5′ AMP activated protein kinase expression in human skeletal muscle: Effects of strength training and type 2 diabetes

Journal of Physiology

Volumn 564, Issue 2, 2005, Pages 563-573

  Wojtaszewski, Jørgen F P ^a   Birk, Jesper B ^a   Frøsig, Christian ^a   Holten, Mads ^b   Pilegaard, Henriette ^c   Dela, Flemming ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ISOENZYME; MESSENGER RNA; 5' AMP ACTIVATED PROTEIN KINASE; 5'-AMP-ACTIVATED PROTEIN KINASE; MULTIENZYME COMPLEX; PROTEIN SERINE THREONINE KINASE; PROTEIN SUBUNIT; AMLODIPINE; CERIVASTATIN; GLIBENCLAMIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA2; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE BETA1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE BETA2; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE GAMMA1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE GAMMA2A; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE GAMMA2B; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE GAMMA3; METFORMIN; TOLBUTAMIDE; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG TARGETING; ENERGY BALANCE; ENZYME ACTIVITY; ENZYME SUBUNIT; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IMMUNOPRECIPITATION; INSULIN SENSITIVITY; LEG MUSCLE; MUSCLE BIOPSY; MUSCLE EXERCISE; MUSCLE METABOLISM; MUSCLE STRENGTH; NON INSULIN DEPENDENT DIABETES MELLITUS; NORMAL HUMAN; PHYSICAL STRESS; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; SKELETAL MUSCLE; TRAINING; BIOSYNTHESIS; COMPARATIVE STUDY; ENZYMOLOGY; EXERCISE; GENE EXPRESSION REGULATION; GENETICS; MIDDLE AGED; PHYSIOLOGY; ADULT; DIET THERAPY; MUSCLE TRAINING; THERAPY EFFECT;

DIABETES MELLITUS, TYPE 2; EXERCISE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; ISOENZYMES; MIDDLE AGED; MULTIENZYME COMPLEXES; MUSCLE, SKELETAL; PROTEIN SUBUNITS; PROTEIN-SERINE-THREONINE KINASES;

EID: 17844400342     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2005.082669     Document Type: Article

References (49)

1. Arad M, Benson DW, Perez-Atayde AR, McKenna WJ, Sparks EA, Kanter RJ, McGarry K, Seidman JG & Seidman CE (2002). Constitutively active AMP kinase mutations cause glycogen storage disease mimicking hypertrophic cardiomyopathy. J Clin Invest 109, 357-362.
2. Barnes BR, Marklund S, Steiler TL, Walter M, Hjalm G, Amarger V et al. (2004). The AMPK-gamma 3 isoform has a key role for carbohydrate and lipid metabolism in glycolytic skeletal muscle. J Biol Chem 279, 38441-38447.
3. Bergeron R, Ren JM, Cadman KS, Moore IK, Perret P, Pypaert M, Young LH, Semenkovich CF & Shulman GI (2001). Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am J Physiol Endocrinol Metab 281, E1340-E1346.
4. Buhl ES, Jessen N, Schmitz O, Pedersen SB, Pedersen O, Holman GD & Lund S (2001). Chronic treatment with 5-aminoimidazole-4-carboxamide-1-beta-d-ribofuranoside increases insulin-stimulated glucose uptake and Glut4 translocation in rat skeletal muscles in a fiber type specific manner. Diabetes 49, 12-17.
5. Chen Z, Heierhorst J, Mann RJ, Mitchelhill KI, Michell BJ, Witters LA, Lynch GS, Kemp BE & Stapleton D (1999). Expression of the AMP-activated protein kinase beta1 and beta2 subunits in skeletal muscle. FEBS Lett 460, 343-348.
6. Chen ZP, McConell GK, Michell BJ, Snow RJ, Canny BJ & Kemp BE (2000). AMPK signaling in contracting human skeletal muscle: acetyl-CoA carboxylase and NO synthase phosphorylation. Am J Physiol Endocrinol Metab 279, E1202-E1206.
7. Cheung CF, Salt IP, Davies A, Hardie DG & Carling D (2000). Characterization of AMP-activated protein kinase gamma subunit isoforms and their role in AMP binding. Biochem J 346, 659-669.
8. Chomczynski P & Sacchi N (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162, 156-159.
9. Dela F, Handberg A, Mikines KJ, Vinten J & Galbo H (1993). GLUT 4 and insulin receptor binding and kinase activity in trained human muscle. J Physiol 469, 615-624.
10. Dela F, Larsen JJ, Mikines KJ, Ploug T, Petersen LN & Galbo H (1995). Insulin stimulated muscle glucose clearance in patients with NIDDM. Diabetes 44, 1010-1020.
11. Dela F, Mikines KJ, Sonne B & Galbo H (1994). Effect of training on interaction between insulin and exercise in human muscle. J Appl Physiol 76, 2386-2393.
12. Dela F, Mikines KJ, von Linstow M, Secher NH & Galbo H (1992). Effect of training on insulin-mediated glucose uptake in human muscle. Am J Physiol 263, E1134-E1143.
13. Durante PE, Mustard KJ, Park SH, Winder WW & Hardie DG (2002). Effects of endurance training on activity and expression of AMP-activated protein kinase isoforms in rat muscles. Am J Physiol Endocrinol Metab 283, E178-E186.
14. Fisher JS, Gao J, Han DH, Holloszy JO & Nolte LA (2002). Activation of AMP kinase enhances sensitivity of muscle glucose transport to insulin. Am J Physiol Endocrinol Metab 282, E18-E23.
15. Frosig C, Jorgensen SB, Hardie DG, Richter EA & Wojtaszewski JF (2004). 5′-AMP-activated protein kinase activity and protein expression are regulated by endurance training in human skeletal muscle. Am J Physiol Endocrinol Metab 286, E411-E417.
16. Fujii N, Hayashi T, Hirshman MF, Smith TJ, Habinowski SA, Kaijser L et al. (2000). Exercise induces isoform specific increase in 5′AMP-activated protein kinase activity in human skeletal muscle. Biochem Biophys Res Commun 273, 1150-1155.
17. Hayashi T, Hirshman MF, Fujii N, Habinowski SA, Witters LA & Goodyear LJ (2000). Metabolic stress and altered glucose transport. Diabetes 49, 527-531.
18. Høojlund K, Mustard KJ, Staehr P, Hardie DG, Beck-Nielsen H, Richter EA & Wojtaszewski JF (2004). AMPK activity and isoform protein expression are similar in muscle of obese subjects with and without type 2 diabetes. Am J Physiol Endocrinol Metab 286, E239-E244.
19. Høojlund K, Mustard KJ, Stæhr P, Hardie DG, Beck-Nielsen H, Richter EA & Wojtaszewski JFP (2003). Expression of AMPK α,β,γ-isoforms and effect of insulin on AMPK activity in skeletal muscle from obese type 2 diabetic subjects. Am J Physiol Endocrinol Metab 286, E239-E244.
20. Holmes BF, Kurth-Kraczek EJ & Winder WW (1999). Chronic activation of 5′-AMP-activated protein kinase increases GLUT-4, hexokinase, and glycogen in muscle. J Appl Physiol 87, 1990-1995.
21. Holten MK, Zacho M, Gaster M, Juel C, Wojtaszewski JF & Dela F (2004). Strength training increases insulin-mediated glucose uptake, GLUT4 content, and insulin signaling in skeletal muscle in patients with type 2 diabetes. Diabetes 53, 294-305.
22. Iglesias MA, Ye JM, Frangioudakis G, Saha AK, Tomas E, Ruderman NB, Cooney GJ & Kraegen EW (2002). AICAR administration causes an apparent enhancement of muscle and liver insulin action in insulin-resistant high-fat-fed rats. Diabetes 51, 2886-2894.
23. Jessen N, Pold R, Buhl ES, Jensen LS, Schmitz O & Lund S (2003). Effects of AICAR and exercise on insulin-stimulated glucose uptake, signaling, and GLUT-4 content in rat muscles. J Appl Physiol 94, 1373-1379.
24. Jøorgensen SB, Viollet B, Andreelli F, Frosig C, Birk JB, Schjerling P, Vaulont S, Richter EA & Wojtaszewski JF (2004). Knockout of the alpha2 but not alpha1 5′-AMP-activated protein kinase isoform abolishes 5-aminoimidazole-4-carboxamide-1-beta-4-ribofuranoside but not contraction-induced glucose uptake in skeletal muscle. J Biol Chem 279, 1070-1079.
25. Koistinen HA, Galuska D, Chibalin AV, Yang J, Zierath JR, Holman GD & Wallberg-Henriksson H (2003). 5-amino-imidazole carboxamide riboside increases glucose transport and cell-surface GLUT4 content in skeletal muscle from subjects with type 2 diabetes. Diabetes 52 1066-1072.
26. Langfort J, Viese M, Ploug T & Dela F (2003). Time course of GLUT4 and AMPK protein expression in human skeletal muscle during one month of physical training. Scand J Med Sports 13, 169-174.
27. Lowry OH & Passonneau JV (1972). A Flexible System of Enzymatic Analysis. Academic Press, Inc, London.
28. Mahlapuu M, Johansson C, Lindgren K, Hjalm G, Barnes BR, Krook A, Zierath JR, Andersson L & Marklund S (2004). Expression profiling of the gamma-subunit isoforms of AMP-activated protein kinase suggests a major role for gamma3 in white skeletal muscle. Am J Physiol Endocrinol Metab 286, E194-E200.
29. Markuns JF, Wojtaszewski JFP & Goodyear LJ (1999). Insulin and exercise decrease glycogen synthase kinase-3 activity by different mechanisms in rat skeletal muscle. J Biol Chem 274, 24896-24900.
30. Milan D, Jeon JT, Looft C, Amarger V, Robic A, Thelander M et al. (2000). A mutation in PRKAG3 associated with excess glycogen content in pig skeletal muscle. Science 288, 1248-1251.
31. Mu J, Barton ER & Birnbaum MJ (2003). Selective suppression of AMP-activated protein kinase in skeletal muscle: update on 'lazy mice'. Biochem Soc Trans 31, 236-241.
32. Musi N, Fujii N, Hirshman MF, Ekberg I, Fröberg S, Ljungqvist O, Thorell A & Goodyear LJ (2001). AMP activated protein kinase is activated in muscle of subjects with type 2 diabetes during exercise. Diabetes 50, 921-927.
33. Musi N, Hirshman MF, Nygren J, Svanfeldt M, Bavenholm P, Rooyackers O et al. (2002). Metformin increases AMP-activated protein kinase activity in skeletal muscle of subjects with type 2 diabetes. Diabetes 51, 2074-2081.
34. Nielsen JN, Mustard KJ, Graham DAYuH, MacDonald CS, Pilegaard H, Goodyear LJ, Hardie DG, Richter EA & Wojtaszewski JF (2003). 5′-AMP-activated protein kinase activity and subunit expression in exercise-trained human skeletal muscle. J Appl Physiol 94, 631-641.
35. Pilegaard H, Ordway GA, Saltin B & Neufer PD (2000). Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 279 E806-E814.
36. Pilegaard H, Saltin B & Neufer PD (2003). Effect of short-term fasting and refeeding on transcriptional regulation of metabolic genes in human skeletal muscle. Diabetes 52, 657-662.
37. Stapleton D, Gao G, Michell BJ, Widmer J, Mitchelhill K, Teh T, House CM, Witters LA & Kemp BE (1994). Mammalian 5′-AMP-activated protein kinase non-catalytic subunits are homologs of proteins that interact with yeast Snf1 protein kinase. J Biol Chem 269, 29343-29346.
38. Stapleton D, Mitchelhill KI, Gao G, Widmer J, Michell BJ, Teh T, House CM, Fernandez CS, Cox T, Witters LA & Kemp BE (1996). Mammalian AMP-activated protein kinase subfamily. J Biol Chem 271, 611-614.
39. Stapleton D, Woollatt E, Mitchelhill KI, Nicholl JK, Fernandez CS, Michell BJ, Witters LA, Power DA, Sutherland GR & Kemp BE (1997). AMP-activated protein kinase isoenzyme family: subunit structure and chromosomal location. FEBS Lett 409, 452-456.
40. Steinberg GR, Smith AC, Van Denderen BJ, Chen Z, Murthy S, Campbell DJ, Heigenhauser GJ, Dyck DJ & Kemp BE (2004). AMP-activated protein kinase is not down-regulated in human skeletal muscle of obese females. J Clin Endocrinol Metab 89, 4575-4580.
41. Thornton C, Snowden MA & Carling D (1998). Identification of a novel AMP-activated protein kinase beta subunit isoform that is highly expressed in skeletal muscle. J Biol Chem 273, 12443-12450.
42. Viollet B, Andreelli F, Jorgensen SB, Perrin C, Geloen A, Flamez D et al. (2003). The AMP-activated protein kinase alpha2 catalytic subunit controls whole-body insulin sensitivity. J Clin Invest 111, 91-98.
43. Winder WW & Hardie DG (1996). Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am J Physiol 270, E299-E304.
44. Winder WW & Hardie DG (1999). AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes. Am J Physiol 277, E1-E10.
45. Wojtaszewski JFP, Nielsen P, Hansen BF, Richter EA & Kiens B (2000). Isoform specific and exercise intensity dependent activation of 5′AMP-activated protein kinase in human skeletal muscle. J Physiol 528, 221-226.
46. Woods A, Cheung PC, Smith FC, Davison MD, Scott J, Beri RK & Carling D (1996a). Characterization of AMP-activated protein kinase beta and gamma subunits. Assembly of the heterotrimeric complex in vitro. J Biol Chem 271, 10282-10290.
47. Woods A, Salt I, Scott J, Hardie DG & Carling D (1996b . The alpha1 and alpha2 isoforms of the AMP-activated protein kinase have similar activities in rat liver but exhibit differences in substrate specificity in vitro. FEBS Lett 397, 347-351.
48. Yu H, Fujii N, Hirshman MF, Pomerleau JM & Goodyear LJ (2004). Cloning and characterization of mouse 5′-AMP-activated protein kinase gamma3 subunit. Am J Physiol Cell Physiol 286, C283-C292.
49. Zong H, Ren JM, Young LH, Pypaert M, Mu J, Birnbaum MJ & Shulman GI (2002). AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci U S A 99, 15983-15987.