Enhanced Expression of the Transcription Factor Nrf2 by Cancer Chemopreventive Agents: Role of Antioxidant Response Element-Like Sequences in the nrf2 Promoter

REFERENCES

• Alam, J., D. Stewart, C. Touchard, S. Boinapally, A. M. K. Choi, and J. L. Cook. 1999. Nrf2, a cap'n'collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274: 26071–26078.
   PubMed Web of Science ®Google Scholar
• Angel, P., K. Hattori, T. Smeal, and M. Karin. 1988. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell 55: 875–885.
   PubMed Web of Science ®Google Scholar
• Boyd, K., J. Wells, J. Gutman, S. M. Bartley, and P. J. Farnham. 1998. c-Myc target gene specificity is determined by a post-DNA-binding mechanism. Proc. Natl. Acad. Sci. USA 95: 13887–13892.
   PubMed Web of Science ®Google Scholar
• Chan, K., and Y. W. Kan. 1999. Nrf2 is essential for protection against acute pulmonary injury in mice. Proc. Natl. Acad. Sci. USA 96: 12731–12736.
   PubMed Web of Science ®Google Scholar
• Chan, K., R. Lu, J. C. Chang, and Y. W. Kan. 1996. 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: 13943–13948.
   PubMed Web of Science ®Google Scholar
• Cho, H.-Y., A. E. Jedlicka, S. P. Reddy, T. W. Kensler, M. Yamamoto, L. Y. Zhang, and S. R. Kleeberger. 2002. Role of Nrf2 in protection against hyperoxic lung injury in mice. Am. J. Respir. Cell Mol. 26: 175–182.
   Google Scholar
• Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156–159.
   PubMed Web of Science ®Google Scholar
• Dhakshinamoorthy, S., and A. K. Jaiswal. 2000. Small Maf (MafG and MafK) proteins negatively regulate antioxidant response element-mediated expression and antioxidant induction of the NAD(P)H:quinone oxidoreductase. J. Biol. Chem. 275: 40134–40141.
   PubMed Web of Science ®Google Scholar
• Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11: 1475–1489.
   PubMed Web of Science ®Google Scholar
• Egner, P. A., T. W. Kensler, T. Prestera, P. Talalay, A. H. Libby, H. H. Joyner, and T. J. Curphey. 1994. Regulation of phase 2 enzyme induction by oltipraz and other dithiolethiones. Carcinogenesis 15: 177–181.
   PubMed Web of Science ®Google Scholar
• Enomoto, A., K. Itoh, E. Nagayoshi, J. Haruta, T. Kimura, T. O'Conner, T. Harada, and M. Yamamoto. 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.
   PubMed Web of Science ®Google Scholar
• Favreau, L. V., and C. B. Pickett. 1995. The rat quinone reductase antioxidant response element. J. Biol. Chem. 270: 24468–24474.
   PubMed Web of Science ®Google Scholar
• Hale, T. K., C. Myers, R. Maitra, T. Kolzau, M. Nishizawa, and A. W. Braithwaite. 2000. Maf transcriptionally activates the mouse p53 promoter and causes a p53-dependent cell death. J. Biol. Chem. 24: 17991–17999.
   Google Scholar
• Hayes, J. D., and L. I. McLellan. 1999. Glutathione and glutathione-dependent enzymes represent a coordinately regulated defence against oxidative stress. Free Radic. Res. 31: 273–300.
   PubMed Web of Science ®Google Scholar
• He, C. H., P. Gong, B. Hu, D. Stewart, M. E. Choi, A. M. Choi, and J. Alam. 2001. Identification of activation transcription 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation. J. Biol. Chem. 276: 20858–20865.
   PubMed Web of Science ®Google Scholar
• Huang, H.-C., T. Nguyen, and C. Pickett. 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: 1–6.
   PubMedGoogle Scholar
• Igarashi, K., K. Itoh, H. Motohashi, N. Hayashi, Y. Matuzaki, H. Nakauchi, M. Nishizawa, and M. Yamamoto. 1995. Activity and expression of murine small Maf family protein Maf K. J. Biol. Chem. 270: 7615–7624.
   PubMedGoogle Scholar
• Ishii, T., K. Itoh, S. Takahashi, H. Sato, T. Yanagawa, Y. Katoh, S. Bannai, and M. Yamamoto. 2000. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-induced genes in macrophages. J. Biol. Chem. 275: 16023–16029.
   PubMed Web of Science ®Google Scholar
• Itoh, K., T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Iatayama, M. Yamamoto, and Y. Nabeshima. 1997. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme gene through antioxidant response elements. Biochem. Biophys. Res. Commun. 236: 313–322.
   PubMed Web of Science ®Google Scholar
• Itoh, K., N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J. D. Engel, and M. Yamamoto. 1999. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13: 76–86.
   PubMed Web of Science ®Google Scholar
• Jeyapaul, J., and A. K. Jaiswal. 2000. Nrf2 and c-Jun regulation of antioxidant response element (ARE)-mediated expression and induction of gamma-glutamylcysteine synthetase heavy subunit gene. Biochem. Pharmacol. 59: 1433–1439.
   PubMed Web of Science ®Google Scholar
• Karin, M. 1999. The beginning of the end: IκB kinase (IKK) and NF-κB activation. J. Biol. Chem. 274: 27339–27342.
   PubMed Web of Science ®Google Scholar
• Kataoka, K., M. Noda, and M. Nishizawa. 1994. Maf nuclear oncoprotein recognizes sequences related to an AP-1 site and forms heterodimers with both Fos and Jun. Mol. Cell. Biol. 14: 700–712.
   PubMed Web of Science ®Google Scholar
• Kensler, T. W., J. D. Groopman, T. R. Sutter, T. J. Curphey, and B. D. Roebuck. 1999. Development of cancer chemopreventive agents: oltipraz as a paradigm. Chem. Res. Toxicol. 12: 113–126.
   PubMed Web of Science ®Google Scholar
• Kim, Y.-C., H. Masutani, Y. Yamaguchi, K. Itoh, M. Yamamoto, and J. Yodoi. 2001. Hemin-induced activation of the thioredoxin gene by Nrf2. J. Biol. Chem. 276: 18399–18406.
   PubMed Web of Science ®Google Scholar
• Kwak, M.-K., P. A. Egner, P. M. Dolan, M. Ramos-Gomez, J. D. Groopman, K. Itoh, M. Yamamoto, and T. W. Kensler. 2001. Role of phase 2 enzyme induction in chemoprotection by dithiolethiones. Mutat. Res. 480: 305–315.
   PubMed Web of Science ®Google Scholar
• Kwak, M.-K., K. Itoh, M. Yamamoto, T. R. Sutter, and T. W. Kensler. 2001. Role of transcription factor Nrf2 in the induction of hepatic phase 2 and antioxidative enzymes in vivo by the cancer chemoprotective agent, 3H-1,2-dithiole-3-thione. Mol. Med. 7: 135–145.
   PubMed Web of Science ®Google Scholar
• Li, Y., and A. K. Jaiswal. 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: 15097–15104.
   PubMed Web of Science ®Google Scholar
• Liptay, S., R. M. Schmid, E. G. Nabel, and G. J. Nabel. 1994. Transcriptional regulation of NF-κB2: evidence for κB-mediated positive and negative autoregulation. Mol. Cell. Biol. 14: 7695–7703.
   PubMed Web of Science ®Google Scholar
• MacMahon, M., K. Itoh, M. Yamamoto, S. A. Chanas, C. J. Henderson, L. I. McLellan, C. R. Wolf, C. Cavin, and J. D. Hayes. 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: 3299–3307.
   PubMedGoogle Scholar
• Moinova, H. R., and R. T. Mulcahy. 1998. An electrophile responsive element (EpRE) regulation of 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: 14683–14689.
   PubMed Web of Science ®Google Scholar
• Mulchay, R. T., M. A. Wartman, H. H. Bailey, and J. J. Gipp. 1997. Constitutive and β-naphthoflavone-induced expression of the human γ-glutamylcycteine synthetase heavy subunit gene is regulated by a distal antioxidant response element/TRE sequence. J. Biol. Chem. 272: 7445–7454.
   PubMedGoogle Scholar
• Nishimura, S., S. Takahashi, T. Kuroha, N. Suwabe, T. Nagasawa, C. Trainor, and M. Yamamoto. 2000. A GATA box in the GATA-1 gene hematopoietic enhancer is a critical element in the network of GATA factors and sites that regulate this gene. Mol. Cell. Biol. 20: 713–723.
   PubMedGoogle Scholar
• Ramos-Gomez, M., M.-K. Kwak, P. M. Dolan, K. Itoh, M. Yamamoto, P. Talalay, and T. W. Kensler. 2001. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzymes inducers is lost in nrf2 transcription factor-deficient mice. Proc. Natl. Acad. Sci. USA 98: 3410–3415.
   PubMed Web of Science ®Google Scholar
• Rushmore, T. H., R. G. King, K. E. Paulson, and C. B. Pickett. 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: 3826–3830.
   PubMed Web of Science ®Google Scholar
• Ryseck, R.-P., and R. Bravo. 1991. c-JUN, JUN B, and JUN D differ in their binding affinities to AP-1 and CRE consensus sequences: effect of FOS proteins. Oncogene 6: 533–542.
   PubMedGoogle Scholar
• Shapiro, T. A., J. W. Fahey, K. L. Wade, K. K. Stephenson, and P. Talalay. 2001. Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: metabolism and excretion in humans. Cancer Epidemiol. Biomarkers Prev. 10: 501–508.
   PubMed Web of Science ®Google Scholar
• Venugopal, R., and A. K. Jaiswal. 1999. Coordinated induction of the c-jun gene with genes encoding quinine oxidoreductases in response to xenobiotics and antioxidants. Biochem. Pharmacol. 58: 597–603.
   PubMedGoogle Scholar
• Venugopal, R., and A. K. Jaiswal. 1996. 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: 14960–14965.
   PubMed Web of Science ®Google Scholar
• Verma, I. M., and P. Sassone-Corsi. 1987. Proto-oncogene fos: complex but versatile regulation. Cell 51: 513–514.
   PubMed Web of Science ®Google Scholar
• Wang, J.-S., X. Shen, X. He, Y.-R. Zhu, B.-C. Zhang, J.-B. Wang, G.-S. Qian, S.-Y. Kuang, A. Zarba, P. A. Egner, L. J. Jacobson, A. Muñoz, K. J. Helzlsouer, J. D. Groopman, and T. W. Kensler. 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.
   PubMed Web of Science ®Google Scholar
• Wasserman, W. W., and W. E. Fahl. 1997. Functional antioxidant response element. Proc. Natl. Acad. Sci. USA 94: 5361–5366.
   PubMed Web of Science ®Google Scholar
• Wild, A. C., H. R. Moinova, and R. T. Mulcahy. 1999. Regulation of γ-glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. J. Biol. Chem. 274: 33627–33636.
   PubMed Web of Science ®Google Scholar
• Yamamoto, M., S. Takahashi, K. Onodera, Y. Muraosa, and J. D. Engel. 1997. Upstream and downstream of erythroid transcription factor GATA-1. Genes Cells 2: 107–115.
   PubMed Web of Science ®Google Scholar
• Yu, R., C. Chen, Y.-Y. Mo, V. Hebbar, E. D. Owuor, T.-H. Tan, and A.-N. T. Kong. 2000. Activation of mitogen-activated protein kinase pathways induces antioxidant response element-mediated gene expression via a Nrf2-dependent mechanism. J. Biol. Chem. 275: 39907–39913.
   PubMed Web of Science ®Google Scholar
• Yuspa, S. H., D. Morgan, U. Lichti, E. F. Spangler, D. Michael, A. Kilkenny, and H. Hennings. 1986. Cultivation and characterization of cells derived from mouse skin papillomas induced by an initiation-promotion protocol. Carcinogenesis 7: 949–958.
   PubMedGoogle Scholar