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(Received for publication, December 24, 1996, and in revised form, February 27, 1997)
From the The concentration of malonyl-CoA, a negative
regulator of fatty acid oxidation, diminishes acutely in contracting
skeletal muscle. To determine how this occurs, the activity and
properties of acetyl-CoA carboxylase
Volume 272, Number 20,
Issue of May 16, 1997
pp. 13255-13261
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.
-AMP-activated Kinase in Skeletal Muscle
,
,
,
,
,
Department of Physiology and Diabetes and
Metabolism Unit, Evans Department of Medicine, Boston University
Medical Center, Boston, Massachusetts 02118, the
¶ Endocrine-Metabolism Division, Department of Medicine and
Biochemistry, Dartmouth Medical School, Hanover, New Hampshire 03756, and 
St. Vincent's Institute of Medical Research, 41 Victoria
Parade, Fitzroy, Victoria 3065, Australia
(ACC-), the skeletal muscle
isozyme that catalyzes malonyl-CoA formation, were examined in rat
gastrocnemius-soleus muscles at rest and during contractions induced by
electrical stimulation of the sciatic nerve. To avoid the problem of
contamination of the muscle extract by mitochondrial carboxylases, an
assay was developed in which ACC- was first purified by
immunoprecipitation with a monoclonal antibody. ACC- was
quantitatively recovered in the immunopellet and exhibited a high
sensitivity to citrate (12-fold activation) and a
Km for acetyl-CoA (120 µM) similar to
that reported for ACC- purified by other means. After 5 min of
contraction, ACC- activity was decreased by 90% despite an apparent
increase in the cytosolic concentration of citrate, a positive
regulator of ACC. SDS-polyacrylamide gel electrophoresis of both
homogenates and immunopellets from these muscles showed a decrease in
the electrophoretic mobility of ACC, suggesting that phosphorylation
could account for the decrease in ACC activity. In keeping with this
notion, citrate activation of ACC purified from contracting muscle was
markedly depressed. In addition, homogenization of the muscles in a
buffer free of phosphatase inhibitors and containing the phosphatase
activators glutamate and MgCl2 or treatment of
immunoprecipitated ACC- with purified protein phosphatase 2A
abolished the decreases in both ACC- activity and electrophoretic mobility caused by contraction. The rapid decrease in ACC- activity after the onset of contractions (50% by 20 s) and its slow
restoration to initial values during recovery (60-90 min) were
paralleled temporally by reciprocal changes in the activity of the 
2
but not the 1 isoform of 5
-AMP-activated protein kinase (AMPK). In
conclusion, the results suggest that the decrease in ACC activity during muscle contraction is caused by an increase in its
phosphorylation, most probably due, at least in part, to activation of
the 2 isoform of AMPK. They also suggest a dual mechanism for ACC
regulation in muscle in which inhibition by phosphorylation takes
precedence over activation by citrate. These alterations in ACC and
AMPK activity, by diminishing the concentration of malonyl-CoA, could be responsible for the increase in fatty acid oxidation observed in
skeletal muscle during exercise.
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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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J. Kim, R. S. Solis, E. B. Arias, and G. D. Cartee Postcontraction insulin sensitivity: relationship with contraction protocol, glycogen concentration, and 5' AMP-activated protein kinase phosphorylation J Appl Physiol, February 1, 2004; 96(2): 575 - 583. [Abstract] [Full Text] [PDF]
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 H. Yu, N. Fujii, M. F. Hirshman, J. M. Pomerleau, and L. J. Goodyear Cloning and characterization of mouse 5'-AMP-activated protein kinase {gamma}3 subunit Am J Physiol Cell Physiol, February 1, 2004; 286(2): C283 - C292. [Abstract] [Full Text]
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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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S. Perrini, J. Henriksson, J. R. Zierath, and U. Widegren Exercise-Induced Protein Kinase C Isoform-Specific Activation in Human Skeletal Muscle Diabetes, January 1, 2004; 53(1): 21 - 24. [Abstract] [Full Text] [PDF]
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D. G. Hardie Minireview: The AMP-Activated Protein Kinase Cascade: The Key Sensor of Cellular Energy Status Endocrinology, December 1, 2003; 144(12): 5179 - 5183. [Abstract] [Full Text] [PDF]
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 K. LEMIEUX, D. KONRAD, A. KLIP, and A. MARETTE The AMP-activated protein kinase activator AICAR does not induce GLUT4 translocation to transverse tubules but stimulates glucose uptake and p38 mitogen-activated protein kinases {alpha} and {beta} in skeletal muscle FASEB J, September 1, 2003; 17(12): 1658 - 1665. [Abstract] [Full Text] [PDF]
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Z.-P. Chen, T. J. Stephens, S. Murthy, B. J. Canny, M. Hargreaves, L. A. Witters, B. E. Kemp, and G. K. McConell Effect of Exercise Intensity on Skeletal Muscle AMPK Signaling in Humans Diabetes, September 1, 2003; 52(9): 2205 - 2212. [Abstract] [Full Text] [PDF]
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D. L. Coven, X. Hu, L. Cong, R. Bergeron, G. I. Shulman, D. G. Hardie, and L. H. Young Physiological role of AMP-activated protein kinase in the heart: graded activation during exercise Am J Physiol Endocrinol Metab, September 1, 2003; 285(3): E629 - E636. [Abstract] [Full Text] [PDF]
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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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S.-Y. Oh, S.-K. Park, J.-W. Kim, Y.-H. Ahn, S.-W. Park, and K.-S. Kim Acetyl-CoA Carboxylase {beta} Gene Is Regulated by Sterol Regulatory Element-binding Protein-1 in Liver J. Biol. Chem., August 1, 2003; 278(31): 28410 - 28417. [Abstract] [Full Text] [PDF]
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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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J. F. P. Wojtaszewski, C. MacDonald, J. N. Nielsen, Y. Hellsten, D. G. Hardie, B. E. Kemp, B. Kiens, and E. A. Richter Regulation of 5'AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle Am J Physiol Endocrinol Metab, April 1, 2003; 284(4): E813 - E822. [Abstract] [Full Text] [PDF]
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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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G. S. Olsen and B. F. Hansen AMP kinase activation ameliorates insulin resistance induced by free fatty acids in rat skeletal muscle Am J Physiol Endocrinol Metab, November 1, 2002; 283(5): E965 - E970. [Abstract] [Full Text] [PDF]
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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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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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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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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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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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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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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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H. Sakoda, T. Ogihara, M. Anai, M. Fujishiro, H. Ono, Y. Onishi, H. Katagiri, M. Abe, Y. Fukushima, N. Shojima, et al. Activation of AMPK is essential for AICAR-induced glucose uptake by skeletal muscle but not adipocytes Am J Physiol Endocrinol Metab, June 1, 2002; 282(6): E1239 - E1244. [Abstract] [Full Text] [PDF]
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H. Ai, J. Ihlemann, Y. Hellsten, H. P. M. M. Lauritzen, D. G. Hardie, H. Galbo, and T. Ploug Effect of fiber type and nutritional state on AICAR- and contraction-stimulated glucose transport in rat muscle Am J Physiol Endocrinol Metab, June 1, 2002; 282(6): E1291 - E1300. [Abstract] [Full Text] [PDF]
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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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S. N. Jakobsen, D. G. Hardie, N. Morrice, and H. E. Tornqvist 5'-AMP-activated Protein Kinase Phosphorylates IRS-1 on Ser-789 in Mouse C2C12 Myotubes in Response to 5-Aminoimidazole-4-carboxamide Riboside J. Biol. Chem., December 7, 2001; 276(50): 46912 - 46916. [Abstract] [Full Text] [PDF]
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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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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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E. A Richter, W. Derave, and J. F P Wojtaszewski Glucose, exercise and insulin: emerging concepts J. Physiol., September 1, 2001; 535(2): 313 - 322. [Abstract] [Full Text] [PDF]
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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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A. Kowluru, H.-Q. Chen, L. M. Modrick, and C. Stefanelli Activation of Acetyl-CoA Carboxylase by a Glutamate- and Magnesium-Sensitive Protein Phosphatase in the Islet {beta}-Cell Diabetes, July 1, 2001; 50(7): 1580 - 1587. [Abstract] [Full Text] [PDF]
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P. Peltoniemi, H. Yki-Järvinen, V. Oikonen, A. Oksanen, T. O. Takala, T. Rönnemaa, M. Erkinjuntti, M. J. Knuuti, and P. Nuutila Resistance to Exercise-Induced Increase in Glucose Uptake During Hyperinsulinemia in Insulin-Resistant Skeletal Muscle of Patients With Type 1 Diabetes Diabetes, June 1, 2001; 50(6): 1371 - 1377. [Abstract] [Full Text]
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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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N. Musi, T. Hayashi, N. Fujii, M. F. Hirshman, L. A. Witters, and L. J. Goodyear AMP-activated protein kinase activity and glucose uptake in rat skeletal muscle Am J Physiol Endocrinol Metab, May 1, 2001; 280(5): E677 - E684. [Abstract] [Full Text] [PDF]
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 L. Abu-Elheiga, M. M. Matzuk, K. A. H. Abo-Hashema, and S. J. Wakil Continuous Fatty Acid Oxidation and Reduced Fat Storage in Mice Lacking Acetyl-CoA Carboxylase 2 Science, March 30, 2001; 291(5513): 2613 - 2616. [Abstract] [Full Text]
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Y. Higaki, M. F. Hirshman, N. Fujii, and L. J. Goodyear Nitric Oxide Increases Glucose Uptake Through a Mechanism That Is Distinct From the Insulin and Contraction Pathways in Rat Skeletal Muscle Diabetes, February 1, 2001; 50(2): 241 - 247. [Abstract] [Full Text]
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