Hintze
Transcriptional basis for exercise limitation in male eNOS-knockout mice with age: heart failure and the fetal phenotype
Am J Physiol Heart Circ Physiol, October 1, 2005; 289(4): H1399 - H1407.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
T. R. Koves, P. Li, J. An, T. Akimoto, D. Slentz, O. Ilkayeva, G. L. Dohm, Z. Yan, C. B. Newgard, and D. M. Muoio
Peroxisome Proliferator-activated Receptor-{gamma} Co-activator 1{alpha}-mediated Metabolic Remodeling of Skeletal Myocytes Mimics Exercise Training and Reverses Lipid-induced Mitochondrial Inefficiency
J. Biol. Chem., September 30, 2005; 280(39): 33588 - 33598.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
R. Cartoni, B. Leger, M. B. Hock, M. Praz, A. Crettenand, S. Pich, J.-L. Ziltener, F. Luthi, O. Deriaz, A. Zorzano, et al.
Mitofusins 1/2 and ERR{alpha} expression are increased in human skeletal muscle after physical exercise
J. Physiol., August 15, 2005; 567(1): 349 - 358.
[Abstract] [Full Text] [PDF]


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J. Appl. Physiol.Home page
A. Lucia, F. Gomez-Gallego, I. Barroso, M. Rabadan, F. Bandres, A. F. San Juan, J. L. Chicharro, U. Ekelund, S. Brage, C. P. Earnest, et al.
PPARGC1A genotype (Gly482Ser) predicts exceptional endurance capacity in European men
J Appl Physiol, July 1, 2005; 99(1): 344 - 348.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
T. Akimoto, S. C. Pohnert, P. Li, M. Zhang, C. Gumbs, P. B. Rosenberg, R. S. Williams, and Z. Yan
Exercise Stimulates Pgc-1{alpha} Transcription in Skeletal Muscle through Activation of the p38 MAPK Pathway
J. Biol. Chem., May 20, 2005; 280(20): 19587 - 19593.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
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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DiabetesHome page
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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FASEB J.Home page
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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Am. J. Physiol. Cell Physiol.Home page
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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Circ. Res.Home page
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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J Mol EndocrinolHome page
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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Am. J. Physiol. Endocrinol. Metab.Home page
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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Circ. Res.Home page
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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Am. J. Physiol. Cell Physiol.Home page
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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Proc. Natl. Acad. Sci. USAHome page
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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DiabetesHome page
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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DiabetesHome page
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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Proc. Natl. Acad. Sci. USAHome page
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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Circ. Res.Home page
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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Genes Dev.Home page
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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Am. J. Physiol. Endocrinol. Metab.Home page
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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Recent Prog Horm ResHome page
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. Appl. Physiol.Home page
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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Mol. Endocrinol.Home page
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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DiabetesHome page
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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Eur Respir JHome page
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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Am. J. Physiol. Endocrinol. Metab.Home page
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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Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
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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J. Appl. Physiol.Home page
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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FASEB J.Home page
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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J. Biol. Chem.Home page
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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Proc. Natl. Acad. Sci. USAHome page
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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Am. J. Physiol. Cell Physiol.Home page
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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FASEB J.Home page
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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Am. J. Physiol. Endocrinol. Metab.Home page
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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