Simultaneous Activation of Nrf2 and Elevation of Dietary and Endogenous Antioxidant Chemicals for Cancer Prevention in Humans

Journal of the American College of Nutrition

Volumn 35, Issue 2, 2016, Pages 175-184

  Prasad, Kedar N ^a  

^a Antioxidant Research Institute   (United States)

Author keywords

antioxidant enzymes; chronic inflammation; oxidative stress; reactive oxygen species

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; BETA CAROTENE; CARESTOL; CARNITINE; CARNOSOL; COLECALCIFEROL; CURCUMIN; EPIGALLOCATECHIN GALLATE; FOLIC ACID; GENISTEIN; HISTONE H3; KAHWEOL; KELCH LIKE ECH ASSOCIATED PROTEIN 1; LYCOPENE; OMEGA 3 FATTY ACID; REACTIVE OXYGEN METABOLITE; RESVERATROL; RETINOL; SELENIUM; SELENOMETHIONINE; SULFORAPHANE; THIOCTIC ACID; TRANSCRIPTION FACTOR NRF2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ZERUMBONE; NFE2L2 PROTEIN, HUMAN;

CANCER INCIDENCE; CANCER PREVENTION; CANCER RISK; CHRONIC INFLAMMATION; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; DETOXIFICATION; DIET; ELECTROPHILIC STRESS; FREE RADICAL SCAVENGING ASSAY; GENE OVEREXPRESSION; HISTONE ACETYLATION; HUMAN; LUNG CANCER; OVARY CANCER; OXIDATIVE STRESS; PHYTOCHEMISTRY; PROSTATE CANCER; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; UPREGULATION; VITAMIN SUPPLEMENTATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASMS; PHYSIOLOGY;

ANTIOXIDANTS; DIET; GENE EXPRESSION REGULATION; HUMANS; NEOPLASMS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS;

EID: 84960278250     PISSN: 07315724     EISSN: 15411087     Source Type: Journal    
DOI: 10.1080/07315724.2014.1003419     Document Type: Review

References (86)

1. C.S.AmericanCancer Society: Facts and Figures, 2013.
2. K.N.Prasad: “Micronutrients in Cancer Prevention: Micronutrients in Health and Disease.” Boca raton, FL: CRC Press, pp 103–123, 2011.
3. A.Valavanidis, T.Vlachogianni, K.Fiotakis, S.Loridas: Pulmonary oxidative stress, inflammation and cancer: Respirable particulate matter, fibrous dusts and ozone as major causes of lung carcinogenesis through reactive oxygen species mechanisms. Int J Environ Res Public Health 10:3886–3907, 2013.
4. K.Kavitha, P.Thiyagarajan, J.Rathna Nandhini, R.Mishra, S.Nagini: Chemopreventive effects of diverse dietary phytochemicals against DMBA-induced hamster buccal pouch carcinogenesis via the induction of Nrf2-mediated cytoprotective antioxidant, detoxification, and DNA repair enzymes. Biochimie 95:1629–1639, 2013.
5. E.R.Kim, D.K.Chang,: Colorectal cancer in inflammatory bowel disease: The risk, pathogenesis, prevention and diagnosis. World J Gastroenterol 20:9872–9881, 2014.
6. S.Hardikar, L.Onstad, X.Song, et al: Inflammation and oxidative stress markers and esophageal adenocarcinoma incidence in a Barrett's esophagus cohort. Cancer Epidemiol Biomarkers Prev 2014.
7. B.Schottker, K.U.Saum, E.H.Jansen, P.Boffetta, A.Trichopoulou, B.Holleczek, A.K.Dieffenbach, H.Brenner: Oxidative stress markers and allcause mortality at older age: A pPopulation-based cohort study. J Gerontol A Biol Sci Med Sci 70:518–524, 2014.
8. Y.Yang, X.Cai, J.Yang, X.Sun, C.Hu, Z.Yan, X.Xu, W.Lu, X.Wang, P.Cao: Chemoprevention of dietary digitoflavone on colitis-associated colon tumorigenesis through inducing Nrf2 signaling pathway and inhibition of inflammation. Mol Cancer 13:48, 2014.
9. J.H.Lee, T.O.Khor, L.Shu, J.Y.Su, F.Fuentes, A.N.Kong: Dietary phytochemicals and cancer prevention: Nrf2 signaling, epigenetics, and cell death mechanisms in blocking cancer initiation and progression. Pharm Therapeutics 137:153–171, 2013.
10. J.Aoi, M.Endo, T.Kadomatsu, K.Miyata, A.Ogata, H.Horiguchi, H.Odagiri, T.Masuda, S.Fukushima, M.Jinnin, S.Hirakawa, T.Sawat, T.Akaiket, H.Ihn, Y.Oike: Angiopoietin-like protein 2 accelerates carcinogenesis by activating chronic inflammation and oxidative stress. Mol Cancer Res 12:239–249, 2014.
11. [No Authors]: Alpha-Tocopherol B-CCPSG: The effect of vitamin E and beta-carotene on the incidence of lung cancer and other cancers in male smokers. N Eng J Med 330:1029–1035, 1994.
12. D.Albanes, O.P.Heinonen, J.K.Huttunen, et al: Effects of alpha-tocopherol and beta-carotene supplements on cancer incidence in the Alpha-Tocopherol Beta-Carotene Cancer Prevention Study. Am J Clin Nutr 62:1427S–1430S, 1995.
13. D.Albanes, O.P.Heinonen, P.R.Taylor, et al: Alpha-Tocopherol and beta-carotene supplements and lung cancer incidence in the alpha-tocopherol, beta-carotene cancer prevention study: Effects of base-line characteristics and study compliance. J Natl Cancer Inst 88:1560–1570, 1996.
14. S.J.Weinstein, M.E.Wright, K.A.Lawson, et al: Serum and dietary vitamin E in relation to prostate cancer risk. Cancer Epidemiol Biomarkers Prev 16:1253–1259, 2007.
15. J.Virtamo, P.R.Taylor, J.Kontto, S.Maannisto, M.Utrianen, S.J.Weinstein, J.Huttunen, D.Albanes: Effects of alpha-tocopherol and beta-carotene supplementation on cancer incidence and mortality: 18-year postintervention follow-up of the Alpha-tocopherol, Beta-carotene Cancer Prevention Study. Int J Cancer 135:178–185, 2014.
16. L.Wang, H.D.Sesso, R.J.Glynn, W.G.Christen, V.Bubes, J.E.Manson, J.E.Buring, J.M.Gaziano: Vitamin E and C supplementation and risk of cancer in men: Posttrial follow-up in the Physicians' Health Study II randomized trial. Am J Clin Nutr 100:915–923, 2014.
17. P.H.Gann, J.Ma, E.Giovannucci, et al: Lower prostate cancer risk in men with elevated plasma lycopene levels: Results of a prospective analysis. Cancer Res 59:1225–1230, 1999.
18. K.Itoh, T.Chiba, S.Takahashi, T.Ishii, K.Igarashi, Y.Katoh, T.Oyake, N.Hayashi, K.Satoh, I.Hatayama, M.Yamamoto, Y.Nabeshima: An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochemical and biophysical research communications 236:313–322, 1997.
19. J.D.Hayes, S.A.Chanas, C.J.Henderson, M.McMahon, C.Sun, G.J.Moffat, C.R.Wolf, M.Yamamoto: The Nrf2 transcription factor contributes both to the basal expression of glutathione S-transferases in mouse liver and to their induction by the chemopreventive synthetic antioxidants, butylated hydroxyanisole and ethoxyquin. Biochem Soc Trans 28:33–41, 2000.
20. K.Chan, X.D.Han, Y.W.Kan: An important function of Nrf2 in combating oxidative stress: Detoxification of acetaminophen. Proc NatlAcad Sci USA 98:4611–4616, 2001.
21. C.P.Ramsey, C.A.Glass, M.B.Montgomery, K.A.Lindi, G.P.Ritson, L.A.Chia, R.L.Hamilton, C.T.Chu, K.L.Jordan-Sciutto: Expression of Nrf2 in neurodegenerative diseases. J Neuropathol Exp Neurol 66:75–85, 2007.
22. P.C.Chen, M.R.Vargas, A.K.Pani, R.J.Smeyne, D.A.Johnson, Y.W.Kan, J.A.Johnson: Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: Critical role for the astrocyte. Proc Natl Acad Sci USA 106:2933–2938, 2009.
23. I.Lastres-Becker, A.Ulusoy, N.G.Innamorato, G.Sahin, A.Rabano, D.Kirik, A.Cuadrado: Alpha-Synuclein expression and Nrf2 deficiency cooperate to aggravate protein aggregation, neuronal death and inflammation in early-stage Parkinson's disease. Hum Mol Genet 21:3173–3192, 2012.
24. M.C.Jaramillo, D.D.Zhang: The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev 27:2179–2191, 2013.
25. C.Geismann, A.Arlt, S.Sebens, H.Schafer: Cytoprotection “gone astray”: Nrf2 and its role in cancer. Onco Targets Ther 7:1497–1518, 2014.
26. A.Namani, Y.Li, X.J.Wang, X.Tang: Modulation of NRF2 signaling pathway by nuclear receptors: Implications for cancer. Biochim Biophys Acta 1843:1875–1885, 2014.
27. B.Padmanabhan, K.I.Tong, T.Ohta, Y.Nakamura, M.Scharlock, M.Ohtsuji, M.I.Kang, A.Kobayashi, S.Yokoyama, M.Yamamoto: Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Molecular Cell 21:689–700, 2006.
28. T.Shibata, T.Ohta, K.I.Tong, A.Kokubu, R.Odogawa, K.Tsuta, H.Asamura, M.Yamamoto, S.Hirahashi: Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy. Proc Natl Acad Sci USA 105:13568–13573, 2008.
29. S.K.Niture, J.W.Kaspar, J.Shen, A.K.Jaiswal: Nrf2 signaling and cell survival. Toxicol Appl Pharmacol 244:37–42, 2010.
30. T.O.Khor, F.Fuentes, L.Shu, X.Paredes-Gonzales, A.Y.Yang, Y.Liu, D.J.Smoraglia, S.Yagasubramanian, W.G.Nelson, A.N.Kong: Epigenetic DNA Methylation of Anti-oxidative Stress Regulator Nrf2 in Human Prostate Cancer. Cancer Prev Res 7:1186–1197, 2014.
31. S.Yu, T.O.Khor, K.L.Cheung, W.Li, T.Y.Wu, Y.Huand, B.A.Foster, Y.W.Kan, A.Kong: Nrf2 expression is regulated by epigenetic mechanisms in prostate cancer of TRAMP mice. PloS One 5:e8579, 2010.
32. I.Stachel, C.Geismann, K.Aden, F.Deisinger, P.Rosenstiel, S.Schreibev, S.Sebens, A.Arit, H.Schafer: Modulation of nuclear factor E2-related factor-2 (Nrf2) activation by the stress response gene immediate early response-3 (IER3) in colonic epithelial cells: a novel mechanism of cellular adaption to inflammatory stress. J Biol Chem 289:1917–1929, 2014.
33. W.Jin, H.Wang, W.Yan, L.Zhu, Z.Hu, Y.Ding, K.Tang: Role of Nrf2 in protection against traumatic brain injury in mice. J Neurotrauma 26:131–139, 2009.
34. D.D.Zhang, S.C.Lo, J.V.Cross, D.J.Templeton, M.Hannink: Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol Cellular Biol 24:10941–10953, 2004.
35. N.F.Villeneuve, W.Tian, T.Wu, Z.Sun, A.Lau, E.Chapman, D.Fang, D.D.Zhang: USP15 negatively regulates Nrf2 through deubiquitination of Keap1. Mol Cell 51:68–79, 2013.
36. J.H.Suh, S.V.Shenvi, B.M.Dixon, H.Liu, A.K.Jaiswal, R.M.Liu, T.M.Hagen: Decline in transcriptional activity of Nrf2 causes age-related loss of glutathione synthesis, which is reversible with lipoic acid. Proc Natl Acad Sci USA 101:3381–3386, 2004.
37. K.S.Chun, J.Kundu, J.K.Kundu, Y.J.Surh: Targeting Nrf2-Keap1 signaling for chemoprevention of skin carcinogenesis with bioactive phytochemicals. Toxicol Lett 229:73–84, 2014.
38. W.S.Jeong, M.Jun, A.N.Kong: Nrf2: A potential molecular target for cancer chemoprevention by natural compounds. Antioxid Redox Signal 8:99–106, 2006.
39. Z.Y.Su, L.Shu, T.O.Khor, J.H.Lee, F.Fuentis, A.N.Kong: A perspective on dietary phytochemicals and cancer chemoprevention: Oxidative stress, nrf2, and epigenomics. Top Curr Chem 329:133–162, 2013.
40. P.Bergstrom, H.C.Andersson, Y.Gao, J.O.Karlsson, C.Nodin, M.F.Anderson, M.Nilsson, O.Hammarsten: Repeated transient sulforaphane stimulation in astrocytes leads to prolonged Nrf2-mediated gene expression and protection from superoxide-induced damage. Neuropharmacol 60:343–353, 2011.
41. C.J.Wruck, M.E.Gotz, T.Herdegen, T.Varogat, L.O.Brandenburg, T.Pufe: Kavalactones protect neural cells against amyloid beta peptide-induced neurotoxicity via extracellular signal-regulated kinase 1/2-dependent nuclear factor erythroid 2-related factor 2 activation. Mol Pharmacol 73:1785–1795, 2008.
42. Y.Zou, B.Hong, L.Fan, L.Zhou, Y.Liu, Q.Wu, X.Zhang, M.Dong: Protective effect of puerarin against beta-amyloid-induced oxidative stress in neuronal cultures from rat hippocampus: Involvement of the GSK-3beta/Nrf2 signaling pathway. Free Radic Res 47:55–63, 2013.
43. Y.D.Xi, H.L.Yu, J.Ding, W.W.Ma, L.H.Yuan, J.F.Feng, Y.X.Xiao, R.Xiao: Flavonoids protect cerebrovascular endothelial cells through Nrf2 and PI3K from beta-amyloid peptide-induced oxidative damage. Curr Neurovasc Res 9:32–41, 2012.
44. H.K.Choi, Y.R.Pokharel, S.C.Lim, H.K.Han, C.S.Ryu, S.K.Kim, M.K.Kwok, K.W.Kang: Inhibition of liver fibrosis by solubilized coenzyme Q10: Role of Nrf2 activation in inhibiting transforming growth factor-beta1 expression. Toxicol Appl Pharmacol 240:377–384, 2009
45. J.Trujillo, Y.I.Chirino, E.Molina-Jijon, A.C.Anderica-Romero, E.Tapia, J.Pedraza-Chaverri: Renoprotective effect of the antioxidant curcumin: Recent findings. Redox Biol 1:448–456, 2013.
46. M.L.Steele, S.Fuller, M.Patel, C.Kersaitis,, L.Ooi, G.Munch: Effect of Nrf2 activators on release of glutathione, cysteinylglycine and homocysteine by human U373 astroglial cells. Redox Biol 1:441–445, 2013.
47. A.Kode, S.Rajendrasozhan, S.Caito, S.R.Yang, I.L.Megson, I.Rahman: Resveratrol induces glutathione synthesis by activation of Nrf2 and protects against cigarette smoke-mediated oxidative stress in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol. 294:L478–488, 2008.
48. L.Gao, J.Wang, K.R.Sekhar, H.Yin, N.F.Yared, S.N.Schneider, S.Sasi, P.Dalton, M.E.Anderson, J.Y.Chan, J.D.Morrow, M.L.Freeman: Novel n-3 fatty acid oxidation products activate Nrf2 by destabilizing the association between Keap1 and Cullin3. J Biol Chem 282:2529–2537, 2007.
49. C.L.Saw, A.Y.Yang, Y.Guo, A.N.Kong: Astaxanthin and omega-3 fatty acids individually and in combination protect against oxidative stress via the Nrf2-ARE pathway. Food Chem Toxicol. 62:869–875, 2013.
50. L.Ji, R.Liu, X.D.Zhang, H.L.Chen, H.Bai, X.Wang, H.L.Zhao, X.Liang, C.X.Hai: N-acetylcysteine attenuates phosgene-induced acute lung injury via up-regulation of Nrf2 expression. Inhal Toxicol 22:535–542, 2010.
51. S.Zambrano, A.J.Blanca, M.V.Ruiz-Armenta, J.L.Miguel-Carrasco, E.Revilla, C.Santa-Maria, A.Mate, C.M.Vazquez: The renoprotective effect of L-carnitine in hypertensive rats is mediated by modulation of oxidative stress-related gene expression. EurJ Nutr 52:1649–1659, 2013.
52. W.Li, T.O.Khor, C.Xu, G.Shen, W.S.Jeong, S.Yu, A.N.Kong: Activation of Nrf2-antioxidant signaling attenuates NFkappaB-inflammatory response and elicits apoptosis. Biochem Pharmacol 76:1485–1489, 2008.
53. J.Kim, Y.N.Cha, Y.J.Surh: A protective role of nuclear factor-erythroid 2-related factor-2 (Nrf2) in inflammatory disorders. Mutat Res 690:12–23, 2010.
54. A.Abate, G.Yang, P.A.Dennery, et al: Synergistic inhibition of cyclooxygenase-2 expression by vitamin E and aspirin. Free Radic Biol Med 29:1135–1142, 2000.
55. S.Devaraj, R.Tang, B.Adams-Huet, et al: Effect of high-dose alpha-tocopherol supplementation on biomarkers of oxidative stress and inflammation and carotid atherosclerosis in patients with coronary artery disease. Am J Clin Nutr 86:1392–1398, 2007.
56. Y.Fu, S.Zheng, J.Lin, et al:Curcumin protects the rat liver from CCl4-caused injury and fibrogenesis by attenuating oxidative stress and suppressing inflammation. Mol Pharmacol 73:399–409, 2008.
57. H.S.Lee, K.K.Jung, J.Y.Cho, et al: Neuroprotective effect of curcumin is mainly mediated by blockade of microglial cell activation. Pharmazie 62:937–942, 2007.
58. A.T.Peairs, J.W.Rankin: Inflammatory Response to a High-fat, Low-carbohydrate Weight Loss Diet: Effect of Antioxidants. Obesity (Silver Spring) 16:1573–1578 2008.
59. S.Rahman, K.Bhatia, A.Q.Khan, et al: Topically applied vitamin E prevents massive cutaneous inflammatory and oxidative stress responses induced by double application of 12-O-tetradecanoylphorbol-13-acetate (TPA) in mice. Chem Biol Interact 172:195–205, 2008.
60. Y.J.Suzuki, B.B.Aggarwal, L.Packer: Alpha-lipoic acid is a potent inhibitor of NF-kappa B activation in human T cells. Biochem Biophys Res Commun 189:1709–1715, 1992.
61. J.Zhu, W.Yong, X.Wu, et al: Anti-inflammatory effect of resveratrol on TNF-alpha-induced MCP-1 expression in adipocytes. Biochem Biophys Res Commun 369:471–477, 2008.
62. S.J.Weinstein, M.E.Wright, P.Pietinen, et al: Serum alpha-tocopherol and gamma-tocopherol in relation to prostate cancer risk in a prospective study. J Natll Cancer Inst 97:396–399, 2005.
63. J.Virtamo, P.Pietinen, J.K.Huttunen, et al: Incidence of cancer and mortality following alpha-tocopherol and beta-carotene supplementation: A postintervention follow-up. JAMA 290:476–485, 2003.
64. J.M.Gaziano, H.D.Sesso, W.G.Christen, et al: Multivitamins in the prevention of cancer in men: The Physicians' Health Study II randomized controlled trial. JAMA 308:1871–1880, 2012.
65. C.H.Hennekens, J.E.Buring, J.E.Manson, et al: Lack of effect of long-term supplementation with beta carotene on the incidence of malignant neoplasms and cardiovascular disease. N Engl J Med 334:1145–1149, 1996.
66. N.R.Cook, I.M.Le, J.E.Manson, et al: Effects of beta-carotene supplementation on cancer incidence by baseline characteristics in the Physicians' Health Study (United States). Cancer Causes Control 11:617–626, 2000.
67. B.K.Dunn, E.S.Richmond, L.M.Minasian, et al: A nutrient approach to prostate cancer prevention: The Selenium and Vitamin E Cancer Prevention Trial (SELECT). Nutr Cancer 62:896–918, 2010.
68. E.A.Klein, I.M.Thompson, Jr., C.M.Tangen, et al: Vitamin E and the risk of prostate cancer: The Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 306:1549–1556, 2011.
69. A.R.Kristal, A.K.Darke, J.S.Morris, et al: Baseline selenium status and effects of selenium and vitamin e supplementation on prostate cancer risk. J Natli Cancer Inst 106:djt456, 2014.
70. W.G.Christen, R.J.Glynn, J.M.Gaziano, et al: Age-related cataract in men in the Selenium and Vitamin E Cancer Prevention Trial Eye Endpoints Study: A randomized clinical trial. JAMA Ophthalmol 133:17–24, 2014.
71. D.Albanes, C.Till, E.A.Klein, et al: Plasma tocopherols and risk of prostate cancer in the Selenium and Vitamin E Cancer Prevention Trial (SELECT). Cancer Prev Res 7:886–895, 2014.
72. J.Lin, N.R.Cook, C.Albert, et al: Vitamins C and E and beta carotene supplementation and cancer risk: A-a randomized controlled trial. J Natl Cancer Inst 101:14–23, 2009.
73. G.S.Omenn, G.E.Goodman, M.D.Thornquist, et al: Risk factors for lung cancer and for intervention effects in CARET, the Beta-Carotene and Retinol Efficacy Trial. J Natl Cancer Inst 88:1550–1559, 1996.
74. V.A.Kirsh, R.B.Hayes, S.T.Mayne, et al: Supplemental and dietary vitamin E, beta-carotene, and vitamin C intakes and prostate cancer risk. J Natli Cancer Inst 98:245–254, 2006.
75. U.Peters, M.F.Leitzmann, N.Chatterjee, et al: Serum lycopene, other carotenoids, and prostate cancer risk: A nested case-control study in the prostate, lung, colorectal, and ovarian cancer screening trial. Cancer Epidemiol Biomarkers Prev 16:962–968, 2007.
76. W.J.Blot, J.Y.Li, P.R.Taylor, et al: Nutrition intervention trials in Linxian, China: Supplementation with specific vitamin/mineral combinations, cancer incidence, and disease-specific mortality in the general population. J Nat Cancer Institute 85:1483–1492, 1993.
77. Y.L.Qiao, S.M.Dawsey, F.Kamangar, et al: Total and cancer mortality after supplementation with vitamins and minerals: Follow-up of the Linxian General Population Nutrition Intervention Trial. J Natl Cancer Inst 101:507–518, 2009.
78. E.D.Gorham, C.F.Garland, F.C.Garland, et al: Vitamin D and prevention of colorectal cancer. J Steroid Biochem Mol Biol 97:179–194, 2005.
79. J.Wactawski-Wende, J.M.Kotchen, G.L.Anderson, et al: Calcium plus vitamin D supplementation and the risk of colorectal cancer. N Engl J Med 354:684–696, 2006
80. R.T.Chlebowski, K.C.Johnson, C.Kooperberg, et al: Calcium plus vitamin D supplementation and the risk of breast cancer. J Natl Cancer Inst 100:1581–1591, 2008.
81. S.E.Vollset, R.Clarke, S.Lewington, et al: Effects of folic acid supplementation on overall and site-specific cancer incidence during the randomised trials: Meta-analyses of data on 50,000 individuals. Lancet 381:1029–1036, 2013
82. G.G.Duthie, J.R.Arthur, W.P.James: Effects of smoking and vitamin E on blood antioxidant status. Am J Clin Nutr 53:1061S–1063S, 1991.
83. H.Kiyosawa, M.Suko, H.Okudaira, et al: Cigarette smoking induces formation of 8-hydroxydeoxyguanosine, one of the oxidative DNA damages in human peripheral leukocytes. Free Radic Res Commun 11:23–27, 1990.
84. A.Z.Reznick, C.E.Cross, M.L.Hu, et al: Modification of plasma proteins by cigarette smoke as measured by protein carbonyl formation. Biochem J 286(Pt 2):607–611, 1992.
85. G.Schectman, J.C.Byrd, R.Hoffmann: Ascorbic acid requirements for smokers: Analysis of a population survey. Am J Clin Nutr 53:1466–1470, 1991.
86. G.F.Vile, C.C.Winterbourn: Inhibition of adriamycin-promoted microsomal lipid peroxidation by beta-carotene, alpha-tocopherol and retinol at high and low oxygen partial pressures. FEBS Lett 238:353–356, 1988.