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J Appl Physiol 87: 1990-1995, 1999;
8750-7587/99 $5.00
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Vol. 87, Issue 5, 1990-1995, November 1999

Chronic activation of 5'-AMP-activated protein kinase increases GLUT-4, hexokinase, and glycogen in muscle

B. F. Holmes, E. J. Kurth-Kraczek, and W. W. Winder

Department of Zoology, Brigham Young University, Provo, Utah 84602

This study was designed to determine whether chronic chemical activation of AMP-activated protein kinase (AMPK) would increase glucose transporter GLUT-4 and hexokinase in muscles similarly to periodic elevation of AMPK that accompanies endurance exercise training. The adenosine analog, 5-aminoimidazole-4-carboxamide ribonucleoside (AICAR), has previously been shown to be taken up by cells and phosphorylated to form a compound (5-aminoimidazole-4-carboxamide ribonucleotide) that mimics the effect of AMP on AMPK. A single injection of AICAR resulted in a marked increase in AMPK in epitrochlearis and gastrocnemius/plantaris muscles 60 min later. When rats were injected with AICAR (1 mg/g body wt) for 5 days in succession and were killed 1 day after the last injection, GLUT-4 was increased by 100% in epitrochlearis muscle and by 60% in gastrocnemius muscle in response to AICAR. Hexokinase was also increased ~2.5-fold in the gastrocnemius/plantaris. Gastrocnemius glycogen content was twofold higher in AICAR-treated rats than in controls. Chronic chemical activation of AMPK, therefore, results in increases in GLUT-4 protein, hexokinase activity, and glycogen, similarly to those induced by endurance training.

acetyl-CoA carboxylase; aminoimidazole-4-carboxamide-riboside; endurance training; fatty acid oxidation; glucose transport; malonyl-CoA; muscle contraction


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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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 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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 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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 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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 CirculationHome page
M. Arad, I. P. Moskowitz, V. V. Patel, F. Ahmad, A. R. Perez-Atayde, D. B. Sawyer, M. Walter, G. H. Li, P. G. Burgon, C. T. Maguire, et al.
Transgenic Mice Overexpressing Mutant PRKAG2 Define the Cause of Wolff-Parkinson-White Syndrome in Glycogen Storage Cardiomyopathy
Circulation, June 10, 2003; 107(22): 2850 - 2856.
[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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 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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 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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 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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 Mayo Clin Proc.Home page
C. Seidman
Genetic Causes of Inherited Cardiac Hypertrophy: Robert L. Frye Lecture
Mayo Clin. Proc., December 1, 2002; 77(12): 1315 - 1319.
[Abstract] [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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 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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 J. Appl. Physiol.Home page
E. Tomas, A. Zorzano, and N. B. Ruderman
Exercise Effects on Muscle Insulin Signaling and Action: Exercise and insulin signaling: a historical perspective
J Appl Physiol, August 1, 2002; 93(2): 765 - 772.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
J. R. Zierath
Exercise Effects of Muscle Insulin Signaling and Action: Invited Review: Exercise training-induced changes in insulin signaling in skeletal muscle
J Appl Physiol, August 1, 2002; 93(2): 773 - 781.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
G. L. Dohm
Exercise Effects on Muscle Insulin Signaling and Action: Invited Review: Regulation of skeletal muscle GLUT-4 expression by exercise
J Appl Physiol, August 1, 2002; 93(2): 782 - 787.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
L. G. D. Fryer, A. Parbu-Patel, and D. Carling
The Anti-diabetic Drugs Rosiglitazone and Metformin Stimulate AMP-activated Protein Kinase through Distinct Signaling Pathways
J. Biol. Chem., July 5, 2002; 277(28): 25226 - 25232.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
F. W. Booth, M. V. Chakravarthy, S. E. Gordon, and E. E. Spangenburg
Waging war on physical inactivity: using modern molecular ammunition against an ancient enemy
J Appl Physiol, July 1, 2002; 93(1): 3 - 30.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
K. Sakamoto and L. J. Goodyear
Exercise Effects on Muscle Insulin Signaling and Action: Invited Review: Intracellular signaling in contracting skeletal muscle
J Appl Physiol, July 1, 2002; 93(1): 369 - 383.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
N. Musi, M. F. Hirshman, J. Nygren, M. Svanfeldt, P. Bavenholm, O. Rooyackers, G. Zhou, J. M. Williamson, O. Ljunqvist, S. Efendic, et al.
Metformin Increases AMP-Activated Protein Kinase Activity in Skeletal Muscle of Subjects With Type 2 Diabetes
Diabetes, July 1, 2002; 51(7): 2074 - 2081.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
E. S. Buhl, N. Jessen, R. Pold, T. Ledet, A. Flyvbjerg, S. B. Pedersen, O. Pedersen, O. Schmitz, and S. Lund
Long-Term AICAR Administration Reduces Metabolic Disturbances and Lowers Blood Pressure in Rats Displaying Features of the Insulin Resistance Syndrome
Diabetes, July 1, 2002; 51(7): 2199 - 2206.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
P. E. Durante, K. J. Mustard, S.-H. Park, W. W. Winder, and D. G. Hardie
Effects of endurance training on activity and expression of AMP-activated protein kinase isoforms in rat muscles
Am J Physiol Endocrinol Metab, July 1, 2002; 283(1): E178 - E186.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. R. Bolster, S. J. Crozier, S. R. Kimball, and L. S. Jefferson
AMP-activated Protein Kinase Suppresses Protein Synthesis in Rat Skeletal Muscle through Down-regulated Mammalian Target of Rapamycin (mTOR) Signaling
J. Biol. Chem., June 28, 2002; 277(27): 23977 - 23980.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
W. G. Aschenbach, M. F. Hirshman, N. Fujii, K. Sakamoto, K. F. Howlett, and L. J. Goodyear
Effect of AICAR Treatment on Glycogen Metabolism in Skeletal Muscle
Diabetes, March 1, 2002; 51(3): 567 - 573.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
J. F.P. Wojtaszewski, S. B. Jorgensen, Y. Hellsten, D. G. Hardie, and E. A. Richter
Glycogen-Dependent Effects of 5-Aminoimidazole-4-Carboxamide (AICA)-Riboside on AMP-Activated Protein Kinase and Glycogen Synthase Activities in RatSkeletal Muscle
Diabetes, February 1, 2002; 51(2): 284 - 292.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
J. S. Fisher, J. Gao, D.-H. Han, J. O. Holloszy, and L. A. Nolte
Activation of AMP kinase enhances sensitivity of muscle glucose transport to insulin
Am J Physiol Endocrinol Metab, January 1, 2002; 282(1): E18 - E23.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
S. R. Paulsen, D. S. Rubink, and W. W. Winder
AMP-activated protein kinase activation prevents denervation-induced decline in gastrocnemius GLUT-4
J Appl Physiol, November 1, 2001; 91(5): 2102 - 2108.
[Abstract] [Full Text] [PDF]

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 GeneticsHome page
D. Ciobanu, J. Bastiaansen, M. Malek, J. Helm, J. Woollard, G. Plastow, and M. Rothschild
Evidence for New Alleles in the Protein Kinase Adenosine Monophosphate-Activated {gamma}3-Subunit Gene Associated With Low Glycogen Content in Pig Skeletal Muscle and Improved Meat Quality
Genetics, November 1, 2001; 159(3): 1151 - 1162.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
W. W. Winder
Energy-sensing and signaling by AMP-activated protein kinase in skeletal muscle
J Appl Physiol, September 1, 2001; 91(3): 1017 - 1028.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
D. Zheng, P. S. MacLean, S. C. Pohnert, J. B. Knight, A. L. Olson, W. W. Winder, and G. L. Dohm
Regulation of muscle GLUT-4 transcription by AMP-activated protein kinase
J Appl Physiol, September 1, 2001; 91(3): 1073 - 1083.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
V. K. Kaushik, M. E. Young, D. J. Dean, T. G. Kurowski, A. K. Saha, and N. B. Ruderman
Regulation of fatty acid oxidation and glucose metabolism in rat soleus muscle: effects of AICAR
Am J Physiol Endocrinol Metab, August 1, 2001; 281(2): E335 - E340.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
S. Terada, T. Yokozeki, K. Kawanaka, K. Ogawa, M. Higuchi, O. Ezaki, and I. Tabata
Effects of high-intensity swimming training on GLUT-4 and glucose transport activity in rat skeletal muscle
J Appl Physiol, June 1, 2001; 90(6): 2019 - 2024.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
N. Musi, N. Fujii, M. F. Hirshman, I. Ekberg, S. Fröberg, O. Ljungqvist, A. Thorell, and L. J. Goodyear
AMP-Activated Protein Kinase (AMPK) Is Activated in Muscle of Subjects With Type 2 Diabetes During Exercise
Diabetes, May 1, 2001; 50(5): 921 - 927.
[Abstract] [Full Text]


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