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J Appl Physiol 88: 2219-2226, 2000;
8750-7587/00 $5.00
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Vol. 88, Issue 6, 2219-2226, June 2000

Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle

W. W. Winder, B. F. Holmes, D. S. Rubink, E. B. Jensen, M. Chen, and J. O. Holloszy

Department of Zoology, Brigham Young University, Provo, Utah 84602; and Department of Internal Medicine, Washington University School of Medicine, St. Louis, Missouri 63110

Muscle contraction causes an increase in activity of 5'-AMP-activated protein kinase (AMPK). This study was designed to determine whether chronic chemical activation of AMPK will increase mitochondrial enzymes, GLUT-4, and hexokinase in different types of skeletal muscle of resting rats. In acute studies, rats were subcutaneously injected with either 5-aminoimidazole-4-carboxamide-1-beta -D-ribofuranoside (AICAR; 1 mg/g body wt) in 0.9% NaCl or with 0.9% NaCl alone and were then anesthetized for collection and freezing of tissues. AMPK activity increased in the superficial, white region of the quadriceps and in soleus muscles but not in the deep, red region of the quadriceps muscle. Acetyl-CoA carboxylase (ACC) activity, a target for AMPK, decreased in all three muscle types in response to AICAR injection but was lowest in the white quadriceps. In rats given daily, 1 mg/g body wt, subcutaneous injections of AICAR for 4 wk, activities of citrate synthase, succinate dehydrogenase, and malate dehydrogenase were increased in white quadriceps and soleus but not in red quadriceps. Cytochrome c and delta -aminolevulinic acid synthase levels were increased in white, but not red, quadriceps. Carnitine palmitoyl-transferase and hydroxy-acyl-CoA dehydrogenase were not significantly increased. Hexokinase was markedly increased in all three muscles, and GLUT-4 was increased in red and white quadriceps. These results suggest that chronic AMPK activation may mediate the effects of muscle contraction on some, but not all, biochemical adaptations of muscle to endurance exercise training.

delta -aminolevulinate synthase; carnitine palmitoyl transferase; citrate synthase; citric acid cycle enzymes; endurance training; GLUT-4; muscle mitochondria


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AMP-activated protein kinase and coordination of hepatic fatty acid metabolism of starved/carbohydrate-refed rats
Am J Physiol Endocrinol Metab, November 1, 2005; 289(5): E794 - E800.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Endocrinol. Metab.Home page
D. Hurst, E. B. Taylor, T. D. Cline, L. J. Greenwood, C. L. Compton, J. D. Lamb, and W. W. Winder
AMP-activated protein kinase kinase activity and phosphorylation of AMP-activated protein kinase in contracting muscle of sedentary and endurance-trained rats
Am J Physiol Endocrinol Metab, October 1, 2005; 289(4): E710 - E715.
[Abstract] [Full Text] [PDF]


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J. Appl. Physiol.Home page
J. L. Smith, P. B. Patil, and J. S. Fisher
AICAR and hyperosmotic stress increase insulin-stimulated glucose transport
J Appl Physiol, September 1, 2005; 99(3): 877 - 883.
[Abstract] [Full Text] [PDF]


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J. Exp. Biol.Home page
C. D. Moyes and C. M. R. LeMoine
Control of muscle bioenergetic gene expression: implications for allometric scaling relationships of glycolytic and oxidative enzymes
J. Exp. Biol., May 1, 2005; 208(9): 1601 - 1610.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
M. Foretz, N. Ancellin, F. Andreelli, Y. Saintillan, P. Grondin, A. Kahn, B. Thorens, S. Vaulont, and B. Viollet
Short-Term Overexpression of a Constitutively Active Form of AMP-Activated Protein Kinase in the Liver Leads to Mild Hypoglycemia and Fatty Liver
Diabetes, May 1, 2005; 54(5): 1331 - 1339.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
R. Pold, L. S. Jensen, N. Jessen, E. S. Buhl, O. Schmitz, A. Flyvbjerg, N. Fujii, L. J. Goodyear, C. F. Gotfredsen, C. L. Brand, et al.
Long-Term AICAR Administration and Exercise Prevents Diabetes in ZDF Rats
Diabetes, April 1, 2005; 54(4): 928 - 934.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
J. V. Swinnen, A. Beckers, K. Brusselmans, S. Organe, J. Segers, L. Timmermans, F. Vanderhoydonc, L. Deboel, R. Derua, E. Waelkens, et al.
Mimicry of a Cellular Low Energy Status Blocks Tumor Cell Anabolism and Suppresses the Malignant Phenotype
Cancer Res., March 15, 2005; 65(6): 2441 - 2448.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Endocrinol. Metab.Home page
E. B. Taylor, D. Hurst, L. J. Greenwood, J. D. Lamb, T. D. Cline, S. N. Sudweeks, and W. W. Winder
Endurance training increases LKB1 and MO25 protein but not AMP-activated protein kinase kinase activity in skeletal muscle
Am J Physiol Endocrinol Metab, December 1, 2004; 287(6): E1082 - E1089.
[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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J. Clin. Endocrinol. Metab.Home page
G. R. Steinberg, A. C. Smith, B. J. W. van Denderen, Z. Chen, S. Murthy, D. J. Campbell, G. J. F. Heigenhauser, D. J. Dyck, and B. E. Kemp
AMP-Activated Protein Kinase Is Not Down-Regulated in Human Skeletal Muscle of Obese Females
J. Clin. Endocrinol. Metab., September 1, 2004; 89(9): 4575 - 4580.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
J. A. Villena, B. Viollet, F. Andreelli, A. Kahn, S. Vaulont, and H. S. Sul
Induced Adiposity and Adipocyte Hypertrophy in Mice Lacking the AMP-Activated Protein Kinase-{alpha}2 Subunit
Diabetes, September 1, 2004; 53(9): 2242 - 2249.
[Abstract] [Full Text] [PDF]


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CirculationHome page
D. Nagata, R. Takeda, M. Sata, H. Satonaka, E. Suzuki, T. Nagano, and Y. Hirata
AMP-Activated Protein Kinase Inhibits Angiotensin II-Stimulated Vascular Smooth Muscle Cell Proliferation
Circulation, July 27, 2004; 110(4): 444 - 451.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
E.-K. Kim, I. Miller, S. Aja, L. E. Landree, M. Pinn, J. McFadden, F. P. Kuhajda, T. H. Moran, and G. V. Ronnett
C75, a Fatty Acid Synthase Inhibitor, Reduces Food Intake via Hypothalamic AMP-activated Protein Kinase
J. Biol. Chem., May 7, 2004; 279(19): 19970 - 19976.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Endocrinol. Metab.Home page
S. A. Clark, Z.-P. Chen, K. T. Murphy, R. J. Aughey, M. J. McKenna, B. E. Kemp, and J. A. Hawley
Intensified exercise training does not alter AMPK signaling in human skeletal muscle
Am J Physiol Endocrinol Metab, May 1, 2004; 286(5): E737 - E743.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
U. Andersson, K. Filipsson, C. R. Abbott, A. Woods, K. Smith, S. R. Bloom, D. Carling, and C. J. Small
AMP-activated Protein Kinase Plays a Role in the Control of Food Intake
J. Biol. Chem., March 26, 2004; 279(13): 12005 - 12008.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Endocrinol. Metab.Home page
C. Frosig, S. B. Jorgensen, D. G. Hardie, E. A. Richter, and J. F. P. Wojtaszewski
5'-AMP-activated protein kinase activity and protein expression are regulated by endurance training in human skeletal muscle
Am J Physiol Endocrinol Metab, March 1, 2004; 286(3): E411 - E417.
[Abstract] [Full Text]


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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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J. Biol. Chem.Home page
S. B. Jorgensen, B. Viollet, F. Andreelli, C. Frosig, J. B. Birk, P. Schjerling, S. Vaulont, E. A. Richter, and J. F. P. Wojtaszewski
Knockout of the {alpha}2 but Not {alpha}1 5'-AMP-activated Protein Kinase Isoform Abolishes 5-Aminoimidazole-4-carboxamide-1-{beta}-4-ribofuranosidebut Not Contraction-induced Glucose Uptake in Skeletal Muscle
J. Biol. Chem., January 9, 2004; 279(2): 1070 - 1079.
[Abstract] [Full Text] [PDF]


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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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EndocrinologyHome page
N. B. Ruderman, A. K. Saha, and E. W. Kraegen
Minireview: Malonyl CoA, AMP-Activated Protein Kinase, and Adiposity
Endocrinology, December 1, 2003; 144(12): 5166 - 5171.
[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. Physiol.Home page
C. T Putman, M. Kiricsi, J. Pearcey, I. M MacLean, J. A Bamford, G. K Murdoch, W. T Dixon, and D. Pette
AMPK activation increases uncoupling protein-3 expression and mitochondrial enzyme activities in rat muscle without fibre type transitions
J. Physiol., August 15, 2003; 551(1): 169 - 178.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
S. I. Itani, A. K. Saha, T. G. Kurowski, H. R. Coffin, K. Tornheim, and N. B. Ruderman
Glucose Autoregulates Its Uptake in Skeletal Muscle: Involvement of AMP-Activated Protein Kinase
Diabetes, July 1, 2003; 52(7): 1635 - 1640.
[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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J. Appl. Physiol.Home page
N. Jessen, R. Pold, E. S. Buhl, L. S. Jensen, O. Schmitz, and S. Lund
Effects of AICAR and exercise on insulin-stimulated glucose uptake, signaling, and GLUT-4 content in rat muscles
J Appl Physiol, April 1, 2003; 94(4): 1373 - 1379.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
S. L. McGee, K. F. Howlett, R. L. Starkie, D. Cameron-Smith, B. E. Kemp, and M. Hargreaves
Exercise Increases Nuclear AMPK {alpha}2 in Human Skeletal Muscle
Diabetes, April 1, 2003; 52(4): 926 - 928.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
K. Hojlund, K. Wrzesinski, P. M. Larsen, S. J. Fey, P. Roepstorff, A. Handberg, F. Dela, J. Vinten, J. G. McCormack, C. Reynet, et al.
Proteome Analysis Reveals Phosphorylation of ATP Synthase beta -Subunit in Human Skeletal Muscle and Proteins with Potential Roles in Type 2 Diabetes
J. Biol. Chem., March 14, 2003; 278(12): 10436 - 10442.
[Abstract] [Full Text] [PDF]


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J. Appl. Physiol.Home page
J. N. Nielsen, K. J. W. Mustard, D. A. Graham, H. Yu, C. S. MacDonald, H. Pilegaard, L. J. Goodyear, D. G. Hardie, E. A. Richter, and J. F. P. Wojtaszewski
5'-AMP-activated protein kinase activity and subunit expression in exercise-trained human skeletal muscle
J Appl Physiol, February 1, 2003; 94(2): 631 - 641.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
M. Yu, N. K Stepto, A. V Chibalin, L. G D Fryer, D. Carling, A. Krook, J. A Hawley, and J. R Zierath
Metabolic and mitogenic signal transduction in human skeletal muscle after intense cycling exercise
J. Physiol., January 15, 2003; 546(2): 327 - 335.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
T. Daniel and D. Carling
Functional Analysis of Mutations in the gamma 2 Subunit of AMP-activated Protein Kinase Associated with Cardiac Hypertrophy and Wolff-Parkinson-White Syndrome
J. Biol. Chem., December 20, 2002; 277(52): 51017 - 51024.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
H. Zong, J. M. Ren, L. H. Young, M. Pypaert, J. Mu, M. J. Birnbaum, and G. I. Shulman
AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation
PNAS, December 10, 2002; 99(25): 15983 - 15987.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
E. Tomas, T.-S. Tsao, A. K. Saha, H. E. Murrey, C. c. Zhang, S. I. Itani, H. F. Lodish, and N. B. Ruderman
Enhanced muscle fat oxidation and glucose transport by ACRP30 globular domain: Acetyl-CoA carboxylase inhibition and AMP-activated protein kinase activation
PNAS, December 10, 2002; 99(25): 16309 - 16313.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Endocrinol. Metab.Home page
J. Stoppani, A. L. Hildebrandt, K. Sakamoto, D. Cameron-Smith, L. J. Goodyear, and P. D. Neufer
AMP-activated protein kinase activates transcription of the UCP3 and HKII genes in rat skeletal muscle
Am J Physiol Endocrinol Metab, December 1, 2002; 283(6): E1239 - E1248.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Endocrinol. Metab.Home page
E. O. Ojuka, T. E. Jones, D.-H. Han, M. Chen, B. R. Wamhoff, M. Sturek, and J. O. Holloszy
Intermittent increases in cytosolic Ca2+ stimulate mitochondrial biogenesis in muscle cells
Am J Physiol Endocrinol Metab, November 1, 2002; 283(5): E1040 - E1045.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
M. A. Iglesias, J.-M. Ye, G. Frangioudakis, A. K. Saha, E. Tomas, N. B. Ruderman, G. J. Cooney, and E. W. Kraegen
AICAR Administration Causes an Apparent Enhancement of Muscle and Liver Insulin Action in Insulin-Resistant High-Fat-Fed Rats
Diabetes, October 1, 2002; 51(10): 2886 - 2894.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
B. R. Barnes, J. W. Ryder, T. L. Steiler, L. G.D. Fryer, D. Carling, and J. R. Zierath
Isoform-Specific Regulation of 5' AMP-Activated Protein Kinase in Skeletal Muscle From Obese Zucker (fa/fa) Rats in Response to Contraction
Diabetes, September 1, 2002; 51(9): 2703 - 2708.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
H. Park, V. K. Kaushik, S. Constant, M. Prentki, E. Przybytkowski, N. B. Ruderman, and A. K. Saha
Coordinate Regulation of Malonyl-CoA Decarboxylase, sn-Glycerol-3-phosphate Acyltransferase, and Acetyl-CoA Carboxylase by AMP-activated Protein Kinase in Rat Tissues in Response to Exercise
J. Biol. Chem., August 30, 2002; 277(36): 32571 - 32577.
[Abstract] [Full Text] [PDF]




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