Skeletal muscle reactive oxygen species: A target of good cop/bad cop for exercise and disease

Redox Report

Volumn 19, Issue 3, 2014, Pages 97-106

  Mason, Shaun ^a   Wadley, Glenn D ^a  

^a DEAKIN UNIVERSITY   (Australia)

Author keywords

Exercise; Mitochondria; Reactive oxygen species; Skeletal muscle

Indexed keywords

ANTIOXIDANT; NITRIC OXIDE SYNTHASE; PHOSPHOLIPASE A2; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; XANTHINE OXIDASE; INSULIN;

BIOGENESIS; DIABETIC PATIENT; HUMAN; INSULIN RESISTANCE; MITOCHONDRION; MUSCLE EXERCISE; MUSCLE HYPERTROPHY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; ANIMAL; EXERCISE; HYPERTROPHY; METABOLISM; MUSCLE CONTRACTION; MUSCLE MITOCHONDRION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; DIABETES MELLITUS, TYPE 2; EXERCISE; HUMANS; HYPERTROPHY; INSULIN; INSULIN RESISTANCE; MITOCHONDRIA, MUSCLE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; REACTIVE OXYGEN SPECIES;

EID: 84897565712     PISSN: 13510002     EISSN: 17432928     Source Type: Journal    
DOI: 10.1179/1351000213Y.0000000077     Document Type: Review

References (92)

1. Holloszy JO, Booth FW. Biochemical adaptations to endurance exercise in muscle. Annu Rev Physiol 1976;38:273-291.
2. Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, Morio B, et al. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 2008;118:789-800.
3. Cline GW, Petersen KF, Krssak M, Shen J, Hundal RS, Trajanoski Z, et al. Impaired glucose transport as a cause of decreased insulin-stimulated muscle glycogen synthesis in type 2 diabetes. N Engl J Med 1999;341:240-246.
4. Koivisto VA, Yki-Jarvinen H, DeFronzo RA. Physical training and insulin sensitivity. Diabetes Metab Rev 1986;1:445-481.
5. Safdar A, Little JP, Stokl AJ, Hettinga BP, Akhtar M, Tarnopolsky MA. Exercise increases mitochondrial PGC 1alpha content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J Biol Chem 2011;286: 10605-10617.
6. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009;417:1-13.
7. Yuzefovych LV, Musiyenko SI, Wilson GL, Rachek LI. Mitochondrial DNA damage and dysfunction, and oxidative stress are associated with endoplasmic reticulum stress, protein degradation and apoptosis in high fat diet-induced insulin resistance mice. PLoS One 2013;8:e54059.
8. Mahadev K, Zilbering A, Zhu L, Goldstein BJ. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade. J Biol Chem 2001;276:21938-21942.
9. Barazzoni R, Zanetti M, Gortan Cappellari G, Semolic A, Boschelle M, Codarin E, et al. Fatty acids acutely enhance insulin-induced oxidative stress and cause insulin resistance by increasing mitochondrial reactive oxygen species (ROS) generation and nuclear factor-kappaB inhibitor (IkappaB)-nuclear factor-kappaB (NFkappaB) activation in rat muscle, in the absence of mitochondrial dysfunction. Diabetologia 2012;55: 773-782.
10. Nethery D, Stofan D, Callahan L, DiMarco A, Supinski G. Formation of reactive oxygen species by the contracting diaphragm is PLA2 dependent. J Appl Physiol 1999;87:792-800.
11. Fisher-Wellman KH, Neufer PD. Linking mitochondrial bioenergetics to insulin resistance via redox biology. Trends Endocrinol Metab 2012;23:142-153.
12. St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 2002;277: 44784-44790.
13. Goldstein BJ, Mahadev K, Wu X, Zhu L, Motoshima H. Role of insulin-induced reactive oxygen species in the insulin signaling pathway. Antioxid Redox Signal 2005;7:1021-1031.
14. Loh K, Deng H, Fukushima A, Cai X, Boivin B, Galic S, et al. Reactive oxygen species enhance insulin sensitivity. Cell Metab 2009;10:260-272.
15. Davies KJA, Quintanilha AT, Brooks GA, Packer L. Free radicals and tissue damage produced by exercise. Biochemical and Biophys Res Commun 1982;107:1198-1205.
16. Gomez-Cabrera MC, Domenech E, Romagnoli M, Arduini A, Borras C, Pallardo FV, 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.
17. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 2006; 440:944-948.
18. Guarente L. Mitochondria-A Nexus for Aging, Calorie Restriction, and Sirtuins. Cell 2008;132:171-176.
19. Lopez-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, et al. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci USA 2006;103: 1768-1773.
20. Sukhanov S, Semprun-Prieto L, Yoshida T, Michael Tabony A, Higashi Y, Galvez S, et al. Angiotensin II, oxidative stress and skeletal muscle wasting. Am J Med Sci 2011;342:143-147.
21. Jang YC, Liu Y, Hayworth CR, Bhattacharya A, Lustgarten MS, Muller FL, et al. Dietary restriction attenuates age-associated muscle atrophy by lowering oxidative stress in mice even in complete absence of CuZnSOD. Aging Cell 2012;11:770-782.
22. Bisbal C, Lambert K, Avignon A. Antioxidants and glucose metabolism disorders. Curr Opin Clin Nutr Metab Care 2010; 13:439-446.
23. Anderson EJ, Lustig ME, Boyle KE, Woodlief TL, Kane DA, Lin CT, et al. Mitochondrial H2O2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 2009;119:573-581.
24. DeFronzo RA, Gunnarsson R, Bjorkman O, Olsson M, Wahren J. Effects of insulin on peripheral and splanchnic glucose metabolism in noninsulin-dependent (type II) diabetes mellitus. J Clin Invest 1985;76:149-155.
25. Bonadonna RC, Del Prato S, Saccomani MP, Bonora E, Gulli G, Ferrannini E, et al. Transmembrane glucose transport in skeletal muscle of patients with non-insulin-dependent diabetes. J Clin Invest 1993;92:486-494.
26. Adams JM, II, Pratipanawatr T, Berria R, Wang E, DeFronzo RA, Sullards MC, et al. Ceramide content is increased in skeletal muscle from obese insulin-resistant humans. Diabetes 2004;53: 25-31.
27. Itani SI, Ruderman NB, Schmieder F, Boden G. Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes 2002;51:2005-2011.
28. Boudina S, Sena S, Sloan C, Tebbi A, Han YH, O'Neill BT, et al. Early mitochondrial adaptations in skeletal muscle to dietinduced obesity are strain dependent and determine oxidative stress and energy expenditure but not insulin sensitivity. Endocrinology 2012;153:2677-2688.
29. Hoehn KL, Salmon AB, Hohnen-Behrens C, Turner N, Hoy AJ, Maghzal GJ, et al. Insulin resistance is a cellular antioxidant defense mechanism. Proc Natl Acad Sci USA 2009;106: 17787-17792.
30. Paglialunga S, van Bree B, Bosma M, Valdecantos MP, Amengual-Cladera E, Jorgensen JA, et al. Targeting of mitochondrial reactive oxygen species production does not avert lipid-induced insulin resistance in muscle tissue from mice. Diabetologia 2012;55:2759-2768.
31. Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove GM, Clark SE, et al. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem 2006;281:35137-35146.
32. Bravard A, Lefai E, Meugnier E, Pesenti S, Disse E, Vouillarmet J, et al. FTO is increased in muscle during type 2 diabetes, and its overexpression in myotubes alters insulin signaling, enhances lipogenesis and ROS production, and induces mitochondrial dysfunction. Diabetes 2011;60:258-268.
33. Lefort N, Glancy B, Bowen B, Willis WT, Bailowitz Z, De Filippis EA, et al. Increased reactive oxygen species production and lower abundance of complex I subunits and carnitine palmitoyltransferase 1B protein despite normal mitochondrial respiration in insulin-resistant human skeletal muscle. Diabetes 2010; 59:2444-2452.
34. Czernichow S, Couthouis A, Bertrais S, Vergnaud AC, Dauchet L, Galan P, et al. Antioxidant supplementation does not affect fasting plasma glucose in the Supplementation with Antioxidant Vitamins and Minerals (SU. VI. MAX) study in France: association with dietary intake and plasma concentrations. Am J Clin Nutr 2006;84:395-399.
35. Heart Protection Study Collaborative G. MRC/BHF Heart Protection Study of antioxidant vitamin supplementation in 20,536 high-risk individuals: a randomised placebo-controlled trial. Lancet 2002;360:23-33.
36. Liu S, Ajani U, Chae C, Hennekens C, Buring JE, Manson JE. Long-term beta-carotene supplementation and risk of type 2 diabetes mellitus: a randomized controlled trial. JAMA 1999;282: 1073-1075.
37. Pashkow FJ. Oxidative stress and inflammation in heart disease: do antioxidants have a role in treatment and/or prevention? Int J Inflam 2011;2011:514623.
38. Biesalski HK, Grune T, Tinz J, Zollner I, Blumberg JB. Reexamination of a meta-analysis of the effect of antioxidant supplementation on mortality and health in randomized trials. Nutrients 2010;2:929-949.
39. Wang X, Liu JZ, Hu JX, Wu H, Li YL, Chen HL, et al. ROSactivated p38 MAPK/ERK-Akt cascade plays a central role in palmitic acid-stimulated hepatocyte proliferation. Free Radic Biol Med 2011;51:539-551.
40. Ge X, Yu Q, Qi W, Shi X, Zhai Q. Chronic insulin treatment causes insulin resistance in 3T3-L1 adipocytes through oxidative stress. Free Radic Res 2008;42:582-591.
41. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, et al. A central role for JNK in obesity and insulin resistance. Nature 2002;420:333-336.
42. Vinayagamoorthi R, Bobby Z, Sridhar MG. Antioxidants preserve redox balance and inhibit c-Jun-N-terminal kinase pathway while improving insulin signaling in fat-fed rats: evidence for the role of oxidative stress on IRS-1 serine phosphorylation and insulin resistance. J Endocrinol 2008;197:287-296.
43. Kamata H, Honda S, Maeda S, Chang L, Hirata H, Karin M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005;120:649-661.
44. Imoto K, Kukidome D, Nishikawa T, Matsuhisa T, Sonoda K, Fujisawa K, et al. Impact of mitochondrial reactive oxygen species and apoptosis signal-regulating kinase 1 on insulin signaling. Diabetes 2006;55:1197-1204.
45. Abdul-Ghani MA, Jani R, Chavez A, Molina-Carrion M, Tripathy D, Defronzo RA. Mitochondrial reactive oxygen species generation in obese non-diabetic and type 2 diabetic participants. Diabetologia 2009;52:574-582.
46. Hey-Mogensen M, Hojlund K, Vind BF, Wang L, Dela F, Beck-Nielsen H, et al. Effect of physical training on mitochondrial respiration and reactive oxygen species release in skeletal muscle in patients with obesity and type 2 diabetes. Diabetologia 2010;53: 1976-1985.
47. Minet AD, Gaster M. Hydrogen peroxide production is not primarily increased in human myotubes established from type 2 diabetic subjects. J Clin Endocrinol Metab 2011;96: E1486-1490.
48. Bhattacharya A, Lustgarten M, Shi Y, Liu Y, Jang YC, Pulliam D, et al. Increased mitochondrial matrix-directed superoxide production by fatty acid hydroperoxides in skeletal muscle mitochondria. Free Radic Biol Med 2011;50:592-601.
49. Zhao B, Summers FA, Mason RP. Photooxidation of Amplex Red to resorufin: implications of exposing the Amplex Red assay to light. Free Radic Biol Med 2012;53:1080-1087.
50. Scheede-Bergdahl C, Penkowa M, Hidalgo J, Olsen DB, Schjerling P, Prats C, et al. Metallothionein-mediated antioxidant defense system and its response to exercise training are impaired in human type 2 diabetes. Diabetes 2005;54: 3089-3094.
51. Torres SH, De Sanctis JB, de LBM, Hernandez N, Finol HJ. Inflammation and nitric oxide production in skeletal muscle of type 2 diabetic patients. J Endocrinol 2004;181:419-427.
52. Brinkmann C, Chung N, Schmidt U, Kreutz T, Lenzen E, Schiffer T, et al. Training alters the skeletal muscle antioxidative capacity in non-insulin-dependent type 2 diabetic men. Scand J Med Sci Sports 2012;22:462-470.
53. Larsen S, Stride N, Hey-Mogensen M, Hansen CN, Andersen JL, Madsbad S, et al. Increased mitochondrial substrate sensitivity in skeletal muscle of patients with type 2 diabetes. Diabetologia 2011;54:1427-1436.
54. Espinosa A, Garcia A, Hartel S, Hidalgo C, Jaimovich E. NADPH oxidase and hydrogen peroxide mediate insulininduced calcium increase in skeletal muscle cells. J Biol Chem 2009;284:2568-2575.
55. Vasilaki A, Csete M, Pye D, Lee S, Palomero J, McArdle F, et al. Genetic modification of the manganese superoxide dismutase/ glutathione peroxidase 1 pathway influences intracellular ROS generation in quiescent, but not contracting, skeletal muscle cells. Free Radic Biol Med 2006;41:1719-1725.
56. Espinosa A, Leiva A, Pena M, Müller M, Debandi A, Hidalgo C, et al. Myotube depolarization generates reactive oxygen species through NAD(P)H oxidase; ROS-elicited Ca2+ stimulates ERK, CREB, early genes. J Cell Physiol 2006;209:379-388.
57. McArdle F, Pattwell DM, Vasilaki A, McArdle A, Jackson MJ. Intracellular generation of reactive oxygen species by contracting skeletal muscle cells. Free Radic Biol Med 2005;39:651-657.
58. Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 2008;88:1243-1276.
59. Sakellariou GK, Vasilaki A, Palomero J, Kayani A, Zibrik L, McArdle A, et al. Studies of mitochondrial and nonmitochondrial sources implicate nicotinamide adenine dinucleotide phosphate oxidase(s) in the increased skeletal muscle superoxide generation that occurs during contractile activity. Antioxid Redox Signal 2013;18:603-621.
60. Michaelson LP, Shi G, Ward CW, Rodney GG. Mitochondrial redox potential during contraction in single intact muscle fibers. Muscle Nerve 2010;42:522-529.
61. Hirschfield W, Moody MR, O'Brien WE, Gregg AR, Bryan RM, Jr., Reid MB. Nitric oxide release and contractile properties of skeletal muscles from mice deficient in type III NOS. Am J Physiol Regul Integr Comp Physiol 2000;278:R95-100.
62. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007;87:315-424.
63. Sahlin K, Broberg S, Ren JM. Formation of inosine monophosphate (IMP) in human skeletal muscle during incremental dynamic exercise. Acta Physiol Scand 1989;136:193-198.
64. Hellsten-Westing Y. Immunohistochemical localization of xanthine oxidase in human cardiac and skeletal muscle. Histochemistry 1993;100:215-222.
65. Bailey DM, Lawrenson L, McEneny J, Young IS, James PE, Jackson SK, et al. Electron paramagnetic spectroscopic evidence of exercise-induced free radical accumulation in human skeletal muscle. Free Radic Res 2007;41:182-190.
66. Veskoukis AS, Nikolaidis MG, Kyparos A, Kokkinos D, Nepka C, Barbanis S, et al. Effects of xanthine oxidase inhibition on oxidative stress and swimming performance in rats. Appl Physiol Nutr Metab 2008;33:1140-1154.
67. Kang C, O'Moore KM, Dickman JR, Ji LL. Exercise activation of muscle peroxisome proliferator-activated receptor-gamma coactivator-1alpha signaling is redox sensitive. Free Radic Biol Med 2009;47:1394-1400.
68. Bejma J, Ji LL. Aging and acute exercise enhance free radical generation in rat skeletal muscle. J Appl Physiol 1999;87: 465-470.
69. Wadley GD, McConell GK. High-dose antioxidant vitamin C supplementation does not prevent acute exercise-induced increases in markers of skeletal muscle mitochondrial biogenesis in rats. J Appl Physiol 2010;108:1719-1726.
70. Wadley GD, Nicolas MA, Hiam D, McConell GK. Xanthine oxidase inhibition attenuates skeletal muscle signaling following acute exercise but does not impair mitochondrial adaptations to endurance training. Am J Physiol Endocrinol Metab 2013;304: E853-E862.
71. Zhang SJ, Sandstrom ME, Lanner JT, Thorell A, Westerblad H, Katz A. Activation of aconitase in mouse fast-twitch skeletal muscle during contraction-mediated oxidative stress. Am J Physiol Cell Physiol 2007;293:C1154-1159.
72. Karamouzis I, Christoulas K, Grekas D, Giannoulis K, Vamvakoudis E, Mandroukas K. The response of muscle interstitial F2-isoprostane (8-ISO-PGF2alpha) during dynamic muscle contractions in humans. Prostaglandins Leukot Essent Fatty Acids 2004;71:87-90.
73. 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.
74. Mitsuishi M, Miyashita K, Itoh H. cGMP rescues mitochondrial dysfunction induced by glucose and insulin in myocytes. Biochem Biophys Res Commun 2008;367:840-845.
75. Wright DC, Han DH, Garcia-Roves PM, Geiger PC, Jones TE, Holloszy JO. Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1alpha expression. J Biol Chem 2007;282:194-199.
76. Wadley GD, Choate J, McConell GK. NOS isoform-specific regulation of basal but not exercise-induced mitochondrial biogenesis in mouse skeletal muscle. J Physiol 2007;585:253-262.
77. Meier P, Renga M, Hoppeler H, Baum O. The impact of antioxidant supplements and endurance exercise on genes of the carbohydrate and lipid metabolism in skeletal muscle of mice. Cell Biochem Funct 2013;31:51-59.
78. Irrcher I, Ljubicic V, Hood DA. Interactions between ROS and AMP kinase activity in the regulation of PGC-1{alpha} transcription in skeletal muscle cells. Am J Physiol Cell Physiol 2009;296:C116-123.
79. Sandstrom ME, Zhang SJ, Bruton J, Silva JP, Reid MB, Westerblad H, et al. Role of reactive oxygen species in contraction-mediated glucose transport in mouse skeletal muscle. J Physiol 2006;575:251-262.
80. Jager S, Handschin C, St-Pierre J, Spiegelman BM. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci USA 2007;104:12017-12022.
81. Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev 2003; 24:78-90.
82. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999;98:115-124.
83. Ristow M, Zarse K, Oberbach A, Kloting N, Birringer M, Kiehntopf M, et al. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci USA 2009;106:8665-8670.
84. Higashida K, Kim SH, Higuchi M, Holloszy JO, Han DH. Normal adaptations to exercise despite protection against oxidative stress. Am J Physiol Endocrinol Metab 2011;301: E779-784.
85. Yfanti C, Akerstrom T, Nielsen S, Nielsen AR, Mounier R, Mortensen OH, et al. Antioxidant supplementation does not alter endurance training adaptation. Med Sci Sports Exerc 2010; 42:1388-1395.
86. Strobel NA, Peake JM, Matsumoto A, Marsh SA, Coombes JS, Wadley GD. Antioxidant supplementation reduces skeletal muscle mitochondrial biogenesis. Med Sci Sports Exerc 2011; 43:1017-1024.
87. Gomez-Cabrera MC, Borras C, Pallardo FV, Sastre J, Ji LL, Vina J. Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats. J Physiol 2005;567:113-120.
88. Hollander J, Fiebig R, Gore M, Bejma J, Ookawara T, Ohno H, et al. Superoxide dismutase gene expression in skeletal muscle: fiber-specific adaptation to endurance training. Am J Physiol 1999;277:R856-862.
89. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006;127:397-408.
90. Ito N, Ruegg UT, Kudo A, Miyagoe-Suzuki Y, Takeda S. Activation of calcium signaling through Trpv1 by nNOS and peroxynitrite as a key trigger of skeletal muscle hypertrophy. Nature Med 2013;19:101-106.
91. Makanae Y, Kawada S, Sasaki K, Nakazato K, Ishii N. Vitamin C administration attenuates overload-induced skeletal muscle hypertrophy in rats. Acta Physiologica 2013;208:57-65.
92. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, et al. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 2009;587:211-217.