Negative regulation of the Nrf1 transcription factor by its N-terminal domain is independent of Keap1: Nrf1, but not Nrf2, is targeted to the endoplasmic reticulum

Biochemical Journal

Volumn 399, Issue 3, 2006, Pages 373-385

  Zhang, Yiguo ^a   Crouch, Dorothy H ^a   Yamamoto, Masayuki ^b   Hayes, John D ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Antioxidant response element; Endoplasmic reticulum; Kelch like ECH associated protein 1 (Keap1); Nuclear factor erythroid 2 p45 subunit related factor 1 (Nrf1); Nuclear factor erythroid 2 p45 subunit related factor 2 (Nrf2); Oxidative stress

Indexed keywords

AMINO ACIDS; BIOLOGICAL ORGANS; CHEMICAL ACTIVATION; GENES; MUTAGENS; POLYPEPTIDES; PROTEINS;

ANTIOXIDANT RESPONSE ELEMENTS; KELCH-LIKE ECH-ASSOCIATED PROTEIN 1 (KEAP1); NUCLEAR FACTOR-ERYTHROID 2 P45 SUBUNIT-RELATED FACTOR 1 (NRF1); NUCLEAR FACTOR-ERYTHROID 2 P45 SUBUNIT-RELATED FACTOR 2 (NRF2); OXIDATIVE STRESSES;

ANTIOXIDANTS;

AMINO ACID DERIVATIVE; DNA GLYCOSYLTRANSFERASE; POLYPEPTIDE; PROTEIN KEAP1; PROTEIN NEH2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; CYTOPLASM; ENDOPLASMIC RETICULUM; FIBROBLAST; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RAT; WILD TYPE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CELL NUCLEUS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOSKELETAL PROTEINS; DNA, COMPLEMENTARY; ENDOPLASMIC RETICULUM; EPITHELIAL CELLS; FIBROBLASTS; GENES, REPORTER; HUMANS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NF-E2-RELATED FACTOR 2; NUCLEAR PROTEINS; NUCLEAR RESPIRATORY FACTOR 1; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; RECOMBINANT FUSION PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; TRANS-ACTIVATION (GENETICS);

EID: 33750543308     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20060725     Document Type: Article

References (58)

1. Hayes, J. D., Ellis, E. M., Neal, G. E., Harrison, D. J. and Manson, M. M. (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, 141-168
2. Nguyen, T., Sherratt, P. J. and Pickett, C. B. (2003) Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 43, 233-260
3. Nguyen, T., Sherratt, P. J., Nioi, P., Yang, C. S. and Pickett, C. B. (2005) Nrf2 controls constitutive and inducible expression of ARE-driven genes through a dynamic pathway involving nucleocytoplasmic shuttling by Keap1. J. Biol. Chem. 280, 32485-32492
4. Venugopal, R. and Jaiswal, A. K. (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. U.S.A. 93, 14960-14965
5. Motohashi, H., O'Connor, T., Katsuoka, F., Engel, J. O. and Yamamoto, M. (2002) Integration and diversity of the regulatory network composed of Maf and CNC families of transcription factors. Gene 294, 1-12
6. Venugopal, R. and Jaiswal, A. K. (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, 3145-3156
7. Leung, L., Kwong, M., Hou, S., Lee, C. and Chan, J. Y. (2003) Deficiency of the Nrf1 and Nrf2 transcription factors results in early embryonic lethality and severe oxidative stress. J. Biol. Chem. 278, 48021-48029
8. Chen, L., Kwong, M., Lu, R., Ginzinger, D., Lee, C., Leung, L. and Chan, J. Y. (2003) Nrf1 is critical for redox balance and survival of liver cells during devetopment. Mol. Cell. Biol. 23, 4673-4686
9. Farmer, S. C., Sun, C. W., Winnier, G. E., Hogan, B. L. and Townes, T. M. (1997) The bZIP transcriplion factor LCR-F1 is essential for mesoderm formation in mouse development. Genes Dev. 11, 786-798
10. Chan, J. Y., Kwong, M., Lu, R., Chang, J., Wang, B., Yen, T. S. and Kan, Y. W. (1998) Targeted disruption of the ubiquitous CNC-bZIP transcription factor, Nrf-1, results in anemia and embryonic lethality in mice. EMBO J. 17, 1779-1787
11. Xu, Z., Chen, L., Leung, L., Yen, T. S., Lee, C. and Chan, J. Y. (2005) Liver-specific inactivation of the Nrf1 gene in adult mouse leads to nonalcoholic steatohepatitis and hepatic neoplasia. Proc. Natl. Acad. Sci. U.S.A. 102, 4120-4125
12. Chan, K., Lu, R., Chang, J. C. and Kan, Y. W. (1996) NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc. Natl. Acad. Sci. U.S.A. 93, 13943-13948
13. Ramos-Gomez, M., Kwak, M. K., Dolan, P. M., Itoh, K., Yamamoto, M., Talalay, P. and Kensler, T. W. (2001) Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 98, 3410-3415
14. Iida, K., Itoh, K., Kumagai, Y., Oyasu, R., Hattori, K., Kawai, K., Shimazui, T., Akaza, H. and Yamamoto, M. (2004) Nrf2 is essential for the chemopreventive efficacy of oltipraz against urinary bladder carcinogenesis. Cancer Res. 64, 6424-6431
15. McMahon, M., Itoh, K., Yamamoto, M., Chanas, S. A., Henderson, C. J., McLellan, L. I., Wolf, C. R., Cavin, C. and Hayes, J. D. (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
16. Luna, L., Skammelsrud, N., Johnsen, O., Abel, K. J., Weber, B. L., Prydz, H. and Kolsto, A, B. (1995) Structural organization and mapping of the human TCF11 gene. Genomics 27, 237-244
17. Luna, L., Johnsen, O., Skartlien, A. H., Pedeutour, F., Turc-Carel, C., Prydz, H. and Kolsto, A. B. (1994) Molecular cloning of a putative novel human bZIP transcription factor on chromosome 17q22. Genomics 22, 553-562
18. Chan, J. Y., Han, X. L. and Kan, Y. W. (1993) Cloning of Nrf1, an NF-E2-related transcription factor, by genetic selection in yeast. Proc. Natl. Acad. Sci. U.S.A. 90, 11371-11375
19. Husberg, C., Murphy, P., Martin, E. and Kolsto, A. B. (2001) Two domains of the human bZIP transcription factor TCF11 are necessary for transactivation. J. Biol. Chem. 276, 17641-17652
20. McKie, J., Johnstone, K., Mattei, M. G. and Scambler, P. (1995) Cloning and mapping of murine Nfe2I1. Genomics 25, 716-719
21. Furukawa, M. and Xiong, Y. (2005) BTB protein Keap1 targets antioxidant transcription factor Nrf2 for ubiquitination by the Cullin 3-Roc1 ligase. Mol. Cell. Biol. 25, 162-171
22. Zhang, D. D., Lo, S. C., Cross, J. V., Templeton, D. J. and Hannink, M. (2004) Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol. Cell. Biol. 24, 10941-10953
23. McMahon, M., Itoh, K., Yamamoto, M. and Hayes, J. D. (2003) Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J. Biol. Chem. 278, 21592-21600
24. Cullinan, S. B., Gordan, J. D., Jin, J., Harper, J. W. and Diehl, J. A. (2004) The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol. Cell. Biol. 24, 8477-8486
25. Dinkova-Kostova, A. T., Holtzclaw, W. D. and Kensler, T. W. (2005) The role of Keap1 in cellular protective responses. Chem. Res. Toxicol. 18, 1779-1791
26. 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 ammo-terminal Neh2 domain. Genes Dev. 13, 76-86
27. McMahon, M., Thomas, N., Itoh, K., Yomamoto, M. and Hayes, J. D. (2006) Dimerisation of substrate adaptors can facilitate cullin-mediated ubiquitylation of proteins by a 'tethering' mechanism: A two-site interaction model for the Nrf2-Keap1 complex. J. Biol. Chem., 281, 24756-24768
28. Katoh, Y., Iida, K., Kang, M. I., Kobayashi, A., Mizukami, M., Tong, K. I., McMahon, M., Hayes, J. D., Itoh, K. and Yamamoto, M. (2005) Evolutionary conserved N-terminal domain of Nrf2 is essential for the Keap1-mediated degradation of the protein by proteasome. Arch. Biochem. Biophys. 433, 342-350
29. Kobayashi, A., Ohta, T. and Yamamoto, M. (2004) Unique function of the Nrf2-Keap1 pathway in the inducible expression of antioxidant and detoxifying enzymes. Methods Enzymol. 378, 273-286
30. Zhang, Y., Cho, Y. Y., Petersen, B. L., Bode, A. M., Zhu, F. and Dong, Z. (2003) Ataxia telangiectasia mutated proteins, MAPKs, and RSK2 are involved in the phosphorylation of STAT3. J. Biol. Chem. 278, 12650-12659
31. Solomin, L., Johansson, C. B., Zetterstrom, R. H., Bissonnette, R. P., Heyman, R. A., Olson, L., Lendahl, U., Frisen, J. and Perlmann, T. (1998) Retinoid-X receptor signalling in the developing spinal cord. Nature 395, 398-402
32. 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
33. Hudson, F. N. and Kavanagh, T. J. (2000) Cloning and characterization of the proximal promoter region of the mouse glutamate-L-cysteine ligase regulatory subunit gene. Biochim. Biophys. Acta 1492, 447-451
34. Mignotte, V., Wall, L., deBoer, E., Grosveld, F. and Romeo, P. H. (1989) Two tissue-specific factors bind the erythroid promoter of the human porphobilinogen deaminase gene. Nucleic Acids Res. 17, 37-54
35. Rushmore, T. H., Morton, M. R. and Pickett, C. B. (1991) The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem. 266, 11632-11639
36. Wakabayashi, N., Itoh, K., Wakabayashi, J., Motohashi, H., Noda, S., Takahashi, S., Imakado, S., Kotsuji, T., Otsuka, F., Roop, D. R., Harada, T. et al. (2003) Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat. Genet. 35, 238-245
37. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
38. Johnsen, O., Murphy, P., Prydz, H. and Kolsto, A. B. (1998) Interaction of the CNC-bZIP factor TCF11/LCR-F1/Nrf1 with MafG: binding-site selection and regulation of transcription. Nucleic Acids Res. 26, 512-520
39. Kozak, M. (2002) Pushing the limits of the scanning mechanism for initiation of translation. Gene 299, 1-34
40. Murphy, P. and Kolsto, A. (2000) Expression of the bZIP transcription factor TCF11 and its potential dimerization partners during development. Mech. Dev. 97, 141-148
41. Smith, M. J. and Koch, G. L. (1989) Multiple zones in the sequence of calreticulin (CRP55, calregulin, HACBP), a major calcium binding ER/SR protein. EMBO J. 8, 3581-3586
42. Brown, M. S. and Goldstein, J. L. (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89, 331-340
43. Haze, K., Yoshida, H., Yanagi, H., Yura, T. and Mori, K. (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell. 10, 3787-3799
44. Stirling, J. and O'Hare, P. (2006) CREB4, a transmembrane bZip transcription factor and potential new substrate for regulation and cleavage by S1P. Mol. Biol. Cell. 17, 413-426
45. Zhang, K., Shen, X., Wu, J., Sakaki, K., Saunders, T., Rutkowski, D. T., Back, S. H. and Kaufman, R. J. (2006) Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124, 587-599
46. Ye, J., Rawson, R. B., Komuro, R., Chen, X., Dave, U. P., Prywes, R., Brown, M. S. and Goldstein, J. L. (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell 6, 1355-1364
47. Cheng, D., Espenshade, P. J., Slaughter, C. A., Jaen, J. C., Brown, M. S. and Goldstein, J. L. (1999) Secreted site-1 protease cleaves peptides corresponding to luminal loop of sterol regulatory element-binding proteins. J. Biol. Chem. 274, 22805-22812
48. Toure, B. B., Munzer, J. S., Basak, A., Benjannet, S., Rochemont, J., Lazure, C., Chretien, M. and Seidah, N. G. (2000) Biosynthesis and enzymatic characterization of human SKI-1/S1P and the processing of its inhibitory prosegment. J. Biol. Chem. 275, 2349-2358
49. Martoglio, B. and Dobberstein, B. (1998) Signal sequences: more than just greasy peptides. Trends Cell. Biol. 8, 410-415
50. Husberg, C., Murphy, P., Bjorgo, E., Kalland, K. H. and Kolsto, A. B. (2003) Cellular localisation and nuclear export of the human bZIP transcription factor TCF11. Biochim. Biophys. Acta 1640, 143-151
51. McMahon, M., Thomas, N., Itoh, K., Yamamoto, M. and Hayes, J. D. (2004) Redox-regulated turnover of Nrf2 is determined by at least two separate protein domains, the redox-sensitive Neh2 degron and the redox-insensitive Neh6 degron. J. Biol. Chem. 279, 31556-31567
52. Kobayashi, M., Itoh, K., Suzuki, T., Osanai, H., Nishikawa, K., Katoh, Y., Takagi, Y. and Yamamoto, M. (2002) Identification of the interactive interface and phylogenic conservation of the Nrf2-Keap1 system. Genes Cells 7, 807-820
53. Velichkova, M. and Hasson, T. (2005) Keap1 regulates the oxidation-sensitive shuttling of Nrf2 into and out of the nucleus via a Crm1-dependent nuclear export mechanism. Mol. Cell. Biol. 25, 4501-4513
54. Motohashi, H. and Yamamoto, M. (2004) Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol. Med. 10, 549-557
55. Padmanabhan, B., Tong, K. I., Ohta, T., Nakamura, Y., Scharlock, M., Ohtsuji, M., Kang, M. I., Kobayashi, A., Yokoyama, S. and Yamamoto, M. (2006) Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Mol. Cell 21, 689-700
56. Zhang, D. D., Lo, S.-C., Cross, J. V., Templeton, D. J. and Hannink, M. (2004) Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol. Cell, Biol. 24, 10941-10953
57. Tong, K. I., Katoh, Y., Kusunoki, H., Itoh, K., Tanaka, T. and Yamamoto, M. (2006) Keap1 recruits Neh2 through binding to ETGE and DLG motifs: characterization of the two-site molecular recognition model. Mol. Cell. Biol. 26, 2887-2900
58. Wang, W. and Chan, J. Y. (2006) Nrf1 is targeted to the endoplasmic reticulum by an N-terminal transmembrane domain. Inhibition of nuclear translocation and transacting function. J. Biol. Chem. 281, 19676-19687