Glucose ingestion during exercise blunts exercise-induced gene expression of skeletal muscle fat oxidative genes

American Journal of Physiology - Endocrinology and Metabolism

Volumn 289, Issue 6, 2005, Pages

  Civitarese, Anthony E ^a   Hesselink, Matthijs K C ^b   Russell, Aaron P ^c   Ravussin, Eric ^a   Schrauwen, Patrick ^b  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c SUVA   (Switzerland)

Author keywords

Exercise diet interaction; Skeletal muscle gene expression

Indexed keywords

ADENOSINE PHOSPHATE; CARBOHYDRATE; CARNITINE PALMITOYLTRANSFERASE; CARNITINE PALMITOYLTRANSFERASE I; CD36 ANTIGEN; FATTY ACID; GLUCOSE; MESSENGER RNA; PHOSPHOTRANSFERASE; PYRUVATE DEHYDROGENASE KINASE 4; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 3; 5' AMP ACTIVATED PROTEIN KINASE; 5'-AMP-ACTIVATED PROTEIN KINASE; CARRIER PROTEIN; INSULIN; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN 3; MULTIENZYME COMPLEX; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE;

ADULT; ARTICLE; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; EXERCISE; FATTY ACID BLOOD LEVEL; FATTY ACID OXIDATION; FATTY ACID TRANSPORT; GENE; GENE EXPRESSION; GLUCOSE INTAKE; HUMAN; HUMAN EXPERIMENT; LIPID METABOLISM; MALE; NORMAL HUMAN; OXIDATION KINETICS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; SKELETAL MUSCLE; BLOOD; BODY MASS; DRUG EFFECT; GENETICS; GLUCOSE BLOOD LEVEL; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ADULT; ANTIGENS, CD36; BIOLOGICAL TRANSPORT; BLOOD GLUCOSE; BODY MASS INDEX; CARBOHYDRATE METABOLISM; CARNITINE O-PALMITOYLTRANSFERASE; CARRIER PROTEINS; EXERCISE; FATTY ACIDS; FATTY ACIDS, NONESTERIFIED; GENE EXPRESSION; GLUCOSE; HUMANS; INSULIN; ION CHANNELS; LIPID METABOLISM; MALE; MITOCHONDRIAL PROTEINS; MULTIENZYME COMPLEXES; MUSCLE, SKELETAL; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES;

EID: 33644667633     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00193.2005     Document Type: Article

References (48)

1. Arkinstall MJ, Tunstall RJ, Cameron-Smith D, and Hawley JA. Regulation of metabolic genes in human skeletal muscle by short-term exercise and diet manipulation. Am J Physiol Endocrinol Metab 287: E25-E31, 2004.
2. Aschenbach WG, Sakamoto K, and Goodyear LJ. 5′ Adenosine monophosphate-activated protein kinase, metabolism and exercise. Sports Med 34: 91-103, 2004.
3. Cameron-Smith D, Burke LM, Angus DJ, Tunstall RJ, Cox GR, Bonen A, Hawley JA, and Hargreaves M. A short-term, high-fat diet up-regulates lipid metabolism and gene expression in human skeletal muscle. Am J Clin Nutr 77: 313-318, 2003.
4. Chomczynski P and Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
5. Coyle EF, Jeukendrup AE, Wagenmakers AJ, and Saris WH. Fatty acid oxidation is directly regulated by carbohydrate metabolism during exercise. Am J Physiol Endocrinol Metab 273: E268-E275, 1997.
6. Febbraio MA, Keenan J, Angus DJ, Campbell SE, and Garnham AP. Preexercise carbohydrate ingestion, glucose kinetics, and muscle glycogen use: effect of the glycemic index. J Appl Physiol 89: 1845-1851, 2000.
7. Febbraio MA and Stewart KL. CHO feeding before prolonged exercise: effect of glycemic index on muscle glycogenolysis and exercise performance. J Appl Physiol 81: 1115-1120, 1996.
8. Greiwe JS, Hickner RC, Hansen PA, Racette SB, Chen MM, and Holloszy JO. Effects of endurance exercise training on muscle glycogen accumulation in humans. J Appl Physiol 87: 222-226, 1999.
9. Hardie DG. AMP-activated protein kinase: a key system mediating metabolic responses to exercise. Med Sci Sports Exerc 36: 28-34, 2004.
10. Hespel P and Richter EA. Glucose uptake and transport in contracting, perfused rat muscle with different pre-contraction glycogen concentrations. J Physiol 427: 347-359, 1990.
11. Hildebrandt AL and Neufer PD. Exercise attenuates the fasting-induced transcriptional activation of metabolic genes in skeletal muscle. Am J Physiol Endocrinol Metab 278: E1078-E1086, 2000.
12. Hildebrandt AL, Pilegaard H, and Neufer PD. Differential transcriptional activation of select metabolic genes in response to variations in exercise intensity and duration. Am J Physiol Endocrinol Metab 285: E1021-E1027, 2003.
13. 2-adrenergic stimulation on energy expenditure, substrate oxidation, and UCP3 expression in humans. Am J Physiol Endocrinol Metab 285: E775-E782, 2003.
14. Holten MK, Zacho M, Gaster M, Juel C, Wojtaszewski JF, and Dela F. 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, 2004.
15. Horowitz JF, Mora-Rodriguez R, Byerley LO, and Coyle EF. Lipolytic suppression following carbohydrate ingestion limits fat oxidation during exercise. Am J Physiol Endocrinol Metab 273: E768-E775, 1997.
16. Houmard JA, Shaw CD, Hickey MS, and Tanner CJ. Effect of short-term exercise training on insulin-stimulated PI 3-kinase activity in human skeletal muscle. Am J Physiol Endocrinol Metab 277: E1055-E1060, 1999.
17. Howlett KF, Sakamoto K, Hirshman MF, Aschenbach WG, Dow M, White MF, and Goodyear LJ. Insulin signaling after exercise in insulin receptor substrate-2-deficient mice. Diabetes 51: 479-483, 2002.
18. Jeukendrup AE, Raben A, Gijsen A, Stegen JH, Brouns F, Saris WH, and Wagenmakers AJ. Glucose kinetics during prolonged exercise in highly trained human subjects: effect of glucose ingestion. J Physiol 515: 579-589, 1999.
19. Kuo CH, Hwang H, Lee MC, Castle AL, and Ivy JL. Role of insulin on exercise-induced GLUT-4 protein expression and glycogen supercompensation in rat skeletal muscle. J Appl Physiol 96: 621-627, 2004.
20. Latruffe N and Vamecq J. Evolutionary aspects of peroxisomes as cell organelles, and of genes encoding peroxisomal proteins. Biol Cell 92: 389-395, 2000.
21. Lee FN, Zhang L, Zheng D, Choi WS, and Youn JH. Insulin suppresses PDK-4 expression in skeletal muscle independently of plasma FFA. Am J Physiol Endocrinol Metab 287: E69-E74, 2004.
22. Luiken JJ, Koonen DP, Willems J, Zorzano A, Becker C, Fischer Y, Tandon NN, Van Der Vusse GJ, Bonen A, and Glatz JF. Insulin stimulates long-chain fatty acid utilization by rat cardiac myocytes through cellular redistribution of FAT/CD36. Diabetes 51: 3113-3119, 2002.
23. Mascaro C, Acosta E, Ortiz JA, Marrero PF, Hegardt FG, and Haro D. Control of human muscle-type carnitine palmitoyltransferase I gene transcription by peroxisome proliferator-activated receptor. J Biol Chem 273: 8560-8563, 1998.
24. McGee SL, Howlett KF, Starkie RL, Cameron-Smith D, Kemp BE, and Hargreaves M. Exercise increases nuclear AMPK alpha2 in human skeletal muscle. Diabetes 52: 926-928, 2003.
25. Motojima K, Passilly P, Peters JM, Gonzalez FJ, and Latruffe N. Expression of putative fatty acid transporter genes are regulated by peroxisome proliferator-activated receptor alpha and gamma activators in a tissue- and inducer-specific manner. J Biol Chem 273: 16710-16714, 1998.
26. Musi N, Fujii N, Hirshman MF, Ekberg I, Froberg S, Ljungqvist O, Thorell A, and Goodyear LJ. AMP-activated protein kinase (AMPK) is activated in muscle of subjects with type 2 diabetes during exercise. Diabetes 50: 921-927, 2001.
27. Nielsen JN, Frosig C, Sajan MP, Miura A, Standaert ML, Graham DA, Wojtaszewski JF, Farese RV, and Richter EA. Increased atypical PKC activity in endurance-trained human skeletal muscle. Biochem Biophys Res Commun 312: 1147-1153, 2003.
28. Peronnet F and Massicotte D. Table of nonprotein respiratory quotient: an update. Can J Sport Sci 16: 23-29, 1991.
29. Peters SJ, Harris RA, Wu P, Pehleman TL, Heigenhauser GJ, and Spriet LL. Human skeletal muscle PDH kinase activity and isoform expression during a 3-day high-fat/low-carbohydrate diet. Am J Physiol Endocrinol Metab 281: E1151-E1158, 2001.
30. Pilegaard H, Keller C, Steensberg A, Helge JW, Pedersen BK, Saltin B, and Neufer PD. Influence of pre-exercise muscle glycogen content on exercise-induced transcriptional regulation of metabolic genes. J Physiol 541: 261-271, 2002.
31. Pilegaard H, Ordway GA, Saltin B, and Neufer PD. Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 279: E806-E814, 2000.
32. Pilegaard H, Saltin B, and Neufer PD. Effect of short-term fasting and refeeding on transcriptional regulation of metabolic genes in human skeletal muscle. Diabetes 52: 657-662, 2003.
33. Rome S, Clement K, Rabasa-Lhoret R, Loizon E, Poitou C, Barsh GS, Riou JP, Laville M, and Vidal H. Microarray profiling of human skeletal muscle reveals that insulin regulates approximately 800 genes during a hyperinsulinemic clamp. J Biol Chem 278: 18063-18068, 2003.
34. Ryder JW, Kawano Y, Galuska D, Fahlman R, Wallberg-Henriksson H, Charron MJ, and Zierath JR. Postexercise glucose uptake and glycogen synthesis in skeletal muscle from GLUT4-deficient mice. FASEB J 13: 2246-2256, 1999.
35. Sato O, Kuriki C, Fukui Y, and Motojima K. Dual promoter structure of mouse and human fatty acid translocase/CD36 genes and unique transcriptional activation by peroxisome proliferator-activated receptor alpha and gamma ligands. J Biol Chem 277: 15703-15711, 2002.
36. Schrauwen P, Hesselink MK, Vaartjes I, Kornips E, Saris WH, Giacobino JP, and Russell A. Effect of acute exercise on uncoupling protein 3 is a fat metabolism-mediated effect. Am J Physiol Endocrinol Metab 282: E11-E17, 2002.
37. Schrauwen P, Troost FJ, Xia J, Ravussin E, and Saris WH. Skeletal muscle UCP2 and UCP3 expression in trained and untrained male subjects. Int J Obes Relat Metab Disord 23: 966-972, 1999.
38. Schrauwen P, van Aggel-Leijssen DP, Hul G, Wagenmakers AJ, Vidal H, Saris WH, and van Baak MA. The effect of a 3-month low-intensity endurance training program on fat oxidation and acetyl-CoA carboxylase-2 expression. Diabetes 51: 2220-2226, 2002.
39. Spina RJ, Chi MM, Hopkins MG, Nemeth PM, Lowry OH, and Holloszy JO. Mitochondrial enzymes increase in muscle in response to 7-10 days of cycle exercise. J Appl Physiol 80: 2250-2254, 1996.
40. Spriet LL and Watt MJ. Regulatory mechanisms in the interaction between carbohydrate and lipid oxidation during exercise. Acta Physiol Scand 178: 443-452, 2003.
41. Sugden MC, Lall HS, Harris RA, and Holness MJ. Selective modification of the pyruvate dehydrogenase kinase isoform profile in skeletal muscle in hyperthyroidism: implications for the regulatory impact of glucose on fatty acid oxidation. J Endocrinol 167: 339-345, 2000.
42. Vissing K, Andersen JL, and Schjerling P. Are exercise-induced genes induced by exercise? FASEB J 19: 94-96, 2005.
43. Wadley GD, Tunstall RJ, Sanigorski A, Collier GR, Hargreaves M, and Cameron-Smith D. Differential effects of exercise on insulin-signaling gene expression in human skeletal muscle. J Appl Physiol 90: 436-440, 2001.
44. Winder WW and Hardie DG. Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am J Physiol Endocrinol Metab 270: E299-E304, 1996.
45. Wojtaszewski JF, Jorgensen SB, Frosig C, MacDonald C, Birk JB, and Richter EA. Insulin signalling: effects of prior exercise. Acta Physiol Scand 178: 321-328, 2003.
46. Wu P, Inskeep K, Bowker-Kinley MM, Popov KM, and Harris RA. Mechanism responsible for inactivation of skeletal muscle pyruvate dehydrogenase complex in starvation and diabetes. Diabetes 48: 1593-1599, 1999.
47. Xi X, Han J, and Zhang JZ. Stimulation of glucose transport by AMP-activated protein kinase via activation of p38 mitogen-activated protein kinase. J Biol Chem 276: 41029-41034, 2001.
48. Yang Y, Creer A, Jemiolo B, and Trappe S. Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J Appl Physiol 98: 1745-1752, 2005.