The Janus Head of Oxidative Stress in Metabolic Diseases and During Physical Exercise

Current Diabetes Reports

Volumn 17, Issue 6, 2017, Pages

  Pesta, Dominik ^a,b   Roden, Michael ^a,b,c  

^a LEIBNIZ CENTER FOR DIABETES RESEARCH AT HEINRICH HEINE UNIVERSITY DÜSSELDORF   (Germany)

^b GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Antioxidant capacity; Exercise; Obesity; Reactive oxygen species; Type 2 diabetes

Indexed keywords

GLUCOSE; REACTIVE OXYGEN METABOLITE;

ADAPTATION; CELL PROLIFERATION; EXERCISE; GLUCOSE TRANSPORT; HUMAN; INSULIN RESISTANCE; MACROMOLECULE; METABOLIC DISORDER; MITOCHONDRIAL BIOGENESIS; MUSCLE MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; REVIEW; TISSUE SPECIFICITY; UPREGULATION; ANIMAL; PATHOLOGY;

ANIMALS; DIABETES MELLITUS, TYPE 2; EXERCISE; HUMANS; INSULIN RESISTANCE; METABOLIC DISEASES; OBESITY; OXIDATIVE STRESS;

EID: 85018326982     PISSN: 15344827     EISSN: 15390829     Source Type: Journal    
DOI: 10.1007/s11892-017-0867-2     Document Type: Review

References (114)

1. Matsuda M, Shimomura I. Increased oxidative stress in obesity: implications for metabolic syndrome, diabetes, hypertension, dyslipidemia, atherosclerosis, and cancer. Obesity Research & Clinical Practice. 2013;7(5):e330–41.
2. Sies H. Oxidative stress: introduction. oxidative stress: oxidants and antioxidants. London: Academic; 1991.
3. Jones DP. Redefining oxidative stress. Antioxid Redox Signal. 2006;8(9–10):1865–79. doi:10.1089/ars.2006.8.1865.
4. Lushchak VI. Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact. 2014;224:164–75. doi:10.1016/j.cbi.2014.10.016.
5. 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(47):44784–90. doi:10.1074/jbc.M207217200.
6. Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol. 2007;47:143–83. doi:10.1146/annurev.pharmtox.47.120505.105122.
7. Circu ML, Aw TY. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med. 2010;48(6):749–62. doi:10.1016/j.freeradbiomed.2009.12.022.
8. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87(1):245–313. doi:10.1152/physrev.00044.2005.
9. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 2007;87(1):315–424. doi:10.1152/physrev.00029.2006.
10. Kelley EE, Khoo NK, Hundley NJ, Malik UZ, Freeman BA, Tarpey MM. Hydrogen peroxide is the major oxidant product of xanthine oxidase. Free Radic Biol Med. 2010;48(4):493–8. doi:10.1016/j.freeradbiomed.2009.11.012.
11. Tu BP, Weissman JS. Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol. 2004;164(3):341–6. doi:10.1083/jcb.200311055.
12. Salvado L, Palomer X, Barroso E, Vazquez-Carrera M. Targeting endoplasmic reticulum stress in insulin resistance. Trends in Endocrinology and Metabolism: TEM. 2015;26(8):438–48. doi:10.1016/j.tem.2015.05.007.
13. Brown DI, Griendling KK. Regulation of signal transduction by reactive oxygen species in the cardiovascular system. Circ Res. 2015;116(3):531–49. doi:10.1161/CIRCRESAHA.116.303584.
14. Fukai T, Ushio-Fukai M. Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal. 2011;15(6):1583–606. doi:10.1089/ars.2011.3999.
15. Margis R, Dunand C, Teixeira FK, Margis-Pinheiro M. Glutathione peroxidase family—an evolutionary overview. FEBS J. 2008;275(15):3959–70. doi:10.1111/j.1742-4658.2008.06542.x.
16. Dikalov SI, Harrison DG. Methods for detection of mitochondrial and cellular reactive oxygen species. Antioxid Redox Signal. 2014;20(2):372–82. doi:10.1089/ars.2012.4886.
17. Stephens JW, Khanolkar MP, Bain SC. The biological relevance and measurement of plasma markers of oxidative stress in diabetes and cardiovascular disease. Atherosclerosis. 2009;202(2):321–9. doi:10.1016/j.atherosclerosis.2008.06.006.
18. Sies H. Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: oxidative eustress. Redox Biol. 2017;11:613–9.
19. Dikalov S, Griendling KK, Harrison DG. Measurement of reactive oxygen species in cardiovascular studies. Hypertension. 2007;49(4):717–27. doi:10.1161/01.HYP.0000258594.87211.6b.
20. Vasquez-Vivar J, Hogg N, Pritchard Jr KA, Martasek P, Kalyanaraman B. Superoxide anion formation from lucigenin: an electron spin resonance spin-trapping study. FEBS Lett. 1997;403(2):127–30.
21. Starkov AA. Measurement of mitochondrial ROS production. Methods Mol Biol. 2010;648:245–55. doi:10.1007/978-1-60761-756-3_16.
22. Zielonka J, Zielonka M, Sikora A, Adamus J, Joseph J, Hardy M, et al. Global profiling of reactive oxygen and nitrogen species in biological systems: high-throughput real-time analyses. J Biol Chem. 2012;287(5):2984–95. doi:10.1074/jbc.M111.309062.
23. Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol. 1978;52:302–10.
24. Moselhy HF, Reid RG, Yousef S, Boyle SP. A specific, accurate, and sensitive measure of total plasma malondialdehyde by HPLC. J Lipid Res. 2013;54(3):852–8. doi:10.1194/jlr.D032698.
25. Janicka M, Kot-Wasik A, Kot J, Namiesnik J. Isoprostanes-biomarkers of lipid peroxidation: their utility in evaluating oxidative stress and analysis. Int J Mol Sci. 2010;11(11):4631–59. doi:10.3390/ijms11114631.
26. Roberts 2nd LJ, Morrow JD. The generation and actions of isoprostanes. Biochim Biophys Acta. 1997;1345(2):121–35.
27. Mayne ST. Antioxidant nutrients and chronic disease: use of biomarkers of exposure and oxidative stress status in epidemiologic research. J Nutr. 2003;133(Suppl 3):933S–40S.
28. Halliwell B. Why and how should we measure oxidative DNA damage in nutritional studies? How far have we come? Am J Clin Nutr. 2000;72(5):1082–7.
29. Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clinica Chimica Acta. 2003;329(1–2):23–38.
30. Grune T, Reinheckel T, Davies KJ. Degradation of oxidized proteins in K562 human hematopoietic cells by proteasome. J Biol Chem. 1996;271(26):15504–9.
31. Woolley JF, Stanicka J, Cotter TG. Recent advances in reactive oxygen species measurement in biological systems. Trends Biochem Sci. 2013;38(11):556–65. doi:10.1016/j.tibs.2013.08.009.
32. Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes. 1991;40(4):405–12.
33. Kumashiro N, Tamura Y, Uchida T, Ogihara T, Fujitani Y, Hirose T, et al. Impact of oxidative stress and peroxisome proliferator-activated receptor gamma coactivator-1alpha in hepatic insulin resistance. Diabetes. 2008;57(8):2083–91. doi:10.2337/db08-0144.
34. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature. 2006;440(7086):944–8. doi:10.1038/nature04634.
35. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004;114(12):1752–61. doi:10.1172/JCI21625.
36. Warolin J, Coenen KR, Kantor JL, Whitaker LE, Wang L, Acra SA, et al. The relationship of oxidative stress, adiposity and metabolic risk factors in healthy black and white American youth. Pediatric Obesity. 2014;9(1):43–52. doi:10.1111/j.2047-6310.2012.00135.x.
37. Al-Aubaidy HA, Jelinek HF. Oxidative DNA damage and obesity in type 2 diabetes mellitus. European Journal of Endocrinology/European Federation of Endocrine Societies. 2011;164(6):899–904. doi:10.1530/EJE-11-0053.
38. Yokota T, Kinugawa S, Yamato M, Hirabayashi K, Suga T, Takada S, et al. Systemic oxidative stress is associated with lower aerobic capacity and impaired skeletal muscle energy metabolism in patients with metabolic syndrome. Diabetes Care. 2013;36(5):1341–6. doi:10.2337/dc12-1161.
39. Karaouzene N, Merzouk H, Aribi M, Merzouk SA, Berrouiguet AY, Tessier C, et al. Effects of the association of aging and obesity on lipids, lipoproteins and oxidative stress biomarkers: a comparison of older with young men. Nutrition, Metabolism, and Cardiovascular Diseases: NMCD. 2011;21(10):792–9. doi:10.1016/j.numecd.2010.02.007.
40. Silver AE, Beske SD, Christou DD, Donato AJ, Moreau KL, Eskurza I, et al. Overweight and obese humans demonstrate increased vascular endothelial NAD(P)H oxidase-p47(phox) expression and evidence of endothelial oxidative stress. Circulation. 2007;115(5):627–37. doi:10.1161/CIRCULATIONAHA.106.657486.
41. 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(10):2444–52. doi:10.2337/db10-0174.
42. 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(3):573–81.
43. 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(4):574–82. doi:10.1007/s00125-009-1264-4.
44. Codoner-Franch P, Navarro-Ruiz A, Fernandez-Ferri M, Arilla-Codoner A, Ballester-Asensio E, Valls-Belles V. A matter of fat: insulin resistance and oxidative stress. Pediatr Diabetes. 2012;13(5):392–9. doi:10.1111/j.1399-5448.2011.00847.x.
45. Park S, Kim M, Paik JK, Jang YJ, Lee SH, Lee JH. Oxidative stress is associated with C-reactive protein in nondiabetic postmenopausal women, independent of obesity and insulin resistance. Clin Endocrinol. 2013;79(1):65–70. doi:10.1111/j.1365-2265.2012.04512.x.
46. Abramson JL, Hooper WC, Jones DP, Ashfaq S, Rhodes SD, Weintraub WS, et al. Association between novel oxidative stress markers and C-reactive protein among adults without clinical coronary heart disease. Atherosclerosis. 2005;178(1):115–21. doi:10.1016/j.atherosclerosis.2004.08.007.
47. Park K, Gross M, Lee DH, Holvoet P, Himes JH, Shikany JM, et al. Oxidative stress and insulin resistance: the coronary artery risk development in young adults study. Diabetes Care. 2009;32(7):1302–7. doi:10.2337/dc09-0259.
48. Kanauchi M, Nishioka H, Hashimoto T. Oxidative DNA damage and tubulointerstitial injury in diabetic nephropathy. Nephron. 2002;91(2):327–9. 58412
49. Shin CS, Moon BS, Park KS, Kim SY, Park SJ, Chung MH, et al. Serum 8-hydroxy-guanine levels are increased in diabetic patients. Diabetes Care. 2001;24(4):733–7.
50. Kant M, Akis M, Calan M, Arkan T, Bayraktar F, Dizdaroglu M, et al. Elevated urinary levels of 8-oxo-2′-deoxyguanosine, (5′R)- and (5′S)-8,5′-cyclo-2′-deoxyadenosines, and 8-iso-prostaglandin F2alpha as potential biomarkers of oxidative stress in patients with prediabetes. DNA repair. 2016; doi:10.1016/j.dnarep.2016.09.004.
51. Song F, Jia W, Yao Y, Hu Y, Lei L, Lin J, et al. Oxidative stress, antioxidant status and DNA damage in patients with impaired glucose regulation and newly diagnosed type 2 diabetes. Clin Sci. 2007;112(12):599–606. doi:10.1042/CS20060323.
52. Dave GS, Kalia K. Hyperglycemia induced oxidative stress in type-1 and type-2 diabetic patients with and without nephropathy. Cell Mol Biol. 2007;53(5):68–78.
53. 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(1):258–68. doi:10.2337/db10-0281.
54. Bruce CR, Carey AL, Hawley JA, Febbraio MA. Intramuscular heat shock protein 72 and heme oxygenase-1 mRNA are reduced in patients with type 2 diabetes: evidence that insulin resistance is associated with a disturbed antioxidant defense mechanism. Diabetes. 2003;52(9):2338–45.
55. Ohara M, Fukui T, Ouchi M, Watanabe K, Suzuki T, Yamamoto S, et al. Relationship between daily and day-to-day glycemic variability and increased oxidative stress in type 2 diabetes. Diabetes Res Clin Pract. 2016;122:62–70. doi:10.1016/j.diabres.2016.09.025.
56. • Konopka AR, Asante A, Lanza IR, Robinson MM, Johnson ML, Dalla Man C, et al. Defects in mitochondrial efficiency and H2O2 emissions in obese women are restored to a lean phenotype with aerobic exercise training. Diabetes. 2015;64(6):2104–15. doi:10.2337/db14-1701. This intervention study provides evidence that impaired mitochondrial bioenergetics in obese women is restored towards that of lean, insulin-sensitive individuals 12 weeks of aerobic exercise.
57. Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, Bray GA, et al. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes. 2005;54(7):1926–33.
58. Gregersen S, Samocha-Bonet D, Heilbronn LK, Campbell LV. Inflammatory and oxidative stress responses to high-carbohydrate and high-fat meals in healthy humans. Journal of Nutrition and Metabolism. 2012;2012:238056. doi:10.1155/2012/238056.
59. Tumova E, Sun W, Jones PH, Vrablik M, Ballantyne CM, Hoogeveen RC. The impact of rapid weight loss on oxidative stress markers and the expression of the metabolic syndrome in obese individuals. J Obes. 2013;2013:729515. doi:10.1155/2013/729515.
60. Ramezanipour M, Jalali M, Sadrzade-Yeganeh H, Keshavarz SA, Eshraghian MR, Bagheri M, et al. The effect of weight reduction on antioxidant enzymes and their association with dietary intake of vitamins A, C and E. Arquivos brasileiros de endocrinologia e metabologia. 2014;58(7):744–9.
61. Bougoulia M, Triantos A, Koliakos G. Plasma interleukin-6 levels, glutathione peroxidase and isoprostane in obese women before and after weight loss. Association with cardiovascular risk factors. Hormones. 2006;5(3):192–9.
62. Johnson JB, Summer W, Cutler RG, Martin B, Hyun DH, Dixit VD, et al. Alternate day calorie restriction improves clinical findings and reduces markers of oxidative stress and inflammation in overweight adults with moderate asthma. Free Radic Biol Med. 2007;42(5):665–74. doi:10.1016/j.freeradbiomed.2006.12.005.
63. Chance B, Sies H, Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev. 1979;59(3):527–605.
64. Staniek K, Nohl H. H(2)O(2) detection from intact mitochondria as a measure for one-electron reduction of dioxygen requires a non-invasive assay system. Biochim Biophys Acta. 1999;1413(2):70–80.
65. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc Natl Acad Sci U S A. 2003;100(14):8466–71. doi:10.1073/pnas.1032913100.
66. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet. 2003;34(3):267–73. doi:10.1038/ng1180.
67. Szendroedi J, Schmid AI, Chmelik M, Toth C, Brehm A, Krssak M, et al. Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes. PLoS Med. 2007;4(5):e154. doi:10.1371/journal.pmed.0040154.
68. Seifert EL, Estey C, Xuan JY, Harper ME. Electron transport chain-dependent and -independent mechanisms of mitochondrial H2O2 emission during long-chain fatty acid oxidation. J Biol Chem. 2010;285(8):5748–58. doi:10.1074/jbc.M109.026203.
69. •• Szendroedi J, Yoshimura T, Phielix E, Koliaki C, Marcucci M, Zhang D, et al. Role of diacylglycerol activation of PKCtheta in lipid-induced muscle insulin resistance in humans. Proc Natl Acad Sci U S A. 2014;111(26):9597–602. doi:10.1073/pnas.1409229111. This paper addresses mechanisms responsible for muscle insulin resistance in humans and supports the hypothesis that activation of protein kinase Cθ by bioactive diacylglycerol and subsequent impairment of insulin signaling plays a major role in the pathogenesis of muscle insulin resistance.
70. Boden G. Endoplasmic reticulum stress: another link between obesity and insulin resistance/inflammation? Diabetes. 2009;58(3):518–9. doi:10.2337/db08-1746.
71. Sharma NK, Das SK, Mondal AK, Hackney OG, Chu WS, Kern PA, et al. Endoplasmic reticulum stress markers are associated with obesity in nondiabetic subjects. J Clin Endocrinol Metab. 2008;93(11):4532–41. doi:10.1210/jc.2008-1001.
72. Boden G, Duan X, Homko C, Molina EJ, Song W, Perez O, et al. Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes. 2008;57(9):2438–44. doi:10.2337/db08-0604.
73. Lenin R, Sankaramoorthy A, Mohan V, Balasubramanyam M. Altered immunometabolism at the interface of increased endoplasmic reticulum (ER) stress in patients with type 2 diabetes. J Leukoc Biol. 2015;98(4):615–22. doi:10.1189/jlb.3A1214-609R.
74. Papa FR. Endoplasmic reticulum stress, pancreatic beta-cell degeneration, and diabetes. Cold Spring Harbor Perspectives in Medicine. 2012;2(9):a007666. doi:10.1101/cshperspect.a007666.
75. Gorlach A, Klappa P, Kietzmann T. The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid Redox Signal. 2006;8(9–10):1391–418. doi:10.1089/ars.2006.8.1391.
76. Nowotny K, Jung T, Hohn A, Weber D, Grune T. Advanced glycation end products and oxidative stress in type 2 diabetes mellitus. Biomol Ther. 2015;5(1):194–222. doi:10.3390/biom5010194.
77. Zhang M, Kho AL, Anilkumar N, Chibber R, Pagano PJ, Shah AM, et al. Glycated proteins stimulate reactive oxygen species production in cardiac myocytes: involvement of Nox2 (gp91phox)-containing NADPH oxidase. Circulation. 2006;113(9):1235–43. doi:10.1161/CIRCULATIONAHA.105.581397.
78. Dillard CJ, Litov RE, Savin WM, Dumelin EE, Tappel AL. Effects of exercise, vitamin E, and ozone on pulmonary function and lipid peroxidation. J Appl Physiol Respir Environ Exerc Physiol. 1978;45(6):927–32.
79. Veskoukis AS, Goutianos G, Paschalis V, Margaritelis NV, Tzioura A, Dipla K, et al. The rat closely mimics oxidative stress and inflammation in humans after exercise but not after exercise combined with vitamin C administration. Eur J Appl Physiol. 2016;116(4):791–804. doi:10.1007/s00421-016-3336-8.
80. Kim KS, Paik IY, Woo JH, Kang BY. The effect of training type on oxidative DNA damage and antioxidant capacity during three-dimensional space exercise. Medical Principles and Practice. 2010;19(2):133–41. doi:10.1159/000273075.
81. Dantas FF, Brasileiro-Santos Mdo S, Batista RM, do Nascimento LS, Castellano LR, Ritti-Dias RM, et al. Effect of strength training on oxidative stress and the correlation of the same with forearm vasodilatation and blood pressure of hypertensive elderly women: a randomized clinical trial. PLoS One. 2016;11(8):e0161178. doi:10.1371/journal.pone.0161178.
82. Roh H-T, Cho S-Y, So W-Y. Obesity promotes oxidative stress and exacerbates blood-brain barrier disruption after high-intensity exercise. J Sport Health Sci. 2016:1–6.
83. Vincent HK, Morgan JW, Vincent KR. Obesity exacerbates oxidative stress levels after acute exercise. Med Sci Sports Exerc. 2004;36(5):772–9.
84. Vincent HK, Vincent KR, Bourguignon C, Braith RW. Obesity and postexercise oxidative stress in older women. Med Sci Sports Exerc. 2005;37(2):213–9.
85. Haxhi J, Leto G, di Palumbo AS, Sbriccoli P, Guidetti L, Fantini C, et al. Exercise at lunchtime: effect on glycemic control and oxidative stress in middle-aged men with type 2 diabetes. Eur J Appl Physiol. 2016;116(3):573–82. doi:10.1007/s00421-015-3317-3.
86. Parker L, Stepto NK, Shaw CS, Serpiello FR, Anderson M, Hare DL, et al. Acute high-intensity interval exercise-induced redox signaling is associated with enhanced insulin sensitivity in obese middle-aged men. Front Physiol. 2016;7:411. doi:10.3389/fphys.2016.00411.
87. Berdichevsky A, Guarente L, Bose A. Acute oxidative stress can reverse insulin resistance by inactivation of cytoplasmic JNK. J Biol Chem. 2010;285(28):21581–9. doi:10.1074/jbc.M109.093633.
88. Bianchi VE, Ribisl PM. Reactive oxygen species response to exercise training and weight loss in sedentary overweight and obese female adults. Journal of Cardiopulmonary Rehabilitation and Prevention. 2015;35(4):263–7. doi:10.1097/HCR.0000000000000114.
89. Gutierrez-Lopez L, Garcia-Sanchez JR, Rincon-Viquez Mde J, Lara-Padilla E, Sierra-Vargas MP, Olivares-Corichi IM. Hypocaloric diet and regular moderate aerobic exercise is an effective strategy to reduce anthropometric parameters and oxidative stress in obese patients. Obesity Facts. 2012;5(1):12–22. doi:10.1159/000336526.
90. Duggan C, Tapsoba JD, Wang CY, Campbell KL, Foster-Schubert K, Gross MD, et al. Dietary weight loss, exercise, and oxidative stress in postmenopausal women: a randomized controlled trial. Cancer Prev Res. 2016;9(11):835–43. doi:10.1158/1940-6207.CAPR-16-0163.
91. Farinha JB, Steckling FM, Stefanello ST, Cardoso MS, Nunes LS, Barcelos RP, et al. Response of oxidative stress and inflammatory biomarkers to a 12-week aerobic exercise training in women with metabolic syndrome. Sports Medicine - Open. 2015;1(1):3. doi:10.1186/s40798-015-0011-2.
92. Medeiros Nda S, de Abreu FG, Colato AS, de Lemos LS, Ramis TR, Dorneles GP, et al. Effects of concurrent training on oxidative stress and insulin resistance in obese individuals. Oxidative Med Cell Longev. 2015;2015:697181. doi:10.1155/2015/697181.
93. • Gram M, Vigelso A, Yokota T, Helge JW, Dela F, Hey-Mogensen M. Skeletal muscle mitochondrial H2O2 emission increases with immobilization and decreases after aerobic training in young and older men. J Physiol. 2015;593(17):4011–27. doi:10.1113/JP270211. This study provides evidence that increased mitochondrial reactive oxygen species production precipitates the detrimental effects of physical inactivity.
94. Pittaluga M, Sgadari A, Dimauro I, Tavazzi B, Parisi P, Caporossi D. Physical exercise and redox balance in type 2 diabetics: effects of moderate training on biomarkers of oxidative stress and DNA damage evaluated through comet assay. Oxidative Med Cell Longev. 2015;2015:981242. doi:10.1155/2015/981242.
95. Dincer S, Altan M, Terzioglu D, Uslu E, Karsidag K, Batu S, et al. Effects of a regular exercise program on biochemical parameters of type 2 diabetes mellitus patients. The Journal of Sports Medicine and Physical Fitness. 2016;56(11):1384–91.
96. •• Vinetti G, Mozzini C, Desenzani P, Boni E, Bulla L, Lorenzetti I, et al. Supervised exercise training reduces oxidative stress and cardiometabolic risk in adults with type 2 diabetes: a randomized controlled trial. Scientific Reports. 2015;5:9238. doi:10.1038/srep09238. This intervention study shows that supervised exercise training was able to improve cardiorespiratory fitness, cardiometabolic risk, and oxidative stress status in individuals with type 2 diabetes.
97. de Oliveira VN, Bessa A, Jorge ML, Oliveira RJ, de Mello MT, De Agostini GG, et al. The effect of different training programs on antioxidant status, oxidative stress, and metabolic control in type 2 diabetes. Applied Physiology, Nutrition, and Metabolism = Physiologie appliquee, nutrition et metabolisme. 2012;37(2):334–44. doi:10.1139/h2012-004.
98. McNeilly AM, McClean C, Murphy M, McEneny J, Trinick T, Burke G, et al. Exercise training and impaired glucose tolerance in obese humans. J Sports Sci. 2012;30(8):725–32. doi:10.1080/02640414.2012.671952.
99. Kasimay O, Ergen N, Bilsel S, Kacar O, Deyneli O, Gogas D, et al. Diet-supported aerobic exercise reduces blood endothelin-1 and nitric oxide levels in individuals with impaired glucose tolerance. Journal of Clinical Lipidology. 2010;4(5):427–34. doi:10.1016/j.jacl.2010.08.001.
100. Wycherley TP, Brinkworth GD, Noakes M, Buckley JD, Clifton PM. Effect of caloric restriction with and without exercise training on oxidative stress and endothelial function in obese subjects with type 2 diabetes. Diabetes Obes Metab. 2008;10(11):1062–73. doi:10.1111/j.1463-1326.2008.00863.x.
101. Brinkmann C, Blossfeld J, Pesch M, Krone B, Wiesiollek K, Capin D, et al. Lipid-peroxidation and peroxiredoxin-overoxidation in the erythrocytes of non-insulin-dependent type 2 diabetic men during acute exercise. Eur J Appl Physiol. 2012;112(6):2277–87. doi:10.1007/s00421-011-2203-x.
102. Krause M, Rodrigues-Krause J, O’Hagan C, Medlow P, Davison G, Susta D, et al. The effects of aerobic exercise training at two different intensities in obesity and type 2 diabetes: implications for oxidative stress, low-grade inflammation and nitric oxide production. Eur J Appl Physiol. 2014;114(2):251–60. doi:10.1007/s00421-013-2769-6.
103. Karstoft K, Clark MA, Jakobsen I, Muller IA, Pedersen BK, Solomon TP, et al. The effects of 2 weeks of interval vs continuous walking training on glycaemic control and whole-body oxidative stress in individuals with type 2 diabetes: a controlled, randomised, crossover trial. Diabetologia. 2016; doi:10.1007/s00125-016-4170-6.
104. Lawler JM, Rodriguez DA, Hord JM. Mitochondria in the middle: exercise preconditioning protection of striated muscle. J Physiol. 2016;594(18):5161–83. doi:10.1113/JP270656.
105. Yun J, Finkel T. Mitohormesis. Cell Metab. 2014;19(5):757–66. doi:10.1016/j.cmet.2014.01.011.
106. 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(Pt 1):251–62. doi:10.1113/jphysiol.2006.110601.
107. Zhang SJ, Sandstrom ME, Aydin J, Westerblad H, Wieringa B, Katz A. Activation of glucose transport and AMP-activated protein kinase during muscle contraction in adenylate kinase-1 knockout mice. Acta Physiol. 2008;192(3):413–20. doi:10.1111/j.1748-1716.2007.01767.x.
108. Merry TL, Dywer RM, Bradley EA, Rattigan S, McConell GK. Local hindlimb antioxidant infusion does not affect muscle glucose uptake during in situ contractions in rat. J Appl Physiol. 2010;108(5):1275–83. doi:10.1152/japplphysiol.01335.2009.
109. Merry TL, Wadley GD, Stathis CG, Garnham AP, Rattigan S, Hargreaves M, et al. N-Acetylcysteine infusion does not affect glucose disposal during prolonged moderate-intensity exercise in humans. J Physiol. 2010;588(Pt 9):1623–34. doi:10.1113/jphysiol.2009.184333.
110. 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. American Journal of Physiology Cell Physiology. 2007;293(3):C1154–9. doi:10.1152/ajpcell.00110.2007.
111. 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 U S A. 2009;106(21):8665–70. doi:10.1073/pnas.0903485106.
112. 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(12):10605–17. doi:10.1074/jbc.M110.211466.
113. Smith BK, Mukai K, Lally JS, Maher AC, Gurd BJ, Heigenhauser GJ, et al. AMP-activated protein kinase is required for exercise-induced peroxisome proliferator-activated receptor co-activator 1 translocation to subsarcolemmal mitochondria in skeletal muscle. J Physiol. 2013;591(6):1551–61. doi:10.1113/jphysiol.2012.245944.
114. Irrcher I, Ljubicic V, Hood DA. Interactions between ROS and AMP kinase activity in the regulation of PGC-1alpha transcription in skeletal muscle cells. American Journal of Physiology Cell Physiology. 2009;296(1):C116–23. doi:10.1152/ajpcell.00267.2007.