Transcription factor Nrf2/MafK regulates rat placental glutathione S-transferase gene during hepatocarcinogenesis

Biochemical Journal

Volumn 380, Issue 2, 2004, Pages 515-521

  Ikeda, Hiromi ^a   Nishi, Shinzo ^a   Sakai, Masaharu ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Hepatoma; MafK; Nrf2 (NF E2 p45 related factor 2); Placental glutathione S transferase gene; Transcriptional control; Tumour marker

Indexed keywords

BIOCHEMISTRY; BIOLOGICAL ORGANS; CARCINOGENS; CELLS; DETOXIFICATION; GENES; LIVING SYSTEMS STUDIES; RNA;

FOOTPRINTING ANALYSIS; HETERODIMERS; LESIONS; TRANSCRIPTION;

ENZYMES;

DIMER; GLUTATHIONE TRANSFERASE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MESSENGER RNA; NF E2 P45 RELATED FACTOR 2; PLACENTA PROTEIN; PROTEIN; TRANSCRIPTION FACTOR NF E2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; DNA FOOTPRINTING; EMBRYO; ENHANCER REGION; GEL MOBILITY SHIFT ASSAY; GENE ACTIVATION; GENE ACTIVITY; GENE EXPRESSION; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; NORTHERN BLOTTING; POINT MUTATION; PRIORITY JOURNAL; REPORTER GENE; WILD TYPE;

ACETYLATION; ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CHROMATIN; DNA-BINDING PROTEINS; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION, NEOPLASTIC; GLUTATHIONE TRANSFERASE; HISTONES; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; MAFK TRANSCRIPTION FACTOR; NF-E2-RELATED FACTOR 2; NUCLEAR PROTEINS; PLACENTA; PRECANCEROUS CONDITIONS; PROMOTER REGIONS (GENETICS); PROTEINS; RATS; RATS, INBRED LEC; RATS, SPRAGUE-DAWLEY; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ANIMALIA; LATEOLABRAX JAPONICUS;

EID: 2942746263     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031948     Document Type: Article

References (41)

1. Mannervik, B. and Danielson, U. H. (1988) Glutathione transferases - structure and catalytic activity. CRC Crit. Rev. Biochem. 23, 283-337
2. Rushmore, T. H. and Pickett, C. B. (1993) Glutathione S-transferases, structure, regulation, and therapeutic implications. J. Biol. Chem. 268, 11475-11478
3. Hayes, J. D. and Pulford, D. J. (1995) 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, 445-600
4. Satoh, K., Kitahara, A., Soma, Y., Inaba, Y., Hatayama, I. and Sato, K. (1985) Purification, induction, and distribution of placental glutathione transferase: a new marker enzyme for preneoplastic cells in the rat chemical hepatocarcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 82, 3964-3968
5. Sato, K., Kitahara, A., Satoh, K., Ishikawa, T., Tatematsu, M. and Ito, N. (1984) The placental form of glutathione S-transferase as a new marker protein for preneoplasia in rat chemical hepatocarcinogenesis. Gann 75, 199-202
6. Kitahara, A., Satoh, K., Nishimura, K., Ishikawa, T., Ruike, K., Sato, K., Tsuda, H. and Ito, N. (1984) Changes in molecular forms of rat hepatic glutathione S-transferase during chemical hepatocarcinogenesis. Cancer Res. 44, 2698-2703
7. Sugioka, Y., Fujii-Kuriyama, Y., Kitagawa, T. and Muramatsu, M. (1985) Changes in polypeptide pattern of rat liver cells during chemical hepatocarcinogenesis. Cancer Res. 45, 365-378
8. Sugioka, Y., Kano, T., Okuda, A., Sakai, M., Kitagawa, T. and Muramatsu, M. (1985) Cloning and the nucleotide sequence of rat glutathione S-transferase P cDNA. Nucleic Acids Res. 13, 6049-6057
9. Sakai, M., Okuda, A. and Muramatsu, M. (1988) Multiple regulatory elements and phorbol 12-O-tetradecanoate 13-acetate responsiveness of the rat placental glutathione transferase gene. Proc. Natl. Acad. Sci. U.S.A. 85, 9456-9460
10. Sakai, M., Okuda, A., Nishi, S. and Muramatsu, M. (1990) Regulation of glutathione transferase P (GST-P) gene expression during chemical hepatocarcinogenesis. Prog. Clin. Biol. Res. 344, 123-138
11. Okuda, A., Imagawa, M., Maeda, Y., Sakai, M. and Muramatsu, M. (1989) Structural and functional analysis of an enhancer GPEI having a phorbol 12-O-tetradecanoate 13-acetate responsive element-like sequence found in the rat glutathione transferase P gene. J. Biol. Chem. 264, 16919-16926
12. Okuda, A., Imagawa, M., Sakai, M. and Muramatsu, M. (1990) Functional cooperativity between two TPA responsive elements in undifferentiated F9 embryonic stem cells. EMBO J. 9, 1131-1135
13. Morimura, S., Suzuki, T., Hochi, S., Yuki, A., Nomura, K., Kitagawa, T., Nagatsu, I., Imagawa, M. and Muramatsu, M. (1993) Trans-activation of glutathione transferase P gene during chemical hepatocarcinogenesis of the rat. Proc. Natl. Acad. Sci. U.S.A. 90, 2065-2068
14. Suzuki, T., Imagawa, M., Hirabayashi, M., Yuki, A., Hisatake, K., Nomura, K., Kitagawa, T. and Muramatsu, M. (1995) Identification of an enhancer responsible for tumor marker gene expression by means of transgenic rats. Cancer Res. 55, 2651-2655
15. Bammler, T. K., Smith, C. A. and Wolf, C. R. (1994) Isolation and characterization of two mouse Pi-class glutathione S-transferase genes. Biochem. J. 298, 385-390
16. Xu, X. and Stambrook, P. J. (1994) Two murine GSTpi genes are arranged in tandem and are differentially expressed. J. Biol. Chem. 269, 30268-30273
17. Dixon, K. H., Cowell, I. G., Xia, C. L., Pemble, S. E., Ketterer, B. and Taylor, J. B. (1989) Control of expression of the human glutathione S-transferase pi gene differs from its rat orthologue. Biochem. Biophys. Res. Commun. 163, 815-822
18. Kano, T., Sakai, M. and Muramatsu, M. (1987) Structure and expression of a human class pi glutathione S-transferase messenger RNA. Cancer Res. 47, 5626-5630
19. Hatayama, I., Satoh, K. and Sato, K. (1986) Developmental and hormonal regulation of the major form of hepatic glutathione S-transferase in male mice. Biochem. Biophys. Res. Commun. 140, 581-588
20. Hatayama, I., Nishimura, S., Narita, T. and Sato, K. (1993) Sex-dependent expression of class pi glutathione S-transferase during chemical hepatocarcinogenesis in B6C3F1 mice. Carcinogenesis 14, 537-538
21. Ikeda, H., Serria, M. S., Kakizaki, I., Hatayama, I., Satoh, K., Tsuchida, S., Muramatsu, M., Nishi, S. and Sakai, M. (2002) Activation of mouse Pi-class glutathione S-transferase gene by Nrf2 (NF-E2-related factor 2) and androgen. Biochem. J. 364, 563-570
22. Favreau, L. V. and Pickett, C. B. (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, 24468-24474
23. Kataoka, K., Noda, M. and Nishizawa, M. (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
24. Andrews, N. C., Erdjument-Bromage, H., Davidson, M. B., Tempst, P. and Orkin, S. H. (1993) Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature (London) 362, 722-728
25. Motohashi, H., O'Connor, T., Katsuoka, F., Engel, J. D. and Yamamoto, M. (2002) Integration and diversity of the regulatory network composed of Maf and CNC families of transcription factors. Gene 294, 1-12
26. Jaiswal, A. K. (2000) Regulation of genes encoding NAD(P)H:quinone oxidoreductases. Free Radical Biol. Med. 29, 254-262
27. Nioi, P., McMahon, M., Itoh, K., Yamamoto, M. and Hayes, J. D. (2003) 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, 337-348
28. Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K., Hatayama, I. 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, 313-322
29. 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
30. Wakabayashi, N., Itoh, K., Wakabayashi, J., Motohashi, H., Noda, S., Takahashi, S., Imakado, S., Kotsuji, T., Otsuka, F., Roop, D. R. et al. (2003) Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat. Genet. 35, 238-245
31. Gunning, P., Leavitt, J., Muscat, G., Ng, S. Y. and Kedes, L. (1987) A human β-actin expression vector system directs high-level accumulation of antisense transcripts. Proc. Natl. Acad. Sci. U.S.A. 84, 4831-4835
32. Chen, C. and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7, 2745-2752
33. Sambrook, J., Fritsch, E. F. and Maniatis, Y. (1989) Assay for β-galactosidase in extracts of mammalian cells. In Molecular Cloning: A Laboratory Manual, 2nd edn, pp. 16.66-16.67, Cold Spring Harbor Laboratory Press, Plainview, NY
34. Sakai, M., Serria, M. S., Ikeda, H., Yoshida, K., Imaki, J. and Nishi, S. (2001) Regulation of c-maf gene expression by Pax6 in cultured cells. Nucleic Acids Res. 29, 1228-1237
35. Solt, D. and Farber, E. (1976) A new principle for the analysis of chemical carcinogenesis. Nature (London) 263, 701-703
36. Satoh, K. and Hatayama, I. (2002) Anomalous elevation of glutathione S-transferase P-form (GST-P) in the elementary process of epigenetic initiation of chemical hepatocarcinogenesis in rats. Carcinogenesis 23, 1193-1198
37. Sakai, M., Matsushima-Hibiya, Y., Nishizawa, M. and Nishi, S. (1995) Suppression of rat glutathione transferase P expression by peroxisome proliferators: interaction between Jun and peroxisome proliferator-activated receptor α. Cancer Res. 55, 5370-5376
38. Masuda, R., Yoshida, M. C., Sasaki, M., Dempo, K. and Mori, M. (1988) High susceptibility to hepatocellular carcinoma development in LEC rats with hereditary hepatitis. Jpn. J. Cancer Res. 79, 828-835
39. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., O'Connor, T. and Yamamoto, M. (2003) Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. Genes Cells 8, 379-391
40. Diccianni, M. B., Imagawa, M. and Muramatsu, M. (1992) The dyad palindromic glutathione transferase P enhancer binds multiple factors including AP1. Nucleic Acids Res. 20, 5153-5138
41. Sambrook, J., Fritsch, E. F. and Maniatis, Y. (1989) Sequencing by the Maxam-Gilbert Method: A Laboratory Manual, 2nd edn, pp. 13.78-13.104, Cold Spring Harbor Laboratory Press, Plainview, NY