Novel insights into the regulation of antioxidant-response-element-mediated gene expression by electrophiles: Induction of the transcriptional repressor BACH1 by Nrf2

Biochemical Journal

Volumn 440, Issue 2, 2011, Pages 167-174

  Jyrkkänen, Henna Kaisa ^a   Kuosmanen, Suvi ^a   Heinäniemi, Merja ^b   Laitinen, Heidi ^a   Kansanen, Emilia ^a   Mella Aho, Eero ^a   Leinonen, Hanna ^a   Ylä Herttuala, Seppo ^a   Levonen, Anna Liisa ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITY OF LUXEMBOURG   (Luxembourg)

Author keywords

Antioxidant response element (ARE); BTB and CNC homology 1 (BACH1); Gene expression; Gene regulation; Nuclear factor erythroid 2 related factor 2 (Nrf2); Transcription factor

Indexed keywords

ELECTROPHILE; LEUCINE; TRANSCRIPTION FACTOR MAF; TRANSCRIPTION FACTOR NRF2;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CONTROLLED STUDY; DETOXIFICATION; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; REGULATORY MECHANISM;

BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; HEK293 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; NF-E2-RELATED FACTOR 2; NITRO COMPOUNDS; OLEIC ACIDS; RESPONSE ELEMENTS; THIOCYANATES;

EID: 81155126130     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110526     Document Type: Article

References (46)

1. 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 (Pubitemid 37372641)
2. 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 (Pubitemid 21906996)
3. Wasserman, W. W. and Fahl, W. E. (1997) Functional antioxidant responsive elements. Proc. Natl. Acad. Sci. U.S.A. 94, 5361-5366 (Pubitemid 27214788)
4. Erickson, A. M., Nevarea, Z., Gipp, J. J. and Mulcahy, R. T. (2002) Identification of a variant antioxidant response element in the promoter of the human glutamate-cysteine ligase modifier subunit gene: revision of the ARE consensus sequence. J. Biol. Chem. 277, 30730-30737 (Pubitemid 34970769)
5. 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 (Pubitemid 37094093)
6. Wang, X., Tomso, D. J., Chorley, B. N., Cho, H. Y., Cheung, V. G., Kleeberger, S. R. and Bell, D. A. (2007) Identification of polymorphic antioxidant response elements in the human genome. Hum. Mol. Genet. 16, 1188-1200 (Pubitemid 47062715)
7. Kensler, T. W., Wakabayashi, N. and Biswal, S. (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47, 89-116
8. Itoh, K., Tong, K. I. and Yamamoto, M. (2004) Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radical Biol. Med. 36, 1208-1213 (Pubitemid 38526314)
9. Zhang, D. D. (2006) Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab. Rev. 38, 769-789
10. Igarashi, K. and Sun, J. (2006) The heme-Bach1 pathway in the regulation of oxidative stress response and erythroid differentiation. Antioxid. Redox Signaling 8, 107-118 (Pubitemid 43324536)
11. Igarashi, K., Hoshino, H., Muto, A., Suwabe, N., Nishikawa, S., Nakauchi, H. and Yamamoto, M. (1998) Multivalent DNA binding complex generated by small maf and Bach1 as a possible biochemical basis for β-globin locus control region complex. J. Biol. Chem. 273, 11783-11790 (Pubitemid 28272083)
12. Ogawa, K., Sun, J., Taketani, S., Nakajima, O., Nishitani, C., Sassa, S., Hayashi, N., Yamamoto, M., Shibahara, S., Fujita, H. and Igarashi, K. (2001) Heme mediates derepression of maf recognition element through direct binding to transcription repressor Bach1. EMBO J. 20, 2835-2843 (Pubitemid 32938566)
13. Suzuki, H., Tashiro, S., Hira, S., Sun, J., Yamazaki, C., Zenke, Y., Ikeda-Saito, M., Yoshida, M. and Igarashi, K. (2004) Heme regulates gene expression by triggering Crm1-dependent nuclear export of Bach1. EMBO J. 23, 2544-2553 (Pubitemid 38988226)
14. Ishikawa, M., Numazawa, S. and Yoshida, T. (2005) Redox regulation of the transcriptional repressor Bach1. Free Radical Biol. Med. 38, 1344-1352 (Pubitemid 40602836)
15. Sun, J., Hoshino, H., Takaku, K., Nakajima, O., Muto, A., Suzuki, H., Tashiro, S., Takahashi, S., Shibahara, S., Alam, J. et al. (2002) Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J. 21, 5216-5224
16. Reichard, J. F., Motz, G. T. and Puga, A. (2007) Heme oxygenase-1 induction by NRF2 requires inactivation of the transcriptional repressor BACH1. Nucleic Acids Res. 35, 7074-7086
17. Kanezaki, R., Toki, T., Yokoyama, M., Yomogida, K., Sugiyama, K., Yamamoto, M., Igarashi, K. and Ito, E. (2001) Transcription factor BACH1 is recruited to the nucleus by its novel alternative spliced isoform. J. Biol. Chem. 276, 7278-7284
18. Sun, J., Muto, A., Hoshino, H., Kobayashi, A., Nishimura, S., Yamamoto, M., Hayashi, N., Ito, E. and Igarashi, K. (2001) The promoter of mouse transcription repressor Bach1 is regulated by Sp1 and trans-activated by Bach1. J. Biochem. (Tokyo) 130, 385-392 (Pubitemid 32845692)
19. Kaspar, J. W. and Jaiswal, A. K. (2010) Antioxidant-induced phosphorylation of tyrosine 486 leads to rapid nuclear export of Bach1 that allows Nrf2 to bind to the antioxidant response element and activate defensive gene expression. J. Biol. Chem. 285, 153-162
20. Kitamuro, T., Takahashi, K., Ogawa, K., Udono-Fujimori, R., Takeda, K., Furuyama, K., Nakayama, M., Sun, J., Fujita, H., Hida, W. et al. (2003) Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells. J. Biol. Chem. 278, 9125-9133 (Pubitemid 36800393)
21. Kansanen, E., Jyrkkanen, H. K., Volger, O. L., Leinonen, H., Kivela, A. M., Hakkinen, S. K., Woodcock, S. R., Schopfer, F. J., Horrevoets, A. J., Ylä-Herttuala, S. et al. (2009) Nrf2-dependent and -independent responses to nitro-fatty acids in human endothelial cells: identification of heat shock response as the major pathway activated by nitro-oleic acid. J. Biol. Chem. 284, 33233-33241
22. 2 on glutathione induction and apoptosis in human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 21, 1846-1851
23. Levonen, A. L., Inkala, M., Heikura, T., Jauhiainen, S., Jyrkkanen, H. K., Kansanen, E., Maatta, K., Romppanen, E., Turunen, P., Rutanen, J. and Ylä-Herttuala, S. (2007) Nrf2 gene transfer induces antioxidant enzymes and suppresses smooth muscle cell growth in vitro and reduces oxidative stress in rabbit aorta in vivo. Arterioscler. Thromb. Vasc. Biol. 27, 741-747 (Pubitemid 46606701)
24. Woodcock, S. R., Marwitz, A. J., Bruno, P. and Branchaud, B. P. (2006) Synthesis of nitrolipids. All four possible diastereomers of nitrooleic acids: (E)- and (Z) -, 9- and 10-nitro-octadec-9-enoic acids. Org. Lett. 8, 3931-3934 (Pubitemid 44432823)
25. 3-mediated negative regulation of the human CYP27B1 gene. Nucleic Acids Res. 35, 2734-2747
26. Jyrkkanen, H. K., Kansanen, E., Inkala, M., Kivela, A. M., Hurttila, H., Heinonen, S. E., Goldsteins, G., Jauhiainen, S., Tiainen, S., Makkonen, H. et al. (2008) Nrf2 regulates antioxidant gene expression evoked by oxidized phospholipids in endothelial cells and murine arteries in vivo. Circ. Res. 103, e1-e9
27. Levonen, A. L., Landar, A., Ramachandran, A., Ceaser, E. K., Dickinson, D. A., Zanoni, G., Morrow, J. D. and Darley-Usmar, V. M. (2004) Cellular mechanisms of redox cell signalling: role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochem. J. 378, 373-382 (Pubitemid 38367228)
28. Wild, A. C., Moinova, H. R. and Mulcahy, R. T. (1999) Regulation of γ-glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2. J. Biol. Chem. 274, 33627-33636 (Pubitemid 129511675)
29. Kansanen, E., Bonacci, G., Schopfer, F. J., Kuosmanen, S. M., Tong, K. I., Leinonen, H., Woodcock, S. R., Yamamoto, M., Carlberg, C., Ylä-Herttuala, S. et al. (2011) Electrophilic nitro-fatty acids activate NRF2 by a KEAP1 cysteine 151-independent mechanism. J. Biol. Chem. 286, 14019-14027
30. Ohtsuji, M., Katsuoka, F., Kobayashi, A., Aburatani, H., Hayes, J. D. and Yamamoto, M. (2008) Nrf1 and Nrf2 play distinct roles in activation of antioxidant response element-dependent genes. J. Biol. Chem. 283, 33554-33562
31. Biswas, M. and Chan, J. Y. (2010) Role of Nrf1 in antioxidant response element-mediated gene expression and beyond. Toxicol. Appl. Pharmacol. 244, 16-20
32. Zenke-Kawasaki, Y., Dohi, Y., Katoh, Y., Ikura, T., Ikura, M., Asahara, T., Tokunaga, F., Iwai, K. and Igarashi, K. (2007) Heme induces ubiquitination and degradation of the transcription factor Bach1. Mol. Cell. Biol. 27, 6962-6971 (Pubitemid 47483643)
33. Hou, W., Tian, Q., Zheng, J. and Bonkovsky, H. L. (2010) MicroRNA-196 represses Bach1 protein and hepatitis C virus gene expression in human hepatoma cells expressing hepatitis C viral proteins. Hepatology 51, 1494-1504
34. Gottwein, E., Mukherjee, N., Sachse, C., Frenzel, C., Majoros, W. H., Chi, J. T., Braich, R., Manoharan, M., Soutschek, J., Ohler, U. and Cullen, B. R. (2007) A viral microRNA functions as an orthologue of cellular miR-155. Nature 450, 1096-1099 (Pubitemid 350273603)
35. Shan, Y., Zheng, J., Lambrecht, R. W. and Bonkovsky, H. L. (2007) Reciprocal effects of micro-RNA-122 on expression of heme oxygenase-1 and hepatitis C virus genes in human hepatocytes. Gastroenterology 133, 1166-1174 (Pubitemid 47494462)
36. Farnham, P. J. (2009) Insights from genomic profiling of transcription factors. Nat. Rev. Genet. 10, 605-616
37. Birney, E., Stamatoyannopoulos, J. A., Dutta, A., Guigó, R., Gingeras, T. R., Margulies, E. H., Weng, Z., Snyder, M., Dermitzakis, E. T., Thurman, R. E. et al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447, 799-816
38. l and gss expression in mouse fibroblasts. J. Biol. Chem. 274, 37491-37498
39. 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 (Pubitemid 28119131)
40. 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 (Pubitemid 27373291)
41. Ryter, S. W., Alam, J. and Choi, A. M. (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86, 583-650
42. Reichard, J. F., Sartor, M. A. and Puga, A. (2008) BACH1 is a specific repressor of HMOX1 that is inactivated by arsenite. J. Biol. Chem. 283, 22363-22370
43. Dhakshinamoorthy, S., Jain, A. K., Bloom, D. A. and Jaiswal, A. K. (2005) Bach1 competes with Nrf2 leading to negative regulation of the antioxidant response element (ARE)-mediated NAD(P)H:quinone oxidoreductase 1 gene expression and induction in response to antioxidants. J. Biol. Chem. 280, 16891-16900 (Pubitemid 41389148)
44. Hintze, K. J., Katoh, Y., Igarashi, K. and Theil, E. C. (2007) Bach1 repression of ferritin and thioredoxin reductase1 is heme-sensitive in cells and in vitro and coordinates expression with heme oxygenase1, β-globin, and NADP(H) quinone (oxido) reductase1. J. Biol. Chem. 282, 34365-34371 (Pubitemid 350159431)
45. MacLeod, A. K., McMahon, M., Plummer, S. M., Higgins, L. G., Penning, T. M., Igarashi, K. and Hayes, J. D. (2009) Characterization of the cancer chemopreventive NRF2-dependent gene battery in human keratinocytes: demonstration that the KEAP1-NRF2 pathway, and not the BACH1-NRF2 pathway, controls cytoprotection against electrophiles as well as redox-cycling compounds. Carcinogenesis 30, 1571-1580
46. Dohi, Y., Alam, J., Yoshizumi, M., Sun, J. and Igarashi, K. (2006) Heme oxygenase-1 gene enhancer manifests silencing activity in a chromatin environment prior to oxidative stress. Antioxid. Redox Signaling 8, 60-67 (Pubitemid 43324531)