The impact of antioxidant supplements and endurance exercise on genes of the carbohydrate and lipid metabolism in skeletal muscle of mice

Cell Biochemistry and Function

Volumn 31, Issue 1, 2013, Pages 51-59

  Meier, Patrick ^a   Renga, Marcello ^a   Hoppeler, Hans ^a   Baum, Oliver ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Antioxidant administration; Carbohydrate and lipid metabolism; Endurance training; PGC 1alpha; ROS metabolism

Indexed keywords

ACETYLCYSTEINE; ANTIOXIDANT; ASCORBIC ACID; CD36 ANTIGEN; CITRATE SYNTHASE; COPPER ZINC SUPEROXIDE DISMUTASE; DRINKING WATER; FATTY ACID BINDING PROTEIN 3; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUCOSE TRANSPORTER 4; GLUTATHIONE DISULFIDE; GLYCOGENIN; MEDIUM CHAIN ACYL COENZYME DEHYDROGENASE; MESSENGER RNA; PEROXIREDOXIN 6; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; STEROL REGULATORY ELEMENT BINDING FACTOR 1C; TAP WATER; UBIDECARENONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; ENDURANCE TRAINING; ENZYME ACTIVITY; GENE EXPRESSION; LIPID METABOLISM; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; SITTING; SKELETAL MUSCLE; TREADMILL EXERCISE;

ACETYLCYSTEINE; ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; CARBOHYDRATE METABOLISM; DRUG EVALUATION, PRECLINICAL; FREE RADICAL SCAVENGERS; GENE EXPRESSION REGULATION; LIPID METABOLISM; MALE; MICE; MICE, INBRED C57BL; MUSCLE PROTEINS; MUSCLE, SKELETAL; PEROXIREDOXIN VI; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL ENDURANCE; RANDOM ALLOCATION; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE; UBIQUINONE;

MURINAE; MUS;

EID: 84872389666     PISSN: 02636484     EISSN: 10990844     Source Type: Journal    
DOI: 10.1002/cbf.2859     Document Type: Article

References (52)

1. Dela F, Mikines KJ, von Linstow M, Secher NH, Galbo H. Effect of training on insulin-mediated glucose uptake in human muscle. Am J Physiol 1992; 263: E1134-1143.
2. Zanesco A, Antunes E. Effects of exercise training on the cardiovascular system: pharmacological approaches. Pharmacol Ther 2007; 114: 307-317. doi:10.1016/j.pharmthera.2007.03.010.
3. Hoppeler H, Howald H, Conley K, et al. Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 1985; 59: 320-327.
4. Yan Z, Okutsu M, Akhtar YN, Lira VA. Regulation of exercise-induced fiber type transformation, mitochondrial biogenesis, and angiogenesis in skeletal muscle. J Appl Physiol 2011; 110: 264-274. doi:10.1152/japplphysiol.00993.2010.
5. Hood DA. Mechanisms of exercise-induced mitochondrial biogenesis in skeletal muscle. Appl Physiol Nutr Metab 2009; 34: 465-472. doi:10.1139/H09-045.
6. Holloszy JO, Kohrt WM, Hansen PA. The regulation of carbohydrate and fat metabolism during and after exercise. Front Biosci 1998; 3: D1011-1027.
7. Greiwe JS, Hickner RC, Hansen PA, Racette SB, Chen MM, Holloszy JO. Effects of endurance exercise training on muscle glycogen accumulation in humans. J Appl Physiol 1999; 87: 222-226.
8. Spriet LL, Watt MJ. Regulatory mechanisms in the interaction between carbohydrate and lipid oxidation during exercise. Acta Physiol Scand 2003; 178: 443-452.
9. Booth FW, Tseng BS, Fluck M, Carson JA. Molecular and cellular adaptation of muscle in response to physical training. Acta Physiol Scand 1998; 162: 343-350.
10. Smith AG, Muscat GE. Skeletal muscle and nuclear hormone receptors: implications for cardiovascular and metabolic disease. Int J Biochem Cell Biol 2005; 37: 2047-2063. doi:10.1016/j.biocel.2005.03.002.
11. Fluck M. Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. J Exp Biol 2006; 209: 2239-2248.
12. Coffey VG, Hawley JA. The molecular bases of training adaptation. Sports Med 2007; 37: 737-763.
13. Hoppeler H, Baum O, Lurman G, Mueller M. Molecular mechanisms of muscle plasticity with exercise. Compr Physiol 2011; 1: 1383-1412. doi:10.1002/cphy.c110029.
14. Kraniou Y, Cameron-Smith D, Misso M, Collier G, Hargreaves M. Effects of exercise on GLUT-4 and glycogenin gene expression in human skeletal muscle. J Appl Physiol 2000; 88: 794-796.
15. Klip A. The many ways to regulate glucose transporter 4. Appl Physiol Nutr Metab 2009; 34: 481-487. doi:10.1139/H09-047.
16. O'Doherty RM, Bracy DP, Granner DK, Wasserman DH. Transcription of the rat skeletal muscle hexokinase II gene is increased by acute exercise. J Appl Physiol 1996; 81: 789-793.
17. Printz RL, Osawa H, Ardehali H, Koch S, Granner DK. Hexokinase II gene: structure, regulation and promoter organization. Biochem Soc Trans 1997; 25: 107-112.
18. Pereira B, Costa Rosa LF, Safi DA, Medeiros MH, Curi R, Bechara EJ. Superoxide dismutase, catalase, and glutathione peroxidase activities in muscle and lymphoid organs of sedentary and exercise-trained rats. Physiol Behav 1994; 56: 1095-1099.
19. Summermatter S, Baum O, Santos G, Hoppeler H, Handschin C. Peroxisome proliferator-activated receptor {gamma} coactivator 1{alpha} (PGC-1{alpha}) promotes skeletal muscle lipid refueling in vivo by activating de novo lipogenesis and the pentose phosphate pathway. J Biol Chem 2010; 285: 32793-32800. doi:10.1074/jbc.M110.145995.
20. Kiens B. Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol Rev 2006; 86: 205-243.
21. Schmitt B, Fluck M, Decombaz J, et al. Transcriptional adaptations of lipid metabolism in tibialis anterior muscle of endurance-trained athletes. Physiol Genomics 2003; 15: 148-157.
22. Horowitz JF, Leone TC, Feng W, Kelly DP, Klein S. Effect of endurance training on lipid metabolism in women: a potential role for PPARalpha in the metabolic response to training. Am J Physiol Endocrinol Metab 2000; 279: E348-355.
23. Shimano H. Sterol regulatory element-binding proteins (SREBPs): transcriptional regulators of lipid synthetic genes. Prog Lipid Res 2001; 40: 439-452.
24. Handschin C, Spiegelman BM. The role of exercise and PGC1alpha in inflammation and chronic disease. Nature 2008; 454: 463-469.
25. Olesen J, Kiilerich K, Pilegaard H. PGC-1alpha-mediated adaptations in skeletal muscle. Pflugers Arch 2010; 460: 153-162.
26. Lira VA, Benton CR, Yan Z, Bonen A. PGC-1alpha regulation by exercise training and its influences on muscle function and insulin sensitivity. Am J Physiol Endocrinol Metab 2010; 299: E145-161. doi:10.1152/ajpendo.00755.2009.
27. Pilegaard H, Saltin B, Neufer PD. Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J Physiol 2003; 546: 851-858.
28. Chin ER, Olson EN, Richardson JA, et al. A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 1998; 12: 2499-2509.
29. Smith MA, Reid MB. Redox modulation of contractile function in respiratory and limb skeletal muscle. Respir Physiol Neurobiol 2006; 151: 229-241. doi:10.1016/j.resp.2005.12.011.
30. Jackson MJ. Redox regulation of adaptive responses in skeletal muscle to contractile activity. Free Radic Biol Med 2009; 47: 1267-1275. doi:10.1016/j.freeradbiomed.2009.09.005.
31. da Rocha RF, de Oliveira MR, Pasquali MA, et al. Vascular redox imbalance in rats submitted to chronic exercise. Cell Biochem Funct 2010; 28: 190-196.
32. Gross M, Baum O, Hoppeler H. Antioxidant supplementation and endurance training: Win or loss? Eur J Sport Sci 2011; 11: 27-32.
33. Powers SK, Talbert EE, Adhihetty PJ. Reactive oxygen and nitrogen species as intracellular signals in skeletal muscle. J Physiol 2011; 589: 2129-2138. doi:10.1113/jphysiol.2010.201327.
34. Pinheiro CH, Silveira LR, Nachbar RT, Vitzel KF, Curi R. Regulation of glycolysis and expression of glucose metabolism-related genes by reactive oxygen species in contracting skeletal muscle cells. Free Radic Biol Med 2010; 48: 953-960. doi:10.1016/j.freeradbiomed.2010.01.016.
35. Hamalainen N, Pette D. The histochemical profiles of fast fiber types IIB, IID, and IIA in skeletal muscles of mouse, rat, and rabbit. J Histochem Cytochem 1993; 41: 733-743.
36. Allen DL, Harrison BC, Maass A, Bell ML, Byrnes WC, Leinwand LA. Cardiac and skeletal muscle adaptations to voluntary wheel running in the mouse. J Appl Physiol 2001; 90: 1900-1908.
37. Baum O, Schlappi S, Huber-Abel FA, Weichert A, Hoppeler H, Zakrzewicz A. The beta-isoform of neuronal nitric oxide synthase (nNOS) lacking the PDZ domain is localized at the sarcolemma. FEBS Lett 2011; 585: 3219-3223.
38. Planitzer G, Miethke A, Baum O. Nitric oxide synthase-1 is enriched in fast-twitch oxidative myofibers. Cell Tissue Res 2001; 306: 325-333.
39. Holloszy JO, Oscai LB, Don IJ, Mole PA. Mitochondrial citric acid cycle and related enzymes: adaptive response to exercise. Biochem Biophys Res Commun 1970; 40: 1368-1373.
40. Srere PA. Citrate synthase. Methods Enzymol 1969; 13: 3-11. doi:10.1016/0076-6879(69)13005-0.
41. Huber-Abel FA, Gerber M, Hoppeler H, Baum O. Exercise-induced angiogenesis correlates with the up-regulated expression of neuronal nitric oxide synthase (nNOS) in human skeletal muscle. Eur J Appl Physiol 2012; 112: 155-162. doi:10.1007/s00421-011-1960-x.
42. Malek MH, Olfert IM. Global deletion of thrombospondin-1 increases cardiac and skeletal muscle capillarity and exercise capacity in mice. Exp Physiol 2009; 94: 749-760. doi:10.1113/expphysiol.2008.045989.
43. Hollander J, Fiebig R, Gore M, et al. Superoxide dismutase gene expression in skeletal muscle: fiber-specific adaptation to endurance training. Am J Physiol 1999; 277: R856-862.
44. Ferreira JC, Bacurau AV, Bueno CR, Jr, et al. Aerobic exercise training improves Ca2+ handling and redox status of skeletal muscle in mice. Exp Biol Med (Maywood) 2010; 235: 497-505. doi:10.1258/ebm.2009.009165.
45. Yfanti C, Akerstrom T, Nielsen S, et al. Antioxidant supplementation does not alter endurance training adaptation. Med Sci Sports Exerc 2010; 42: 1388-1395. doi:10.1249/MSS.0b013e3181cd76be.
46. Roberts LA, Beattie K, Close GL, Morton JP. Vitamin C consumption does not impair training-induced improvements in exercise performance. Int J Sports Physiol Perform 2011; 6: 58-69.
47. Gomez-Cabrera MC, Domenech E, Romagnoli M, et al. Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance. Am J Clin Nutr 2008; 87: 142-149.
48. Ristow M, Zarse K, Oberbach A, et al. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci U S A 2009; 106: 8665-8670. doi:10.1073/pnas.0903485106.
49. Yfanti C, Nielsen AR, Akerstrom T, et al. Effect of antioxidant supplementation on insulin sensitivity in response to endurance exercise training. Am J Physiol Endocrinol Metab 2011; 300: E761-770. doi:10.1152/ajpendo.00207.2010.
50. Sekiya M, Hiraishi A, Touyama M, Sakamoto K. Oxidative stress induced lipid accumulation via SREBP1c activation in HepG2 cells. Biochem Biophys Res Commun 2008; 375: 602-607. doi:10.1016/j.bbrc.2008.08.068.
51. Silveira LR, Pilegaard H, Kusuhara K, Curi R, Hellsten Y. The contraction induced increase in gene expression of peroxisome proliferator-activated receptor (PPAR)-gamma coactivator 1alpha (PGC-1alpha), mitochondrial uncoupling protein 3 (UCP3) and hexokinase II (HKII) in primary rat skeletal muscle cells is dependent on reactive oxygen species. Biochim Biophys Acta 2006; 1763: 969-976. doi:10.1016/j.bbamcr.2006.06.010.
52. Irrcher I, Ljubicic V, Hood DA. Interactions between ROS and AMP kinase activity in the regulation of PGC-1alpha transcription in skeletal muscle cells. Am J Physiol Cell Physiol 2009; 296: C116-123. doi:10.1152/ajpcell.00267.2007.