Induction of phase 2 antioxidant enzymes by broccoli sulforaphane: Perspectives in maintaining the antioxidant activity of vitamins A, C, and E

Frontiers in Genetics

Volumn 3, Issue JAN, 2012, Pages

  Boddupalli, Sekhar ^a   Mein, Jonathan R ^a   Lakkanna, Shantala ^a   James, Don R ^a  

^a MONSANTO COMPANY   (United States)

Author keywords

Antioxidant enzymes; Broccoli sulforaphane; Phase II enzymes; Vitamins ACE

Indexed keywords

BRASSICA OLERACEA VAR. BOTRYTIS; BRASSICA OLERACEA VAR. CAPITATA; BRASSICA OLERACEA VAR. GEMMIFERA; BRASSICA OLERACEA VAR. ITALICA;

EID: 84863979230     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2012.00007     Document Type: Review

References (160)

1. Alnouti, Y., and Klaassen, C. D. (2008). Regulation of sulfotransferase enzymes by prototypical microsomal enzyme inducers in mice. J. Pharmacol. Exp. Ther. 324, 612-621.
2. Ambrosone, C. B., McCann, S. E., Freudenheim, J. L., Marshall, J. R., Zhang, Y., and Shields, P. G. (2004). Breast cancer risk in premenopausal women is inversely associated with consumption of broccoli, a source of isothiocyanates, but is not modified by GST genotype. J. Nutr. 134, 1134-1138.
3. Barber, S. C., Mead, R. J., and Shaw, P. J. (2006). Oxidative stress in ALS: a mechanism of neurodegeneration and a therapeutic target. Biochim. Biophys. Acta 1762, 1051-1067.
4. Bentley, A. R., Emrani, P., and Cassano, P. A. (2008). Genetic variation and gene expression in antioxidant related enzymes and risk of COPD: a systematic review. Thorax 63, 956-961.
5. Benzie, I. F., and Wachtel-Galor, S. (2010). Vegetarian diets and public health: biomarker and redox connections. Antioxid. Redox Signal. 13, 1575-1591.
6. Bianchet, M. A., Faig, M., and Amzel, L. M. (2004). Structure and mechanism of NAD[P]H:quinone acceptor oxidoreductases (NQO). Meth. Enzymol. 382, 144-174.
7. Bindoli, A., Valente, M., and Cavallini, L. (1985). Inhibition of lipid peroxidation by alpha-tocopherolquinone and alpha-tocopherolhydroquinone. Biochem. Int. 10, 753-761.
8. Board, P. G., Coggan, M., Chelvanayagam, G., Easteal, S., Jermiin, L. S., Schulte, G. K., Danley, D. E., Hoth, L. R., Griffor, M. C., Kamath, A. V., Rosner, M. H., Chrunyk, B. A., Perregaux, D. E., Gabel, C. A., Geoghegan, K. F., and Pandit, J. (2000). Identification, characterization, and crystal structure of the Omega class glutathione transferases. J. Biol. Chem. 275, 24798-24806.
9. Bowry, V. W., Ingold, K. U., and Stocker, R. (1992). Vitamin E in human low-density lipoprotein. When and how this antioxidant becomes a pro-oxidant. Biochem. J. 288(Pt 2), 341-344.
10. Bruno, R. S., Leonard, S. W., Atkinson, J., Montine, T. J., Ramakrishnan, R., Bray, T. M., and Traber, M. G. (2006). Faster plasma vitamin E disappearance in smokers is normalized by vitamin C supplementation. Free Radic. Biol. Med. 40, 689-697.
11. Buettner, G. R. (1993). The pecking order of free radicals and antioxidants: lipid peroxidation, alpha-tocopherol, and ascorbate. Arch. Biochem. Biophys. 300, 535-543.
12. Buettner, G. R., and Jurkiewicz, B. A. (1996). Catalytic metals, ascorbate and free radicals: combinations to avoid. Radiat. Res. 145, 532-541.
13. Chan, K., and Kan, Y. W. (1999). Nrf2 is essential for protection against acute pulmonary injury in mice. Proc. Natl. Acad. Sci. U.S.A. 96, 12731-12736.
14. Conaway, C. C., Getahun, S. M., Liebes, L. L., Pusateri, D. J., Topham, D. K., Botero-Omary, M., and Chung, F. L. (2000). Disposition of glucosinolates and sulforaphane in humans after ingestion of steamed and fresh broccoli. Nutr. Cancer 38, 168-178.
15. Cornblatt, B. S., Ye, L., Dinkova-Kostova, A. T., Erb, M., Fahey, J. W., Singh, N. K., Chen, M. S., Stierer, T., Garrett-Mayer, E., Argani, P., Davidson, N. E., Talalay, P., Kensler, T. W., and Visvanathan, K. (2007). Preclinical and clinical evaluation of sulforaphane for chemoprevention in the breast. Carcinogenesis 28, 1485-1490.
16. Cornelis, M. C., El-Sohemy, A., and Campos, H. (2007). GSTT1 genotype modifies the association between cruciferous vegetable intake and the risk of myocardial infarction. Am. J. Clin. Nutr. 86, 752-758.
17. Cotton, S. C., Sharp, L., Little, J., and Brockton, N. (2000). Glutathione S-transferase polymorphisms and colorectal cancer: a HuGE review. Am. J. Epidemiol. 151, 7-32.
18. Dinkova-Kostova, A. T., Fahey, J. W., Wade, K. L., Jenkins, S. N., Shapiro, T. A., Fuchs, E. J., Kerns, M. L., and Talalay, P. (2007). Induction of the phase 2 response in mouse and human skin by sulforaphane-containing broccoli sprout extracts. Cancer Epidemiol. Biomarkers Prev. 16, 847-851.
19. Dinkova-Kostova, A. T., and Talalay, P. (2008). Direct and indirect antioxidant properties of inducers of cytoprotective proteins. Mol Nutr Food Res 52(Suppl. 1), S128-S138.
20. Edmands, W. M., Beckonert, O. P., Stella, C., Campbell, A., Lake, B. G., Lindon, J. C., Holmes, E., and Gooderham, N. J. (2011). Identification of human urinary biomarkers of cruciferous vegetable consumption by metabonomic profiling. J. Proteome Res. 10, 4513-4521.
21. Eggler, A. L., Liu, G., Pezzuto, J. M., Van Breemen, R. B., and Mesecar, A. D. (2005). Modifying specific cysteines of the electrophile-sensing human Keap1 protein is insufficient to disrupt binding to the Nrf2 domain Neh2. Proc. Natl. Acad. Sci. U.S.A. 102, 10070-10075.
22. Enomoto, A., Itoh, K., Nagayoshi, E., Haruta, J., Kimura, T., O'Connor, T., Harada, T., and Yamamoto, M. (2001). High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol. Sci. 59, 169-177.
23. Fahey, J. W., and Kensler, T. W. (2007). Role of dietary supplements/nutraceuticals in chemoprevention through induction of cytoprotective enzymes. Chem. Res. Toxicol. 20, 572-576.
24. Fahey, J. W., Zhang, Y., and Talalay, P. (1997). Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc. Natl. Acad. Sci. U.S.A. 94, 10367-10372.
25. Fahn, S., and Cohen, G. (1992). The oxidant stress hypothesis in Parkinson's disease: evidence supporting it. Ann. Neurol. 32, 804-812.
26. Faig, M., Bianchet, M. A., Talalay, P., Chen, S., Winski, S., Ross, D., and Amzel, L. M. (2000). Structures of recombinant human and mouse NAD(P)H:quinone oxidoreductases: species comparison and structural changes with substrate binding and release. Proc. Natl. Acad. Sci. U.S.A. 97, 3177-3182.
27. Fenwick, G. R., Heaney, R. K., and Mullin, W. J. (1983). Glucosinolates and their breakdown products in food and food plants. Crit. Rev. Food Sci. Nutr. 18, 123-201.
28. Fernando, M. R., Satake, M., Monnier, V. M., and Lou, M. F. (2004). Thioltransferase mediated ascorbate recycling in human lens epithelial cells. Invest. Ophthalmol. Vis. Sci. 45, 230-237.
29. Feskanich, D., Ziegler, R. G., Michaud, D. S., Giovannucci, E. L., Speizer, F. E., Willett, W. C., and Colditz, G. A. (2000). Prospective study of fruit and vegetable consumption and risk of lung cancer among men and women. J. Natl. Cancer Inst. 92, 1812-1823.
30. Food and Nutrition Board and Institute of Medicine. (2000a). "Vitamin C," in Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium, and Carotenoids, ed. National Academy of Sciences (Washington, DC: National Academy Press), 95-185.
31. Food and Nutrition Board and Institute of Medicine. (2000b). "Vitamin E," in Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium, and Carotenoids, ed. National Academy of Sciences (Washington, DC: National Academy Press), 186-283.
32. Fowke, J. H., Morrow, J. D., Motley, S., Bostick, R. M., and Ness, R. M. (2006). Brassica vegetable consumption reduces urinary F2-isoprostane levels independent of micronutrient intake. Carcinogenesis 27, 2096-2102.
33. Fowke, J. H., Shu, X. O., Dai, Q., Shintani, A., Conaway, C. C., Chung, F. L., Cai, Q., Gao, Y. T., and Zheng, W. (2003). Urinary isothiocyanate excretion, Brassica consumption, and gene polymorphisms among women living in Shanghai, China. Cancer Epidemiol. Biomarkers Prev. 12, 1536-1539.
34. Gao, X., Dinkova-Kostova, A. T., and Talalay, P. (2001). Powerful and prolonged protection of human retinal pigment epithelial cells, keratinocytes, and mouse leukemia cells against oxidative damage: the indirect antioxidant effects of sulforaphane. Proc. Natl. Acad. Sci. U.S.A. 98, 15221-15226.
35. Gao, X., and Talalay, P. (2004). Induction of phase 2 genes by sulforaphane protects retinal pigment epithelial cells against photooxidative damage. Proc. Natl. Acad. Sci. U.S.A. 101, 10446-10451.
36. Gasper, A. V., Al-Janobi, A., Smith, J. A., Bacon, J. R., Fortun, P., Atherton, C., Taylor, M. A., Hawkey, C. J., Barrett, D. A., and Mithen, R. F. (2005). Glutathione S-transferase M1 polymorphism and metabolism of sulforaphane from standard and high-glucosinolate broccoli. Am. J. Clin. Nutr. 82, 1283-1291.
37. Gasper, A. V., Traka, M., Bacon, J. R., Smith, J. A., Taylor, M. A., Hawkey, C. J., Barrett, D. A., and Mithen, R. F. (2007). Consuming broccoli does not induce genes associated with xenobiotic metabolism and cell cycle control in human gastric mucosa. J. Nutr. 137, 1718-1724.
38. Gille, L., Staniek, K., Rosenau, T., Duvigneau, J. C., and Kozlov, A. V. (2010). Tocopheryl quinones and mitochondria. Mol. Nutr. Food Res. 54, 601-615.
39. Ginsberg, G., Guyton, K., Johns, D., Schimek, J., Angle, K., and Sonawane, B. (2010). Genetic polymorphism in metabolism and host defense enzymes: implications for human health risk assessment. Crit. Rev. Toxicol. 40, 575-619.
40. Groopman, J. D., Dematos, P., Egner, P. A., Love-Hunt, A., and Kensler, T. W. (1992). Molecular dosimetry of urinary aflatoxin-N7-guanine and serum aflatoxin-albumin adducts predicts chemoprotection by 1,2-dithiole-3-thione in rats. Carcinogenesis 13, 101-106.
41. Hail, N. Jr., Cortes, M., Drake, E. N., and Spallholz, J. E. (2008). Cancer chemoprevention: a radical perspective. Free Radic. Biol. Med. 45, 97-110.
42. Halpner, A. D., Handelman, G. J., Harris, J. M., Belmont, C. A., and Blumberg, J. B. (1998). Protection by vitamin C of loss of vitamin E in cultured rat hepatocytes. Arch. Biochem. Biophys. 359, 305-309.
43. Hayashi, T., Kanetoshi, A., Nakamura, M., Tamura, M., and Shirahama, H. (1992). Reduction of alpha-tocopherolquinone to alpha-tocopherolhydroquinone in rat hepatocytes. Biochem. Pharmacol. 44, 489-493.
44. Hayes, J. D., Flanagan, J. U., and Jowsey, I. R. (2005). Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45, 51-88.
45. Hayes, J. D., and Strange, R. C. (2000). Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology 61, 154-166.
46. He, X., and Ma, Q. (2009). NRF2 cysteine residues are critical for oxidant/electrophile-sensing, Kelch-like ECH-associated protein-1-dependent ubiquitination-proteasomal degradation, and transcription activation. Mol. Pharmacol. 76, 1265-1278.
47. Ho, E., Clarke, J. D., and Dashwood, R. H. (2009). Dietary sulforaphane, a histone deacetylase inhibitor for cancer prevention. J. Nutr. 139, 2393-2396.
48. Holmgren, A. (1985). Thioredoxin. Annu. Rev. Biochem. 54, 237-271.
49. Hu, R., Hebbar, V., Kim, B. R., Chen, C., Winnik, B., Buckley, B., Soteropoulos, P., Tolias, P., Hart, R. P., and Kong, A. N. (2004). In vivo pharmacokinetics and regulation of gene expression profiles by isothiocyanate sulforaphane in the rat. J. Pharmacol. Exp. Ther. 310, 263-271.
50. Hu, R., Xu, C., Shen, G., Jain, M. R., Khor, T. O., Gopalkrishnan, A., Lin, W., Reddy, B., Chan, J. Y., and Kong, A. N. (2006). Gene expression profiles induced by cancer chemopreventive isothiocyanate sulforaphane in the liver of C57BL/6J mice and C57BL/6J/Nrf2 (-/-) mice. Cancer Lett. 243, 170-192.
51. Hybertson, B. M., Gao, B., Bose, S. K., and Mccord, J. M. (2011). Oxidative stress in health and disease: the therapeutic potential of Nrf2 activation. Mol. Aspects Med. 32, 234-246.
52. Ikegami, H., Ono, M., Fujisawa, T., Hiromine, Y., Kawabata, Y., and Yamato, E. (2008). Molecular scanning of the gene for thioredoxin, an antioxidative and antiapoptotic protein, and genetic susceptibility to type 1 diabetes. Ann. N. Y. Acad. Sci. 1150, 103-105.
53. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K., Hatayama, I., Yamamoto, M., and Nabeshima, Y. (1997). An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236, 313-322.
54. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., Igarashi, K., Engel, J. D., and Yamamoto, M. (1999). Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13, 76-86.
55. Jaiswal, A. K. (2004a). Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic. Biol. Med. 36, 1199-1207.
56. Jaiswal, A. K. (2004b). Regulation of antioxidant response element-dependent induction of detoxifying enzyme synthesis. Meth. Enzymol. 378, 221-238.
57. Joseph, M. A., Moysich, K. B., Freudenheim, J. L., Shields, P. G., Bowman, E. D., Zhang, Y., Marshall, J. R., and Ambrosone, C. B. (2004). Cruciferous vegetables, genetic polymorphisms in glutathione S-transferases M1 and T1, and prostate cancer risk. Nutr. Cancer 50, 206-213.
58. Joshipura, K. J., Ascherio, A., Manson, J. E., Stampfer, M. J., Rimm, E. B., Speizer, F. E., Hennekens, C. H., Spiegelman, D., and Willett, W. C. (1999). Fruit and vegetable intake in relation to risk of ischemic stroke. JAMA 282, 1233-1239.
59. Juge, N., Mithen, R. F., and Traka, M. (2007). Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cell. Mol. Life Sci. 64, 1105-1127.
60. Kalthoff, S., Ehmer, U., Freiberg, N., Manns, M. P., and Strassburg, C. P. (2010). Interaction between oxidative stress sensor Nrf2 and xenobiotic-activated aryl hydrocarbon receptor in the regulation of the human phase II detoxifying UDP-glucuronosyltransferase 1A10. J. Biol. Chem. 285, 5993-6002.
61. Kelsey, K. T., Ross, D., Traver, R. D., Christiani, D. C., Zuo, Z. F., Spitz, M. R., Wang, M., Xu, X., Lee, B. K., Schwartz, B. S., and Wiencke, J. K. (1997). Ethnic variation in the prevalence of a common NAD(P)H quinone oxidoreductase polymorphism and its implications for anti-cancer chemotherapy. Br. J. Cancer 76, 852-854.
62. Kensler, T. W., Chen, J. G., Egner, P. A., Fahey, J. W., Jacobson, L. P., Stephenson, K. K., Ye, L., Coady, J. L., Wang, J. B., Wu, Y., Sun, Y., Zhang, Q. N., Zhang, B. C., Zhu, Y. R., Qian, G. S., Carmella, S. G., Hecht, S. S., Benning, L., Gange, S. J., Groopman, J. D., and Talalay, P. (2005). Effects of glucosinolate-rich broccoli sprouts on urinary levels of aflatoxin-DNA adducts and phenanthrene tetraols in a randomized clinical trial in He Zuo township, Qidong, People's Republic of China. Cancer Epidemiol. Biomarkers Prev. 14, 2605-2613.
63. Kensler, T. W., Egner, P. A., Davidson, N. E., Roebuck, B. D., Pikul, A., and Groopman, J. D. (1986). Modulation of aflatoxin metabolism, aflatoxin-N7-guanine formation, and hepatic tumorigenesis in rats fed ethoxyquin: role of induction of glutathione S-transferases. Cancer Res. 46, 3924-3931.
64. Kirby, J., Halligan, E., Baptista, M. J., Allen, S., Heath, P. R., Holden, H., Barber, S. C., Loynes, C. A., Wood-Allum, C. A., Lunec, J., and Shaw, P. J. (2005). Mutant SOD1 alters the motor neuronal transcriptome: implications for familial ALS. Brain 128, 1686-1706.
65. Kiser, P. D., and Palczewski, K. (2010). Membrane-binding and enzymatic properties of RPE65. Prog. Retin. Eye Res. 29, 428-442.
66. Kiyohara, C., Yoshimasu, K., Takayama, K., and Nakanishi, Y. (2005). NQO1, MPO, and the risk of lung cancer: a HuGE review. Genet. Med. 7, 463-478.
67. Kobayashi, A., Kang, M. I., Okawa, H., Ohtsuji, M., Zenke, Y., Chiba, T., Igarashi, K., and Yamamoto, M. (2004). Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 24, 7130-7139.
68. Kohar, I., Baca, M., Suarna, C., Stocker, R., and Southwell-Keely, P. T. (1995). Is alpha-tocopherol a reservoir for alpha-tocopheryl hydroquinone? Free Radic. Biol. Med. 19, 197-207.
69. Kolm, R. H., Danielson, U. H., Zhang, Y., Talalay, P., and Mannervik, B. (1995). Isothiocyanates as substrates for human glutathione transferases: structure-activity studies. Biochem. J. 311(Pt 2), 453-459.
70. Kolsch, H., Linnebank, M., Lutjohann, D., Jessen, F., Wullner, U., Harbrecht, U., Thelen, K. M., Kreis, M., Hentschel, F., Schulz, A., Von Bergmann, K., Maier, W., and Heun, R. (2004). Polymorphisms in glutathione S-transferase omega-1 and AD, vascular dementia, and stroke. Neurology 63, 2255-2260.
71. Kong, L., Tanito, M., Huang, Z., Li, F., Zhou, X., Zaharia, A., Yodoi, J., Mcginnis, J. F., and Cao, W. (2007). Delay of photoreceptor degeneration in tubby mouse by sulforaphane. J. Neurochem. 101, 1041-1052.
72. Kushad, M. M., Brown, A. F., Kurilich, A. C., Juvik, J. A., Klein, B. P., Wallig, M. A., and Jeffery, E. H. (1999). Variation of glucosinolates in vegetable crops of Brassica oleracea. J. Agric. Food Chem. 47, 1541-1548.
73. Landar, A., and Darley-Usmar, V. M. (2003). Nitric oxide and cell signaling: modulation of redox tone and protein modification. Amino Acids 25, 313-321.
74. Law, M. R., Wald, N. J., and Thompson, S. G. (1994). By how much and how quickly does reduction in serum cholesterol concentration lower risk of ischaemic heart disease? BMJ 308, 367-372.
75. Li, F., Hullar, M. A., Beresford, S. A., and Lampe, J. W. (2011). Variation of glucoraphanin metabolism in vivo and ex vivo by human gut bacteria. Br. J. Nutr. 106, 408-416.
76. Li, Y. J., Oliveira, S. A., Xu, P., Martin, E. R., Stenger, J. E., Scherzer, C. R., Hauser, M. A., Scott, W. K., Small, G. W., Nance, M. A., Watts, R. L., Hubble, J. P., Koller, W. C., Pahwa, R., Stern, M. B., Hiner, B. C., Jankovic, J., Goetz, C. G., Mastaglia, F., Middleton, L. T., Roses, A. D., Saunders, A. M., Schmechel, D. E., Gullans, S. R., Haines, J. L., Gilbert, J. R., Vance, J. M., Pericak-Vance, M. A., Hulette, C., and Welsh-Bohmer, K. A. (2003). Glutathione S-transferase omega-1 modifies age-at-onset of Alzheimer disease and Parkinson disease. Hum. Mol. Genet. 12, 3259-3267.
77. Liebler, D. C., Kaysen, K. L., and Kennedy, T. A. (1989). Redox cycles of vitamin E: hydrolysis and ascorbic acid dependent reduction of 8a-(alkyldioxy)tocopherones. Biochemistry 28, 9772-9777.
78. Lietz, G., Lange, J., and Rimbach, G. (2010). Molecular and dietary regulation of beta, beta-carotene 15, 15'-monooxygenase 1 (BCMO1). Arch. Biochem. Biophys. 502, 8-16.
79. Linster, C. L., and Van Schaftingen, E. (2007). Vitamin C. Biosynthesis, recycling and degradation in mammals. FEBS J. 274, 1-22.
80. Maellaro, E., Del Bello, B., Sugherini, L., Santucci, A., Comporti, M., and Casini, A. F. (1994). Purification and characterization of glutathione-dependent dehydroascorbate reductase from rat liver. Biochem. J. 301(Pt 2), 471-476.
81. Mansuy, D. (2011). Brief historical overview and recent progress on cytochromes P450: adaptation of aerobic organisms to their chemical environment and new mechanisms of prodrug bioactivation. Ann. Pharm. Fr. 69, 62-69.
82. Mattson, M. P. (2004). Pathways towards and away from Alzheimer's disease. Nature 430, 631-639.
83. May, J. M., Cobb, C. E., Mendiratta, S., Hill, K. E., and Burk, R. F. (1998). Reduction of the ascorbyl free radical to ascorbate by thioredoxin reductase. J. Biol. Chem. 273, 23039-23045.
84. May, J. M., Mendiratta, S., Hill, K. E., and Burk, R. F. (1997). Reduction of dehydroascorbate to ascorbate by the selenoenzyme thioredoxin reductase. J. Biol. Chem. 272, 22607-22610.
85. Meplan, C., Hughes, D. J., Pardini, B., Naccarati, A., Soucek, P., Vodickova, L., Hlavata, I., Vrana, D., Vodicka, P., and Hesketh, J. E. (2010). Genetic variants in selenoprotein genes increase risk of colorectal cancer. Carcinogenesis 31, 1074-1079.
86. Meyer, D. J., Crease, D. J., and Ketterer, B. (1995). Forward and reverse catalysis and product sequestration by human glutathione S-transferases in the reaction of GSH with dietary aralkyl isothiocyanates. Biochem. J. 306(Pt 2), 565-569.
87. Meyer, U. A. (1996). Overview of enzymes of drug metabolism. J. Pharmacokinet. Biopharm. 24, 449-459.
88. Miller, A. B., Altenburg, H. P., Bueno-De-Mesquita, B., Boshuizen, H. C., Agudo, A., Berrino, F., Gram, I. T., Janson, L., Linseisen, J., Overvad, K., Rasmuson, T., Vineis, P., Lukanova, A., Allen, N., Amiano, P., Barricarte, A., Berglund, G., Boeing, H., Clavel-Chapelon, F., Day, N. E., Hallmans, G., Lund, E., Martinez, C., Navarro, C., Palli, D., Panico, S., Peeters, P. H., Quiros, J. R., Tjonneland, A., Tumino, R., Trichopoulou, A., Trichopoulos, D., Slimani, N., and Riboli, E. (2004). Fruits and vegetables and lung cancer: findings from the European Prospective Investigation into Cancer and Nutrition. Int. J. Cancer 108, 269-276.
89. Minelli, C., Wei, I., Sagoo, G., Jarvis, D., Shaheen, S., and Burney, P. (2011). Interactive effects of antioxidant genes and air pollution on respiratory function and airway disease: a HuGE review. Am. J. Epidemiol. 173, 603-620.
90. Mirmiran, P., Noori, N., Zavareh, M. B., and Azizi, F. (2009). Fruit and vegetable consumption and risk factors for cardiovascular disease. Metabolism 58, 460-468.
91. Mitchell, J., Morris, A., and De Belleroche, J. (2009). Thioredoxin reductase 1 haplotypes modify familial amyotrophic lateral sclerosis onset. Free Radic. Biol. Med. 46, 202-211.
92. Morrow, J. D., Roberts, L. J., Daniel, V. C., Awad, J. A., Mirochnitchenko, O., Swift, L. L., and Burk, R. F. (1998). Comparison of formation of D2/E2-isoprostanes and F2-isoprostanes in vitro and in vivo-effects of oxygen tension and glutathione. Arch. Biochem. Biophys. 353, 160-171.
93. Mukherjee, B., Salavaggione, O. E., Pelleymounter, L. L., Moon, I., Eckloff, B. W., Schaid, D. J., Wieben, E. D., and Weinshilboum, R. M. (2006). Glutathione S-transferase omega 1 and omega 2 pharmacogenomics. Drug Metab. Dispos. 34, 1237-1246.
94. Neuhouser, M. L., Patterson, R. E., Thornquist, M. D., Omenn, G. S., King, I. B., and Goodman, G. E. (2003). Fruits and vegetables are associated with lower lung cancer risk only in the placebo arm of the beta-carotene and retinol efficacy trial (CARET). Cancer Epidemiol. Biomarkers Prev. 12, 350-358.
95. Neuzil, J., Witting, P. K., and Stocker, R. (1997). Alpha-tocopheryl hydroquinone is an efficient multifunctional inhibitor of radical-initiated oxidation of low density lipoprotein lipids. Proc. Natl. Acad. Sci. U.S.A. 94, 7885-7890.
96. Niki, E. (1987). Interaction of ascorbate and alpha-tocopherol. Ann. N. Y. Acad. Sci. 498, 186-199.
97. Nowak, M., Swietochowska, E., Wielkoszynski, T., Marek, B., Karpe, J., Gorski, J., Glogowska-Szelag, J., Kos-Kudla, B., and Ostrowska, Z. (2003). Changes in blood antioxidants and several lipid peroxidation products in women with age-related macular degeneration. Eur. J. Ophthalmol. 13, 281-286.
98. Ohlemiller, K. K., Hughes, R. M., Mosinger-Ogilvie, J., Speck, J. D., Grosof, D. H., and Silverman, M. S. (1995). Cochlear and retinal degeneration in the tubby mouse. Neuroreport 6, 845-849.
99. Packer, J. E., Slater, T. F., and Willson, R. L. (1979). Direct observation of a free radical interaction between vitamin E and vitamin C. Nature 278, 737-738.
100. Paiva, L., Marcos, R., Creus, A., Coggan, M., Oakley, A. J., and Board, P. G. (2008). Polymorphism of glutathione transferase Omega 1 in a population exposed to a high environmental arsenic burden. Pharmacogenet. Genomics 18, 1-10.
101. Park, J. B., and Levine, M. (1996). Purification, cloning and expression of dehydroascorbic acid-reducing activity from human neutrophils: identification as glutaredoxin. Biochem. J. 315(Pt 3), 931-938.
102. Peters, U., Chatterjee, N., Hayes, R. B., Schoen, R. E., Wang, Y., Chanock, S. J., and Foster, C. B. (2008). Variation in the selenoenzyme genes and risk of advanced distal colorectal adenoma. Cancer Epidemiol. Biomarkers Prev. 17, 1144-1154.
103. Petri, N., Tannergren, C., Holst, B., Mellon, F. A., Bao, Y., Plumb, G. W., Bacon, J., O'Leary, K. A., Kroon, P. A., Knutson, L., Forsell, P., Eriksson, T., Lennernas, H., and Williamson, G. (2003). Absorption/metabolism of sulforaphane and quercetin, and regulation of phase II enzymes, in human jejunum in vivo. Drug Metab. Dispos. 31, 805-813.
104. Pimentel, L. (2003). Scurvy: historical review and current diagnostic approach. Am. J. Emerg. Med. 21, 328-332.
105. Riedl, M. A., Saxon, A., and Diaz-Sanchez, D. (2009). Oral sulforaphane increases phase II antioxidant enzymes in the human upper airway. Clin. Immunol. 130, 244-251.
106. Riso, P., Brusamolino, A., Moro, M., and Porrini, M. (2009). Absorption of bioactive compounds from steamed broccoli and their effect on plasma glutathione S-transferase activity. Int. J. Food Sci. Nutr. 60(Suppl. 1), 56-71.
107. Roebuck, B. D., Liu, Y. L., Rogers, A. E., Groopman, J. D., and Kensler, T. W. (1991). Protection against aflatoxin B1-induced hepatocarcinogenesis in F344 rats by 5-(2-pyrazinyl)-4-methyl-1,2-dithiole-3-thione (oltipraz): predictive role for short-term molecular dosimetry. Cancer Res. 51, 5501-5506.
108. Ross, D., Kepa, J. K., Winski, S. L., Beall, H. D., Anwar, A., and Siegel, D. (2000a). NAD(P)H:quinone oxidoreductase 1 (NQO1): chemoprotection, bioactivation, gene regulation and genetic polymorphisms. Chem. Biol. Interact. 129, 77-97.
109. Ross, S. A., Mccaffery, P. J., Drager, U. C., and De Luca, L. M. (2000b). Retinoids in embryonal development. Physiol. Rev. 80, 1021-1054.
110. Ross, D., and Siegel, D. (2004). NAD(P)H:quinone oxidoreductase 1 (NQO1, DT-diaphorase), functions and pharmacogenetics. Meth. Enzymol. 382, 115-144.
111. Ross, R. K., Yuan, J. M., Yu, M. C., Wogan, G. N., Qian, G. S., Tu, J. T., Groopman, J. D., Gao, Y. T., and Henderson, B. E. (1992). Urinary aflatoxin biomarkers and risk of hepatocellular carcinoma. Lancet 339, 943-946.
112. Rothman, N., Smith, M. T., Hayes, R. B., Traver, R. D., Hoener, B., Campleman, S., Li, G. L., Dosemeci, M., Linet, M., Zhang, L., Xi, L., Wacholder, S., Lu, W., Meyer, K. B., Titenko-Holland, N., Stewart, J. T., Yin, S., and Ross, D. (1997). Benzene poisoning, a risk factor for hematological malignancy, is associated with the NQO1 609C->T mutation and rapid fractional excretion of chlorzoxazone. Cancer Res. 57, 2839-2842.
113. Saaranen, M. J., Karala, A. R., Lappi, A. K., and Ruddock, L. W. (2010). The role of dehydroascorbate in disulfide bond formation. Antioxid. Redox Signal. 12, 15-25.
114. Schmuck, E., Cappello, J., Coggan, M., Brew, J., Cavanaugh, J. A., Blackburn, A. C., Baker, R. T., Eyre, H. J., Sutherland, G. R., and Board, P. G. (2008). Deletion of Glu155 causes a deficiency of glutathione transferase Omega 1-1 but does not alter sensitivity to arsenic trioxide and other cytotoxic drugs. Int. J. Biochem. Cell Biol. 40, 2553-2559.
115. Schmuck, E. M., Board, P. G., Whitbread, A. K., Tetlow, N., Cavanaugh, J. A., Blackburn, A. C., and Masoumi, A. (2005). Characterization of the monomethylarsonate reductase and dehydroascorbate reductase activities of Omega class glutathione transferase variants: implications for arsenic metabolism and the age-at-onset of Alzheimer's and Parkinson's diseases. Pharmacogenet. Genomics 15, 493-501.
116. Seow, A., Shi, C. Y., Chung, F. L., Jiao, D., Hankin, J. H., Lee, H. P., Coetzee, G. A., and Yu, M. C. (1998). Urinary total isothiocyanate (ITC) in a population-based sample of middle-aged and older Chinese in Singapore: relationship with dietary total ITC and glutathione S-transferase M1/T1/P1 genotypes. Cancer Epidemiol. Biomarkers Prev. 7, 775-781.
117. Seow, A., Vainio, H., and Yu, M. C. (2005). Effect of glutathione-S-transferase polymorphisms on the cancer preventive potential of isothiocyanates: an epidemiological perspective. Mutat. Res. 592, 58-67.
118. Shapiro, T. A., Fahey, J. W., Wade, K. L., Stephenson, K. K., and Talalay, P. (1998). Human metabolism and excretion of cancer chemoprotective glucosinolates and isothiocyanates of cruciferous vegetables. Cancer Epidemiol. Biomarkers Prev. 7, 1091-1100.
119. Shapiro, T. A., Fahey, J. W., Wade, K. L., Stephenson, K. K., and Talalay, P. (2001). Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: metabolism and excretion in humans. Cancer Epidemiol. Biomarkers Prev. 10, 501-508.
120. Siegel, D., Bolton, E. M., Burr, J. A., Liebler, D. C., and Ross, D. (1997). The reduction of alpha-tocopherolquinone by human NAD(P)H: quinone oxidoreductase: the role of alpha-tocopherolhydroquinone as a cellular antioxidant. Mol. Pharmacol. 52, 300-305.
121. Siegel, D., and Ross, D. (2000). Immunodetection of NAD(P)H:quinone oxidoreductase 1 (NQO1) in human tissues. Free Radic. Biol. Med. 29, 246-253.
122. Sies, H. (1997). Oxidative stress: oxidants and antioxidants. Exp. Physiol. 82, 291-295.
123. Simonian, N. A., and Coyle, J. T. (1996). Oxidative stress in neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol. 36, 83-106.
124. Smith, M. T. (1999). Benzene, NQO1, and genetic susceptibility to cancer. Proc. Natl. Acad. Sci. U.S.A. 96, 7624-7626.
125. Spitz, M. R., Duphorne, C. M., Detry, M. A., Pillow, P. C., Amos, C. I., Lei, L., De Andrade, M., Gu, X., Hong, W. K., and Wu, X. (2000). Dietary intake of isothiocyanates: evidence of a joint effect with glutathione S-transferase polymorphisms in lung cancer risk. Cancer Epidemiol. Biomarkers Prev. 9, 1017-1020.
126. Steck, S. E., Gammon, M. D., Hebert, J. R., Wall, D. E., and Zeisel, S. H. (2007). GSTM1, GSTT1, GSTP1, and GSTA1 polymorphisms and urinary isothiocyanate metabolites following broccoli consumption in humans. J. Nutr. 137, 904-909.
127. Suido, H., Tanaka, T., Tabei, T., Takeuchi, A., Okita, M., Kishimoto, T., Kasayama, S., and Higashino, K. (2002). A mixed green vegetable and fruit beverage decreased the serum level of low-density lipoprotein cholesterol in hypercholesterolemic patients. J. Agric. Food Chem. 50, 3346-3350.
128. Szent-Gyorgyi, A. (1928). Observations on the function of peroxidase systems and the chemistry of the adrenal cortex: description of a new carbohydrate derivative. Biochem. J. 22, 1387-1409.
129. Takai, M., Suido, H., Tanaka, T., Kotani, M., Fujita, A., Takeuchi, A., Makino, T., Sumikawa, K., Origasa, H., Tsuji, K., and Nakashima, M. (2003). LDL-cholesterol-lowering effect of a mixed green vegetable and fruit beverage containing broccoli and cabbage in hypercholesterolemic subjects. Rinsho Byori 51, 1073-1083.
130. Tanito, M., Masutani, H., Kim, Y. C., Nishikawa, M., Ohira, A., and Yodoi, J. (2005). Sulforaphane induces thioredoxin through the antioxidant-responsive element and attenuates retinal light damage in mice. Invest. Ophthalmol. Vis. Sci. 46, 979-987.
131. Tanito, M., Masutani, H., Nakamura, H., Oka, S., Ohira, A., and Yodoi, J. (2002). Attenuation of retinal photooxidative damage in thioredoxin transgenic mice. Neurosci. Lett. 326, 142-146.
132. Tanumihardjo, S. A. (2004). Assessing vitamin A status: past, present and future. J. Nutr. 134, 290S-293S.
133. Thiele, J. J., Schroeter, C., Hsieh, S. N., Podda, M., and Packer, L. (2001). The antioxidant network of the stratum corneum. Curr. Probl. Dermatol. 29, 26-42.
134. Thimmulappa, R. K., Mai, K. H., Srisuma, S., Kensler, T. W., Yamamoto, M., and Biswal, S. (2002). Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 62, 5196-5203.
135. Thomas, S. R., and Stocker, R. (2000). Molecular action of vitamin E in lipoprotein oxidation: implications for atherosclerosis. Free Radic. Biol. Med. 28, 1795-1805.
136. Traber, M. G., and Atkinson, J. (2007). Vitamin E, antioxidant and nothing more. Free Radic. Biol. Med. 43, 4-15.
137. Traver, R. D., Horikoshi, T., Danenberg, K. D., Stadlbauer, T. H., Danenberg, P. V., Ross, D., and Gibson, N. W. (1992). NAD(P)H:quinone oxidoreductase gene expression in human colon carcinoma cells: characterization of a mutation which modulates DT-diaphorase activity and mitomycin sensitivity. Cancer Res. 52, 797-802.
138. Traver, R. D., Siegel, D., Beall, H. D., Phillips, R. M., Gibson, N. W., Franklin, W. A., and Ross, D. (1997). Characterization of a polymorphism in NAD(P)H: quinone oxidoreductase (DT-diaphorase). Br. J. Cancer 75, 69-75.
139. Trujillo, E., Davis, C., and Milner, J. (2006). Nutrigenomics, proteomics, metabolomics, and the practice of dietetics. J. Am. Diet. Assoc. 106, 403-413.
140. U. S. Department of Agriculture, U. S. Department of Health and Human Services. (2010). Dietary Guidelines for Americans, 2010. Washington, DC: U.S. Government Printing Office.
141. Van Poppel, G., Verhoeven, D. T., Verhagen, H., and Goldbohm, R. A. (1999). Brassica vegetables and cancer prevention. Epidemiology and mechanisms. Adv. Exp. Med. Biol. 472, 159-168.
142. Verhoeven, D. T., Goldbohm, R. A., Van Poppel, G., Verhagen, H., and Van Den Brandt, P. A. (1996). Epidemiological studies on Brassica vegetables and cancer risk. Cancer Epidemiol. Biomarkers Prev. 5, 733-748.
143. Voorrips, L. E., Goldbohm, R. A., Van Poppel, G., Sturmans, F., Hermus, R. J., and Van Den Brandt, P. A. (2000). Vegetable and fruit consumption and risks of colon and rectal cancer in a prospective cohort study: The Netherlands Cohort Study on Diet and Cancer. Am. J. Epidemiol. 152, 1081-1092.
144. Wang, J. S., Shen, X., He, X., Zhu, Y. R., Zhang, B. C., Wang, J. B., Qian, G. S., Kuang, S. Y., Zarba, A., Egner, P. A., Jacobson, L. P., Munoz, A., Helzlsouer, K. J., Groopman, J. D., and Kensler, T. W. (1999). Protective alterations in phase 1 and 2 metabolism of aflatoxin B1 by oltipraz in residents of Qidong, People's Republic of China. J. Natl. Cancer Inst. 91, 347-354.
145. Wang, L. I., Giovannucci, E. L., Hunter, D., Neuberg, D., Su, L., and Christiani, D. C. (2004). Dietary intake of cruciferous vegetables, glutathione S-transferase (GST) polymorphisms and lung cancer risk in a Caucasian population. Cancer Causes Control 15, 977-985.
146. Wasserman, W. W., and Fahl, W. E. (1997). Functional antioxidant responsive elements. Proc. Natl. Acad. Sci. U.S.A. 94, 5361-5366.
147. Wells, W. W., Xu, D. P., Yang, Y. F., and Rocque, P. A. (1990). Mammalian thioltransferase (glutaredoxin) and protein disulfide isomerase have dehydroascorbate reductase activity. J. Biol. Chem. 265, 15361-15364.
148. Whitbread, A. K., Tetlow, N., Eyre, H. J., Sutherland, G. R., and Board, P. G. (2003). Characterization of the human Omega class glutathione transferase genes and associated polymorphisms. Pharmacogenetics 13, 131-144.
149. Winkler, B. S., Orselli, S. M., and Rex, T. S. (1994). The redox couple between glutathione and ascorbic acid: a chemical and physiological perspective. Free Radic. Biol. Med. 17, 333-349.
150. World Cancer Research Fund, and American Institute for Cancer Research. (2007). Food, Nutrition, Physical Activity, and the Prevention of Cancer: A Global Perspective. Washington, DC: American Institute for Cancer Research.
151. Wu, J. H., and Croft, K. D. (2007). Vitamin E metabolism. Mol. Aspects Med. 28, 437-452.
152. Xu, C., Yuan, X., Pan, Z., Shen, G., Kim, J. H., Yu, S., Khor, T. O., Li, W., Ma, J., and Kong, A. N. (2006). Mechanism of action of isothiocyanates: the induction of ARE-regulated genes is associated with activation of ERK and JNK and the phosphorylation and nuclear translocation of Nrf2. Mol. Cancer Ther. 5, 1918-1926.
153. Xu, D. P., Washburn, M. P., Sun, G. P., and Wells, W. W. (1996). Purification and characterization of a glutathione dependent dehydroascorbate reductase from human erythrocytes. Biochem. Biophys. Res. Commun. 221, 117-121.
154. Zhang, D. D., Lo, S. C., Cross, J. V., Templeton, D. J., and Hannink, M. (2004). Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol. Cell. Biol. 24, 10941-10953.
155. Zhang, X., Shu, X. O., Xiang, Y. B., Yang, G., Li, H., Gao, J., Cai, H., Gao, Y. T., and Zheng, W. (2011). Cruciferous vegetable consumption is associated with a reduced risk of total and cardiovascular disease mortality. Am. J. Clin. Nutr. 94, 240-246.
156. Zhang, Y., Kolm, R. H., Mannervik, B., and Talalay, P. (1995). Reversible conjugation of isothiocyanates with glutathione catalyzed by human glutathione transferases. Biochem. Biophys. Res. Commun. 206, 748-755.
157. Zhang, Y., Talalay, P., Cho, C. G., and Posner, G. H. (1992). A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc. Natl. Acad. Sci. U.S.A. 89, 2399-2403.
158. Zhang, Y., and Tang, L. (2007). Discovery and development of sulforaphane as a cancer chemopreventive phytochemical. Acta Pharmacol. Sin. 28, 1343-1354.
159. Zhong, L., and Holmgren, A. (2000). Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations. J. Biol. Chem. 275, 18121-18128.
160. Zhou, H., Brock, J., Casarotto, M. G., Oakley, A. J., and Board, P. G. (2011). Novel folding and stability defects cause a deficiency of human glutathione transferase omega 1. J. Biol. Chem. 286, 4271-4279.