Resistance exercise increases AMPK activity and reduces 4E-BP1 phosphorylation and protein synthesis in human skeletal muscle

Journal of Physiology

Volumn 576, Issue 2, 2006, Pages 613-624

  Dreyer, Hans C ^a   Fujita, Satoshi ^b   Cadenas, Jerson G ^b   Chinkes, David L ^b   Volpi, Elena ^b   Rasmussen, Blake B ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA2; INITIATION FACTOR 4E BINDING PROTEIN 1; ISOTOPE; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHOTRANSFERASE; PROTEIN KINASE B; UNCLASSIFIED DRUG; AMP ACTIVATED PROTEIN KINASE ALPHA 2; S6 KINASE 1; TRANSCRIPTION FACTOR E2F;

ADULT; ARTICLE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; EXERCISE TOLERANCE; FEMALE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MALE; MUSCLE BIOPSY; MUSCLE BLOOD FLOW; MUSCLE METABOLISM; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STATISTICAL SIGNIFICANCE; TRANSLATION INITIATION; TRANSLATION REGULATION; VASTUS LATERALIS MUSCLE; CONTROLLED STUDY; ENZYME ACTIVATION; FRACTIONAL SYNTHETIC RATE; ISOTOPE LABELING; PROTEIN DEGRADATION; PROTEIN SYNTHESIS INHIBITION; RESISTANCE TRAINING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADULT; AMINO ACIDS; AMP-ACTIVATED PROTEIN KINASES; BIOPSY; EXERCISE; FEMALE; GLUCOSE; HUMANS; HYDROGEN-ION CONCENTRATION; LACTATES; MALE; MULTIENZYME COMPLEXES; MUSCLE PROTEINS; MUSCLE, SKELETAL; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; REGIONAL BLOOD FLOW; TOR SERINE-THREONINE KINASES; WEIGHT LIFTING;

EID: 33749351995     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.113175     Document Type: Article

References (58)

1. Anthony JC, Lang CH, Crozier SJ, Anthony TG, MacLean DA, Kimball SR & Jefferson LS (2002). Contribution of insulin to the translational control of protein synthesis in skeletal muscle by leucine. Am J Physiol Endocrinol Metab 282, E1092-E1101.
2. Atherton PJ, Babraj J, Smith K, Singh J, Rennie MJ & Wackerhage H (2005). Selective activation of AMPK-PGC-1alpha or PKB-TSC2-mTOR signaling can explain specific adaptive responses to endurance or resistance training-like electrical muscle stimulation. FASEB J 19, 786-788.
3. Baar K & Esser K (1999). Phosphorylation of p70 (S6k) correlates with increased skeletal muscle mass following resistance exercise. Am J Physiol 276, C120-C127.
4. Biolo G, Maggi SP, Williams BD, Tipton KD & Wolfe RR (1995). Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. Am J Physiol Endocrinol Metab 268, E514-E520.
5. Bolster DR, Crozier SJ, Kimball SR & Jefferson LS (2002). AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J Biol Chem 277, 23977-23980.
6. Bolster DR, Kubica N, Crozier SJ, Williamson DL, Farrell PA, Kimball SR & Jefferson LS (2003a). Immediate response of mammalian target of rapamycin (mTOR)-mediated signalling following acute resistance exercise in rat skeletal muscle. J Physiol 553, 213-220.
7. Browne GJ, Finn SG & Proud CG (2004). Stimulation of the AMP-activated protein kinase leads to activation of eukaryotic elongation factor 2 kinase and to its phosphorylation at a novel site, serine 398. J Biol Chem 279, 12220-12231.
8. Browne GJ & Proud CG (2002). Regulation of peptide-chain elongation in mammalian cells. Eur J Biochem 269, 5360-5368.
9. Bylund-Fellenius AC, Ojamaa KM, Flaim KE, Li JB, Wassner SJ & Jefferson LS (1984). Protein synthesis versus energy state in contracting muscles of perfused rat hindlimb. Am J Physiol Endocrinol Metab 246, E297-E305.
10. Calder AG, Anderson SE, Grant I, McNurlan MA & Garlick PJ (1992). The determination of low d5-phenylalanine enrichment (0.002-0.09 atom percent excess), after conversion to phenylethylamine, in relation to protein turnover studies by gas chromatography/electron ionization mass spectrometry. Rapid Commun Mass Spectrom 6, 421-424.
11. Carraro F, Stuart CA, Hartl WH, Rosenblatt J & Wolfe RR (1990). Effect of exercise and recovery on muscle protein synthesis in human subjects. Am J Physiol Endocrinol Metab 259, E470-E476.
12. Caso G & Garlick PJ (2005). Control of muscle protein kinetics by acid-base balance. Curr Opin Clin Nutr Metab Care 8, 73-76.
13. Caso G, Garlick BA, Casella GA, Sasvary D & Garlick PJ (2004). Acute metabolic acidosis inhibits muscle protein synthesis in rats. Am J Physiol Endocrinol Metab 287, E90-E96.
14. Caso G, Garlick BA, Casella GA, Sasvary D & Garlick PJ (2005). Response of protein synthesis to hypercapnia in rats: Independent effects of acidosis and hypothermia. Metabolism 54, 841-847.
15. Chen ZP, Stephens TJ, Murthy S, Canny BJ, Hargreaves M, Witters LA, Kemp BE & McConell GK (2003). Effect of exercise intensity on skeletal muscle AMPK signaling in humans. Diabetes 52, 2205-2212.
16. Cheng SW, Fryer LG, Carling D & Shepherd PR (2004). Thr2446 is a novel mammalian target of rapamycin (mTOR) phosphorylation site regulated by nutrient status. J Biol Chem 279, 15719-15722.
17. Coffey VG, Zhong Z, Shield A, Canny BJ, Chibalin AV, Zierath JR & Hawley JA (2006). Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans. FASEB J 20, 190-192.
18. Cuthbertson DJ, Babraj JA, Smith K, Wilkes E, Fedele MJ, Esser K & Rennie MJ (2006). Anabolic signalling and protein synthesis in human skeletal muscle after dynamic shortening or lengthening exercise. Am J Physiol Endocrinol Metab 290, E731-E738.
19. Davis TA & Karl IE (1986). Response of muscle protein turnover to insulin after acute exercise and training. Biochem J 240, 651-657.
20. Dohm GL, Kasperek GJ, Tapscott EB & Beecher GR (1980). Effect of exercise on synthesis and degradation of muscle protein. Biochem J 188, 255-262.
21. Durham WJ, Miller SL, Yeckel CW, Chinkes DL, Tipton KD, Rasmussen BB & Wolfe RR (2004). Leg glucose and protein metabolism during an acute bout of resistance exercise in humans. J Appl Physiol 97, 1379-1386.
22. Fujii N, Hayashi T, Hirshman MF, Smith JT, Habinowski SA, Kaijser L, Mu J, Ljungqvist O, Birnbaum MJ, Witters LA, Thorell A & Goodyear LJ (2000). Exercise induces isoform-specific increase in 5′AMP-activated protein kinase activity in human skeletal muscle. Biochem Biophys Res Commun 273, 1150-1155.
23. Hahn-Windgassen A, Nogueira V, Chen CC, Skeen JE, Sonenberg N & Hay N (2005). Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. J Biol Chem 280, 32081-32089.
24. Hardie DG (2005). New roles for the LKB1 → AMPK pathway. Curr Opin Cell Biol 17, 167-173.
25. Hardie DG & Carling D (1997). The AMP-activated protein kinase -fuel gauge of the mammalian cell?Eur J Biochem 246, 259-273.
26. Hardie DG, Salt IP & Davies SP (2000). Analysis of the role of the AMP-activated protein kinase in the response to cellular stress. Methods Mol Biol 99, 63-74.
27. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, Frenguelli BG & Hardie DG (2005). Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2, 9-19.
28. Horman S, Browne G, Krause U, Patel J, Vertommen D, Bertrand L, Lavoinne A, Hue L, Proud C & Rider M (2002). Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol 12, 1419-1423.
29. Inoki K, Zhu T & Guan KL (2003). TSC2 mediates cellular energy response to control cell growth and survival. Cell 115, 577-590.
30. Jorfeldt L & Wahren J (1971). Leg blood flow during exercise in man. Clin Sci 41, 459-473.
31. Karlsson HKR, Nilsson P-A, Nilsson J, Chibalin AV, Zierath JR & Blomstrand E (2004). Branched-chain amino acids increase p70S6K phosphorylation in human skeletal muscle after resistance exercise. Am J Physiol Endocrinol Metab 287, E1-E7.
32. Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H, Tempst P & Sabatini DM (2002). mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110, 163-175.
33. Kleger GR, Turgay M, Imoberdorf R, McNurlan MA, Garlick PJ & Ballmer PE (2001). Acute metabolic acidosis decreases muscle protein synthesis but not albumin synthesis in humans. Am J Kidney Dis 38, 1199-1207.
34. Koopman R, Zorenc AH, Gransier RJ, Cameron-Smith D & van Loon LJ (2006). Increase in S6K1 phosphorylation in human skeletal muscle following resistance exercise occurs mainly in type II muscle fibers. Am J Physiol Endocrinol Metab 290, E1245-E1252.
35. Long X, Lin Y, Ortiz-Vega S, Yonezawa K & Avruch J (2005). Rheb binds and regulates the mTOR kinase. Curr Biol 15, 702-713.
36. MacDougall JD, Gibala MJ, Tarnopolsky MA, MacDonald JR, Interisano SA & Yarasheski KE (1995). The time course for elevated muscle protein synthesis following heavy resistance exercise. Can J Appl Physiol 20, 480-486.
37. McConell GK, Lee-Young RS, Chen ZP, Stepto NK, Huynh NN, Stephens TJ, Canny BJ & Kemp BE (2005). Short-term exercise training in humans reduces AMPK signalling during prolonged exercise independent of muscle glycogen. J Physiol 568, 665-676.
38. Phillips SM, Tipton KD, Aarsland A, Wolf SE & Wolfe RR (1997). Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol Endocrinol Metab 273, E99-E107.
39. Rasmussen BB, Hancock CR & Winder WW (1998). Postexercise recovery of skeletal muscle malonyl-CoA, acetyl-CoA carboxylase, and AMP-activated protein kinase. J Appl Physiol 85, 1629-1634.
40. Rasmussen BB & Phillips SM (2003). Contractile and nutritional regulation of human muscle growth. Exerc Sport Sci Rev 31, 127-131.
41. Rasmussen BB, Tipton KD, Miller SL, Wolf SE & Wolfe RR (2000). An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise. J Appl Physiol 88, 386-392.
42. Rasmussen BB & Winder WW (1997). Effect of exercise intensity on skeletal muscle malonyl-CoA and acetyl-CoA carboxylase. J Appl Physiol 83, 1104-1109.
43. Rennie MJ, Edwards RH, Krywawych S, Davies CT, Halliday D, Waterlow JC & Millward DJ (1981). Effect of exercise on protein turnover in man. Clin Sci (Lond) 61, 627-639.
44. Roepstorff C, Halberg N, Hillig T, Saha AK, Ruderman NB, Wojtaszewski JF, Richter EA & Kiens B (2005). Malonyl-CoA and carnitine in regulation of fat oxidation in human skeletal muscle during exercise. Am J Physiol Endocrinol Metab 288, E133-E142.
45. Rose AJ, Broholm C, Kiillerich K, Finn SG, Proud CG, Rider MH, Richter EA & Kiens B (2005). Exercise rapidly increases eukaryotic elongation factor 2 phosphorylation in skeletal muscle of men. J Physiol 569, 223-228.
46. Sarbassov DD, Ali SM & Sabatini DM (2005). Growing roles for the mTOR pathway. Curr Opin Cell Biol 17, 596-603.
47. Sarbassov DD & Sabatini DM (2005). Redox regulation of the nutrient-sensitive raptor-mTOR pathway and complex. J Biol Chem 25, 39505-39509.
48. Smith EM, Finn SG, Tee AR, Browne GJ & Proud CG (2005). The tuberous sclerosis protein TSC2 is not required for the regulation of the mammalian target of rapamycin by amino acids and certain cellular stresses. J Biol Chem 280, 18717-18727.
49. Stephens TJ, Chen ZP, Canny BJ, Michell BJ, Kemp BE & McConell GK (2002). Progressive increase in human skeletal muscle AMPKalpha2 activity and ACC phosphorylation during exercise. Am J Physiol Endocrinol Metab 282, 688-694.
50. Tee AR & Proud CG (2002). Caspase cleavage of initiation factor 4E-binding protein 1 yields a dominant inhibitor of cap-dependent translation and reveals a novel regulatory motif. Mol Cell Biol 22, 1674-1683.
51. Wang X, Beugnet A, Murakami M, Yamanaka S & Proud CG (2005). Distinct signaling events downstream of mTOR cooperate to mediate the effects of amino acids and insulin on initiation factor 4E-binding proteins. Mol Cell Biol 25, 2558-2572.
52. Wang X, Li W, Williams M, Terada N, Alessi DR & Proud CG (2001). Regulation of elongation factor 2 kinase by p90 RSK1 and p70, S6 kinase. EMBO J 20, 4370-4379.
53. Winder WW & Hardie DG (1996). Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am J Physiol Endocrinol Metab 270, E299-E304.
54. Winder WW & Hardie DG (1999). AMP-activated protein kinase, a metabolic master switch: Possible roles in type 2 diabetes. Am J Physiol Endocrinol Metab 277, E1-E10.
55. Wojtaszewski JF, MacDonald C, Nielsen JN, Hellsten Y, Hardie DG, Kemp BE, Kiens B & Richter EA (2003). Regulation of 5′AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle. Am J Physiol Endocrinol Metab 284, E813-E822.
56. Wolfe RR & Chinkes DL (2005). Isotope Tracers in Metabolic Research: Principles and Practice of Kinetic Analysis, 2nd edn. Wiley-Liss, Hoboken, New Jersey.
57. 2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2, 21-33.
58. Yu M, Stepto NK, Chibalin AV, Fryer LG, Carling D, Krook A, Hawley JA & Zierath JR (2003). Metabolic and mitogenic signal transduction in human skeletal muscle after intense cycling exercise. J Physiol 546, 327-335.