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Oxidative Medicine and Cellular Longevity
Volume 2012 (2012), Article ID 741545, 15 pages
http://dx.doi.org/10.1155/2012/741545
Review Article

Regular Physical Exercise as a Strategy to Improve Antioxidant and Anti-Inflammatory Status: Benefits in Type 2 Diabetes Mellitus

1Laboratory of Pharmacology and Experimental Therapeutics, IBILI, Medicine Faculty, University of Coimbra, 3000-354 Coimbra, Portugal
2ESAV, Polytechnic Institute of Viseu, 3504-510 Viseu, Portugal
3Centre for the Study of Education, Technologies and Health, Polytechnic Institute of Viseu, 3504-510 Viseu, Portugal
4Rehabilitation Medicine and Sports Medicine, Medicine Faculty, Coimbra University, 3000-354 Coimbra, Portugal

Received 20 April 2012; Revised 28 June 2012; Accepted 11 July 2012

Academic Editor: Chad M. Kerksick

Copyright © 2012 Edite Teixeira de Lemos et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. E. Lamb and B. J. Goldstein, “Modulating an oxidative-inflammatory cascade: potential new treatment strategy for improving glucose metabolism, insulin resistance, and vascular function,” International Journal of Clinical Practice, vol. 62, no. 7, pp. 1087–1095, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Gupta, E. Chough, J. Daley et al., “Hyperglycemia increases endothelial superoxide that impairs smooth muscle cell Na+-K+-ATpase activity,” American Journal of Physiology, vol. 282, no. 3, pp. C560–C566, 2002. View at Scopus
  3. W. Dröge, “Free radicals in the physiological control of cell function,” Physiological Reviews, vol. 82, no. 1, pp. 47–95, 2002. View at Scopus
  4. H. C. Lee and Y. H. Wei, “Oxidative stress, mitochondrial DNA mutation, and apoptosis in aging,” Experimental Biology and Medicine, vol. 232, no. 5, pp. 592–606, 2007. View at Scopus
  5. P. Storz, “Reactive oxygen species in tumor progression,” Frontiers in Bioscience, vol. 10, no. 2, pp. 1881–1896, 2005. View at Scopus
  6. N. R. Madamanchi, A. Vendrov, and M. S. Runge, “Oxidative stress and vascular disease,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 1, pp. 29–38, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Venkateshappa, G. Harish, R. B. Mythri, et al., “Increased oxidative damage and decreased antioxidant function in aging human substantia nigra compared to striatum: implications for Parkinson's diseaseNeurochemical,” Research, vol. 37, no. 2, pp. 358–369, 2012. View at Publisher · View at Google Scholar
  8. J. C. Pickup, “Inflammation and activated innate immunity in the pathogenesis of type 2 diabletes,” Diabetes Care, vol. 27, no. 3, pp. 813–823, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Pacher, J. S. Beckman, and L. Liaudet, “Nitric oxide and peroxynitrite in health and disease,” Physiological Reviews, vol. 87, no. 1, pp. 315–424, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Yang, X. Jin, C. W. Kei Lam, and S. K. Yan, “Oxidative stress and diabetes mellitus,” Clinical Chemical Laboratorial Medicine, vol. 49, no. 11, pp. 1773–1782, 2011.
  11. L. Gao and G. E. Mann, “Vascular NAD(P)H oxidase activation in diabetes: a double-edged sword in redox signalling,” Cardiovascular Research, vol. 82, no. 1, pp. 9–20, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Ceriello, K. Esposito, L. Piconi et al., “Oscillating glucose is more deleterious to endothelial function and oxidative stress than mean glucose in normal and type 2 diabetic patients,” Diabetes, vol. 57, no. 5, pp. 1349–1354, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. P. C. Calder, R. Albers, J. M. Antoine, et al., “Inflammatory disease processes and interactions with nutrition,” British Journal of Nutrition, vol. 101, supplement 1, pp. S1–45, 2009.
  14. D. C. Lieb, K. Henri Parson, G. Mamikunian, and A. I. Vinik, “Cardiac autonomic imbalance in newly diagnosed and established diabetes is associated with markers of adipose tissue inflammation,” Experimental Diabetes Research, vol. 2012, Article ID 878760, 8 pages, 2012. View at Publisher · View at Google Scholar
  15. R. Jankord and B. Jemiolo, “Influence of physical activity on serum IL-6 and IL-10 levels in healthy older men,” Medicine and Science in Sports and Exercise, vol. 36, no. 6, pp. 960–964, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Ouchi, S. Kihara, Y. Arita et al., “Adiponectin, an adipocyte-derived plasma protein, inhibits endothelial NF-κB signaling through a cAMP-dependent pathway,” Circulation, vol. 102, no. 11, pp. 1296–1301, 2000. View at Scopus
  17. C. S. Oliveira, F. M. A. Giuffrida, F. Crispim, et al., “ADIPOQ and adiponectin: the common ground of hyperglycemia and coronary artery disease?” Arquivos Brasileiros de Endocrinologia & Metabologia, vol. 55, no. 7, pp. 446–454, 2011.
  18. W. Huang and C. K. Glass, “Nuclear receptors and inflammation control: molecular mechanisms and pathophysiological relevance,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, no. 8, pp. 1542–1549, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. J. L. Evans, I. D. Goldfine, B. A. Maddux, and G. M. Grodsky, “Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes,” Endocrine Reviews, vol. 23, no. 5, pp. 599–622, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Lindström, P. Ilanne-Parikka, M. Peltonen et al., “Sustained reduction in the incidence of type 2 diabetes by lifestyle intervention: follow-up of the Finnish Diabetes Prevention Study,” The Lancet, vol. 368, no. 9548, pp. 1673–1679, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. S. S. Bassuk and J. E. Manson, “Epidemiological evidence for the role of physical activity in reducing risk of type 2 diabetes and cardiovascular disease,” Journal of Applied Physiology, vol. 99, no. 3, pp. 1193–1204, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Finaud, G. Lac, and E. Filaire, “Oxidative stress: relationship with exercise and training,” Sports Medicine, vol. 36, no. 4, pp. 327–358, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. M. C. Gomez-Cabrera, E. Domenech, and J. Viña, “Moderate exercise is an antioxidant: upregulation of antioxidant genes by training,” Free Radical Biology and Medicine, vol. 44, no. 2, pp. 126–131, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. G. Caimi, B. Canino, G. Amodeo, M. Montana, and R. L. Presti, “Lipid peroxidation and total antioxidant status in unprofessional athletes before and after a cardiopulmonary test,” Clinical Hemorheology and Microcirculation, vol. 43, no. 3, pp. 235–241, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Gleeson, “Immune function in sport and exercise,” Journal of Applied Physiology, vol. 103, no. 2, pp. 693–699, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. B. K. Pedersen and L. Hoffman-Goetz, “Exercise and the immune system: regulation, integration, and adaptation,” Physiological Reviews, vol. 80, no. 3, pp. 1055–1081, 2000. View at Scopus
  27. L. K. Stewart, M. G. Flynn, W. W. Campbell et al., “The influence of exercise training on inflammatory cytokines and C-reactive protein,” Medicine and Science in Sports and Exercise, vol. 39, no. 10, pp. 1714–1719, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. K. L. Timmerman, M. G. Flynn, P. M. Coen, M. M. Markofski, and B. D. Pence, “Exercise training-induced lowering of inflammatory (CD14+CD16+) monocytes: a role in the anti-inflammatory influence of exercise?” Journal of Leukocyte Biology, vol. 84, no. 5, pp. 1271–1278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. L. E. Fridlyand and L. H. Philipson, “Reactive species and early manifestation of insulin resistance in type 2 diabetes,” Diabetes, Obesity and Metabolism, vol. 8, no. 2, pp. 136–145, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Ceriello, “New insights on oxidative stress and diabetic complications may lead to a “causal” antioxidant therapy,” Diabetes Care, vol. 26, no. 5, pp. 1589–1596, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. T. Heitzer, T. Schlinzig, K. Krohn, T. Meinertz, and T. Münzel, “Endothelial dysfunction, oxidative stress, and risk of cardiovascular events in patients with coronary artery disease,” Circulation, vol. 104, no. 22, pp. 2673–2678, 2001. View at Scopus
  32. D. M. Niedowicz and D. L. Daleke, “The role of oxidative stress in diabetic complications,” Cell Biochemistry and Biophysics, vol. 43, no. 2, pp. 289–330, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Ceriello, L. Quagliaro, M. D'Amico et al., “Acute hyperglycemia induces nitrotyrosine formation and apoptosis in perfused heart from rat,” Diabetes, vol. 51, no. 4, pp. 1076–1082, 2002. View at Scopus
  34. M. R. Sayed, M. M. Iman, and A. S. Dawlat, “Biochemical changes in experimental diabetes before and after treatment with mangifera indica and psidium guava extracts,” Journal of Pharmaceutical and Biomedical Sciences, vol. 2, pp. 29–41, 2011.
  35. L. Zhang, A. Zalewski, Y. Liu et al., “Diabetes-induced oxidative stress and low-grade inflammation in porcine coronary arteries,” Circulation, vol. 108, no. 4, pp. 472–478, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Monnier, E. Mas, C. Ginet et al., “Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes,” Journal of the American Medical Association, vol. 295, no. 14, pp. 1681–1687, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Pitocco, F. Zaccardi, E. Di Stasio et al., “Role of asymmetric-dimethyl-l-arginine (ADMA) and nitrite/nitrate (NOx) in the pathogenesis of oxidative stress in female subjects with uncomplicated type 1 diabetes mellitus,” Diabetes Research and Clinical Practice, vol. 86, no. 3, pp. 173–176, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. F. Giacco and M. Brownlee, “Oxidative stress and diabetic complications,” Circulation Research, vol. 107, no. 9, pp. 1058–1070, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. J. L. Rains and S. K. Jain, “Oxidative stress, insulin signaling, and diabetes,” Free Radical Biology and Medicine, vol. 50, no. 5, pp. 567–575, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Pitocco, F. Zaccardi, E. Di Stasio et al., “Oxidative stress, nitric oxide, and diabetes,” Review of Diabetic Studies, vol. 7, no. 1, pp. 15–25, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. I. Afanas'Ev, “Signaling of reactive oxygen and nitrogen species in diabetes mellitus,” Oxidative Medicine and Cellular Longevity, vol. 3, no. 6, pp. 361–373, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. A. P. Rolo and C. M. Palmeira, “Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress,” Toxicology and Applied Pharmacology, vol. 212, no. 2, pp. 167–178, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. J. C. Yoon, A. Ng, B. H. Kim, A. Bianco, R. J. Xavier, and S. J. Elledge, “Wnt signaling regulates mitochondrial physiology and insulin sensitivity,” Genes and Development, vol. 24, no. 14, pp. 1507–1518, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Mantel, S. V. Messina-Graham, and H. E. Broxmeyer, “Superoxide flashes, reactive oxygen species, and the mitochondrial permeability transition pore: potential implications for hematopoietic stem cell function,” Current Opinion in Hematology, vol. 18, no. 4, pp. 208–213, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. T. J. Guzik, S. Mussa, D. Gastaldi et al., “Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase,” Circulation, vol. 105, no. 14, pp. 1656–1662, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. D. J. Leehey, M. A. Isreb, S. Marcic, A. K. Singh, and R. Singh, “Effect of high glucose on superoxide in human mesangial cells: role of angiotensin II,” Nephron, vol. 100, no. 1, pp. 46–53, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Yang, E. Foster, and A. M. Kahn, “Insulin-stimulated NAD(P)H oxidase activity increases migration of cultured vascular smooth muscle cells,” American Journal of Hypertension, vol. 18, no. 10, pp. 1329–1334, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Matsumoto, I. Koshiishi, T. Inoguchi, H. Nawata, and H. Utsumi, “Confirmation of superoxide generation via xanthine oxidase in streptozotocin-induced diabetic mice,” Free Radical Research, vol. 37, no. 7, pp. 767–772, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. R. Natarajan and J. L. Nadler, “Lipoxygenases and lipid signaling in vascular cells in diabetes,” Frontiers in Bioscience, vol. 8, pp. s783–s795, 2003. View at Scopus
  50. P. Dandona and A. Aljada, “A rational approach to pathogenesis and treatment of type 2 diabetes mellitus, insulin resistance, inflammation, and atherosclerosis,” American Journal of Cardiology, vol. 90, no. 5, pp. 27G–33G, 2002. View at Scopus
  51. N. Shanmugam, I. T. G. Gonzalo, and R. Natarajan, “Molecular mechanisms of high glucose-induced cyclooxygenase-2 expression in monocytes,” Diabetes, vol. 53, no. 3, pp. 795–802, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Kiritoshi, T. Nishikawa, K. Sonoda et al., “Reactive oxygen species from mitochondria induce cyclooxygenase-2 gene expression in human mesangial cells: potential role in diabetic nephropathy,” Diabetes, vol. 52, no. 10, pp. 2570–2577, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. A. A. Caro and A. I. Cederbaum, “Oxidative stress, toxicology, and pharmacology of CYP2E1,” Annual Review of Pharmacology and Toxicology, vol. 44, pp. 27–42, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. R. A. DeFronzo, “Insulin resistance, lipotoxicity, type 2 diabetes and atherosclerosis: the missing links. The Claude Bernard Lecture 2009,” Diabetologia, vol. 53, no. 7, pp. 1270–1287, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. Z. Wang, S. D. Hall, J. F. Maya, L. Li, A. Asghar, and J. C. Gorski, “Diabetes mellitus increases the in vivo activity of cytochrome P450 2E1 in humans,” British Journal of Clinical Pharmacology, vol. 55, no. 1, pp. 77–85, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Enriquez, I. Leclercq, G. C. Farrell, and G. Robertson, “Altered expression of hepatic CYP2E1 and CYP4A in obese, diabetic ob/ob mice, and fa/fa Zucker rats,” Biochemical and Biophysical Research Communications, vol. 255, no. 2, pp. 300–306, 1999. View at Publisher · View at Google Scholar · View at Scopus
  57. H. Cortez-Pinto, M. C. De Moura, and C. P. Day, “Non-alcoholic steatohepatitis: from cell biology to clinical practice,” Journal of Hepatology, vol. 44, no. 1, pp. 197–208, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. K. E. Wellen and G. S. Hotamisligil, “Obesity-induced inflammatory changes in adipose tissue,” Journal of Clinical Investigation, vol. 112, no. 12, pp. 1785–1788, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. S. M. Furler, S. K. Gan, A. M. Poynten, D. J. Chisholm, L. V. Campbell, and A. D. Kriketos, “Relationship of adiponectin with insulin sensitivity in humans, independent of lipid availability,” Obesity, vol. 14, no. 2, pp. 228–234, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. T. Kadowaki, T. Yamauchi, N. Kubota, K. Hara, K. Ueki, and K. Tobe, “Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome,” Journal of Clinical Investigation, vol. 116, no. 7, pp. 1784–1792, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. W. Cai, L. Zhu, X. Chen, J. Uribarri, and M. Peppa, “Association of advanced glycoxidation end products and inflammation markers with thrombosis of arteriovenous grafts in hemodialysis patients,” American Journal of Nephrology, vol. 26, no. 2, pp. 181–185, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. Y. Yano, E. C. Gabazza, N. Kitagawa et al., “Tumor necrosis, factor-α is associated with increased protein C activation in nonobese type 2 diabetic patients,” Diabetes Care, vol. 27, no. 3, pp. 844–845, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. K. Maedler, G. A. Spinas, D. Dyntar, W. Moritz, N. Kaiser, and M. Y. Donath, “Distinct effects of saturated and monounsaturated fatty acids on β-cell turnover and function,” Diabetes, vol. 50, no. 1, pp. 69–76, 2001. View at Scopus
  64. M. Cnop, J. C. Hannaert, A. Y. Grupping, and D. G. Pipeleers, “Low density lipoprotein can cause death of islet β-cells by its cellular uptake and oxidative modification,” Endocrinology, vol. 143, no. 9, pp. 3449–3453, 2002. View at Publisher · View at Google Scholar · View at Scopus
  65. W. El-Assaad, J. Buteau, M. L. Peyot et al., “Saturated fatty acids synergize with elevated glucose to cause pancreatic β-cell death,” Endocrinology, vol. 144, no. 9, pp. 4154–4163, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. V. Poitout and R. P. Robertson, “Minireview: secondary β-cell failure in type 2 diabetes—a convergence of glucotoxicity and lipotoxicity,” Endocrinology, vol. 143, no. 2, pp. 339–342, 2002. View at Publisher · View at Google Scholar · View at Scopus
  67. D. Tousoulis, A. M. Kampoli, N. Papageorgiou, et al., “Pathophysiology of atherosclerosis: the role of inflammation,” Current Pharmaceutical Design, vol. 17, no. 37, pp. 4089–4110, 2011.
  68. M. I. Schmidt, B. B. Duncan, A. R. Sharrett et al., “Markers of inflammation and prediction of diabetes mellitus in adults (Atherosclerosis Risk in Communities study): a cohort study,” The Lancet, vol. 353, no. 9165, pp. 1649–1652, 1999. View at Publisher · View at Google Scholar · View at Scopus
  69. P. Dandona, A. Aljada, and A. Bandyopadhyay, “Inflammation: the link between insulin resistance, obesity and diabetes,” Trends in Immunology, vol. 25, no. 1, pp. 4–7, 2004. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Festa, R. D'Agostino, G. Howard, L. Mykkänen, R. P. Tracy, and S. M. Haffner, “Chronic subclinical inflammation as part of the insulin resistance syndrome: the insulin resistance atherosclerosis study (IRAS),” Circulation, vol. 102, no. 1, pp. 42–47, 2000. View at Scopus
  71. H. Kaneto, T. A. Matsuoka, N. Katakami et al., “Oxidative stress and the JNK pathway are involved in the development of type 1 and type 2 diabetes,” Current Molecular Medicine, vol. 7, no. 7, pp. 674–686, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. Y. Taniyama and K. K. Griendling, “Reactive oxygen species in the vasculature: molecular and cellular mechanisms,” Hypertension, vol. 42, no. 6, pp. 1075–1081, 2003. View at Publisher · View at Google Scholar · View at Scopus
  73. M. A. Creager, T. F. Lüscher, F. Cosentino, and J. A. Beckman, “Diabetes and vascular disease. Pathophysiology, clinical consequences, and medical therapy: part I,” Circulation, vol. 108, no. 12, pp. 1527–1532, 2003. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Hirosumi, G. Tuncman, L. Chang et al., “A central, role for JNK in obesity and insulin resistance,” Nature, vol. 420, no. 6913, pp. 333–336, 2002. View at Publisher · View at Google Scholar · View at Scopus
  75. J. P. Bastard, M. Maachi, C. Lagathu et al., “Recent advances in the relationship between obesity, inflammation, and insulin resistance,” European Cytokine Network, vol. 17, no. 1, pp. 4–12, 2006. View at Scopus
  76. J. F. Keaney Jr., M. G. Larson, R. S. Vasan, et al., “Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham Study,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 23, no. 3, pp. 434–439, 2003.
  77. V. Poitout and R. P. Robertson, “Glucolipotoxicity: fuel excess and β-cell dysfunction,” Endocrine Reviews, vol. 29, no. 3, pp. 351–366, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. D. H. van Raalte and M. Diamant, “Glucolipotoxicity and beta cells in type 2 diabetes mellitus: target for durable therapy?” Diabetes Research and Clinical Practice, vol. 93,supplement 1, pp. S37–S46, 2011.
  79. J. D. McGarry, “Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes,” Diabetes, vol. 51, no. 1, pp. 7–18, 2002. View at Scopus
  80. G. X. Shen, “Oxidative stress and diabetic cardiovascular disorders: roles of mitochondria and NADPH oxidase,” Canadian Journal of Physiology and Pharmacology, vol. 88, no. 3, pp. 241–248, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. Z. Fatehi-Hassanabad, C. B. Chan, and B. L. Furman, “Reactive oxygen species and endothelial function in diabetes,” European Journal of Pharmacology, vol. 636, no. 1–3, pp. 8–17, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Goebeler, R. Gillitzer, K. Kilian et al., “Multiple signaling pathways regulate NF-κB-dependent transcription of the monocyte chemoattractant protein-1 gene in primary endothelial cells,” Blood, vol. 97, no. 1, pp. 46–55, 2001. View at Publisher · View at Google Scholar · View at Scopus
  83. J. Lindström, A. Louheranta, M. Mannelin et al., “The finnish diabetes prevention study (DPS): lifestyle intervention and 3-year results on diet and physical activity,” Diabetes Care, vol. 26, no. 12, pp. 3230–3236, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Kodama, S. Tanaka, K. Saito et al., “Effect of aerobic exercise training on serum levels of high-density lipoprotein cholesterol: a meta-analysis,” Archives of Internal Medicine, vol. 167, no. 10, pp. 999–1008, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. T. Saito, et al., “Lifestyle modification and prevention of type 2 diabetes in overweight Japanese with impaired fasting glucose levels: a randomized controlled trial,” Archives of Internal Medicine, vol. 171, no. 15, pp. 1352–1360, 2011.
  86. N. Ahmadi, S. Eshaghian, R. Huizenga, K. Sosnin, R. Ebrahimi, and R. Siegel, “Effects of intense exercise and moderate caloric restriction on cardiovascular risk factors and inflammation,” American Journal of Medicine, vol. 124, no. 10, pp. 978–982, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. C. A. Slentz, C. J. Tanner, L. A. Bateman et al., “Effects of exercise training intensity on pancreatic β-cell function,” Diabetes Care, vol. 32, no. 10, pp. 1807–1811, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. M. F. Belotto, J. Magdalon, H. G. Rodrigues et al., “Moderate exercise improves leucocyte function and decreases inflammation in diabetes,” Clinical and Experimental Immunology, vol. 162, no. 2, pp. 237–243, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. L. Bjork, N. T. Jenkins, S. Witkowski, and J. M. Hagberg, “Nitro-oxidative stress biomarkers in active and inactive men,” International Journal of Sports Medicine, vol. 33, no. 4, pp. 279–284, 2012.
  90. E. T. de Lemos, F. Reis, S. Baptista, et al., “Efeitos do exercício físico aeróbio no perfil metabólico e oxidativo de ratos diabéticos tipo 2,” Boletim da SPHM, vol. 22, no. 1, pp. 16–28, 2007.
  91. E. T. de Lemos, F. Reis, S. Baptista et al., “Exercise training is associated with improved levels of C-reactive protein and adiponectin in ZDF (type 2) diabetic rats,” Medical Science Monitor, vol. 13, no. 8, pp. BR168–BR174, 2007. View at Scopus
  92. E. Teixeira de Lemos, F. Reis, S. Baptista et al., “Exercise training decreases proinflammatory profile in Zucker diabetic (type 2) fatty rats,” Nutrition, vol. 25, no. 3, pp. 330–339, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. S. Lee, Y. Park, M. Y. Zuidema, M. Hannink, and C. Zhang, “Effects of interventions on oxidative stress and inflammation of cardiovascular diseases,” World Journal of Cardiology, vol. 3, no. 1, pp. 18–24, 2011.
  94. S. Golbidi and I. Laher, “Antioxidant therapy in human endocrine disorders,” Medical Science Monitor, vol. 16, no. 1, pp. RA9–RA24, 2010. View at Scopus
  95. T. S. Chang, C. S. Cho, S. Park, S. Yu, W. K. Sang, and G. R. Sue, “Peroxiredoxin III, a mitochondrion-specific peroxidase, regulates apoptotic signaling by mitochondria,” Journal of Biological Chemistry, vol. 279, no. 40, pp. 41975–41984, 2004. View at Publisher · View at Google Scholar · View at Scopus
  96. S. G. Rhee, S. W. Kang, T. S. Chang, W. Jeong, and K. Kim, “Peroxiredoxin, a novel family of peroxidases,” IUBMB Life, vol. 52, no. 1-2, pp. 35–41, 2001. View at Publisher · View at Google Scholar · View at Scopus
  97. C. E. Cooper, N. B. Vollaard, T. Choueiri, and M. T. Wilson, “Exercise, free radicals and oxidative stress,” Biochemical Society Transactions, vol. 30, no. 2, pp. 280–285, 2002. View at Scopus
  98. M. L. Urso and P. M. Clarkson, “Oxidative stress, exercise, and antioxidant supplementation,” Toxicology, vol. 189, no. 1-2, pp. 41–54, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. C. K. Roberts, D. Won, S. Pruthi, S. S. Lin, and R. J. Barnard, “Effect of a diet and exercise intervention on oxidative stress, inflammation and monocyte adhesion in diabetic men,” Diabetes Research and Clinical Practice, vol. 73, no. 3, pp. 249–259, 2006. View at Publisher · View at Google Scholar · View at Scopus
  100. H. Nojima, H. Watanabe, K. Yamane et al., “Effect of aerobic exercise training on oxidative stress in patients with type 2 diabetes mellitus,” Metabolism, vol. 57, no. 2, pp. 170–176, 2008. View at Publisher · View at Google Scholar · View at Scopus
  101. T. P. Wycherley, G. D. Brinkworth, M. Noakes, J. D. Buckley, and P. M. Clifton, “Effect of caloric restriction with and without exercise training on oxidative stress and endothelial function in obese subjects with type 2 diabetes,” Diabetes, Obesity and Metabolism, vol. 10, no. 11, pp. 1062–1073, 2008. View at Publisher · View at Google Scholar · View at Scopus
  102. S. Golbidi, M. Badran, and I. Laher, “Antioxidant and anti-inflammatory effects of exercise in diabetic patients,” Experimental Diabetes Research, vol. 2012, Article ID 941868, 16 pages, 2012. View at Publisher · View at Google Scholar
  103. Z. Radák, M. Sasvári, C. Nyakas et al., “Regular training modulates the accumulation of reactive carbonyl derivatives in mitochondrial and cytosolic fractions of rat skeletal muscle,” Archives of Biochemistry and Biophysics, vol. 383, no. 1, pp. 114–118, 2000. View at Publisher · View at Google Scholar · View at Scopus
  104. Y. Nishida, M. Iyadomi, Y. Higaki, H. Tanaka, M. Hara, and K. Tanaka, “Influence of physical activity intensity and aerobic fitness on the anthropometric index and serum uric acid concentration in people with obesity,” Internal Medicine, vol. 50, no. 19, pp. 2121–2128, 2011.
  105. F. Moien-Afshari, S. Ghosh, M. Khazaei, T. J. Kieffer, R. W. Brownsey, and I. Laher, “Exercise restores endothelial function independently of weight loss or hyperglycaemic status in db/db mice,” Diabetologia, vol. 51, no. 7, pp. 1327–1337, 2008. View at Publisher · View at Google Scholar · View at Scopus
  106. J. Hollander, R. Fiebig, M. Gore et al., “Superoxide dismutase gene expression in skeletal muscle: fiber-specific adaptation to endurance training,” American Journal of Physiology, vol. 277, no. 3, pp. R856–R862, 1999. View at Scopus
  107. Y. Zhi-Wen, L. Dan, L. Wen-Hua, and J. Tian-Ru, “Role of nuclear factor (erythroid-derived 2)-like 2 in metabolic homeostasis and insulin action: a novel opportunity for diabetes treatment?” World Journal of Diabetes, vol. 3, no. 1, pp. 19–28, 2012.
  108. J. S. Chen, P. H. Huang, C. H. Wang et al., “Nrf-2 mediated heme oxygenase-1 expression, an antioxidant-independent mechanism, contributes to anti-atherogenesis and vascular protective effects of Ginkgo biloba extract,” Atherosclerosis, vol. 214, no. 2, pp. 301–309, 2011. View at Publisher · View at Google Scholar · View at Scopus
  109. M. D. Ferrer, A. Sureda, J. M. Batle, P. Tauler, J. A. Tur, and A. Pons, “Scuba diving enhances endogenous antioxidant defenses in lymphocytes and neutrophils,” Free Radical Research, vol. 41, no. 3, pp. 274–281, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. A. M. Niess, F. Passek, I. Lorenz et al., “Expression of the antioxidant stress protein heme oxygenase-1 (HO-1) in human leukocytes: acute and adaptational responses to endurance exercise,” Free Radical Biology and Medicine, vol. 26, no. 1-2, pp. 184–192, 1999. View at Publisher · View at Google Scholar · View at Scopus
  111. J. Peake and K. Suzuki, “Neutrophil activation, antioxidant supplements and exercise-induced oxidative stress,” Exercise Immunology Review, vol. 10, pp. 129–141, 2004. View at Scopus
  112. T. Jansen, M. Hortmann, M. Oelze et al., “Conversion of biliverdin to bilirubin by biliverdin reductase contributes to endothelial cell protection by heme oxygenase-1-evidence for direct and indirect antioxidant actions of bilirubin,” Journal of Molecular and Cellular Cardiology, vol. 49, no. 2, pp. 186–195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  113. P. D. Thompson, S. F. Crouse, B. Goodpaster, D. Kelley, N. Moyna, and L. Pescatello, “The acute versus the chronic response to exercise,” Medicine and Science in Sports and Exercise, vol. 33, no. 6, supplement, pp. S438–S445, 2001. View at Scopus
  114. H. M. Alessio, A. E. Hagerman, B. K. Fulkerson, J. Ambrose, R. E. Rice, and R. L. Wiley, “Generation of reactive oxygen species after exhaustive aerobic and isometric exercise,” Medicine and Science in Sports and Exercise, vol. 32, no. 9, pp. 1576–1581, 2000. View at Scopus
  115. J. Viña, A. Gimeno, J. Sastre et al., “Mechanism of free radical production in exhaustive exercise in humans and rats; role of xanthine oxidase and protection by allopurinol,” IUBMB Life, vol. 49, no. 6, pp. 539–544, 2000. View at Scopus
  116. R. T. Iborra, I. C. D. Ribeiro, M. Q. T. S. Neves et al., “Aerobic exercise training improves the role of high-density lipoprotein antioxidant and reduces plasma lipid peroxidation in type 2 diabetes mellitus,” Scandinavian Journal of Medicine and Science in Sports, vol. 18, no. 6, pp. 742–750, 2008. View at Publisher · View at Google Scholar · View at Scopus
  117. E. Teixeira de Lemos, R. Pinto, J. Oliveira, et al., “Differential effects of acute (extenuating) and chronic (training) exercise on inflammation and oxidative stress status in an animal model of type 2 diabetes mellitus,” Mediators of Inflammation, vol. 2011, Article ID 253061, 8 pages, 2011. View at Publisher · View at Google Scholar
  118. E. Teixeira-Lemos, S. Nunes, F. Teixeira, and F. Reis, “Regular physical exercise training assists in preventing type 2 diabetes development: focus on its antioxidant and anti-inflammatory properties,” Cardiovascular Diabetology, vol. 10, article 12, 2011. View at Publisher · View at Google Scholar · View at Scopus
  119. T. Fukai, M. R. Siegfried, M. Ushio-Fukai, Y. Cheng, G. Kojda, and D. G. Harrison, “Regulation of the vascular extracellular superoxide dismutase by nitric oxide and exercise training,” Journal of Clinical Investigation, vol. 105, no. 11, pp. 631–1639, 2000. View at Scopus
  120. N. Lauer, T. Suvorava, U. Rüther et al., “Critical involvement of hydrogen peroxide in exercise-induced up-regulation of endothelial NO synthase,” Cardiovascular Research, vol. 65, no. 1, pp. 254–262, 2005. View at Publisher · View at Google Scholar · View at Scopus
  121. J. Grijalva, S. Hicks, X. Zhao et al., “Exercise training enhanced myocardial endothelial nitric oxide synthase (eNOS) function in diabetic Goto-Kakizaki (GK) rats,” Cardiovascular Diabetology, vol. 7, article 34, 2008. View at Publisher · View at Google Scholar · View at Scopus
  122. T. P. Wycherley, G. D. Brinkworth, M. Noakes, J. D. Buckley, and P. M. Clifton, “Effect of caloric restriction with and without exercise training on oxidative stress and endothelial function in obese subjects with type 2 diabetes,” Diabetes, Obesity and Metabolism, vol. 10, no. 11, pp. 1062–1073, 2008. View at Publisher · View at Google Scholar · View at Scopus
  123. R. Hambrecht, V. Adams, S. Erbs et al., “Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase,” Circulation, vol. 107, no. 25, pp. 3152–3158, 2003. View at Publisher · View at Google Scholar · View at Scopus
  124. C. Leeuwenburgh and J. W. Heinecke, “Oxidative stress and antioxidants in exercise,” Current Medicinal Chemistry, vol. 8, no. 7, pp. 829–838, 2001. View at Scopus
  125. R. J. Johnson, D. H. Kang, D. Feig et al., “Is there a pathogenetic role for uric acid in hypertension and cardiovascular and renal disease?” Hypertension, vol. 41, no. 6, pp. 1183–1190, 2003. View at Publisher · View at Google Scholar · View at Scopus
  126. E. Manzato, “Uric acid: An old actor for a new role,” Internal and Emergency Medicine, vol. 2, no. 1, pp. 1–2, 2007. View at Publisher · View at Google Scholar · View at Scopus
  127. Y. Y. Sautin and R. J. Johnson, “Uric acid: the oxidant-antioxidant paradox,” Nucleosides, Nucleotides and Nucleic Acids, vol. 27, no. 6-7, pp. 608–619, 2008. View at Publisher · View at Google Scholar · View at Scopus
  128. G. Lazarevic, S. Antic, T. Cvetkovic, P. Vlahovic, I. Tasic, and V. Stefanovic, “A physical activity programme and its effects on insulin resistance and oxidative defense in obese male patients with type 2 diabetes mellitus,” Diabetes and Metabolism, vol. 32, no. 6, pp. 583–590, 2006. View at Publisher · View at Google Scholar · View at Scopus
  129. R. S. Rector, S. O. Warner, Y. Liu et al., “Exercise and diet induced weight loss improves measures of oxidative stress and insulin sensitivity in adults with characteristics of the metabolic syndrome,” American Journal of Physiology, vol. 293, no. 2, pp. E500–E506, 2007. View at Publisher · View at Google Scholar · View at Scopus
  130. H. K. Vincent, C. Bourguignon, and K. R. Vincent, “Resistance training lowers exercise-induced oxidative stress and homocysteine levels in overweight and obese older adults,” Obesity, vol. 14, no. 11, pp. 1921–1930, 2006. View at Scopus
  131. V. N. Oliveira, A. Bessa, M. L. Jorge, 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, vol. 37, no. 2, pp. 334–344, 2012.
  132. C. Kasapis and P. D. Thompson, “The effects of physical activity on serum C-reactive protein and inflammatory markers: a systematic review,” Journal of the American College of Cardiology, vol. 45, no. 10, pp. 1563–1569, 2005. View at Publisher · View at Google Scholar · View at Scopus
  133. K. E. Fallon, S. K. Fallon, and T. Boston, “The acute phase response and exercise: court and field sports,” British Journal of Sports Medicine, vol. 35, no. 3, pp. 170–173, 2001. View at Publisher · View at Google Scholar · View at Scopus
  134. U. N. Das, “Anti-inflammatory nature of exercise,” Nutrition, vol. 20, no. 3, pp. 323–326, 2004. View at Publisher · View at Google Scholar · View at Scopus
  135. A. M. W. Petersen and B. K. Pedersen, “The anti-inflammatory effect of exercise,” Journal of Applied Physiology, vol. 98, no. 4, pp. 1154–1162, 2005. View at Publisher · View at Google Scholar · View at Scopus
  136. R. Starkie, S. R. Ostrowski, S. Jauffred, M. Febbraio, and B. K. Pedersen, “Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans,” The FASEB Journal, vol. 17, no. 8, pp. 884–886, 2003. View at Scopus
  137. B. K. Pedersen and M. A. Febbraio, “Muscle as an endocrine organ: focus on muscle-derived interleukin-6,” Physiological Reviews, vol. 88, no. 4, pp. 1379–1406, 2008. View at Publisher · View at Google Scholar · View at Scopus
  138. E. Z. Fisman and A. Tenenbaum, “The ubiquitous interleukin-6: a time for reappraisal,” Cardiovascular Diabetology, vol. 9, article 62, 2010. View at Publisher · View at Google Scholar · View at Scopus
  139. B. K. Pedersen, “IL-6 signalling in exercise and disease,” Biochemical Society Transactions, vol. 35, no. 5, pp. 1295–1297, 2007. View at Publisher · View at Google Scholar · View at Scopus
  140. M. A. Febbraio and B. K. Pedersen, “Muscle-derived interleukin-6: mechanisms for activation and possible biological roles,” The FASEB Journal, vol. 16, no. 11, pp. 1335–1347, 2002. View at Publisher · View at Google Scholar · View at Scopus
  141. P. Matthys, T. Mitera, H. Heremans, J. Van Damme, and A. Billiau, “Anti-gamma interferon and anti-interleukin-6 antibodies affect staphylococcal enterotoxin B-induced weight loss, hypoglycemia, and cytokine release in D-galactosamine-sensitized and unsensitized mice,” Infection and Immunity, vol. 63, no. 4, pp. 1158–1164, 1995. View at Scopus
  142. C. Keller, P. Keller, M. Giralt, J. Hidalgo, and B. K. Pedersen, “Exercise normalises overexpression of TNF-α in knockout mice,” Biochemical and Biophysical Research Communications, vol. 321, no. 1, pp. 179–182, 2004. View at Publisher · View at Google Scholar · View at Scopus
  143. K. R. Wilund, “Is the anti-inflammatory effect of regular exercise responsible for reduced cardiovascular disease?” Clinical Science, vol. 112, no. 11-12, pp. 543–555, 2007. View at Publisher · View at Google Scholar · View at Scopus
  144. K. A. Simpson and M. A. F. Singh, “Effects of exercise on adiponectin: a systematic review,” Obesity, vol. 16, no. 2, pp. 241–256, 2008. View at Publisher · View at Google Scholar · View at Scopus
  145. T. Yatagai, Y. Nishida, S. Nagasaka et al., “Relationship between exercise training-induced increase in insulin sensitivity and adiponectinemia in healthy men,” Endocrine Journal, vol. 50, no. 2, pp. 233–238, 2003. View at Publisher · View at Google Scholar · View at Scopus
  146. A. D. Kriketos, S. K. Gan, A. M. Poynten, S. M. Furler, D. J. Chisholm, and L. V. Campbell, “Exercise increases adiponectin levels and insulin sensitivity in humans,” Diabetes Care, vol. 27, no. 2, pp. 629–630, 2004. View at Publisher · View at Google Scholar · View at Scopus
  147. M. Blüher, J. W. Bullen, J. H. Lee et al., “Circulating adiponectin and expression of adiponectin receptors in human skeletal muscle: associations with metabolic parameters and insulin resistance and regulation by physical training,” Journal of Clinical Endocrinology and Metabolism, vol. 91, no. 6, pp. 2310–2316, 2006. View at Publisher · View at Google Scholar · View at Scopus
  148. L. Martin-Cordero, J. J. Garcia, E. Giraldo, M. De la Fuente, R. Manso, and E. Ortega, “Influence of exercise on the circulating levels and macrophage production of IL-1β and IFNγ affected by metabolic syndrome: an obese Zucker rat experimental animal model,” European Journal of Applied Physiology, vol. 107, no. 5, pp. 535–543, 2009. View at Publisher · View at Google Scholar · View at Scopus
  149. L. Martín-Cordero, J. J. García, M. D. Hinchado, E. Bote, R. Manso, and E. Ortega, “Habitual physical exercise improves macrophage IL-6 and TNF-α deregulated release in the obese zucker rat model of the metabolic syndrome,” NeuroImmunoModulation, vol. 18, no. 2, pp. 123–130, 2010. View at Publisher · View at Google Scholar · View at Scopus
  150. K. R. Rabin, Y. Kamari, I. Avni, E. Grossman, and Y. Sharabi, “Adiponectin: linking the metabolic syndrome to its cardiovascular consequences,” Expert Review of Cardiovascular Therapy, vol. 3, no. 3, pp. 465–471, 2005. View at Publisher · View at Google Scholar · View at Scopus
  151. R. L. Hull, G. T. Westermark, P. Westermark, and S. E. Kahn, “Islet amyloid: a critical entity in the pathogenesis of type 2 diabetes,” Journal of Clinical Endocrinology and Metabolism, vol. 89, no. 8, pp. 3629–3643, 2004. View at Publisher · View at Google Scholar · View at Scopus
  152. A. K. Andersson, M. Flodström, and S. Sandler, “Cytokine-induced inhibition of insulin release from mouse pancreatic β-cells deficient in inducible nitric oxide synthase,” Biochemical and Biophysical Research Communications, vol. 281, no. 2, pp. 396–403, 2001. View at Publisher · View at Google Scholar · View at Scopus
  153. M. Y. Donath, M. Böni-Schnetzler, H. Ellingsgaard, P. A. Halban, and J. A. Ehses, “Cytokine production by islets in health and diabetes: cellular origin, regulation and function,” Trends in Endocrinology and Metabolism, vol. 21, no. 5, pp. 261–267, 2010. View at Publisher · View at Google Scholar · View at Scopus
  154. K. Minato, Y. Shiroya, Y. Nakae, and T. Kondo, “The effect of chronic exercise on the rat pancreas,” International Journal of Pancreatology, vol. 27, no. 2, pp. 151–156, 2000.
  155. K. Shima, Z. Min, Y. Noma et al., “Exercise training in Otsuka Long-Evans Tokushima Fatty rat, a model of spontaneous non-insulin-dependent diabetes mellitus: effects on the B-cell mass, insulin content and fibrosis in the pancreas,” Diabetes Research and Clinical Practice, vol. 35, no. 1, pp. 11–19, 1997. View at Publisher · View at Google Scholar · View at Scopus
  156. F. Dela, M. E. von Linstow, K. J. Mikine, and H. Galbo, “Physical training may enhance beta-cell function in type 2 diabetes,” American Journal of Physiology, vol. 287, no. 5, pp. 1024–1031, 2004.
  157. B. K. Pedersen, “The diseasome of physical inactivity—and the role of myokines in muscle-fat cross talk,” Journal of Physiology, vol. 587, no. 23, pp. 5559–5568, 2009. View at Publisher · View at Google Scholar · View at Scopus
  158. M. C. Gomez-Cabrera, E. Domenech, M. Romagnoli et al., “Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance,” American Journal of Clinical Nutrition, vol. 87, no. 1, pp. 142–149, 2008. View at Scopus
  159. M. C. Gomez-Cabrera, E. Domenech, and J. Viña, “Moderate exercise is an antioxidant: upregulation of antioxidant genes by training,” Free Radical Biology and Medicine, vol. 44, no. 2, pp. 126–131, 2008. View at Publisher · View at Google Scholar · View at Scopus
  160. S. Sachdev and K. J. A. Davies, “Production, detection, and adaptive responses to free radicals in exercise,” Free Radical Biology and Medicine, vol. 44, no. 2, pp. 215–223, 2008. View at Publisher · View at Google Scholar · View at Scopus