Oral glucose ingestion attenuates exercise-induced activation of 5′-AMP-activated protein kinase in human skeletal muscle

Biochemical and Biophysical Research Communications

Volumn 342, Issue 3, 2006, Pages 949-955

  Akerstrom, Thorbjorn C A ^a   Birk, Jesper B ^a   Klein, Ditte K ^a   Erikstrup, Christian ^a   Plomgaard, Peter ^a   Pedersen, Bente Klarlund ^a   Wojtaszewski, Jørgen F P ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

AMPK; Exercise; Glucose; Skeletal muscle

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADENOSINE PHOSPHATE; FATTY ACID; GLUCOSE; GLYCEROL; GLYCOGEN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE;

ADULT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; EXERCISE; GLUCOSE BLOOD LEVEL; GLUCOSE INTAKE; GLYCOGEN MUSCLE LEVEL; HUMAN; KNEE FUNCTION; MALE; MUSCLE BIOPSY; NORMAL HUMAN; OXIDATION; PHOSPHORYLATION; PRIORITY JOURNAL; RANDOMIZATION; SKELETAL MUSCLE; VASTUS LATERALIS MUSCLE; WORKLOAD;

ADMINISTRATION, ORAL; ADULT; ENZYME ACTIVATION; EXERCISE; GLUCOSE; GLYCOGEN; HUMANS; MALE; MULTIENZYME COMPLEXES; MUSCLE, SKELETAL; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; QUADRICEPS MUSCLE; TIME FACTORS;

EID: 33644635526     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.02.057     Document Type: Article

References (56)

1. P. Andersen, and B. Saltin Maximal perfusion of skeletal muscle in man J. Physiol. 366 1985 233 249
2. C. Beauloye, A.S. Marsin, L. Bertrand, U. Krause, D.G. Hardie, J.L. Vanoverschelde, and L. Hue Insulin antagonizes AMP-activated protein kinase activation by ischemia or anoxia in rat hearts, without affecting total adenine nucleotides FEBS Lett. 505 2001 348 352
3. J. Bergstrom Percutaneous needle biopsy of skeletal muscle in physiological and clinical research Scand. J. Clin. Lab. Invest. 35 1975 609 616
4. D. Carling The AMP-activated protein kinase cascade-a unifying system for energy control Trends Biochem. Sci. 29 2004 18 24
5. 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 52 2003 2205 2212
6. A.R. Coggan, and E.F. Coyle Carbohydrate ingestion during prolonged exercise: effects on metabolism and performance Exerc. Sport Sci. Rev. 19 1991 1 40
7. E.F. Coyle, A.R. Coggan, M.K. Hemmert, and J.L. Ivy Muscle glycogen utilization during prolonged strenuous exercise when fed carbohydrate J. Appl. Physiol. 61 1986 165 172
8. K. De Bock, E.A. Richter, A.P. Russell, B.O. Eijnde, W. Derave, M. Ramaekers, E. Koninckx, B. Leger, J. Verhaeghe, and P. Hespel Exercise in the fasted state facilitates fibre type-specific intramyocellular lipid breakdown and stimulates glycogen resynthesis in humans J. Physiol. 564 2005 649 660
9. D. Dean, J.R. Daugaard, M.E. Young, A. Saha, D. Vavvas, S. Asp, B. Kiens, K.H. Kim, L. Witters, E.A. Richter, and N. Ruderman Exercise diminishes the activity of acetyl-CoA carboxylase in human muscle Diabetes 49 2000 1295 1300
10. W. Derave, H. Ai, J. Ihlemann, L.A. Witters, S. Kristiansen, E.A. Richter, and T. Ploug Dissociation of AMP-activated protein kinase activation and glucose transport in contracting slow-twitch muscle Diabetes 49 2000 1281 1287
11. D.B. Dill, and D.L. Costill Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration J. Appl. Physiol. 37 1974 247 248
12. C. Duan, and W.W. Winder Nerve stimulation decreases malonyl-CoA in skeletal muscle J. Appl. Physiol. 72 1992 901 904
13. N. Fujii, T. Hayashi, M.F. Hirshman, J.T. Smith, S.A. Habinowski, L. Kaijser, J. Mu, O. Ljungqvist, M.J. Birnbaum, L.A. Witters, A. Thorell, and L.J. Goodyear Exercise induces isoform-specific increase in 5′AMP-activated protein kinase activity in human skeletal muscle Biochem. Biophys. Res. Commun. 273 2000 1150 1155
14. D.G. Hardie AMP-activated protein kinase: a key system mediating metabolic responses to exercise Med. Sci. Sports Exerc. 36 2004 28 34
15. D.G. Hardie, D. Carling, and M. Carlson The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu. Rev. Biochem. 67 1998 821 855
16. M. Hargreaves Interactions between muscle glycogen and blood glucose during exercise Exerc. Sport Sci. Rev. 25 1997 21 39
17. M. Hargreaves, G. McConell, and J. Proietto Influence of muscle glycogen on glycogenolysis and glucose uptake during exercise in humans J. Appl. Physiol. 78 1995 288 292
18. K. Hojlund, K.J. Mustard, P. Staehr, D.G. Hardie, H. Beck-Nielsen, E.A. Richter, and J.F. Wojtaszewski 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 2004 E239 E244
19. E.R. Hudson, D.A. Pan, J. James, J.M. Lucocq, S.A. Hawley, K.A. Green, O. Baba, T. Terashima, and D.G. Hardie A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias Curr. Biol. 13 2003 861 866
20. 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 52 2003 1635 1640
21. A.E. Jeukendrup Regulation of fat metabolism in skeletal muscle Ann. NY Acad. Sci. 967 2002 217 235
22. A.E. Jeukendrup, A. Raben, A. Gijsen, J.H. Stegen, F. Brouns, W.H. Saris, and A.J. Wagenmakers Glucose kinetics during prolonged exercise in highly trained human subjects: effect of glucose ingestion J. Physiol. 515 Pt. 2 1999 579 589
23. A.E. Jeukendrup, A.J. Wagenmakers, J.H. Stegen, A.P. Gijsen, F. Brouns, and W.H. Saris Carbohydrate ingestion can completely suppress endogenous glucose production during exercise Am. J. Physiol. 276 1999 E672 E683
24. B.B. Kahn, T. Alquier, D. Carling, and D.G. Hardie AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism Cell Metab. 1 2005 15 25
25. G.K. McConell, R.S. Lee-Young, Z.P. Chen, N.K. Stepto, N.N. Huynh, T.J. Stephens, B.J. Canny, and B.E. Kemp Short-term exercise training in humans reduces AMPK signalling during prolonged exercise independent of muscle glycogen J. Physiol. 568 2005 665 676
26. G.F. Merrill, E.J. Kurth, B.B. Rasmussen, and W.W. Winder Influence of malonyl-CoA and palmitate concentration on rate of palmitate oxidation in rat muscle J. Appl. Physiol. 85 1998 1909 1914
27. Y. Minokoshi, T. Alquier, N. Furukawa, Y.B. Kim, A. Lee, B. Xue, J. Mu, F. Foufelle, P. Ferre, M.J. Birnbaum, B.J. Stuck, and B.B. Kahn AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus Nature 428 2004 569 574
28. R. Mora-Rodriguez, B.J. Hodgkinson, L.O. Byerley, and E.F. Coyle Effects of beta-adrenergic receptor stimulation and blockade on substrate metabolism during submaximal exercise Am. J. Physiol. Endocrinol. Metab. 280 2001 E752 E760
29. N. Musi, N. Fujii, M.F. Hirshman, I. Ekberg, S. Froberg, 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 50 2001 921 927
30. J.N. Nielsen, J.F. Wojtaszewski, R.G. Haller, D.G. Hardie, B.E. Kemp, E.A. Richter, and J. Vissing Role of 5′AMP-activated protein kinase in glycogen synthase activity and glucose utilization: insights from patients with McArdle's disease J. Physiol. 541 2002 979 989
31. L.M. Odland, G.J. Heigenhauser, G.D. Lopaschuk, and L.L. Spriet Human skeletal muscle malonyl-CoA at rest and during prolonged submaximal exercise Am. J. Physiol. 270 1996 E541 E544
32. L.M. Odland, R.A. Howlett, G.J. Heigenhauser, E. Hultman, and L.L. Spriet Skeletal muscle malonyl-CoA content at the onset of exercise at varying power outputs in humans Am. J. Physiol. 274 1998 E1080 E1085
33. 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. 277 2002 32571 32577
34. J.V. Passonneau, P.D. Gatfield, D.W. Schulz, and O.H. Lowry An enzymic method for measurement of glycogen Anal. Biochem. 19 1967 315 326
35. F. Peronnet, and D. Massicotte Table of nonprotein respiratory quotient: an update Can. J. Sport Sci. 16 1991 23 29
36. G. Polekhina, A. Gupta, B.J. Michell, B. van Denderen, S. Murthy, S.C. Feil, I.G. Jennings, D.J. Campbell, L.A. Witters, M.W. Parker, B.E. Kemp, and D. Stapleton AMPK beta subunit targets metabolic stress sensing to glycogen Curr. Biol. 13 2003 867 871
37. B.B. Rasmussen, and W.W. Winder Effect of exercise intensity on skeletal muscle malonyl-CoA and acetyl-CoA carboxylase J. Appl. Physiol. 83 1997 1104 1109
38. C. Roepstorff, N. Halberg, T. Hillig, A.K. Saha, N.B. Ruderman, J.F. Wojtaszewski, E.A. Richter, and B. Kiens Malonyl-CoA and carnitine in regulation of fat oxidation in human skeletal muscle during exercise Am. J. Physiol. Endocrinol. Metab. 288 2005 E133 E142
39. J.A. Romijn, E.F. Coyle, L.S. Sidossis, X.J. Zhang, and R.R. Wolfe Relationship between fatty acid delivery and fatty acid oxidation during strenuous exercise J. Appl. Physiol. 79 1995 1939 1945
40. N.B. Ruderman, H. Park, V.K. Kaushik, D. Dean, S. Constant, M. Prentki, and A.K. Saha AMPK as a metabolic switch in rat muscle, liver and adipose tissue after exercise Acta Physiol. Scand. 178 2003 435 442
41. I.P. Salt, G. Johnson, S.J. Ashcroft, and D.G. Hardie AMP-activated protein kinase is activated by low glucose in cell lines derived from pancreatic beta cells, and may regulate insulin release Biochem. J. 335 Pt. 3 1998 533 539
42. D. Stapleton, K.I. Mitchelhill, G. Gao, J. Widmer, B.J. Michell, T. Teh, C.M. House, C.S. Fernandez, T. Cox, L.A. Witters, and B.E. Kemp Mammalian AMP-activated protein kinase subfamily J. Biol. Chem. 271 1996 611 614
43. T.J. Stephens, Z.P. Chen, B.J. Canny, B.J. Michell, B.E. Kemp, and G.K. McConell Progressive increase in human skeletal muscle AMPKalpha2 activity and ACC phosphorylation during exercise Am. J. Physiol. Endocrinol. Metab. 282 2002 E688 E694
44. G. van Hall, M. Sacchetti, G. Radegran, and B. Saltin Human skeletal muscle fatty acid and glycerol metabolism during rest, exercise and recovery J. Physiol. 543 2002 1047 1058
45. L.J. van Loon, P.L. Greenhaff, D. Constantin-Teodosiu, W.H. Saris, and A.J. Wagenmakers The effects of increasing exercise intensity on muscle fuel utilisation in humans J. Physiol. 536 2001 295 304
46. D. Vavvas, A. Apazidis, A.K. Saha, J. Gamble, A. Patel, B.E. Kemp, L.A. Witters, and N.B. Ruderman Contraction-induced changes in acetyl-CoA carboxylase and 5′-AMP-activated kinase in skeletal muscle J. Biol. Chem. 272 1997 13255 13261
47. M.J. Watt, A.G. Holmes, G.R. Steinberg, J.L. Mesa, B.E. Kemp, and M.A. Febbraio Reduced plasma FFA availability increases net triacylglycerol degradation, but not GPAT or HSL activity, in human skeletal muscle Am. J. Physiol. Endocrinol. Metab. 287 2004 E120 E127
48. W.W. Winder Energy-sensing and signaling by AMP-activated protein kinase in skeletal muscle J. Appl. Physiol. 91 2001 1017 1028
49. W.W. Winder, J. Arogyasami, I.M. Elayan, and D. Cartmill Time course of exercise-induced decline in malonyl-CoA in different muscle types Am. J. Physiol. 259 1990 E266 E271
50. W.W. Winder, and D.G. Hardie AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes Am. J. Physiol. 277 1999 E1 E10
51. W.W. Winder, and B.F. Holmes Insulin stimulation of glucose uptake fails to decrease palmitate oxidation in muscle if AMPK is activated J. Appl. Physiol. 89 2000 2430 2437
52. J.F. Wojtaszewski, J.B. Birk, C. Frosig, M. Holten, H. Pilegaard, and F. Dela 5′AMP activated protein kinase expression in human skeletal muscle: effects of strength training and type 2 diabetes J. Physiol. 564 2005 563 573
53. J.F. 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 rat skeletal muscle Diabetes 51 2002 284 292
54. J.F. 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. 284 2003 E813 E822
55. J.F. Wojtaszewski, M. Mourtzakis, T. Hillig, B. Saltin, and H. Pilegaard Dissociation of AMPK activity and ACCbeta phosphorylation in human muscle during prolonged exercise Biochem. Biophys. Res. Commun. 298 2002 309 316
56. J.F. Wojtaszewski, P. Nielsen, B.F. Hansen, E.A. Richter, and B. Kiens Isoform-specific and exercise intensity-dependent activation of 5′-AMP-activated protein kinase in human skeletal muscle J. Physiol. 528 Pt. 1 2000 221 226