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Oxidative Stress and Antioxidants in Disease and Cancer: A Review

  • Published : 2014.06.15

Abstract

Reactive oxygen species (ROS), highly reactive molecules, are produced by living organisms as a result of normal cellular metabolism and environmental factors, and can damage nucleic acids and proteins, thereby altering their functions. The human body has several mechanisms to counteract oxidative stress by producing antioxidants. A shift in the balance between oxidants and antioxidants in favor of oxidants is termed as "oxidative stress". Paradoxically, there is a large body of research demonstrating the general effect of oxidative stress on signaling pathways, less is known about the initial and direct regulation of signaling molecules by ROS, or what we term the "oxidative interface." This review focuses on the molecular mechanisms through which ROS directly interact with critical signaling molecules to initiate signaling in a broad variety of cellular processes, such as proliferation and survival (MAP kinases and PI3 kinase), ROS homeostasis, and antioxidant gene regulation (Ref-1 and Nrf-2). This review also deals with classification as well as mechanisms of formation of free radicals, examining their beneficial and deleterious effects on cellular activities and focusing on the potential role of antioxidants in preventing and repairing damage caused by oxidative stress. A discussion of the role of phytochemical antioxidants in oxidative stress, disease and the epigenome is included.

References

  1. Agarwal A, Banerjee A, Banerjee UC (2011). Xanthine oxidoreductase: a journey from purine metabolism to cardiovascular excitation-contraction coupling. Crit Rev Biotechnol, 31, 264-80. https://doi.org/10.3109/07388551.2010.527823
  2. Ambrus A, Torocsik B, Tretter L, et al (2011). Stimulation of reactive oxygen species generation by disease-causing mutations of lipoamide dehydrogenase. Hum Mol Genet, 20, 2984-95. https://doi.org/10.1093/hmg/ddr202
  3. Arts IC, Hollman PC (2005). Polyphenols and disease risk in epidemiologic studies. Am J Clin Nutr, 81, 317-25.
  4. Bors W, Michel C (2002). Chemistry of the antioxidant effect of polyphenols. Ann N Y Acad Sci, 957, 57-69. https://doi.org/10.1111/j.1749-6632.2002.tb02905.x
  5. Cantrell DA (2001). Phosphoinositide 3-kinase signalling pathways. J Cell Sci, 114, 1439-45.
  6. Bucci E (2009). Thermodynamic approach to oxygen delivery in vivo by natural and artificial oxygen carriers. Biophys Chem, 142, 1-6. https://doi.org/10.1016/j.bpc.2008.12.009
  7. Bylund J, Brown KL, Movitz C, et al (2010). Intracellular generation of superoxide by the phagocyte NADPH oxidase: how, where, and what for? Free Radic Biol Med, 49, 1834-45. https://doi.org/10.1016/j.freeradbiomed.2010.09.016
  8. Cai Z, Yan LJ (2013). Protein oxidative modifications: beneficial roles in disease and health. J Biochem Pharmacol Res, 1, 15-26.
  9. Chatterjee M, Saluja R, Kanneganti S,et al (2007). Biochemical and molecular evaluation of neutrophil NOS in spontaneously hypertensive rats. Cell Mol Biol, 53, 84-93.
  10. Choi DY, Lee YJ, Hong JT, et al (2012). Antioxidant properties of natural polyphenols and their therapeutic potentials for Alzheimer's disease. Brain Res Bull, 87, 144-153. https://doi.org/10.1016/j.brainresbull.2011.11.014
  11. Choi TG, Lee J, Ha J, et al (2011). Apoptosis signal-regulating kinase 1 is an intracellular inducer of p38 MAPK-mediated myogenic signalling in cardiac myoblasts. Biochim Biophys Acta, 1813, 1412-21. https://doi.org/10.1016/j.bbamcr.2011.04.001
  12. Chung HS, Wang SB, Venkatraman V, et al (2013). Cysteine oxidative posttranslational modifications: emerging regulation in the cardiovascular system. Circ Res, 112, 382-92. https://doi.org/10.1161/CIRCRESAHA.112.268680
  13. Devadas S, Zaritskaya L, Rhee SG, et al (2002). Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and fas ligand expression. J Exp Med, 10, 59-70.
  14. Donaldson MS (2004). Nutrition and cancer: A review of the evidence for an anti-cancer diet. Nutr J, 3, 19-25. https://doi.org/10.1186/1475-2891-3-19
  15. Ferguson LR, Schlothauer RC (2012). The potential role of nutritional genomics tools in validating high health foods for cancer control: broccoli as example. Mol Nutr Food Res, 56, 126-46. https://doi.org/10.1002/mnfr.201100507
  16. Drose S, Brandt U (2012). Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv Exp Med Biol, 748, 145-69. https://doi.org/10.1007/978-1-4614-3573-0_6
  17. Duthie SJ (2011). Epigenetic modifications and human pathologies: cancer and CVD. Proc Nutr Soc, 70, 47-56. https://doi.org/10.1017/S0029665110003952
  18. Fang J, Sawa T, Akaike T, et al (2002). Tumor-targeted delivery of polyethylene glycol-conjugated D-amino acid oxidase for antitumor therapy via enzymatic generation of hydrogen peroxide. Cancer Res, 62, 3138-43.
  19. Finkel T (2011). Signal transduction by reactive oxygen species. J Cell Biol, 194, 7-15. https://doi.org/10.1083/jcb.201102095
  20. Forester SC, Lambert JD (2011). The role of antioxidant versus pro-oxidant effects of green tea polyphenols in cancer prevention. Mol Nutr Food Res, 55, 844-54. https://doi.org/10.1002/mnfr.201000641
  21. Friedberg EC, Meira LB (2006). Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage version 7. DNA Repair, 5, 189-209. https://doi.org/10.1016/j.dnarep.2005.09.009
  22. Genestra M (2007). Oxyl radicals, redox-sensitive signalling cascades and antioxidants. Review. Cell Signal, 19, 1807-19. https://doi.org/10.1016/j.cellsig.2007.04.009
  23. Gloire G, Legrand-Poels S, Piette J (2006). NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem Pharmacol, 10, 1493-505.
  24. Gupta RK, Patel AK, Kumar R, et al (2012). Interactions between oxidative stress, lipid profile and antioxidants in breast cancer: a case control study. Asian Pac J Cancer Prev, 13, 6295-8. https://doi.org/10.7314/APJCP.2012.13.12.6295
  25. Hollman PC, Cassidy A, Comte B, et al (2011). The biological relevance of direct antioxidant effects of polyphenols for cardiovascular health in humans is not established. J Nutr, 141, 989-1009. https://doi.org/10.3945/jn.110.131490
  26. Gupta RK, Singh N (2013). Morinda citrifolia (Noni) alter oxidative stress marker and antioxidant activity in cervical cancer cell Lines. Asian Pac J Cancer Prev, 14, 4603-6. https://doi.org/10.7314/APJCP.2013.14.8.4603
  27. Halliwell B (2007). Biochemistry of oxidative stress. Biochem Soc Trans, 35, 1147-50. https://doi.org/10.1042/BST0351147
  28. Hildeman DA (2004). Regulation of T-cell apoptosis by reactive oxygen species. Free Radic Biol Med, 10, 1496-504.
  29. Ichijo H, Nishida E, Irie K, et al (1997). Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science, 275, 90-4. https://doi.org/10.1126/science.275.5296.90
  30. Jones DP (2006). Redefining oxidative stress. Antioxid Redox Signal, 10, 1865-79.
  31. Kareyeva AV, Grivennikova VG, Vinogradov AD (2012). Mitochondrial hydrogen peroxide production as determined by the pyridine nucleotide pool and its redox state. Biochim Biophys Acta, 1817, 1879-85. https://doi.org/10.1016/j.bbabio.2012.03.033
  32. Kwon J, Lee SR, Yang KS, et al (2004). Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc Natl Acad Sci USA, 101, 16419-24. https://doi.org/10.1073/pnas.0407396101
  33. Lambert JD, Elias RJ (2010). The antioxidant and pro-oxidant activities of green tea polyphenols: a role in cancer prevention. Arch Biochem Biophys, 501, 65-72. https://doi.org/10.1016/j.abb.2010.06.013
  34. Lee SR, Yang KS, Kwon J, et al (2002). Reversible inactivation of the tumor suppressor PTEN by $H_{2}O_{2}$. J Biol Chem, 277, 20336-42. https://doi.org/10.1074/jbc.M111899200
  35. Lenaz G (2012). Mitochondria and reactive oxygen species. Which role in physiology and pathology? Adv Exp Med Biol, 942, 93-136. https://doi.org/10.1007/978-94-007-2869-1_5
  36. Pacher P, Beckman JS, Liaudet L (2007). Nitric oxide and peroxynitrite in health and disease. Physiol Rev, 87, 315-424. https://doi.org/10.1152/physrev.00029.2006
  37. Leslie NR, Downes CP (2002). PTEN: The down side of PI 3-kinase signalling. Cell Signal, 14, 285-95. https://doi.org/10.1016/S0898-6568(01)00234-0
  38. Mittler R, Vanderauwera S, Suzuki N, et al (2011). ROS signaling: the new wave? Trends Plant Sci, 10, 300-9.
  39. Nicholson SK, Tucker GA, Brameld JM (2010). Physiological concentrations of dietary polyphenols regulate vascular endothelial cell expression of genes important in cardiovascular health. Br J Nutr, 103, 1398-403. https://doi.org/10.1017/S0007114509993485
  40. Perron NR, Wang HC, Deguire SN, et al (2010). Kinetics of iron oxidation upon polyphenol binding. Dalton Trans, 39, 9982-7. https://doi.org/10.1039/c0dt00752h
  41. Prokai L, Yan LJ, Vera-Serrano JL, et al (2007). Mass spectrometry-based survey of age-associated protein carbonylation in rat brain mitochondria. J Mass Spectrom, 42, 1583-9. https://doi.org/10.1002/jms.1345
  42. Ramos JW (2008). The regulation of extracellular signal-regulated kinase (ERK) in mammalian cells. Int J Biochem Cell Biol, 40, 2707-19. https://doi.org/10.1016/j.biocel.2008.04.009
  43. Rao RS, Moller IM (2011). Pattern of occurrence and occupancy of carbonylation sites in proteins. Proteomics, 11, 4166-73. https://doi.org/10.1002/pmic.201100223
  44. Ray PD, Huang BW, Tsuji Y (2012). Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal, 24, 981-90. https://doi.org/10.1016/j.cellsig.2012.01.008
  45. Sakamoto K, Iwasaki K, Sugiyama H, et al (2009). Role of the tumor suppressor PTEN in antioxidant responsive element-mediated transcription and associated histone modifications. Mol Biol Cell, 20, 1606-17. https://doi.org/10.1091/mbc.E08-07-0762
  46. Scalbert A, Johnson IT, Saltmarsh M (2005). Polyphenols: antioxidants and beyond. Am J Clin Nutr, 81, 215-7.
  47. Tell G, Quadrifoglio F, Tiribelli C, et al (2009). The many functions of APE1/Ref-1: not only a DNA repair enzyme. Antioxid Redox Signal, 11, 601-20. https://doi.org/10.1089/ars.2008.2194
  48. Seo JH, Ahn Y, Lee SR, et al (2005). The major target of the endogenously generated reactive oxygen species in response to insulin stimulation is phosphatase and tensin homolog and not phosphoinositide-3 kinase (PI-3 kinase) in the PI-3 kinase/Akt pathway. Mol Biol Cell, 16, 348-57.
  49. Spatafora C, Tringali C (2012). Natural-derived polyphenols as potential anticancer agents. Anticancer Agents Med Chem, 12, 902-18. https://doi.org/10.2174/187152012802649996
  50. Stadtman ER (2001). Protein oxidation in aging and age-related diseases. Ann N Y Acad Sci, 928, 22-38.
  51. Tobiume K, Matsuzawa A, Takahashi T, et al (2001). ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep, 2, 222-8. https://doi.org/10.1093/embo-reports/kve046
  52. Valko M, Rhodes CJ, Moncol J, et al (2006). Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact, 160, 1-40. https://doi.org/10.1016/j.cbi.2005.12.009
  53. Weston CR, Davis RJ (2007). The JNK signal transduction pathway. Curr Opin Cell Biol, 19, 142-9. https://doi.org/10.1016/j.ceb.2007.02.001
  54. Willcox JK, Ash SL, Catignani GL (2004). Antioxidants and prevention of chronic disease. Review. Crit Rev Food Sci Nutr, 44, 275-95. https://doi.org/10.1080/10408690490468489
  55. Wood LG, Wark PA, Garg ML (2010). Antioxidant and anti-inflammatory effects of resveratrol in airway disease. Antioxid Redox Signal, 13, 1535-48. https://doi.org/10.1089/ars.2009.3064
  56. Xanthoudakis S, Miao G, Wang F, et al (1992). Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO J, 11, 3323-35.
  57. Xanthoudakis S, Miao GG, Curran T (1994). The redox and DNA-repair activities of Ref-1 are encoded by nonoverlapping domains. Proc Natl Acad Sci USA, 91, 23-7. https://doi.org/10.1073/pnas.91.1.23
  58. Yan LJ, Sohal RS (1998). Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proc Natl Acad Sci USA, 95, 12896-901. https://doi.org/10.1073/pnas.95.22.12896
  59. Young I, Woodside J (2001). Antioxidants in health and disease. J Clin Pathol, 54, 176-86. https://doi.org/10.1136/jcp.54.3.176
  60. Zhang Q, Zou P, Zhan H, et al (2011). Dihydrolipoamide dehydrogenase and cAMP are associated with cadmium-mediated Leydig cell damage. Toxicol Lett, 205, 183-9. https://doi.org/10.1016/j.toxlet.2011.06.003

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