Protection against electrophile and oxidative stress by induction of phase 2 genes: The quest for the elusive sensor that responds to inducers

Advances in Enzyme Regulation

Volumn 44, Issue 1, 2004, Pages 335-367

  Holtzclaw, W David ^a   Dinkova Kostova, Albena T ^a   Talalay, Paul ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Ah receptor, aryl hydrocarbon receptor; AHH, aryl hydrocarbon hydroxylase; ARE (EpRE), antioxidant (electrophile) response element; BHA, 2(3) tert butyl 4 hydroxyanisole; BHT, 3,5 di tert butyl 4 hydroxytoluene; t BHQ, tert butylhydroquinone

Indexed keywords

ANTINEOPLASTIC AGENT; ANTIOXIDANT; DNA BINDING PROTEIN; ERYTHROID SPECIFIC DNA BINDING FACTOR; TRANSCRIPTION FACTOR;

ANIMAL; CELL TRANSFORMATION; CONFERENCE PAPER; DRUG EFFECT; GENE EXPRESSION REGULATION; HUMAN; OXIDATIVE STRESS; PHYSIOLOGY;

ANIMALS; ANTICARCINOGENIC AGENTS; ANTINEOPLASTIC AGENTS; ANTIOXIDANTS; CELL TRANSFORMATION, NEOPLASTIC; DNA-BINDING PROTEINS; ERYTHROID-SPECIFIC DNA-BINDING FACTORS; GENE EXPRESSION REGULATION; HUMANS; OXIDATIVE STRESS; TRANSCRIPTION FACTORS;

EID: 9644272830     PISSN: 00652571     EISSN: None     Source Type: Book Series    
DOI: 10.1016/j.advenzreg.2003.11.013     Document Type: Conference Paper

References (161)

1. Adams J., Kelso R., Cooley L. The kelch repeat superfamily of proteins. propellers of cell function Trends Cell Biol. 10:2000;17-24
2. Alberts D., Colvin O.M., Conney A.H., Ernster V.L., Garber J.E., Greenwalt P., Gudas L.J., Hong K.H., Kelloff G.J., Kramer R.A., Lerman C.E., Mangelsdorf D.J., Matter A., Minna J.D., Nelson V W.G., Pezzuto J.M., Prendergast F., Rusch V.W., Sporn M.B., Wattenberg L.W., Weinstein I.B. Prevention of cancer in the next millennium. report of the chemoprevention working group to the American Association for Cancer Research Cancer Res. 59:1999;4743-4758
3. Allison A.C., Mallucci L. Uptake of hydrocarbon carcinogens by lysosomes. Nature. 203:1964;1024-1027
4. Andrews N.C., Erdjument-Bromage H., Davidson M.B., Tempst P., Orkin S.H. Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature. 362:1993;722-728
5. Ansher S.S., Dolan P., Bueding E. Chemoprotective effects of two dithiolthiones and of butylated hydroxy-anisole against carbon tetrachloride and acetaminophen toxicity. Hepatology. 3:1983;932-935
6. Ansher S.S., Dolan P., Bueding E. Biochemical effects of dithiolthiones. Food Chem Toxicol. 24:1986;405-415
7. Anwar A., Dehn D., Siegel D., Kepa J.K., Tang L.J., Pietenpol J.A., Ross D. Interaction of human NAD(P)H:quinone oxidoreductase 1 (NQO1) with the tumor suppressor protein p53 in cells and cell-free systems. J Biol Chem. 278:2003;10368-10373
8. Asher G., Lotem J., Cohen B., Sachs L., Shaul Y. Regulation of p53 stability and p53-dependent apoptosis by NADH quinone oxidoreductase 1. Proc Natl Acad Sci USA. 98:2001;1188-1193
9. Asher G., Lotem J., Kama R., Sachs L., Shaul Y. NQO1 stabilizes p53 through a distinct pathway. Proc Natl Acad Sci USA. 99:2002;3099-3104
10. Asher G., Lotem J., Sachs L., Kahana C., Shaul Y. Mdm-2 and ubiquitin-independent p53 proteasomal degradation regulated by NQO1. Proc Natl Acad Sci USA. 99:2002;13125-13130
11. Batzinger R.P., Ou S.-.Y.L., Bueding E. Antimutagenic effects of 2(3)-tert-butyl-4-hydroxyanisole and of antimicrobial agents. Cancer Res. 38:1978;4478-4485
12. Bayney R.M., Morton M.R., Favreau L.V., Pickett C.B. Rat liver NAD(P)H:quinone reductase. Regulation of quinone reductase gene expression by planar aromatic compounds and determination of the exon structure of the quinone reductase structural gene. J Biol Chem. 264:1989;21793-21797
13. Benson A.M., Batzinger R.P., Ou S.-.Y.L., Bueding E., Cha Y.-.N., Talalay P. Elevation of hepatic glutathione S-transferases and protection against mutagenic metabolites of benzo(a)pyrene by dietary antioxidants. Cancer Res. 38:1978;4486-4495
14. Benson A.M., Barretto P.B., Stanley J.S. Induction of DT-diaphorase by anticarcinogenic sulfur compounds in mice. J Natl Cancer Inst. 76:1986;467-473
15. Benson A.M., Cha Y.-.N., Bueding E., Heine H.S., Talalay P. Elevation of extrahepatic glutathione S-transferase and epoxide hydratase activities by 2(3)-tert-butyl-4-hydroxyanisole. Cancer Res. 39:1979;2971-2977
16. Benson A.M., Hunkeler M.J., Talalay P. Increase of NAD(P)H:quinone reductase by dietary antioxidants. possible role in protection against carcinogenesis and toxicity Proc Natl Acad Sci USA. 77:1980;5216-5220
17. Berenblum I. The modifying influence of dichloroethyl sulphide on the induction of tumours in mice by tar. J Pathol Bacteriol. 32:1929;425-434
18. Beyer R.E., Segura-Aguilar J., Di Bernardo S., Cavazzoni M., Fato R., Fiorentini D., Galli M.C., Setti M., Landi L., Lenaz G. The role of DT-diaphorase in the maintenance of the reduced antioxidant form of coenzyme Q in membrane systems. Proc Natl Acad Sci USA. 93:1996;2528-2532
19. Bloom D.A., Jaiswal A.K. Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant responce element-mediated NAD(P)H quinone oxidoreductase-1 gene expression. J Biol Chem. 278:2003;44675-44682
20. Bock K.W., Eckle T., Ouzzine M., Fournel-Gigleux S. Coordinate induction by antioxidants of UDP-glucuronosyltransferase UGT1A6 and the apical conjugate export pump MRP2 (multidrug resistance protein 2) in Caco-2 cells. Biochem Pharmacol. 59:2000;467-470
21. Bradfield C.A., Bjeldanes L.F. Effect of dietary indole-3-carbinol on intestinal and hepatic monooxygenase, glutathione S-transferase and epoxide hydrolase activities in the rat. Food Chem Toxicol. 22:1984;977-982
22. Cha Y.-.N., Bueding E. Effect of 2(3)-tert-butyl-4-hydroxyanisole administration on the activities of several hepatic microsomal and cytoplasmic enzymes in mice. Biochem Pharmacol. 28:1979;1917-1921
23. Cha Y.-.N., Heine H.S. Comparative effects of dietary administration of 2(3)-tert-butyl-4-hydroxyanisole and 3,5-di-tert-butyl-4-hydroxytoluene on several hepatic enzyme activities in mice and rats. Cancer Res. 42:1982;2609-2615
24. Cha Y.-.N., Martz F., Bueding E. Enhancement of liver microsome epoxide hydratase activity in rodents by treatment with 2(3)-tert-butyl-4- hydroxyanisole. Cancer Res. 38:1978;4496-4498
25. Chan K., Kan Y.W. Nrf2 is essential for protection against acute pulmonary injury in mice. Proc Natl Acad Sci USA. 96:1999;12731-12736
26. Chan K., Lu R., Chang J.C., Kan Y.W. NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc Natl Acad Sci USA. 93:1996;13943-13948
27. Chanas S.A., Jiang Q., McMahon M., McWalter G.K., McLellan L.I., Elcombe C.R., Henderson C.J., Wolf C.R., Moffat G.J., Itoh K., Yamamoto M., Hayes J.D. Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gsta1, Gsta2, Gstm1, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice. Biochem J. 365:2002;405-416
28. Cheng J., Mielnicki L.M., Pruitt S.C., Maquat L.E. Nucleotide sequence of murine triosephosphate isomerase cDNA. Nucleic Acids Res. 18(14):1990;4261
29. Cho H.Y., Jedlicka A.E., Reddy S.P., Kensler T.W., Yamamoto M., Zhang L.Y., Kleeberger S.R. Role of NRF2 in protection against hyperoxic lung injury in mice. Am J Respir Cell Mol Biol. 26:2002;175-182
30. Ciaccio P.J., Jaiswal A.K., Tew K.D. Regulation of human dihydrodiol dehydrogenase by Michael acceptor xenobiotics. J Biol Chem. 269:1994;15558-15562
31. Conney A.H. Induction of drug-metabolizing enzymes. a path to the discovery of multiple cytochromes p450 Annu Rev Pharmacol Toxicol. 43:2003;1-30
32. Conney A.H., Miller E.C., Miller J.A. The metabolism of methylated aminoazo dyes V. Evidence for induction of enzyme synthesis in the rat by 3-methylcholanthrene. Cancer Res. 16:1956;450-459
33. Crabtree H.G. Retardation of the rate of tumor induction by hydrolyzing chlor-compounds. Cancer Res. 1:1941;39-43
34. Crabtree H.G. The influence of bromobenzene on the induction of skin tumors by 3,4-benzpyrene. Cancer Res. 4:1944;688-693
35. Crabtree H.G. Influence of unsaturated dibasic acids on the induction of skin tumors by chemical carcinogens. Cancer Res. 5:1945;346-351
36. Crabtree H.G. Anti-carcinogenesis. Br Med Bull. 4:1946-1947;345-348
37. De Long M.J., Prochaska H.J., Talalay P. Tissue-specific induction patterns of cancer-protective enzymes in mice by tert-butyl-4-hydroxyanisole and related substituted phenols. Cancer Res. 45:1985;546-551
38. De Long M.J., Prochaska H.J., Talalay P. Induction of NAD(P)H:quinone reductase in murine hepatoma cells by phenolic antioxidants, azo dyes, and other chemoprotectors. a model system for the study of anticarcinogens Proc Natl Acad Sci USA. 83:1986;787-791
39. 1-450 in the induction of NAD(P)H:quinone reductase in a murine hepatoma cell line and its mutants. Carcinogenesis. 8:1987;1549-1553
40. Denison M.S., Fisher J.M., Whitlock J.B. Jr. The DNA recognition site for the dioxin-Ah receptor complex. J Biol Chem. 263:1988;7221-7224
41. 4 12-hydroxydehydrogenase/15-oxoprostaglandin 13-reductase. J Biol Chem. 276:2001;40803-40810
42. Dinkova-Kostova A.T. Protection against cancer by plant phenylpropenoids. induction of mammalian anticarcinogenic enzymes Mini Rev Med Chem. 2:2002;595-610
43. Dinkova-Kostova A.T., Holtzclaw W.D., Cole R.N., Itoh K., Wakabayashi N., Katoh Y., Yamamoto M., Talalay P. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci USA. 99:2002;11908-11913
44. Dinkova-Kostova A.T., Massiah M.A., Bozak R.E., Hicks R.J., Talalay P. Potency of Michael reaction acceptors as inducers of enzymes that protect against carcinogenesis depends on their reactivity with sulfhydryl groups. Proc Natl Acad Sci USA. 98:2001;3404-3409
45. Doll R., Peto R. The causes of cancer. quantitative estimates of avoidable risks of cancer in the United States today J Natl Cancer Inst. 66:1981;1191-1308
46. Eftekharpour E., Holmgren A., Juurlink B.H. Thioredoxin reductase and glutathione synthesis is upregulated by t-butylhydroquinone in cortical astrocytes but not in cortical neurons. Glia. 31:2000;241-248
47. 1 aldehyde reductase gene, AKR7A1. Structure and chromosomal localization of AKR7A1 as well as identification of antioxidant response elements in the gene promoter. Carcinogenesis. 24:2003;727-737
48. Enomoto A., Itoh K., Nagayoshi E., Haruta J., Kimura T., O'Connor T., Harada T., Yamamoto M. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol Sci. 59:2001;169-177
49. Epstein S.S., Joshi S., Andrea J., Forsyth J., Mantel N. The null effect of antioxidants on the carcinogenicity of 3,4,9,10-dibenzpyrene to mice. Life Sci. 6:1967;225-233
50. Fahey J.W., Haristoy X., Dolan P.M., Kensler T.W., Scholtus I., Stephenson K.K., Talalay P., Lozniewski A. Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobacter pylori and prevents benzo[a]pyrene-induced stomach tumors. Proc Natl Acad Sci USA. 99:2002;7610-7615
51. Favreau L.V., Pickett C.B. Transcriptional regulation of the rat NAD(P)H:quinone reductase gene. Identification of the regulatory elements controlling basal level expression and inducible expression by planar aromatic compounds and phenolic antioxidants. J Biol Chem. 266:1991;4556-4561
52. Felton J.S., Ketley J.N., Jakoby W.B., Aitio A., Bend J.R., Nebert D.W. Hepatic glutathione transferase activity induced by polycyclic aromatic compounds. lack of correlation with the murine Ah locus Mol Pharmacol. 18:1980;559-564
53. Frankfurt O.S., Lipchina L.P., Bunto T.V., Emanuel N.M. Effect of 4-methyl-2,6-di-tert-butylphenol (Ionol) on induction of liver tumors in rats. Biull Eksp Biol Med USSR. 64:1967;86-88
54. Friling R.S., Bensimon A., Tichauer Y., Daniel V. Xenobiotic-inducible expression of murine glutathione S-transferase Ya subunit gene is controlled by an electrophile-responsive element. Proc Natl Acad Sci USA. 87:1990;6258-6262
55. Friling R.S., Bergelson S., Daniel V. Two adjacent AP-1-like sites form the electrophile-responsive element of the murine glutathione S-transferase Ya subunit gene. Proc Natl Acad Sci USA. 89:1992;668-672
56. Gielen J.E., Goujon F.M., Nebert D.W. Genetic regulation of aryl hydrocarbon hydroxylase induction II. Simple Mendelian expression in mouse tissues in vivo. J Biol Chem. 247:1972;1125-1137
57. 2 is mediated by the stress response elements and transcription factor Nrf2. Antioxid Redox Signal. 4:2002;249-257
58. Hayes J.D., McLellan L.I. Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic Res. 31:1999;273-300
59. Hayes J.D., Pulford D.J. The glutathione S-transferase supergene family. regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance Crit Rev Biochem Mol Biol. 30:1995;445-600
60. Hintze K.J., Keck A.S., Finley J.W., Jeffery E.H. Induction of hepatic thioredoxin reductase activity by sulforaphane, both in Hepa1c1c7 cells and in male Fisher 344 rats. J Nutr Biochem. 14:2003;173-179
61. Hintze K.J., Wald K.A., Zeng H., Jeffery E.H., Finley J.W. Thioredoxin reductase in human hepatoma cells is transcriptionally regulated by sulforaphane and other electrophiles via an antioxidant response element. J Nutr. 133:2003;2721-2727
62. Hirayama A., Yoh K., Nagase S., Ueda A., Itoh K., Morito N., Hirayama K., Takahashi S., Yamamoto M., Koyama A. EPR imaging of reducing activity in Nrf2 transcriptional factor-deficient mice. Free Radic Biol Med. 34:2003;1236-1242
63. Huang H.C., Nguyen T., Pickett C.B. Regulation of the antioxidant response element by protein kinase C-mediated phosphorylation of NF-E2-related factor 2. Proc Natl Acad Sci USA. 97:2000;12475-12480
64. Huang H.C., Nguyen T., Pickett C.B. Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. J Biol Chem. 277:2002;42769-42774
65. Huggins C., Pataki J. Aromatic azo derivatives preventing mammary cancer and adrenal injury from 7,12-dimethylbenz(a)anthracene. Proc Natl Acad Sci USA. 53:1965;791-796
66. Ishii T., Itoh K., Takahashi S., Sato H., Yanagawa T., Katoh Y., Bannai S., Yamamoto M. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem. 275:2000;16023-16029
67. Itoh K., Chiba T., Takahashi S., Ishii T., Igarashi K., Katoh Y., Oyake T., Hayashi N., Satoh K., Hatayama I., Yamamoto M., Nabeshima Y. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 236:1997;313-322
68. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13:1999;76-86
69. Itoh K., Wakabayashi N., Katoh Y., Ishii T., O'Connor T., Yamamoto M. Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells. 8:2003;379-391
70. Jaffe W.G. The influence of wheat germ oil on the production of tumors in rats by methylcholanthrene. Exp Med Surg. 4:1946;278-282
71. 1) gene structure and induction by dioxin. Biochemistry. 30:1991;10647-10653
72. Kataoka K., Noda M., Nishizawa M. Maf nuclear oncoprotein recognizes sequences related to an AP-1 site and forms heterodimers with both Fos and Jun. Mol Cell Biol. 14:1994;700-712
73. Katoh Y., Itoh K., Yoshida E., Miyagishi M., Fukamizu A., Yamamoto M. Two domains of Nrf2 cooperatively bind CBP, a CREB binding protein, and synergistically activate transcription. Genes Cells. 6:2001;857-868
74. Keen J.H., Habig W.H., Jakoby W.B. Mechanism for the several activities of the glutathione S-transferases. J Biol Chem. 251:1976;6183-6188
75. Kelly V.P., Ellis E.M., Manson M.M., Chanas S.A., Moffat G.J., McLeod R., Judah D.J., Neal G.E., Hayes J.D. Chemoprevention of aflatoxin B1 hepatocarcinogenesis by coumarin, a natural benzopyrone that is a potent inducer of aflatoxin B1-aldehyde reductase, the glutathione S-transferase A5 and P1 subunits, and NAD(P)H:quinone oxidoreductase in rat liver. Cancer Res. 60:2000;957-969
76. Kensler T.W. Chemoprevention by inducers of carcinogen detoxication enzymes. Environ Health Perspect. 105(Suppl. 4):1997;965-970
77. 1 binding to DNA in vivo in rats fed phenolic antioxidants, ethoxyquin and a dithiothione. Carcinogenesis. 6:1985;759-763
78. Kimura S., Smith H.H., Hankinson O., Nebert D.W. Analysis of two benzo[α]pyrene-resistant mutants of the mouse hepatoma Hepa-1 P450 gene via cDNA expression in yeast. EMBO J. 6:1987;1929-1933
79. Kobayashi M., Itoh K., Suzuki T., Osanai H., Nishikawa K., Katoh Y., Takagi Y., Yamamoto M. Identification of the interactive interface and phylogenic conservation of the Nrf2-Keap1 system. Genes Cells. 7:2002;807-820
80. Kuo M.T., Bao J., Furuichi M., Yamane Y., Gomi A., Savaraj N., Masuzawa T., Ishikawa T. Frequent coexpression of MRP/GS-X pump and γ- glutamylcysteine synthetase mRNA in drug-resistant cells, untreated tumor cells, and normal mouse tissues. Biochem Pharmacol. 55:1998;605-615
81. Kumaki K., Jensen N.M., Shire J.G.M., Nebert D.W. Genetic differences in induction of cytosol reduced-NAD(P)H:menadione oxidoreductase and microsomal aryl hydrocarbon hydroxylase in the mouse. J Biol Chem. 252:1977;157-165
82. Lacassagne A., Buu-Hoi N.P., Rudali G. Induction of the carcinogenic action of the carcinogenic action produced by a weakly carcinogenic hydrocarbon on a highly active carcinogenic hydrocarbon. Br J Exp Pathol. 26:1945;5-12
83. Li Y., Jaiswal A.K. Regulation of human NAD(P)H:quinone oxidoreductase gene. Role of AP1 binding site contained within human antioxidant response element. J Biol Chem. 267:1992;15097-15104
84. Lolis E., Alber T., Davenport R.C., Rose D., Hartman F.C., Petsko G.A. Structure of yeast triosephosphate isomerase at 1.9-Å resolution. Biochemistry. 29:1990;6609-6618
85. McMahon M., Itoh K., Yamamoto M., Chanas S.A., Henderson C.J., McLellan L.I., Wolf C.R., Cavin C., Hayes J.D. The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Res. 61:2001;3299-3307
86. McMahon M., Itoh K., Yamamoto M., Hayes J.D. Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J Biol Chem. 278:2003;21592-21600
87. Meechan R.J., McCafferty D.E., Jones R.S. 3-Methylcholanthrene as an inhibitor of hepatic cancer induced by 3′-methyl-4-dimethylaminoazobenzene in the diet of the rat. a determination of the time relationships Cancer Res. 13:1953;802-806
88. Miller A.G., Israel D., Whitlock J.P. Jr. Biochemical and genetic analysis of variant mouse hepatoma cells defective in the induction of benzo(α)pyrene-metabolizing enzyme activity. J Biol Chem. 258:1983;3523-3527
89. Miller J.A., Miller E.C. The carcinogenic aminoazo dyes. Adv Cancer Res. 1:1953;339-396
90. Miller JA, Miller EC. Ultimate chemical carcinogens as reactive mutagenic electrophiles. In: Hiatt HH, Watson JD, Winsten JA, editors. Origins of human cancer. Cold Spring Harbor Conferences on Cell Proliferation, vol. 4, Book B, Cold Spring Harbor, NY: Cold Spring Harbor Press; 1977. p. 605-627.
91. Miller E.C., Miller J.A. Searches for ultimate chemical carcinogens and their reactions with cellular macromolecules. Fortner J.C., Rhoads J.E. Accomplishments in cancer research. 1980;63-98 Lippincott, Philadelphia
92. Miller E.C., Miller J.A., Brown R.R., MacDonald J.C. On the protective action of certain polycyclic aromatic hydrocarbons against carcinogenesis by aminoazodyes and 2-acetylaminofluorene. Cancer Res. 18:1958;469-477
93. Miller E.C., Miller J.A., Hartmann H. N-hydroxy-2-acetylaminofluorene. a metabolite of 2-acetylaminofluorene with increased carcinogenic activity in the rat Cancer Res. 21:1961;815-824
94. Miller E.C., Miller J.A., Enomoto M. The comparative carcinogenicities of 2-acetylaminofluorene and its N-hydroxy metabolite in mice, hamsters, and guinea pigs. Cancer Res. 24:1964;2018-2025
95. Moi P., Chan K., Asunis I., Cao A., Kan Y.W. Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the β-globin locus control region. Proc Natl Acad Sci USA. 91:1994;9926-9930
96. Moinova H.R., Mulcahy R.T. An electrophile responsive element (EpRE) regulates β-naphthoflavone induction of the human γ-glutamylcysteine synthetase regulatory subunit gene. Constitutive expression is mediated by an adjacent AP-1 site. J Biol Chem. 273:1998;14683-14689
97. Mulcahy R.T., Wartman M.A., Bailey H.H., Gipp J.J. Constitutive and β-naphthoflavone-induced expression of the human γ-glutamylcysteine synthetase heavy subunit gene is regulated by a distal antioxidant response element/TRE sequence. J Biol Chem. 272:1997;7445-7454
98. Nguyen T., Rushmore T.H., Pickett C.B. Transcriptional regulation of a rat liver glutathione S-transferase Ya subunit gene. Analysis of the antioxidant response element and its activation by the phorbol ester 12-O- tetradecanoylphorbol-13-acetate. J Biol Chem. 269:1994;13656-13662
99. Nguyen T., Sherratt P.J., Huang H.C., Yang C.S., Pickett C.B. Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J Biol Chem. 278:2003;4536-4541
100. Nioi P., McMahon M., Itoh K., Yamamoto M., Hayes J.D. Identification of a novel Nrf2-regulated antioxidant response element (ARE) in the mouse NAD(P)H:quinone oxidoreductase 1 gene. reassessment of the ARE consensus sequence Biochem J. 374:2003;337-348
101. Numazawa S., Ishikawa M., Yoshida A., Tanaka S., Yoshida T. Atypical protein kinase C mediates activation of NF-E2-related factor 2 in response to oxidative stress. Am J Physiol Cell Physiol. 285:2003;C334-42
102. Okuda A., Sakai M., Muramatsu M. The structure of the rat glutathione S-transferase P gene and related pseudogenes. J Biol Chem. 262:1987;3858-3863
103. Otieno M.A., Kensler T.W., Guyton K.Z. Chemoprotective 3H-1,2-dithiole-3-thione induces antioxidant genes in vivo. Free Radic Biol Med. 28:2000;944-952
104. Paulson K.E., Darnell J.E. Jr., Rushmore T., Pickett C.B. Analysis of the upstream elements of the xenobiotic compound-inducible and positionally regulated glutathione S-transferase Ya gene. Mol Cell Biol. 10:1990;1841-1852
105. Pearson W.R., Windle J.J., Morrow J.F., Benson A.M., Talalay P. Increased synthesis of glutathione S-transferases in response to anticarcinogenic antioxidants. cloning and measurement of messenger RNA J Biol Chem. 258:1983;2052-2062
106. Pietsch E.C., Chan J.Y., Torti F.M., Torti S.V. Nrf2 mediates the induction of ferritin H in response to xenobiotics and cancer chemopreventive dithiolethiones. J Biol Chem. 278:2003;2361-2369
107. Poland A., Glover E. Stereospecific high affinity binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin by hepatic cytosol. J Biol Chem. 251:1976;4936-4946
108. Poland A., Knutson J.C. 2,3,7,8-Tetrachlorodibenzo-p-dioxin and related halogenated aromatic hydrocarbons. examination of the mechanism of toxicity Ann Rev Pharmacol Toxicol. 22:1982;517-552
109. Polednak A.P. Projected number of cancers diagnosed in the US elderly population, 1990 through 2030. Am J Public Health. 84:1994;1136-1313
110. Polednak A.P. Estimating the prevalence of cancer in the United States. Cancer. 80:1997;136-141
111. Prestera T., Talalay P. Electrophile and antioxidant regulation of enzymes that detoxify carcinogens. Proc Natl Acad Sci USA. 92:1995;8965-8969
112. Prestera T., Holtzclaw W.D., Zhang Y., Talalay P. Chemical and molecular regulation of enzymes that detoxify carcinogens. Proc Natl Acad Sci USA. 90:1993;2965-2969
113. Prestera T., Zhang Y., Spencer S.R., Wilczak C.A., Talalay P. The electrophile counterattack response. protection against neoplasia and toxicity Adv Enzyme Regul. 33:1993;281-296
114. Prestera T., Talalay P., Alam J., Ahn Y.I., Lee P.J., Choi A.M.K. Parallel induction of heme oxygenase-1 and chemoprotective phase 2 enzymes by electrophiles and antioxidants. regulation by upstream antioxidant-responsive elements (ARE) Mol Med. 1:1995;827-837
115. Primiano T., Kensler T.W., Kuppusamy P., Zweier J.L., Sutter T.R. Induction of hepatic heme oxygenase-1 and ferritin in rats by cancer chemopreventive dithiolethiones. Carcinogenesis. 17:1996;2291-2296
116. Primiano T., Li Y., Kensler T.W., Trush M.A., Sutter T.R. Identification of dithiolethione-inducible gene-1 as a leukotriene B4 12-hydroxydehydrogenase. implications for chemoprevention Carcinogenesis. 19:1998;999-1005
117. Prochaska H.J., Bregman H.S., De Long M.J., Talalay P. Specificity of induction of cancer protective enzymes by analogues of tert-butyl-4- hydroxyanisole (BHA). Biochem Pharmacol. 34:1985;3909-3914
118. Prochaska H.J., De Long M.J., Talalay P. On the mechanism of induction of cancer-protective enzymes. a unifying proposal Proc Natl Acad Sci USA. 82:1985;8232-8236
119. Prochaska H.J., Santamaria A.B. Direct measurement of NAD(P)H:quinone reductase from cells cultured in microtitre wells. a screening assay for anticarcinogenic enzyme inducers Anal Biochem. 169:1988;328-336
120. Prochaska H.J., Santamaria A.B., Talalay P. Rapid detection of inducers of enzymes that protect against carcinogens. Proc Natl Acad Sci USA. 89:1992;2394-2398
121. Prochaska H.J., Talalay P. Regulatory mechanisms of monofunctional and bifunctional anticarcinogenic enzyme inducers in murine liver. Cancer Res. 48:1988;4776-4782
122. Ramos-Gomez M., Kwak M.K., Dolan P.M., Itoh K., Yamamoto M., Talalay P., Kensler T.W. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci USA. 98:2001;3410-3415
123. Ransone L.J., Verma I.M. Nuclear proto-oncogenes fos and jun. Annu Rev Cell Biol. 6:1990;539-557
124. Reimann S.P., Hall E.M. Protective action of sulfhydryl against carcinogenesis induced with 1,2,5,6-di-benzanthracene. Arch Pathol. 22:1936;55-61
125. Richardson H.L., Cunningham L. The inhibitory action of methylcholanthrene on rats fed the azo dye 3′-methyl-4- dimethylaminoazobenzene. Cancer Res. 11:1951;274
126. Richardson H.L., Stier A.R., Borsos-Nachtnebel E. Liver tumor inhibition and adrenal histologic responses in rats to which 3′-methyl-4- dimethylaminoazobenzene and 20-methylcholanthrene were simultaneously administered. Cancer Res. 12:1952;356-361
127. Riegel B., Wartman W.R., Hill W.T., Reeb B.B., Shubik P., Stanger D.W. Delay of methylcholanthrene skin carcinogenesis in mice by 1,2,5,6- dibenzofluorene. Cancer Res. 11:1951;301-303
128. Rushmore T.H., King R.G., Paulson K.E., Pickett C.B. Regulation of glutathione S-transferase Ya subunit gene expression. identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds Proc Natl Acad Sci USA. 87:1990;3826-3830
129. Rushmore T.H., Morton M.R., Pickett C.B. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem. 266:1991;11632-11639
130. Rushmore T.H., Pickett C.B. Transcriptional regulation of the rat glutathione S-transferase Ya subunit gene. Characterization of a xenobiotic-responsive element controlling inducible expression by phenolic antioxidants. J Biol Chem. 265:1990;14648-14653
131. Siegel D., Bolton E.M., Burr J.A., Liebler D.C., Ross D. The reduction of α-tocopherolquinone by human NAD(P)H:quinone oxidoreductase. the role of α-tocopherolhydroquinone as a cellular antioxidant Mol Pharmacol. 52:1997;300-305
132. Simons S.S. Jr., Pons M., Johnson D.F. α-Keto mesylate. a reactive, thiol specific functional group J Org Chem. 45:1980;3084-3088
133. Snyder G.H., Cennerazzo M.J., Karalis A.J., Field D. Electrostatic influence of local cysteine environments on disulfide exchange kinetics. Biochemistry. 20:1981;6509-6519
134. Sparnins V.L., Chuan J., Wattenberg L.W. Enhancement of glutathione S-transferase activity of the esophagus by phenols lactones, and benzyl isothiocyanate. Cancer Res. 42:1982;1205-1207
135. Spencer S.R., Wilczak C.A., Talalay P. Induction of glutathione transferases and NAD(P)H:quinone reductase by fumaric acid derivatives in rodent cells and tissues. Cancer Res. 50:1990;7871-7875
136. Spencer S.R., Xue L., Klenz E.M., Talalay P. The potency of inducers of NAD(P)H:(quinone-acceptor) oxidoreductase parallels their efficiency as substrates for glutathione transferases. Structural and electronic correlations. Biochem J. 273:1991;711-717
137. Stewart D., Killeen E., Naquin R., Alam S., Alam J. Degradation of transcription factor Nrf2 via the ubiquitin-proteasome pathway and stabilization by cadmium. J Biol Chem. 278:2003;2396-2402
138. Talalay P. Chemoprotection against cancer by induction of phase 2 enzymes. BioFactors. 12:2000;5-11
139. Talalay P., Fahey J.W. Phytochemicals from cruciferous plants protect against cancer by modulating carcinogen metabolism. J Nutr. 131:2001;3027S-3033S
140. Talalay P., Batzinger R.P., Benson A.M., Bueding E., Cha Y.N. Biochemical studies on the mechanisms by which dietary antioxidants suppress mutagenic activity. Adv Enzyme Regul. 17:1978;23-36
141. Talalay P., De Long M.J., Prochaska H.J. Identification of a common chemical signal regulating the induction of enzymes that protect against chemical carcinogenesis. Proc Natl Acad Sci USA. 85:1988;8261-8265
142. Talalay P., Dinkova-Kostova A.T., Holtzclaw W.D. Importance of phase 2 gene regulation in protection against electrophile and reactive oxygen toxicity and carcinogenesis. Adv Enzyme Regul. 43:2003;121-134
143. Talalay P., Fahey J.W., Holtzclaw W.D., Prestera T., Zhang Y. Chemoprotection against cancer by phase 2 enzyme induction. Toxicol Lett. 82/83:1995;173-179
144. Tsuji Y., Ayaki H., Whitman S.P., Morrow C.S., Torti S.V., Torti F.M. Coordinate transcriptional and translational regulation of ferritin in response to oxidative stress. Mol Cell Biol. 20:2000;5818-5827
145. Vogelstein B., Kinzler K.W. The multistep nature of cancer. Trends Genet. 9:1993;138-141
146. Wakabayashi N., Dinkova-Kostova A.T., Holtzclaw W.D., Kang M.-.I.I., Kobayashi A., Yamamoto M., Kensler T.W., Talalay P. Protection against electrophile and oxidant stress by induction of the phase 2 response. Fate of cysteines of the Keap1 sensor modified by inducers Proc Natl Acad Sci USA. 101:2004;2040-2045
147. Wakabayashi N., Itoh K., Wakabayashi J., Motohashi H., Noda S., Takahashi S., Imakado S., Kotsuji T., Otsuka F., Roop D.R., Harada T., Engel J.D., Yamamoto M. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet. 35:2003;238-245
148. Wasserman W.W., Fahl W.E. Functional antioxidant responsive elements. Proc Natl Acad Sci USA. 94:1997;5361-5366
149. Wattenberg L.W. Inhibition of carcinogenic and toxic effects of polycyclic hydrocarbons by phenolic antioxidants and ethoxyquin. J Natl Cancer Inst. 48:1972;1425-1430
150. Wattenberg L.W. Inhibition of carcinogenic and toxic effects of polycyclic hydrocarbons by several sulfur-containing compounds. J Natl Cancer Inst. 52:1974;1583-1587
151. Wattenberg L.W., Page M.A., Leong J.L. Induction of increased benzpyrene hydroxylase activity by flavones and related compounds. Cancer Res. 28:1968;934-937
152. Wattenberg L.W., Speier J., Kotake A. Effects of antioxidants on metabolism of aromatic polycyclic hydrocarbons. Adv Enzyme Regul. 14:1976;313-322
153. Whitlock J.P. Jr. Induction of cytochrome P4501A1. Annu Rev Pharmacol Toxicol. 39:1999;103-125
154. Williams R.T. Comparative patterns of drug metabolism. Fed Proc. 26:1967;1029-1039
155. Williams-Ashman H.G., Huggins C. Oxidation of reduced pyridine nucleotides in mammary gland and adipose tissue following treatment with polynuclear hydrocarbons. Med Exp. 4:1961;223-226
156. Yamane Y., Furuichi M., Song R., Van N.T., Mulcahy R.T., Ishikawa T., Kuo M.T. Expression of multidrug resistance protein/GS-X pump and
157. Yu R., Chen C., Mo Y.Y., Hebbar V., Owuor E.D., Tan T.H., Kong A.N. Activation of mitogen-activated protein kinase pathways induces antioxidant response element-mediated gene expression via a Nrf2-dependent mechanism. J Biol Chem. 275:2000;39907-39913
158. Zhu M., Chapman W.G., Oberley M.J., Wasserman W.W., Fahl W.E. Polymorphic electrophile response elements in the mouse glutathione S-transferase GSTa1 gene that confer increased induction. Cancer Lett. 164:2001;113-118
159. Zipper L.M., Mulcahy R.T. Inhibition of ERK and p38 MAP kinases inhibits binding of Nrf2 and induction of GCS genes. Biochem Biophys Res Commun. 278:2000;484-492
160. Zipper L.M., Mulcahy R.T. The Keap1 BTB/POZ dimerization function is required to sequester Nrf2 in cytoplasm. J Biol Chem. 277:2002;36544-36552
161. Zipper L.M., Mulcahy R.T. Erk activation is required for Nrf2 nuclear localization during pyrrolidine dithiocarbamate induction of glutamate cysteine ligase modulatory gene expression in HepG2 cells. Toxicol Sci. 73:2003;124-134