Nrf2 signaling in coordinated activation of antioxidant gene expression

Free Radical Biology and Medicine

Volumn 36, Issue 10, 2004, Pages 1199-1207

  Jaiswal, Anil K ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Antioxidant genes; Antioxidant response element; ARE; Electrophile response element; EpRE; Expression and coordinated induction; Free radicals; NF E2 related factors; Nrf2; Protein kinase C; Reactive oxygen species

Indexed keywords

ANTIOXIDANT; NUCLEAR FACTOR; PROTEASOME; PROTEIN C FOS; PROTEIN DERIVATIVE; PROTEIN KINASE C; SERINE; TRANSCRIPTION FACTOR FRA 1; TRANSCRIPTION FACTOR MAFG; TRANSCRIPTION FACTOR MAFK; TRANSCRIPTION FACTOR NF E2; TRANSCRIPTION FACTOR NF E2 RELATED NUCLEAR FACTOR 1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

CELL ACTIVITY; CYTOPLASM; CYTOSOL; DNA RESPONSIVE ELEMENT; ELECTRICITY; ENZYME INDUCTION; EXPOSURE; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE INDUCTION; GENE TRANSLOCATION; HUMAN; MOLECULAR MECHANICS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ANTIOXIDANTS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; PHOSPHORYLATION; PROTEIN KINASE C; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS;

EID: 1942520367     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2004.02.074     Document Type: Review

References (90)

1. Breimer L.H. Molecular mechanisms of oxygen radical carcinogenesis and mutagenesis: the role of DNA base damage. Mol. Carcinog. 3:1990;188-197.
2. Meneghini R. Iron homeostasis, oxidative stress, and DNA damage. Free Radic. Biol. Med. 23:1997;783-792.
3. 2: oxidant air pollutants and more. Environ. Health Perspect. 102(Suppl. 10):1994;179-184.
4. Ward J.F. The complexity of DNA damage: relevance to biological consequences. Int. J. Radic. Biol. 66:1994;427-432.
5. Grisham M.B., McCord J.M. Chemistry and cytotoxicity of reactive oxygen metabolites. Physiology of oxygen radicals. 1986;1-18 Waverly Press, Baltimore.
6. Thelen M., Dewald B., Baggiolini M. Neutrophil signal transduction and activation of the respiratory burst. Physiol. Rev. 73:1993;797-821.
7. Kerr M.E., Bender C.M., Monti E.J. An introduction to oxygen free radicals. Heart Lung. 25:1996;200-209.
8. Wei Y.H. Oxidative stress and mitochondrial DNA mutations in human aging. Proc. Soc. Exp. Biol. Med. 217:1998;53-63.
9. Kasprzak K.S. Possible role of oxidative damage in metal-induced carcinogenesis. Cancer Invest. 13:1995;411-430.
10. Suzuki Y.J., Forman H.J., Sevanian A. Oxidants as stimulators of signal transduction. Free Radic. Biol. Med. 22:1997;269-285.
11. Breen A.P., Murphy J.A. Reactions of oxyl radicals with DNA. Free Radic. Biol. Med. 18:1995;1033-1077.
12. Dhakshinamoorthy S., Long D.J. II, Jaiswal A.K. Antioxidant regulation of genes encoding enzymes that detoxify xenobiotics and carcinogens. Curr. Top. Cell. Regul. 36:2000;201-206.
13. Jaiswal A.K. Regulation of genes encoding NAD(P)H:quinone oxdoreductases. Free Radic. Biol. Med. 29:2000;254-262.
14. Bloom D., Dhakshinamoorthy S., Wang W., Celli C.M., Jaiswal A.K. Role of NF-E2 related factors in oxidative stress. Storey K.B., Storey J.M. Cell and molecular responses to stress. Protein adaptation and signal transduction. Vol. 2:2001;229-238 Elsevier, Amsterdam.
15. Rosen G.M., Pou S., Ramos C.L., Cohen M.S., Britigan B.E. Free radicals and phagocytic cells. FASEB J. 9:1995;200-209.
16. Bauer C.E., Elsen S., Bird T.H. Mechanisms for redox control of gene expression. Annu. Rev. Microbiol. 53:1999;495-523.
17. Zheng M., Storz G. Redox sensing by prokaryotic transcription factors. Biochem. Pharmacol. 59:2000;1-6.
18. Schulze-Osthoff K., Bauer M., Vogt M., Weesselborg S., Baeuerle P.A. Forman H.J., Cadenas E. Reactive oxygen intermediates as primary signals and second messengers in the activation of transcription factors. 1997;239-259 Chapman & Hall, New York.
19. Joseph P., Jaiswal A.K. NAD(P)H:quinone oxidoreductase1 (DT diaphorase) specifically prevents the formation of benzo(a)pyrene quinone-DNA adducts generated by cytochrome P4501A1 and P450 reductase. Proc. Natl. Acad. Sci. USA. 91:1994;8413-8417.
20. Pickett C.B., Lu A.Y.H. Glutathione S-transferases: gene structure, regulation and biological function. Annu. Rev. Biochem. 58:1989;743-764.
21. Tsuchida S., Sato K. Glutathione transferases and cancer. Crit. Rev. Biochem. Mol. Biol. 27:1992;337-384.
22. Kretzschmar M., Reinhardt D., Schlechtweg J., Machnik G., Klinger W., Schirrmeister W. Glutathione homeostasis in rats chronically treated with ethanol: evidence for an increased hepatic GSH export in vivo. Exp. Toxicol. Pathol. 44:1992;344-348.
23. Choi A.M., Alam J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am. J. Respir. Cell. Mol. Biol. 15:1996;9-19.
24. Mulkahy R.T., Wartman M.A., Bailey 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.
25. Angel P., Karin M. The role of Jun, Fos and AP-1 complex in cell proliferation and transformation. Biochim. Biophys. Acta. 1072:1991;129-157.
26. Xie T., Belinsky M., Xu Y., Jaiswal A.K. ARE- and TRE- mediated regulation of gene expression: response to xenobiotics and antioxidants. J. Biol. Chem. 270:1995;6894-6900.
27. 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.
28. Rushmore T.H., Pickett C.B. Glutathione-S-transferases, structure, regulation and therapeutic implications. J. Biol. Chem. 268:1993;11475-11478.
29. 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.
30. 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.
31. Wasserman W., Fahl W.E. Functional antioxidant responsive elements. Proc. Natl. Acad. Sci. USA. 94:1997;5361-5366.
32. Venugopal R., Jaiswal A.K. Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc. Natl. Acad. Sci. USA. 93:1996;14960-14965.
33. Alam J., Stewart D., Touchard C., Boinapally S., Choi M.K., Cook J.L. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274:1999;26071-26078.
34. Wild A.C., Moinova H.R., Mulcahy R.T. Regulation of γ- glutamylcysteine synthetase subunit gene expression by transcription factor Nrf2. J. Biol. Chem. 274:1999;33627-33636.
35. Nguyen T., Huang H.C., Pickett C.B. Transcriptional regulation of the antioxidant response element: activation by Nrf2 and repression by MafK. J. Biol. Chem. 275:2000;15466-15473.
36. Andrews N.C., Erdjument-Bromage H., Davidson M.B., Tempst P., Orikin S.H. Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature. 339:1993;722-727.
37. Ney P.A., Sorrentino B.P., McDonaugh K.T., Nienhuis A.W. Tandem AP-1-binding sites within the human beta-globin dominant control region function as an inducible enhancer in erythroid cells. Genes Dev. 4:1990;993-1006.
38. Moi P., Kan Y.W. Synergistic enhancement of globin gene expression by activator protein-1-like proteins. Proc. Natl. Acad. Sci. USA. 87:1990;9000-9004.
39. Liu D., Chang J.C., Moi P., Liu W., Kan Y.W., Curtin P.T. Dissection of the enhancer activity of beta-globin 5′ DNase I-hypersensitive site 2 in transgenic mice. Proc. Natl. Acad. Sci. USA. 89:1992;3899-3903.
40. Mignotte V., Eleouet J.F., Raich N., Romeo P.H. Cis- and trans-acting elements involved in the regulation of the erythroid promoter of the human porphobilinogen deaminase gene. Proc. Natl. Acad. Sci. USA. 86:1989;6522-6548.
41. Igarashi K., Kataoka K., Nishizawa M., Yamamoto M. Regulation of transcription of erythroid factor NF-E2 p45 with small Maf proteins. Nature. 367:1994;568-572.
42. Shivdasani R., Orkin S.H. Erythropoiesis and globin gene expression in mice lacking the transcription factor NF-E2. Proc. Natl. Acad. Sci. USA. 92:1995;8690-8694.
43. Chan J.Y., Han X., Kan Y.W. Cloning of Nrf1, an NF-E2-related transcription factor, by genetic selection in yeast. Proc. Natl. Acad. Sci. USA. 90:1993;11371-11375.
44. 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 β-globin locus control region. Proc. Natl. Acad. Sci. USA. 91:1994;9926-9930.
45. Kobayashi A., Ito E., Toki T., Kogame K., Takahashi S., Igarashi K., Hayashi N., Yamamoto M. Molecular cloning and functional characterization of a new cap'n'collar family transcription factor Nrf3. J. Biol. Chem. 274:1999;6443-6452.
46. Chan J.Y., Kwong M., Lu R., Chang J., Wang B., Yen T.S., Kan Y.W. Targeted disruption of the ubiquitous CNC-bZIP transcription factor, Nrf-1, results in anemia and embryonic lethality in mice. EMBO J. 17:1998;1779-1787.
47. Chan K., Lu R., Chang J.C., Kan Y.W. Nrf2, a member of the NF-E2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc. Natl. Acad. Sci. USA. 93:1996;13943-13948.
48. Itoh K., Chiba T., Takahashi S., Ishii T., Igarashi K., Katoh K., 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.
49. Kwak M.K., Wakabayashi N., Greelaw J.K., Yamamoto M., Kensler T.W. Antioxidants enhance mammalian proteosome expression through the Keap1-Nrf2 signaling pathway. Mol. Cell. Biol. 23:2003;8786-8794.
50. Kwong M., Kan Y.W., Chan J.Y. The CNC basic leucine zipper factor, Nrf1, is essential for cell survival in response to oxidative stress-inducing agents. J. Biol. Chem. 274:1999;37491-37498.
51. Leung L., Kwong M., Hou S., Lee C., Chan J.Y. Deficiency of the Nrf1 and Nrf2 transcription factors results in early embryonic lethality and severe oxidative stress. J. Biol. Chem. 278:2003;48021-48029.
52. Venugopal R., Jaiswal A.K. Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene. 17:1998;3145-3156.
53. Fujiwara K.T., Ashida K., Nishina H., Iba H., Miyajima N., Nishizawa M., Kawai S. Two new members of the maf oncogene family, mafK and mafF, encode nuclear b-zip proteins lacking putative trans-activator domain. Oncogene. 8:1993;2371-2380.
54. Kataoka K., Nishizawa M., Kawai S. Structure-function analysis of the maf oncogene product, a member of the β-zip family. J. Virol. 67:1993;2133-2141.
55. 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.
56. Kim M.J., Andrews N.C. Human MafG is a functional partner for p45 NF-E2 in activating globin gene expression. Blood. 89:1997;3925-3935.
57. Marini M.G., Chan K., Casula L., Kan Y.W., Cao A., Moi P. hMAF, a small human transcription factor that heterodimerizes specifically with Nrf1 and Nrf2. J. Biol. Chem. 272:1997;16490-16497.
58. Dhakshinamoorthy S., Jaiswal A.K. Small Maf (MafG and MafK) proteins negatively regulate ARE-mediated expression and antioxidant induction of the NAD(P)H: quinone oxidoreductase 1 gene. J. Biol. Chem. 275:2000;40134-40141.
59. Wilkinson J. IV, Radjendirane V., Pfeiffer G.R., Jaiswal A.K., Clapper M.L. Disruption of c-Fos leads to increased expression of NAD(P)H:quinone oxidoreductase 1 and glutathione S-transferase. Biochem. Biophys. Res. Commun. 253:1998;855-858.
60. 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.
61. Dhakshinamoorthy S., Jaiswal A.K. Functional characterization and role of INrf2 in antioxidant response element-mediated expression and antioxidant induction of NAD(P)H:quinone oxidoreductase1 gene. Oncogene. 20:2001;3906-3917.
62. Albagli O., Dhordain P., Deweindt C., Lecocq G., Leprince D. The BTB/POZ domain: a new protein-protein interaction motif common to DNA- and actin-binding proteins. Cell Growth Differ. 6:1995;1193-1198.
63. Kim I.F., Mohammadi E., Huang R.C.C. Isolation and characterization of IPP, a novel human gene coding an actin-binding, KELCH-like protein. Gene. 228:1999;73-83.
64. Sekhar K.R., Yan X.X., Freeman M.L. Nrf2 degradation by the ubiquitin proteasome pathway is inhibited by KIAA0132, the human homolog to INrf2. Oncogene. 21:2002;6829-6834.
65. 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.
66. 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.
67. 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.
68. Bloom D.A., Jaiswal A.K. Phosphorylation of Nrf2 at Ser(40) 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 response element-mediated NAD(P)H:quinone oxidoreductase-1 gene expression. J. Biol. Chem. 278:2003;44675-44682.
69. Zhang D.D., Hannink M. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol. Cell. Biol. 23:2003;8137-8151.
70. 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.
71. Li J., Lee J.M., Johnson J.A. 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. 277:2002;388-394.
72. 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.
73. Pinkus R., Weiner L.M., Daniel V. Role of oxidants and antioxidants in the induction of AP-1, NF-κB, and glutathione S-transferase gene expression. J. Biol. Chem. 271:1996;13422-13429.
74. Favreau L.V., Pickett C.B. Transcriptional regulation of the rat NAD(P)H:quinone reductase gene: identification of regulatory elements controlling basal level expression and inducible expression by planar aromatic compounds and phenolic antioxidants. J. Biol. Chem. 266:1991;4556-4561.
75. Li Y., Jaiswal A.K. Human antioxidant response element regulation of type 1 NAD(P)H:quinone oxidoreductase gene expression: effect of sulfhydryl modifying agents. Eur. J. Biochem. 226:1994;31-39.
76. Yu R., Chen C., Mo Y.Y., Hebbar V., Owuor E.D., Tann T.H., Kong A.N.T. 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.
77. Alam J., Wicks C., Stewart D., Gong P., Touchard C., Otterbein S., Choi A.M., Burow M.E., Tou J. Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells: role of p38 kinase and Nrf2 transcription factor. J. Biol. Chem. 275:2000;27694-27702.
78. Huang H.C., Nguyen T., Pickett C.B. Regulation of the antioxidant reponse element by protein kinase C-mediated phosphorylation of NF-E2-related factor 2. Proc. Natl. Acad. Sci. USA. 97:2000;12475-12480.
79. 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.
80. Lee J.M., Hanson J.M., Chu W.A., Johnson J.A. Phosphatidylinositol 3-kinase, not extracellular signal-regulated kinase, regulates activation of the antioxidant-responsive element in IMR-32 human neuroblastoma cells. J. Biol. Chem. 276:2001;20011-20016.
81. Kong A.N., Owuer E., Yu R., Hebbar V., Chen C., Hu R., Mandlekar S. Induction of xenobiotic enzymes by the MAP kinase pathway and the antioxidant or electrophile response element (ARE/EpRE). Drug Metab. Rev. 33:2001;255-271.
82. 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.
83. Kang K.W., Cho I.J., Lee C.H., Kim S.G. Essential role of phosphatidylinositol 3-kinase-dependent CCAAT/enhancer binding protein beta activation in the induction of glutathione S-transferase by oltipraz. J. Natl. Cancer Inst. 95:2003;53-66.
84. 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 Hep-G2 cells. Toxicol. Sci. 73:2003;124-134.
85. 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-C342.
86. Parekh D.B., Ziegler W., Parker P.J. Multiple pathways control protein kinase C phosphorylation. EMBO J. 19:2000;496-503.
87. Kobayashi M., Itoh K., Suzuki T., Osanai H., Nishizawa 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.
88. 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.
89. Levonen A.L., Landar A., Ramachandran A., Ceaser E.K., Dickinson D.A., Zanoni G., Morror J.D., Darley-Usmar V.M. Cellular mechanisms of redox cell signaling: the role of cysteine modification in controlling antioxidant defenses in response to electrophilic lipid oxidation products. Biochem. J. 378:2004;373-382.
90. 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.