The ability of exercise-associated oxidative stress to trigger redox-sensitive signalling responses

Antioxidants

Volumn 6, Issue 3, 2017, Pages

  Webb, Richard ^a   Hughes, Michael G ^a   Thomas, Andrew W ^a   Morris, Keith ^a  

^a CARDIFF METROPOLITAN UNIVERSITY   (United Kingdom)

Author keywords

Chronic inflammatory conditions; Free radicals; Hormesis; Liver X receptor alpha (LXR ); Oxidative stress; Peroxisome proliferator activated receptor gamma (PPAR ); Redox sensitive cell signalling

Indexed keywords

EID: 85027357889     PISSN: None     EISSN: 20763921     Source Type: Journal    
DOI: 10.3390/antiox6030063     Document Type: Review

References (118)

1. Evans, L.W.; Omaye, S.T. Use of Saliva Biomarkers to Monitor Efficacy of Vitamin C in Exercise-Induced Oxidative Stress. Antioxidants 2017, 6, 5. [CrossRef] [PubMed]
2. McLeay, Y.; Stannard, S.; Houltham, S.; Starck, C. Dietary thiols in exercise: Oxidative stress defence, exercise performance, and adaptation. J. Int. Soc. Sports Nutr. 2017, 14, 1–8. [CrossRef] [PubMed]
3. Steinbacher, P. Impact of oxidative stress on exercising skeletal muscle. Biomolecules 2015, 5, 356–377. [CrossRef] [PubMed]
4. Bild, W.; Ciobica, A.; Padurariu, M.; Bild, V. The interdependence of the reactive species of oxygen, nitrogen, and carbon. J. Physiol. Biochem. 2013, 69, 147–154. [CrossRef] [PubMed]
5. Harman, D. Aging: A theory based on free radical and radiation chemistry. J. Gerontol. 1956, 11, 298–300. [CrossRef] [PubMed]
6. Desler, C.; Marcker, M.L.; Singh, K.K.; Rasmussen, L.J. The importance of mitochondrial DNA in aging and cancer. J. Aging Res. 2011, 407536, 1–9. [CrossRef] [PubMed]
7. Lagouge, M.; Larsson, N.G. The role of mitochondrial DNA mutations and free radicals in disease and ageing. J. Intern. Med. 2013, 273, 529–543. [CrossRef] [PubMed]
8. Jackson, M.J. Control of reactive oxygen species production in contracting skeletal muscle. Antioxid. Redox Signal. 2011, 15, 2477–2486. [CrossRef] [PubMed]
9. Powers, S.K.; Jackson, M.J. Exercise-induced oxidative stress: Cellular mechanisms and impact on muscle force production. Physiol. Rev. 2008, 88, 1243–1276. [CrossRef] [PubMed]
10. Vasilaki, A.; Mansouri, A.; van Remmen, H.; van der Meulen, J.H.; Larkin, L.; Richardson, A.G.; McArdle, A.; Faulkner, J.A.; Jackson, M.J. Free radical generation by skeletal muscle of adult and old mice: Effect of contractile activity. Aging Cell 2006, 5, 109–117. [CrossRef] [PubMed]
11. Palomero, J.; Pye, D.; Kabayo, T.; Spiller, D.G.; Jackson, M.J. In situ detection and measurement of intracellular reactive oxygen species in single isolated mature skeletal muscle fibers by real time fluorescence microscopy. Antioxid. Redox Signal. 2008, 10, 1463–1474. [CrossRef] [PubMed]
12. Teixeira de Lemos, E.; Pinto, R.; Oliveira, J.; Garrido, P.; Sereno, J.; Mascarenhas-Melo, F.; Páscoa-Pinheiro, J.; Teixeira, F.; Reis, F. Differential effects of acute (extenuating) and chronic (training) exercise on inflammation and oxidative stress status in an animal model of type 2 diabetes mellitus. Mediat. Inflamm. 2011, 2011, 253061. [CrossRef] [PubMed]
13. Luo, H.; Chiang, H.H.; Louw, M.; Susanto, A.; Chen, D. Nutrient Sensing and the Oxidative Stress Response. Trends Endocrinol. Metab. 2017, 28, 449–460. [CrossRef] [PubMed]
14. Balaban, R.S.; Nemoto, S.; Finkel, T. Mitochondria, oxidants, and aging. Cell 2005, 120, 483–495. [CrossRef] [PubMed]
15. Lane, N. The Vital Question: Why Is Life the Way It Is? 1st ed.; Profile Books Ltd.: London, UK, 2015; pp. 237–279. ISBN 9781781250365.
16. Douarre, C.; Sourbier, C.; Dalla Rosa, I.; Brata Das, B.; Redon, C.E.; Zhang, H.; Neckers, L.; Pommier, Y. Mitochondrial topoisomerase I is critical for mitochondrial integrity and cellular energy metabolism. PLoS ONE 2012, 7, 1–12. [CrossRef] [PubMed]
17. Khiati, S.; Baechler, S.A.; Factor, V.M.; Zhang, H.; Huang, S.Y.; Dalla Rosa, I.; Sourbier, C.; Neckers, L.; Thorgeirsson, S.S.; Pommier, Y. Lack of mitochondrial topoisomerase I (TOP1mt) impairs liver regeneration. Proc. Natl. Acad. Sci. USA 2015, 112, 11282–11287. [CrossRef] [PubMed]
18. Irrcher, I.; Ljubicic, V.; Hood, D.A. 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–C123. [CrossRef] [PubMed]
19. Safdar, A.; Little, J.P.; Stokl, A.J.; Hettinga, B.P.; Akhtar, M.; Tarnopolsky, M.A. Exercise increases mitochondrial PGC-1alpha content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J. Biol. Chem. 2011, 286, 10605–10617. [CrossRef] [PubMed]
20. Russell, A.P.; Wada, S.; Vergani, L.; Hock, M.B.; Lamon, S.; Léger, B.; Ushida, T.; Cartoni, R.; Wadley, G.D.; Hespel, P.; et al. Disruption of skeletal muscle mitochondrial network genes and miRNAs in amyotrophic lateral sclerosis. Neurobiol. Dis. 2013, 49, 107–117. [CrossRef] [PubMed]
21. Lin, J.; Wu, H.; Tarr, P.T.; Zhang, C.Y.; Wu, Z.; Boss, O.; Michael, L.F.; Puigserver, P.; Isotani, E.; Olson, E.N.; et al. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 2002, 418, 797–801. [CrossRef] [PubMed]
22. Calvo, J.A.; Daniels, T.G.; Wang, X.; Paul, A.; Lin, J.; Spiegelman, B.M.; Stevenson, S.C.; Rangwala, S.M. Muscle-specific expression of PPARgamma coactivator-1alpha improves exercise performance and increases peak oxygen uptake. J. Appl. Physiol. 2008, 104, 1304–1312. [CrossRef] [PubMed]
23. Russell, A.P.; Foletta, V.C.; Snow, R.J.; Wadley, G.D. Skeletal muscle mitochondria: A major player in exercise, health and disease. Biochim. Biophys. Acta 2014, 1840, 1276–1284. [CrossRef] [PubMed]
24. Keller, P.; Vollaard, N.B.; Gustafsson, T.; Gallagher, I.J.; Sundberg, C.J.; Rankinen, T.; Britton, S.L.; Bouchard, C.; Koch, L.G.; Timmons, J.A. A transcriptional map of the impact of endurance exercise training on skeletal muscle phenotype. J. Appl. Physiol. 2011, 110, 46–59. [CrossRef] [PubMed]
25. Gomez-Cabrera, M.C.; Domenech, E.; Romagnoli, M.; Arduini, A.; Borras, C.; Pallardo, F.V.; Sastre, J.; Viña, J. 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. [PubMed]
26. Li, Y.; Zhu, H.; Kuppusamy, P.; Zweier, J.L.; Trush, M.A. Mitochondrial Electron Transport Chain-Derived Superoxide Exits Macrophages: Implications for Mononuclear Cell-Mediated Pathophysiological Processes. React. Oxyg. Species (Apex) 2016, 1, 81–98. [CrossRef] [PubMed]
27. Nagy, L.; Tontonoz, P.; Alvarez, J.G.; Chen, H.; Evans, R.M. Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell 1998, 93, 229–240. [CrossRef]
28. Amanso, A.; Lyle, A.N.; Griendling, K.K. NADPH Oxidases and Measurement of Reactive Oxygen Species. Methods Mol. Biol. 2017, 1527, 219–232. [CrossRef] [PubMed]
29. Poli, G.; Biasi, F.; Leonarduzzi, G. Oxysterols in the pathogenesis of major chronic diseases. Redox Biol. 2013, 1, 125–130. [CrossRef] [PubMed]
30. Khassaf, M.; McArdle, A.; Esanu, C.; Vasilaki, A.; McArdle, F.; Griffiths, R.D.; Brodie, D.A.; Jackson, M.J. Effect of Vitamin C supplements on antioxidant defence and stress proteins in human lymphocytes and skeletal muscle. J. Physiol. 2003, 549 Pt 2, 645–652. [CrossRef] [PubMed]
31. Davies, N.A.; Watkeys, L.; Butcher, L.; Potter, S.; Hughes, M.G.; Moir, H.; Morris, K.; Thomas, A.W.; Webb, R. The contributions of oxidative stress, oxidised lipoproteins and AMPK towards exercise-associated PPARγ signalling within human monocytic cells. Free Radic. Res. 2015, 49, 45–56. [CrossRef] [PubMed]
32. Butcher, L.; Backx, K.; Roberts, A.; Thomas, A.; Webb, R.; Morris, K. Low-intensity exercise exerts beneficial effects on plasma lipids via PPARγ. Med. Sci. Sports Exerc. 2008, 40, 1–7. [CrossRef] [PubMed]
33. Thompson, P.W.; Bayliffe, A.I.; Warren, A.P.; Lamb, J.R. Interleukin-10 is upregulated by nanomolar rosiglitazone treatment of mature dendritic cells and human CD4+ T cells. Cytokine 2007, 39, 184–191. [CrossRef] [PubMed]
34. Yoo, H.Y.; Chang, M.S.; Rho, H.M. Induction of the rat Cu/Zn superoxide dismutase gene through the peroxisome proliferator-responsive element by arachidonic acid. Gene 1999, 234, 87–91. [CrossRef]
35. Zhou, Y.; Jia, S.; Wang, C.; Chen, Z.; Chi, Y.; Li, J.; Xu, G.; Guan, Y.; Yang, J. FAM3A is a target gene of peroxisome proliferator-activated receptor gamma. Biochim. Biophys. Acta 2013, 1830, 4160–4170. [CrossRef] [PubMed]
36. Nunn, A.V.; Bell, J.; Barter, P. The integration of lipid-sensing and anti-inflammatory effects: How the PPARs play a role in metabolic balance. Nucl. Recept. 2007, 5, 1–13. [CrossRef] [PubMed]
37. Janowski, B.A.; Willy, P.J.; Devi, T.R.; Falck, J.R.; Mangelsdorf, D.J. An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature 1996, 383, 728–731. [CrossRef] [PubMed]
38. Mitro, N.; Mak, P.A.; Vargas, L.; Godio, C.; Hampton, E.; Molteni, V.; Kreusch, A.; Saez, E. The nuclear receptor LXR is a glucose sensor. Nature 2007, 445, 219–223. [CrossRef] [PubMed]
39. Li, Y.; Bolten, C.; Bhat, B.G.; Woodring-Dietz, J.; Li, S.; Prayaga, S.K.; Xia, C.; Lala, D.S. Induction of human liver X receptor alpha gene expression via an autoregulatory loop mechanism. Mol. Endocrinol. 2002, 16, 506–514. [CrossRef] [PubMed]
40. Pawar, A.; Botolin, D.; Mangelsdorf, D.J.; Jump, D.B. The role of liver X receptor-alpha in the fatty acid regulation of hepatic gene expression. J. Biol. Chem. 2003, 278, 40736–40743. [CrossRef] [PubMed]
41. Kennedy, M.A.; Venkateswaran, A.; Tarr, P.T.; Xenarios, I.; Kudoh, J.; Shimizu, N.; Edwards, P.A. Characterization of the human ABCG1 gene: Liver X receptor activates an internal promoter that produces a novel transcript encoding an alternative form of the protein. J. Biol. Chem. 2001, 276, 39438–39447, Erratum in: J. Biol. Chem. 2002, 277, 17375. [CrossRef] [PubMed]
42. Li, A.C.; Glass, C.K. PPAR- and LXR-dependent pathways controlling lipid metabolism and the development of atherosclerosis. J. Lipid Res. 2004, 45, 2161–2173. [CrossRef] [PubMed]
43. Hetzel, M.; Walcher, D.; Grüb, M.; Bach, H.; Hombach, V.; Marx, N. Inhibition of MMP-9 expression by PPARγ activators in human bronchial epithelial cells. Thorax 2003, 58, 778–783. [CrossRef] [PubMed]
44. Schroen, D.J.; Brinckerhoff, C.E. Nuclear hormone receptors inhibit matrix metalloproteinase (MMP) gene expression through diverse mechanisms. Gene Expr. 1996, 6, 197–207. [PubMed]
45. Novak, U.; Cocks, B.G.; Hamilton, J.A. A labile repressor acts through the NF-κB-like binding sites of the human urokinase gene. Nucleic Acids Res. 1991, 19, 3389–3393. [CrossRef] [PubMed]
46. Lee, W.; Mitchell, P.; Tjian, R. Purified transcription factor AP-1 interacts with TPA-inducible enhancer elements. Cell 1987, 49, 741–752. [CrossRef]
47. Thompson, J.E.S.; Webb, R.; Hewlett, P.; Llewellyn, D.; McDonnell, B.J. Matrix metalloproteinase-9 and augmentation index are reduced with an 8-week green-exercise walking programme. J. Hypertens. 2013, 2, 127–133. [CrossRef]
48. Calabrese, E.J.; Baldwin, L.A. Defining hormesis. Hum. Exp. Toxicol. 2002, 21, 91–97. [CrossRef] [PubMed]
49. Radak, Z.; Chung, H.Y.; Koltai, E.; Taylor, A.W.; Goto, S. Exercise, oxidative stress and hormesis. Ageing Res. Rev. 2007, 7, 34–42. [CrossRef] [PubMed]
50. Ristow, M.; Zarse, K.; Oberbach, A.; Klöting, N.; Birringer, M.; Kiehntopf, M.; Stumvoll, M.; Kahn, C.R.; Blüher, M. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc. Natl. Acad. Sci. USA 2009, 106, 8665–8670. [CrossRef] [PubMed]
51. Gems, D.; Partridge, L. Stress-Response Hormesis and Aging: That Which Dones Not Kill Us Makes Us Stronger. Cell Metabolism 2008, 7, 200–203. [CrossRef] [PubMed]
52. McArdle, F.; Spiers, S.; Aldemir, H.; Vasilaki, A.; Beaver, A.; Iwanejko, L.; McArdle, A.; Jackson, M.J. Preconditioning of skeletal muscle against contraction-induced damage: The role of adaptations to oxidants in mice. J. Physiol. 2004, 561 Pt 1, 233–244. [CrossRef] [PubMed]
53. Mahoney, D.J.; Parise, G.; Melov, S.; Safdar, A.; Tarnopolsky, M.A. Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J. 2005, 19, 1498–1500. [CrossRef] [PubMed]
54. Thomas, A.W.; Davies, N.A.; Moir, H.; Watkeys, L.; Ruffino, J.-S.; Isa, S.A.; Butcher, L.R.; Hughes, M.G.; Morris, K.; Webb, R. Exercise-associated generation of PPARγ ligands activates PPARγ signalling events and upregulates genes related to lipid metabolism. J. Appl. Physiol. 2012, 112, 806–815. [CrossRef] [PubMed]
55. Ruffino, J.-S.; Davies, N.A.; Morris, K.; Ludgate, M.; Zhang, L.; Webb, R.; Thomas, A.W. Moderate-intensity exercise alters monocyte M1 and M2 marker gene expression in sedentary females: Putative roles for PPARγ and IL-6. Eur. J. Appl. Physiol. 2016, 116, 1671–1682. [CrossRef] [PubMed]
56. Webb, R.; Thompson, J.E.S.; Ruffino, J.-S.; Davies, N.A.; Watkeys, L.; Hooper, S.; Jones, P.M.; Walters, G.; Clayton, D.; Thomas, A.W.; et al. An Evaluation of Cardiovascular Risk-Lowering Health Benefits Accruing from Laboratory-based, Community-based and Exercise-Referral Exercise Programmes. BMJ Open Sport Exerc. Med. 2016, 2, e000089. [CrossRef] [PubMed]
57. Yakeu, G.; Butcher, L.; Isa, S.; Webb, R.; Roberts, A.; Thomas, A.W.; Backx, K.; James, P.E.; Morris, K. Low-intensity exercise triggers monocyte polarisation into the M2 anti-inflammatory phenotype. Atherosclerosis 2010, 212, 668–673. [CrossRef] [PubMed]
58. Smith, S.A. Central role of the adipocyte in the insulin-sensitizing and cardiovascular risk modifying actions of the thiazolidinediones. Biochimie 2003, 85, 1219–1230. [CrossRef] [PubMed]
59. Brewer, H.B.; Remaley, A.T.; Neufeld, E.B.; Basso, F.; Joyce, C. Regulation of plasma high-density lipoprotein levels by the ABCA1 transporter and the emerging role of high-density lipoprotein in the treatment of cardiovascular disease. Arterioscler. Thromb. Vasc. Biol. 2004, 24, 1755–1760. [CrossRef] [PubMed]
60. Tsekouras, Y.E.; Yanni, A.E.; Bougatsas, D.; Kavouras, S.A.; Sidossis, L.S. A single bout of brisk walking increases basal very low-density lipoprotein triacylglycerol clearance in young men. Metabolism 2007, 56, 1037–1043. [CrossRef] [PubMed]
61. Szanto, A.; Balint, B.L.; Nagy, Z.S.; Barta, E.; Dezso, B.; Pap, A.; Szeles, L.; Poliska, S.; Oros, M.; Evans, R.M.; et al. STAT6 transcription factor is a facilitator of the nuclear receptor PPARγ-regulated gene expression in macrophages and dendritic cells. Immunity 2010, 33, 699–712. [CrossRef] [PubMed]
62. Katzmarzyk, P.T.; Church, T.S.; Blair, S.N. Cardiorespiratory fitness attenuates the effects of the metabolic syndrome on all-cause and cardiovascular disease mortality in men. Arch. Intern. Med. 2004, 164, 1092–1097. [CrossRef] [PubMed]
63. Schuch, F.B.; Vancampfort, D.; Richards, J.; Rosenbaum, S.; Ward, P.B.; Stubbs, B. Exercise as a treatment for depression: A meta-analysis adjusting for publication bias. Psychiatr. Res. 2016, 77, 42–51. [CrossRef] [PubMed]
64. Monteiro-Junior, R.S.; Cevada, T.; Oliveira, B.R.; Lattari, E.; Portugal, E.M.; Carvalho, A.; Deslandes, A.C. We need to move more: Neurobiological hypotheses of physical exercise as a treatment for Parkinson’s disease. Med. Hypotheses 2015, 85, 537–541. [CrossRef] [PubMed]
65. Ivanova, S.; Vasileva, L. Current and emerging strategies in osteoporosis management. Curr. Pharm. Des. 2017. [CrossRef]
66. Ruiz-Casado, A.; Martín-Ruiz, A.; Pérez, L.M.; Provencio, M.; Fiuza-Luces, C.; Lucia, A. Exercise and the Hallmarks of Cancer. Trends Cancer 2017, 3, 423–441. [CrossRef] [PubMed]
67. Olefsky, J.M.; Glass, C.K. Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 2010, 72, 219–246. [CrossRef] [PubMed]
68. Wynn, T.A.; Chawla, A.; Pollard, J.W. Macrophage biology in development, homeostasis and disease. Nature 2013, 496, 445–455. [CrossRef] [PubMed]
69. Hevener, A.L.; Olefsky, J.M.; Reichart, D.; Nguyen, M.T.; Bandyopadyhay, G.; Leung, H.Y.; Watt, M.J.; Benner, C.; Febbraio, M.A.; Nguyen, A.K.; et al. Macrophage PPARγ is required for normal skeletal muscle and hepatic insulin sensitivity and full antidiabetic effects of thiazolidinediones. J. Clin. Investig. 2007, 117, 1658–1669. [CrossRef] [PubMed]
70. Odegaard, J.I.; Ricardo-Gonzalez, R.R.; Goforth, M.H.; Morel, C.R.; Subramanian, V.; Mukundan, L.; Red Eagle, A.; Vats, D.; Brombacher, F.; Ferrante, A.W.; et al. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 2007, 447, 1116–1120. [CrossRef] [PubMed]
71. Meeusen, R. Exercise, nutrition and the brain. Sports Med. 2014, 1, S47–S56. [CrossRef] [PubMed]
72. Chen, W.; Zhang, X.; Huang, W.-J. Inflammation in neurodegenerative diseases. Mol. Med. Rep. 2016, 13, 3391–3396. [CrossRef] [PubMed]
73. Noh, H.; Jeon, J.; Seo, H. Systemic injection of LPS induces region-specific neuroinflammation and mitochondrial dysfunction in normal mouse brain. Neurochem. Int. 2014, 69, 35–40. [CrossRef] [PubMed]
74. Waisman, A.; Ginhoux, F.; Greter, M. Homeostasis of Microglia in the Adult Brain: Review of Novel Microglia Depletion Systems. Trends Immunol. 2015, 36, 625–636. [CrossRef] [PubMed]
75. Koizumi, S.; Shigemoto-Mogami, Y.; Nasu-Tada, K.; Shinozaki, Y.; Ohsawa, K.; Tsuda, M.; Joshi, B.V.; Jacobson, K.A.; Kohsaka, S.; Inoue, K. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 2007, 446, 1091–1109. [CrossRef] [PubMed]
76. Davalos, D.; Grutzendler, J.; Yang, G.; Kim, J.V.; Zuo, Y.; Jung, S.; Littman, D.R.; Dustin, M.L.; Gan, W.B. ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 2005, 8, 752–758. [CrossRef] [PubMed]
77. Nimmerjahn, A.; Kirchhoff, F.; Helmchen, F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308, 1314–1318. [CrossRef] [PubMed]
78. Orihuela, R.; McPherson, C.M.; Harry, G.J. Microglial M1/M2 polarization and metabolic states. Br. J. Pharmacol. 2016, 173, 649–665. [CrossRef] [PubMed]
79. Faustino, J.V.; Wang, X.; Johnson, C.E.; Klibanov, A.; Derugin, N.; Wendland, M.F.; Vexler, Z.S. Microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke. J. Neurosci. 2011, 31, 12992–13001. [CrossRef] [PubMed]
80. Miró-Mur, F.; Pérez-de-Puig, I.; Ferrer-Ferrer, M.; Urra, X.; Justicia, C.; Chamorro, A.; Planas, A.M. Immature monocytes recruited to the ischemic mouse brain differentiate into macrophages with features of alternative activation. Brain Behav. Immun. 2016, 53, 18–33. [CrossRef] [PubMed]
81. Wattananit, S.; Tornero, D.; Graubardt, N.; Memanishvili, T.; Monni, E.; Tatarishvili, J.; Miskinyte, G.; Ge, R.; Ahlenius, H.; Lindvall, O.; et al. Monocyte-Derived Macrophages Contribute to Spontaneous Long-Term Functional Recovery after Stroke in Mice. J. Neurosci. 2016, 36, 4182–4195. [CrossRef] [PubMed]
82. Lu, Y.; Dong, Y.; Tucker, D.; Wang, R.; Ahmed, M.E.; Brann, D.; Zhang, Q. Treadmill Exercise Exerts Neuroprotection and Regulates Microglial Polarization and Oxidative Stress in a Streptozotocin-Induced Rat Model of Sporadic Alzheimer’s Disease. J. Alzheimers Dis. 2017, 56, 1469–1484. [CrossRef] [PubMed]
83. Gleeson, M.; Bishop, N.C.; Stensel, D.J.; Lindley, M.R.; Mastana, S.S.; Nimmo, M.A. The anti-inflammatory effects of exercise: Mechanisms and implications for the prevention and treatment of disease. Nat. Rev. Immunol. 2011, 11, 607–615. [CrossRef] [PubMed]
84. DREAM (Diabetes REduction Assessment with ramipril and rosiglitazone Medication) Trial Investigators. Effect of rosiglitazone on the frequency of diabetes in patients with impaired glucose tolerance or impaired fasting glucose: A randomised controlled trial. Lancet 2006, 368, 1096–1105. [CrossRef]
85. Morton, J.P.; Kayani, A.C.; McArdle, A.; Drust, B. The exercise-induced stress response of skeletal muscle, with specific emphasis on humans. Sports Med. 2009, 39, 643–662. [CrossRef] [PubMed]
86. Marinangeli, C.P.; Varady, K.A.; Jones, P.J. Plant sterols combined with exercise for the treatment of hypercholesterolemia: Overview of independent and synergistic mechanisms of action. J. Nutr. Biochem. 2006, 17, 217–224. [CrossRef] [PubMed]
87. Kang, C.; O’Moore, K.M.; Dickman, J.R.; Ji, L.L. Exercise activation of muscle peroxisome proliferator-activated receptor-gamma coactivator-1alpha signaling is redox sensitive. Free Radic. Biol. Med. 2009, 47, 1394–1400. [CrossRef] [PubMed]
88. Petersen, A.C.; McKenna, M.J.; Medved, I.; Murphy, K.T.; Brown, M.J.; Della Gatta, P.; Cameron-Smith, D. Infusion with the antioxidant N-acetylcysteine attenuates early adaptive responses to exercise in human skeletal muscle. Acta Physiol. (Oxf.) 2012, 204, 382–392. [CrossRef] [PubMed]
89. Strobel, N.A.; Peake, J.M.; Matsumoto, A.; Marsh, S.A.; Coombes, J.S.; Wadley, G.D. Antioxidant supplementation reduces skeletal muscle mitochondrial biogenesis. Med. Sci. Sports Exerc. 2011, 43, 1017–1024. [CrossRef] [PubMed]
90. Cardenia, V.; Rodriguez-Estrada, M.T.; Lorenzini, A.; Bandini, E.; Angeloni, C.; Hrelia, S.; Malaguti, M. Effect of broccoli extract enriched diet on liver cholesterol oxidation in rats subjected to exhaustive exercise. J. Steroid. Biochem. Mol. Biol. 2017, 169, 137–144. [CrossRef] [PubMed]
91. Ryan, M.J.; Dudash, H.J.; Docherty, M.; Geronilla, K.B.; Baker, B.A.; Haff, G.G.; Cutlip, R.G.; Alway, S.E. Vitamin E and C supplementation reduces oxidative stress, improves antioxidant enzymes and positive muscle work in chronically loaded muscles of aged rats. Exp. Gerontol. 2010, 45, 882–895. [CrossRef] [PubMed]
92. Medved, I.; Brown, M.J.; Bjorksten, A.R.; Murphy, K.T.; Petersen, A.C.; Sostaric, S.; Gong, X.; McKenna, M.J. N-acetylcysteine enhances muscle cysteine and glutathione availability and attenuates fatigue during prolonged exercise in endurance-trained individuals. J. Appl. Physiol. 2004, 97, 1477–1485. [CrossRef] [PubMed]
93. Reid, M.B.; Stokić, D.S.; Koch, S.M.; Khawli, F.A.; Leis, A.A. N-acetylcysteine inhibits muscle fatigue in humans. J. Clin. Investig. 1994, 94, 2468–2474. [CrossRef] [PubMed]
94. Yfanti, C.; Akerström, T.; Nielsen, S.; Nielsen, A.R.; Mounier, R.; Mortensen, O.H.; Lykkesfeldt, J.; Rose, A.J.; Fischer, C.P.; Pedersen, B.K. Antioxidant supplementation does not alter endurance training adaptation. Med. Sci. Sports Exerc. 2010, 42, 1388–1395. [CrossRef] [PubMed]
95. Petersen, E.W.; Ostrowski, K.; Ibfelt, T.; Richelle, M.; Offord, E.; Halkjaer-Kristensen, J.; Pedersen, B.K. Effect of vitamin supplementation on cytokine response and on muscle damage after strenuous exercise. Am. J. Physiol. Cell Physiol. 2001, 280, C1570–C1575. [PubMed]
96. Higashida, K.; Kim, S.H.; Higuchi, M.; Holloszy, J.O.; Han, D.H. Normal adaptations to exercise despite protection against oxidative stress. Am. J. Physiol. Endocrinol. Metab. 2011, 301, E779–E784. [CrossRef] [PubMed]
97. Roberts, L.A.; Beattie, K.; Close, G.L.; Morton, J.P. Vitamin C consumption does not impair training-induced improvements in exercise performance. Int. J. Sports Physiol. Perform. 2011, 6, 58–69. [CrossRef] [PubMed]
98. Theodorou, A.A.; Nikolaidis, M.G.; Paschalis, V.; Koutsias, S.; Panayiotou, G.; Fatouros, I.G.; Koutedakis, Y.; Jamurtas, A.Z. No effect of antioxidant supplementation on muscle performance and blood redox status adaptations to eccentric training. Am. J. Clin. Nutr. 2011, 93, 1373–1383. [CrossRef] [PubMed]
99. Nikolaidis, M.G.; Kerksick, C.M.; Lamprecht, M.; McAnulty, S.R. Does Vitamin C and E supplementation impair the favorable adaptations of regular exercise? Oxid. Med. Cell. Longev. 2012, 707941, 1–11. [CrossRef] [PubMed]
100. Gomez-Cabrera, M.C.; Ristow, M.; Vina, J. Antioxidant supplements in exercise: Worse than useless? Am. J. Physiol. Endocrinol. Metab. 2012, 302, E476–E477. [CrossRef] [PubMed]
101. Sobal, J.; Marquart, L.F. Vitamin/mineral supplement use among athletes: A review of the literature. Int. J. Sport Nutr. 1994, 4, 320–334. [CrossRef] [PubMed]
102. National Institutes of Health (NIH) Office of Dietary Supplements Fact Sheets. Available online: https://ods.od.nih.gov/factsheets/list-all/(accessed on 30 June 2017).
103. UK National Health Service ”NHS Choices” Website. Available online: http://www.nhs.uk/Conditions/vitamins-minerals/Pages/Vitamin-E.aspx (accessed on 30 June 2017).
104. Bendich, A. Food and Nutrition Board Panel on Antioxidants and Related Compounds, Institute of Medicine and National Academy of Sciences. In Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium, and Carotenoids, 1st ed.; Glade, M.J., Ed.; National Academies Press: Washington, DC, USA, 2000; Volume 17, p. 364. ISBN 978-0-309-06935-9.
105. Novotny, J.A.; Fadel, J.G.; Holstege, D.M.; Furr, H.C.; Clifford, A.J. This kinetic, bioavailability, and metabolism study of RRR-α-tocopherol in healthy adults suggests lower intake requirements than previous estimates. J. Nutr. 2012, 142, 2105–2111. [CrossRef] [PubMed]
106. Jubri, Z.; Latif, A.A.; Top, A.G.; Ngah, W.Z. Perturbation of cellular immune functions in cigarette smokers and protection by palm oil Vitamin E supplementation. Nutr. J. 2013, 12, 2–9. [CrossRef] [PubMed]
107. Baker, H.; DeAngelis, B.; Baker, E.; Khalil, M.; Frank, O. Human plasma patterns during 14 days ingestion of Vitamin E, beta-carotene, ascorbic acid, and their various combinations. J. Am. Coll. Nutr. 1996, 15, 159–163. [CrossRef] [PubMed]
108. Levine, M.; Conry-Cantilena, C.; Wang, Y.; Welch, R.W.; Washko, P.W.; Dhariwal, K.R.; Park, J.B.; Lazarev, A.; Graumlich, J.F.; King, J.; et al. Vitamin C pharmacokinetics in healthy volunteers: Evidence for a recommended dietary allowance. Proc. Natl. Acad. Sci. USA 1996, 93, 3704–3709. [CrossRef] [PubMed]
109. Sánchez-Moreno, C.; Cano, M.P.; de Ancos, B.; Plaza, L.; Olmedilla, B.; Granado, F.; Martín, A. Effect of orange juice intake on Vitamin C concentrations and biomarkers of antioxidant status in humans. Am. J. Clin. Nutr. 2003, 78, 454–460. [PubMed]
110. Sánchez-Moreno, C.; Cano, M.P.; Ancos, B.; Plaza, L.; Olmedilla, B.; Granado, F.; Martín, A. High-pressurized orange juice consumption affects plasma Vitamin C, antioxidative status and inflammatory markers in healthy humans. J. Nutr. 2003, 133, 2204–2209. [PubMed]
111. Njus, D.; Kelley, P.M. Vitamins C and E donate single hydrogen atoms in vivo. FEBS Lett. 1991, 284, 147–151. [CrossRef]
112. Wolber, F.M.; McGrath, M.; Jackson, F.; Wylie, K.; Broomfield, A. Cysteic Acid in Dietary Keratin is Metabolized to Glutathione and Liver Taurine in a Rat Model of Human Digestion. Nutrients 2016, 8, 104. [CrossRef] [PubMed]
113. American College of Sports Medicine and the American Diabetes Association. Exercise and Type 2 Diabetes. Joint Position Statement. Med. Sci. Sports Exerc. 2010, 42, 2282–2303. [CrossRef]
114. Moore, G.F.; Raisanen, L.; Moore, L.; Ud Din, N.; Murphy, S. Mixed-method process evaluation of the Welsh National Exercise Referral Scheme. Health Educ. 2013, 113, 476–501. [CrossRef]
115. Hagger, M.S.; Wood, C.W.; Stiff, C.; Chatzisarantis, N.L.D. Self-regulation and self-control in exercise: The strength-energy model. Int. Rev. Sport Exerc. Psychol. 2010, 3, 62–86. [CrossRef]
116. Tierney, S.; Mamas, M.; Woods, S.; Rutter, M.K.; Gibson, M.; Neyses, L.; Deaton, C. What strategies are effective for exercise adherence in heart failure? A systematic review of controlled studies. Heart Fail Rev. 2012, 17, 107–115. [CrossRef] [PubMed]
117. Nissen, S.E.; Wolski, K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N. Engl. J. Med. 2007, 356, 2457–2471. [CrossRef] [PubMed]
118. Leal, I.; Romio, S.A.; Schuemie, M.; Oteri, A.; Sturkenboom, M.; Trifirò, G. Prescribing pattern of glucose lowering drugs in the United Kingdom in the last decade: A focus on the effects of safety warnings about rosiglitazone. Br. J. Clin. Pharmacol. 2013, 75, 861–868. [CrossRef] [PubMed]