Nrf2 Neh5 domain is differentially utilized in the transactivation of cytoprotective genes

Biochemical Journal

Volumn 404, Issue 3, 2007, Pages 459-466

  Zhang, Jianyong ^a   Hosoya, Tomonori ^b   Maruyama, Atsushi ^b   Nishikawa, Keizo ^a   Maher, Jonathan M ^a   Ohta, Tsutomu ^c   Motohashi, Hozumi ^a,d   Fukamizu, Akiyoshi ^a   Shibahara, Shigeki ^e   Itoh, Ken ^b,d   Yamamoto, Masayuki ^a,d  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b HIROSAKI UNIVERSITY   (Japan)

^c NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Actin; Antioxidant responsive element (ARE); Brahma related gene 1 (BRG1); cAMP response element binding protein binding protein (CBP); Haem oxygenase 1 (HO 1); Nuclear factor erythroid 2 related factor 2 (Nrf2)

Indexed keywords

ACTINIDES; EPITAXIAL LAYERS; TRANSCRIPTION FACTORS;

ANTIOXIDANT-RESPONSIVE ELEMENT (ARE); CAMP-RESPONSE-ELEMENT-BINDING PROTEIN-BINDING PROTEIN (CBP); HAEM OXYGENASE 1 (HO-1); NUCLEAR FACTOR ERYTHROID 2-RELATED FACTOR 2 (NRF2);

GENES;

BETA ACTIN; BLASTICIDIN S; CYCLIC AMP BINDING PROTEIN; GLUTAMATE CYSTEINE LIGASE; HYGROMYCIN B; OXYGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TETRACYCLINE; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CELL CULTURE; CELL PROTECTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENZYME ACTIVITY; ENZYME ASSAY; GENE ACTIVATION; GENE CONTROL; GENE DELETION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NEH5 GENE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; TRANSACTIVATION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CREB-BINDING PROTEIN; CYTOPROTECTION; DNA HELICASES; GENES, REPORTER; HEME OXYGENASE-1; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NF-E2-RELATED FACTOR 2; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS;

EID: 34250743585     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061611     Document Type: Article

References (44)

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. 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
3. 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
4. Kobayashi, A., Kang, M. I., Okawa, H., Ohtsuji, M., Zenke, Y., Chiba, T., Igarashi, K. and Yamamoto, M. (2004) Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 24, 7130-7139
5. Itoh, K., Tong, K. I. and Yamamoto, M. (2004) Molecular mechanism activating nrf2-keap1 pathway in regulation of adaptive response to electrophiles. Free Radicals Biol. Med. 36, 1208-1213
6. Itoh, K., Igarashi, K., Hayashi, N., Nishizawa, M. and Yamamoto, M. (1995) Cloning and characterization of a novel erythroid cell-derived CNC family transcription factor heterodimerizing with the small Maf family proteins. Mol. Cell. Biol. 15, 4184-4193
7. Motohashi, H., Katsuoka, F., Engel, J. D. and Yamamoto, M. (2004) Small Maf proteins serve as transcriptional cofactors for keratinocyte differentiation in the Keap1-Nrf2 regulatory pathway. Proc. Natl. Acad. Sci. U.S.A. 101, 6379-6384
8. 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
9. Inamdar, N. M., Ahn, Y. I. and 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 for MAF and NF-E2 transcription factors. Biochem. Biophys. Res. Commun. 221, 570-576
10. Alam, J. and Cook, J. L. (2003) Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr. Pharm. Des. 9, 2499-2511
11. Primiano, T., Sutter, T. R. and Kensler, T. W. (1997) Antioxidant-inducible genes. Adv. Pharmacol. 38, 293-328
12. Thimmulappa, R. K., Mai, K. H., Srisuma, S., Kensler, T. W., Yamamoto, M. and Biswal, S. (2002) Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 62, 5196-5203
13. Hayashi, A., Suzuki, H., Itoh, K., Yamamoto, M. and Sugiyama, Y. (2003) Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance-associated protein 1 in mouse embryo fibroblasts. Biochem. Biophys. Res. Commun. 310, 824-829
14. Vollrath, V., Wielandt, A. M., Iruretagoyena, M. and Chianale, J. (2006) Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem. J. 395, 599-609
15. 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
16. Chan, K., Han, X. D. and Kan, Y. W. (2001) An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc. Natl. Acad. Sci. U.S.A. 98, 4611-4616
17. Aoki, Y., Sato, H., Nishimura, N., Takahashi, S., Itoh, K. and Yamamoto, M. (2001) Accelerated DNA adduct formation in the lung of the Nrf2 knockout mouse exposed to diesel exhaust. Toxicol. Appl. Pharmacol. 173, 154-160
18. Cho, H. Y., Jedlicka, A. E., Reddy, S. P., Kensler, T. W., Yamamoto, M., Zhang, L. Y. and Kleeberger, S. R. (2002) Role of NRF2 in protection against hyperoxic lung injury in mice. Am. J. Respir. Cell Mol. Biol. 26, 175-182
19. Lee, J. M., Chan, K., Kan, Y. W. and Johnson, J. A. (2004) Targeted disruption of Nrf2 causes regenerative immune-mediated hemolytic anemia. Proc. Natl. Acad. Sci. U.S.A. 101, 9751-9756
20. 2. Mol. Cell. Biol. 24, 36-45
21. Li, J., Stein, T. D. and Johnson, J. A. (2004) Genetic dissection of systemic autoimmune disease in Nrf2-deficient mice. Physiol. Genomics 18, 261-272
22. Dinkova-Kostova, A. T., Liby, K. T., Stephenson, K. K., Holtzclaw, W. D., Gao, X., Suh, N., Williams, C., Risingsong, R., Honda, T., Gribble, G. W. et al. (2005) Extremely potent triterpenoid inducers of the phase 2 response: correlations of protection against oxidant and inflammatory stress. Proc. Natl. Acad. Sci. U.S.A. 102, 4584-4589
23. Chen, X. L., Dodd, G., Thomas, S., Zhang, X., Wasserman, M. A., Rovin, B. H. and Kunsch, C. (2006) Activation of Nrf2/ARE pathway protects endothelial cells from oxidant injury and inhibits inflammatory gene expression. Am. J. Physiol. Heart Circ. Physiol. 290, 1862-1870
24. Yet, S. F., Layne, M. D., Liu, X., Chen, Y. H., Ith, B., Sibinga, N. E. and Perrella, M. A (2003) Absence of heme oxygenase-1 exacerbates atherosclerotic lesion formation and vascular remodeling. FASEB J. 17, 1759-1761
25. Wakabayashi, N., Dinkova-Kostova, A. T., Holtzclaw, W. D., Kang, M. I., Kobayashi, A., Yamamoto, M., Kensler, T. W. and Talalay, P. (2004) Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc. Natl. Acad. Sci. U.S.A. 101, 2040-2045
26. Kobayashi, A., Kang, M. I., Watai, Y., Tong, K. I., Shibata, T., Uchida, K. and Yamamoto, M. (2006) Oxidative and electrophilic stresses activate Nrf2 through inhibition of ubiquitination activity of Keap1. Mol. Cell. Biol. 26, 221-229
27. 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
28. Katoh, Y., Itoh, K., Yoshida, E., Miyagishi, M., Fukamizu, A. and Yamamoto, M. (2001) Two domains of Nrf2 cooperatively bind CBP, a CREB binding protein, and synergistically activate transcription. Genes Cells 6, 857-868
29. Zhang, J., Ohta, T., Maruyama, A., Hosoya, T., Nishikawa, K., Maher, J. M., Shibahara, S., Itoh, K. and Yamamoto, M. (2006) BRG1 interacts with Nrf2 to selectively mediate HO-1 induction in response to oxidative stress. Mol. Cell. Biol. 26, 7942-7952
30. Nioi, P., Nguyen, T., Sherratt, P. J. and Pickett, C. B. (2005) The carboxy-terminal Neh3 domain of Nrf2 is required for transcriptional activation. Mol. Cell. Biol. 25, 10895-10906
31. Kobayashi, A., Ito, E., Toki, T., Kogame, K., Takahashi, S., Igarashi, K., Hayashi, N. and Yamamoto, M. (1999) Molecular cloning and functional characterization of a new Cap' n' collar family transcription factor Nrf3. J. Biol. Chem. 274, 6443-6452
32. Toki, T., Itoh, J., Kitazawa, J., Arai, K., Hatakeyama, K., Akasaka, J., Igarashi, K., Nomura, N., Yokoyama, M., Yamamoto, M. and Ito, E. (1997) Human small Maf proteins form heterodimers with CNC family transcription factors and recognize the NF-E2 motif. Oncogene 14, 1901-1910
33. Fukuoka, M., Daitoku, H., Hatta, M., Matsuzaki, H., Umemura, S. and Fukamizu, A. (2003) Negative regulation of forkhead transcription factor AFX (Foxo4) by CBP-induced acetylation. Int. J. Mol. Med. 12, 503-508
34. Ankenbauer, T., Kleinschmidt, J. A., Walsh, M. J., Weiner, O. H. and Franke, W. W. (1989) Identification of a widespread nuclear actin binding protein. Nature. 342, 822-825
35. Hofmann, W. A., Stojiljkovic, L., Fuchsova, B., Vargas, G. M., Mavrommatis, E., Philimonenko, V., Kysela, K., Goodrich, J. A., Lessard, J. L., Hope, T. J. et al. (2004) Actin is part of pre-initiation complexes and is necessary for transcription by RNA polymerase II. Nat. Cell Biol. 6, 1094-1101
36. Rando, O. J., Zhao, K., Janmey, P. and Crabtree, G. R. (2002) Phosphatidylinositol-dependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex. Proc. Natl. Acad. Sci. U.S.A. 99, 2824-2829
37. Shen, X., Ranallo, R., Choi, E. and Wu, C. (2003) Involvement of actin-related proteins in ATP-dependent chromatin remodeling. Mol. Cell 12, 147-155
38. Olave, I. A., Reck-Peterson, S. L. and Crabtree, G. R. (2002) Nuclear actin and actin-related proteins in chromatin remodeling. Annu. Rev. Biochem. 71, 755-781
39. Miralles, F. and Visa, N. (2006) Actin in transcription and transcription regulation. Curr. Opin. Cell Biol. 18, 261-266
40. Kang, K. W., Lee, S. J., Park, J. W. and Kim, S. G. (2002) Phosphatidylinositol 3-kinase regulates nuclear translocation of NF-E2-related factor 2 through actin rearrangement in response to oxidative stress. Mol. Pharmacol. 62, 1001-1010
41. Zhao, K., Wang, W., Rando, O. J., Xue, Y., Swiderek, K., Kuo, A. and Crabtree, G. R. (1998) Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95, 625-636
42. Rosonina, E., Bakowski, M. A., McCracken, S. and Blencowe, B. J. (2003) Transcriptional activators control splicing and 3′-end cleavage levels. J. Biol. Chem. 278, 43034-43040
43. Rosonina, E., Ip, J. Y., Calarco, J. A., Bakowski, M. A., Emili, A., McCracken, S., Tucker, P., Ingles, C. J. and Blencowe; B. J. (2005) Role for PSF in mediating transcriptional activator-dependent stimulation of pre-mRNA processing in vivo. Mol. Cell. Biol. 25, 6734-6746
44. Lai, M. C., Teh, B. H. and Tarn, W. Y. (1999) A human papillomavirus E2 transcriptional activator. The interactions with cellular splicing factors and potential function in pre-mRNA processing. J. Biol. Chem. 274, 11832-11841