Regulatory Mechanisms Controlling Gene Expression Mediated by the Antioxidant Response Element

Annual Review of Pharmacology and Toxicology

Volumn 43, Issue , 2003, Pages 233-260

  Nguyen, Truyen ^a   Sherratt, Philip J ^a   Pickett, Cecil B ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Chemoprevention; Nrf2; Oxidative stress; Signal transduction

Indexed keywords

3 HYDROXYCOUMARIN; ACTIVATING TRANSCRIPTION FACTOR 4; ANTIOXIDANT; BETA NAPHTHOFLAVONE; BUTYLATED HYDROXYANISOLE; BZIP PROTEIN; DRUG METABOLIZING ENZYME; ENZYME; ETHOXYQUIN; KEAP1 PROTEIN; MALEIC ACID DIETHYL ESTER; MITOGEN ACTIVATED PROTEIN KINASE; OLTIPRAZ; PHENOL DERIVATIVE; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE; POLYAMINE MODULATED FACTOR 1 PROTEIN; PROTEIN; PROTEIN KINASE C; PYRROLIDINE DITHIOCARBAMATE; SMALL MAF PROTEIN; SULFORAPHANE; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NF E2; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; XENOBIOTIC AGENT; DNA BINDING PROTEIN; NFE2L2 PROTEIN, HUMAN; NFE2L2 PROTEIN, RAT; TRANSACTIVATOR PROTEIN;

ANTIOXIDANT RESPONSIVE ELEMENT; CHEMOPROPHYLAXIS; DNA RESPONSIVE ELEMENT; ENHANCER REGION; ENZYME INDUCTION; GENE ACTIVITY; GENE EXPRESSION REGULATION; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; GENETICS; METABOLISM; RAT; TRANSACTIVATION;

ANIMALS; ANTIOXIDANTS; DNA-BINDING PROTEINS; HUMANS; NF-E2-RELATED FACTOR 2; RATS; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS;

EID: 0037763721     PISSN: 03621642     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.pharmtox.43.100901.140229     Document Type: Review

References (105)

1. Rushmore TH, Morton MR, Pickett CB. 1991. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem. 266:11632-39
2. Hayes JD, McLellan LI. 1999. Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Rad. Res. 31:273-300
3. Moinova HR, Mulcahy RT. 1998. An electrophile responsive element (EpRE) regulates β-naphthoflavone induction of the human γ-glutamylcysteine synthetase regulatory subunit gene. J. Biol. Chem. 273:14683-89
4. Wild AC, Gipp JJ, Mulcahy RT. 1998. Overlapping antioxidant response element sequences mediate basal and 8-naphthoflavone-induced expression of the human γ-glutamylcysteine sunthetase catalytic subunit gene. Biochem. J. 332: 373-81
5. , Kim Y-C, Masutani H, Yamaguchi Y, Itoh K, Yamamoto M, et al. 2001. Hemin-induced activation of the thioredoxin gene by Nrf2. J. Biol. Chem. 276:18399-406
6. Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, et al. 2000. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J. Biol. Chem. 275:16023-29
7. Rushmore TH, Pickett CB. 1990. Transcriptional regulation of the rat glutathione S-transferase Ya subunit gene. Characterization of a xenobiotic-reponsive element controlling inducible expression by phenolic antioxidants. J. Biol. Chem. 265:14648-53
8. Favreau LV, Pickett CB. 1991. Transcriptional regulation of the rat NAD(P)H: quinone reductase gene. Identification of regulatory element: controlling basal and inducible expression by planar aromatic compounds and phenolic antioxidants. J. Biol. Chem. 66:4556-61
9. Jaiswal AK. 1991. Human NAD(P)H:quinone oxidoreductase (NQO1) gene structure and induction by dioxin. Biochemistry 30:10647-513
10. McMahon M, Itoh K, Yamamoto M, Chanas SA, Henderson CJ, et al. 2001. 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. 61:3299-307
11. Prochaska HJ, De Long MJ, Talalay P. 1985. On the mechanism of induction of cancer-protective enzymes: a unifying proposal. Proc. Natl. Acad. Sci. USA 82:8232-36
12. Whitlock JP Jr. 1999. Induction of cytochrome P4501A1. Annu. Rev. Pharmacol. Toxicol. 39:103-25
13. Reyes H, Reisz-Porszasz S, Hankinson O. 1992. Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor. Science 256:1193-95
14. Swanson HI, Chan WK, Bradfield CA. 1995. DNA binding specificities and pairing rules of the Ah receptor, ARNT, and SIM proteins. J. Biol. Chem. 270: 26292-302
15. Rushmore TH, King RG, Paulson KE, Pickett CB. 1990. 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 87:3826-30
16. Prochaska HJ, Talalay P. 1988. Regulatory mechanisms of monofunctional and bifunctional anticarcinogenic enzyme inducers in murine liver. Cancer Res. 48:4776-82
17. Telakowski-Hopkins CA, King RG, Pickett CB. 1988. Glutathione S-transferase Ya subunit gene: identification of regulatory elements required for basal level and inducible expression. Proc. Natl. Acad. Sci. USA 85:1000-4
18. Friling RS, Bensimon A, Tichauer Y, Daniel V. 1990. Xenobiotic-inducible expression of murine glutathione S-transferase Ya subunit gene is controlled by an electrophile-responsive element. Proc. Natl. Acad. Sci. USA 87:6258-62
19. Favreau LV, Pickett CB. 1995. The rat quinone reductase antioxidant response element. Identification of the nucleotide sequence required for basal and inducible activity and detection of antioxidant response element-binding proteins in hepatoma and non-hepatoma cell lines. J. Biol. Chem. 270:24468-74
20. Li Y, Jaiswal AK. 1992, Regulation of human NAD(P)H:quinone oxidoreductase gene. Role of AP-1 binding site contained within human antioxidant response element. J. Biol. Chem. 267:15097-104
21. Xie T, Belinsky M, Xu Y, Jaiswal AK. 1995. ARE- and TRE-mediated regulation of gene expression. Response to xenobiotics and antioxidants. J. Biol. Chem. 270:6894-900
22. Talalay P, Fahey JW, Holtzclaw WD, Prestera T, Zhang Y. 1995. Chemoprotection against cancer by phase 2 enzyme induction. Toxicol. Lett. 82-83:173-79
23. Bonnesen C, Eggleston IM, Hayes JD. 2001. Dietary indoles and isothiocyanates that are generated from cruciferous vegetables can both stimulate apoptosis and confer protection against DNA damage in human colon cell lines, Cancer Res. 61:6120-30
24. Kwak M-K, Egner PA, Dolan PM, Ramos-Gomez M, Groopman JD, et al. 2001. Role of phase 2 enzyme induction in chemoprotection by dithiolethiones. Mutat. Res. 480-481:305-15
25. Prestera T, Talalay P. 1995. Electrophile and antioxidant regulation of enzymes that detoxify carcinogens. Proc. Natl. Acad. Sci. USA 92:8965-69
26. Ren Y, Smith A. 1995. Mechansim of metallothionein gene regulation by heme-hemopexin. J. Biol. Chem. 270: 23988-95
27. Inamdar NM, Ahn YI, Alam J. 1996. The heme-responsive element of the mouse heme oxygenase-1 gene is an extended AP-1 binding site that resembles the recognition sequences of MAF and NF-E2 transcription factors. Biochem. Biophys. Res. Commun. 221:570-76
28. Dinkova-Kostova AT, Massiah MA, Bozak RE, Hicks RJ, Talalay P. 2001. 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 98:3404-9
29. Ketterer B, Meyer DJ. 1989. Glutathione transferases: a possible role in the detoxification and repair of DNA and lipid hydroperoxides. Mutat. Res. 214:33-40
30. Bao Y, Jemth P, Mannervik B, Williamson G. 1997. Reduction of thymine hydroperoxide by phospholipid hydroperoxide glutathione peroxidase and gluatathione transferases. FEBS Lett. 410: 210-12
31. Talalay P, Benson AM. 1982. Elevation of quinone reductase activity by anticarcinogenic antioxidants. Adv. Enzyme Regul. 20:287-300
32. Ryter SW, Tyrrell RM. 2000. The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic. Biol. Med. 28:289-309
33. Guengerich FP, Shimada T. 1998. Activation of procarcinogens by human cytochrome P450 enzymes. Mutat. Res. 400:201-13
34. Hayes JD, Ellis EM, Neal GE, Harrison DJ, Manson MM. 1999. Cellular response to cancer chemopreventive agents: contribution of the antioxidant responsive element to the adaptive response to oxidative and chemical stress. Biochem. Soc. Symp. 64:141-68
35. Hayes JD, McLeod R, Ellis EM, Pulford DJ, Irleand LS, et al. 1996. Regulation of glutathione S-transferases and aldehyde reductase by chemoprotectors: studies of mechansims responsible for inducible resistance to aflatoxin B1. IARC Sci. Publ. 139:175-87
36. Kelly VP, Ellis EM, Manson MM, Chanas SA, Moffat GJ. 2000. 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. 60:957-69
37. Kensler TW, Curphey TJ, Maxiutenko Y, Roebuck BD. 2000. Chemoprotection by organosulfur inducers of phase 2 enzymes: dithiolethiones and dothiins. Drug Metabol. Drug Interact. 17:3-22
38. Potter JD, Steinmetz K. 1996. Vegetables, fruit and phytoestrogens as preventive agents. In Principles of Chemoprevention, ed. BW Stewart, D McGregor, P Kleihues. No. 139: IARC Scientific Publications, pp. 61-90. Lyon, France: Int. Agency Res. Cancer
39. Shapiro TA, Fahey JW, Wade KL, Stephenson KK, Talalay P. 2001. Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: metabolism and excretion in humans. Cancer Epidemiol. Biomarkers Prev. 10:501-8
40. Dinkova-Kostova AT, Abeygunawardana C, Talalay P. 1998. Chemoprotective properties of phenylpropenoids, bis(benzylidene)cycloalkanones, and related Michael reaction acceptors: correlation of potencies as phase 2 enzyme inducers and radical scavengers. J. Med. Chem. 41:5287-96
41. Mulcahy RT, Wartman MA, Bailey H, Gipp JJ. 1997. 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. 272:7445-54
42. Johnsen Ø, Murphy P, Prydz H, Kolstø AB. 1998. Interaction of the CNC-bZIP factor TCF11/LCR-F1/Nrf1 with MafG: binding-site selection and regulation of transcription. Nucleic Acids Res. 26(2):512-20
43. Wasserman WW, Fahl WE. 1997. Functional antioxidant responsive elements. Proc. Natl. Acad. Sci. USA 94:5361-66
44. Whitmarsh AJ, Davis RJ. 1996. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J. Mol. Med. 74(10): 589-607
45. Nguyen T, Rushmore TH, Pickett CB. 1994. 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-tetra-deanoylphorbol-13-acetate. J. Biol. Chem. 269: 13656-62
46. Yoshioka K, Deng T, Cavigelli M, Karin M. 1995. Antitumor promotion by phenolic antioxidants: inhibition of AP-1 activity through induction of Fra expression. Proc. Natl. Acad. Sci. USA 92:4972-76
47. Friling RS, Bergelson S, Daniel V. 1992. Two adjacent AP-1-like binding sites form the electrophile-responsive element of the murine glutathione S-transferase Ya subunit gene. Proc. Natl. Acad. Sci. USA 89:668-72
48. Venugopal R, Jaiswal AK. 1996. Nrf1 and Nrf2 positively and e-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase, gene. Proc. Natl. Acad. Sci. USA 93:14960-65
49. Wild AC, Moinova HR, Mulcahy RT. 1999. Regulation of γ -glutamylcysteine synthetase regulatory subunit gene expression by the transcription factor Nrf2. J. Biol. Chem. 274:33627-36
50. Alam J, Stewart D, Touchard C, Boinapally S, Choi AMK, et al. 1999. Nrf2, a Cap 'n' Collar transcription factor, regulates induction of the heme oxigenase-1 gene. J. Biol. Chem. 274:26071-78
51. Nguyen T, Huang HC, Pickett CB. 2000. Transcriptional regulation of the antioxidant response element. Activation by Nrf2 and repression by MafK. J. Biol. Chem. 275:15466-73
52. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, et al. 1997. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236:313-22
53. Moi P, Chan K, Asunis I, Cao A, Kan YW. 1994. 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 91:9926-30
54. Andrews NC, Erdjument-Bromage H, Davidson MB, Temspt P, Orkin SH. 1993. Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature 362:722-28
55. Ney PA, Andrews NC, Jane SM, Safer B, Purucker ME, et al. 1993. Purification of the human NF-E2 complex: cDNA cloning of the hematopoietic cell-specific subunit and evidence for an associated partner. Mol. Cell. Biol. 11(9):5604-12
56. Igarashi K, Kataoka K, Itoh K, Hayashi N, Nishizawa M, et al. 1994. Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Mafproteins. Nature 367:568-72
57. Chan JY, Han XL, Kan YW. 1993. Cloning of Nrf1, an NF-E2-related transcription factor, by genetic selection in yeast. Proc. Natl. Acad. Sci. USA 90: 11371-75
58. Chanas SA, Jiang Q, McMahon M, McWalter GK, McLellan LI, et al. 2002. Loss of 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. 365:405-16
59. Venugopal R, Jaiswal AK. 1998. Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 17:3145-56
60. Chan K, Kan YW. 1999. Nrf2 is essential for protection against acute pulmonary injury in mice. Proc. Natl. Acad. Sci. USA 96:12731-36
61. Chan K, Han XD, Kan YW. 2001. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc. Natl. Acad. Sci. USA 98:4611-16
62. Enomoto A, Itoh K, Nagayoshi E, Haruta J, Kimura T, et al. 2001. High sensitivity of Nr2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol. Sci. 59:169-77
63. Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, et al. 2001. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in Nrf2 transcription-deficient mice. Proc. Natl. Acad. Sci. USA 98:3410-15
64. Motohashi H, Shavit JA, Igarashi K, Yamamoto M, Engel JD. 1997. The world according to Maf. Nucleic Acids Res. 25(15):2953-59
65. Kerppola TK, Curran T. 1994. A conserved region adjacent to the basic domain is required for recognition of an extended DNA binding site by Maf/ Nr1 family proteins. Oncogene 9:3149-58
66. Kotkow KJ, Orkin SH. 1995. Dependence of globin gene expression in mouse erythroleukemia cells on the NF-E2 heterodimer. Mol. Cell. Biol. 15(8): 4640-47
67. Blank V, Kim MJ, Andrews NC. 1997. Human MafG is a functional partner for p45 NF-E2 in activating globin gene expression. Blood 89(11):3925-35
68. Marini MG, Chan K, Casula L, Kan YW, Cao A, et al. 1997. hMAF, a small human transcription factor that heterodimerizes specifically with Nrf1 and Nrf2. J. Biol. Chem. 272:16490-97
69. Oyake T, Itoh K, Motohashi H, Hayashi N, Hoshino H, et al. 1996. Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol. Cell. Biol. 16:6083-95
70. Kataoka K, Igarashi K, Itoh K, Fujiwara KT, Noda M, et al. 1995. Small Maf proteins heterodimerize with Fos and may act as competitive repressors of the NF-E2 transcription factor. Mol. Cell. Biol. 15:2180-90
71. Dhakshinamoorthy S, Jaiswal AK. 2000. Small Maf (MafG and MafK) proteins negatively regulate antioxidant response element-mediated expression and antioxidant induction of the NAD(P)H:quinone oxidoreductase 1 gene. J. Biol. Chem. 275:40134-41
72. Gong P, Hu B, Stewart D, Ellerbe M, Figuera YG, et al. 2001. Cobalt induces heme oxigenase-1 expression by a hypoxia-inducible factor-independent mechanism in Chinese hamster ovary cells. J. Biol. Chem. 276:27018-25
73. Husberg C, Murphy P, Martin E, Kolstø AB. 2001. Two domains of the human bZIP transcription factor TCF11 are necessary for transactivation. J. Biol. Chem. 276:17641-52
74. Nagai T, Igarashi K, Akasaka J, Furuyama K, Fujita H, et al. 1998. Regulation of NF-E2 activity in erythroleukemia cell differentiation. J. Biol. Chem. 273:5358-65
75. Moran JA, Dahl ER, Mulcahy RT. 2002. Differential induction of mafF, mafG and mafK expression by electrophile-response element activators. Biochem. J. 361:371-77
76. Motohashi H, Katsuoka F, Shavit JA, Engel JD, Yamamoto M. 2000. Positive or negative MARE-dependent transcriptional regulation is determined by the abundance of small Maf proteins. Cell 103:865-75
77. Myhrstad MCW, Husberg C, Murphy P, Nordström O, Blomhoff JO, et al. 2001. TCF/Nrf1 overexpression increases the intracellular glutathione level and can transactivate the γ-glutamylcysteine synthetase (GCS) heavy subunit promoter. Biochim. Biophys. Acta 1517:212-19
78. Chan JY, Kwong M, Lu R, Chang J, Wang B, et al. 1998. Targeted disruption of the ubiquitous CNC-bZIP transcription factor, Nrf1, results in anemia and embryonic lethality in mice. EMBO J. 17:1779-87
79. 1, and gss expression in mouse fibroblasts. J. Biol. Chem. 274:37491-98
80. Kobayashi A, Ito E, Toki T, Kogame K, Takahashi S, et al. 1999. Molecular cloning and functional characterization of a new cap 'n' collar family transcription factor Nrf3. J. Biol. Chem. 274:6443-52
81. He CH, Gong P, Hu B, Stewart D, Choi ME, et al. 2001. Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxigenase-1 gene regulation. J. Biol. Chem. 276:20858-65
82. 1-acetyltransferase gene. J. Biol. Chem. 274:22095-101
83. 1-acetyltransferase (SSAT) gene, Biochem. J. 355:45-49
84. Yu R, Lei W, Mandlejar S, Weber MJ, Der CJ, et al. 1999. Role of a mitogen-activated protein kinase pathway in the induction of Phase II detoxifying enzymes by chemicals. J. Biol. Chem. 274:27545-52
85. Yu R, Mandlekar S, Lei W, Fahl WE, Tan T-H, et al. 2000, p38 Mitogen-activated protein kinase negatively regulates the induction of Phase II drug-metabolizing enzymes that detoxify carcinogens. J. Biol. Chem. 275:2322-27
86. Yu R, Chen C, Mo Y-Y, Owuor ED, Tan T-H, et al. 2000. Activation of mitogen-activated protein kinase pathways induces 1 antioxidant response element-mediated gene expression via a Nrf2-dependent mechanism, J. Biol. Chem. 275:39907-13
87. Zipper LM, Mulcahy RT. 2000. Inhibition of ERK and p38 MAP kinases inhibits binding of Nrf2 and induction of GCS genes. Biochem. Biophys. Res. Commun. 278:484-92
88. Simon C, Simon M, Vucelic G, Hicks MJ, Plinkert PK, et al. 2001. The p38 SAPK pathway regulates the expression of the MMP-9 collagenase via AP-1 dependent promoter activation. Exp. Cell Res. 271:344-55
89. Davies SP, Reddy H, Caivano M, Cohen P. 2000. Specificity and mechansism of action of some commonly used protein kinase inhibitors. Biochem. J. 351:91-105
90. Alam J, Wicks C, Stewart D, Gong P, Touchard C, et al. 2000. Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 epithelial cells. J. Biol. Chem. 275:27694-702
91. Masuya Y, Hioki K, Tokunaga R, Taketani S. 1998. Involvement of the tyrosine phosphorylation pathway in induction of human heme oxygenase-1 by hemin, sodium arsenite, and cadmium chloride, J. Biochem. 124:628-33
92. Kang KW, Ryu JH, Kim SG. 2000. The essential role of phosphatidylinositol 3-kinase and the p38 mitogen-activated protein kinase activation in the antioxidant response element-mediated rGSTA2 induction by decreased glutathione in H4IIE hepatoma cells. Mol. Pharmacol. 58:1017-25
93. Kang KW, Cho MK, Lee CH, Kim SG. 2001. Activation of phosphatidylinositol 3-kinase and Akt by tert-butylhydroquinone is responsible for antioxidant response element-mediated rGSTA2 induction in H4IIE cells. Mol. Pharmacol. 59:1147-56
94. Reiners JJ Jr, Lee J-Y, Clift RE, Dudley DT, Myrand SP. 1998. PD98059 is an equipotent antagonist of the aryl hydrocarbon receptor and inhibitor of mitogen-activated protein kinase. Mol. Pharmacol. 53:438-45
95. Lee J-M, Hanson JM, Chu WA, Johnson JA. 2001. Phosphatidylinositol 3-kinase, not extracellular signal-regulated kinase, regulates activation of the antioxidant-responsive element in IMR-32 human neuroblastoma cells. J. Biol. Chem. 276: 20011-16
96. Li J, Lee J-M, Johnson JA. 2002. Microarray analysis reveals an antioxidant responsive element-driven gene set involved in conferring protection from an oxidative stress-induced apoptosis in IMR-32 cells. J. Biol. Chem. 277:388-94
97. Huang H-C, Nguyen T, Pickett CB. 2000. Regulation of the antioxidant response element by protein kinase C-mediated phosphorylation of NF-E2 related factor 2. Proc. Natl. Acad. Sci. USA 97:12475-80
98. Ann Le Good J, Ziegler WH, Parekh DB, Alessi DR, Cohen P, et al. 1998. Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1. Science 281:2042-45
99. Clerk A, Sugden PH. 2001. Untangling the web specific signaling from PKC isoforms to MAPK cascades. Circ. Res. 89:847-49
100. Heidkamp MC, Bayer AL, Martin JL, Samarel AM. 2001. Differential activation of mitogen-activated protein kinase cascades and apoptosis by protein kinase C ε and δ in neonatal rat ventricular myocytes. Circ. Res. 89:882-90
101. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, et al. 1999. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13:76-86
102. Dhakshinamoorthy, S, Jaiswal AK. 2001. Functional characterization and role of Inrf2 in antioxidant response element-mediated expression and antioxidant induction of NAD(P)H:quinone oxidoreductase 1 gene. Oncogene 20:3906-17
103. Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, et al 1998. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17:2596-606
104. Cho S-G, Lee YH, Park H-S, Ryoo K, Kang KW, et al. 2001. Glutathione S-transferase Mu modulates the stress-activated signals by suppressing apoptosis signal-regulating kinase 1. J. Biol. Chem. 276:12749-55
105. Adler V, Yin Z, Fuchs, SY, Benezra M, Rosario L, et al. (1991). Regulation of JNK signaling by GSTp. EMBO J. 18:1321-34