Bromodomain and extraterminal proteins suppress NF-E2-related factor 2-mediated antioxidant gene expression

Journal of Immunology

Volumn 192, Issue 10, 2014, Pages 4913-4920

  Michaeloudes, Charalambos ^a   Mercado, Nicolas ^a   Clarke, Colin ^a   Bhavsar, Pankaj K ^a   Adcock, Ian M ^a   Barnes, Peter J ^a   Chung, Kian Fan ^a  

^a ROYAL BROMPTON HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; HEME OXYGENASE 1; MESSENGER RNA; PROTEIN BRD2; PROTEIN BRD3; PROTEIN BRD4; PROTEIN BRDT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANTIOXIDANT ASSAY; ARTICLE; BINDING AFFINITY; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION; GENE INTERACTION; HO 1 GENE; HUMAN; HUMAN CELL; MONOCYTE; NQO1 GENE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; SMOOTH MUSCLE FIBER;

AZEPINES; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEME OXYGENASE-1; HUMANS; HYDROGEN PEROXIDE; MALE; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; NUCLEAR PROTEINS; OXIDANTS; OXIDATIVE STRESS; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRIAZOLES;

EID: 84901256398     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301984     Document Type: Article

References (42)

1. Rahman, I., and I. M. Adcock. 2006. Oxidative stress and redox regulation of lung inflammation in COPD. Eur. Respir. J. 28: 219-242.
2. Sturrock, A., T. P. Huecksteadt, K. Norman, K. Sanders, T. M. Murphy, P. Chitano, K. Wilson, J. R. Hoidal, and T. P. Kennedy. 2007. Nox4 mediates TGF-beta1-induced retinoblastoma protein phosphorylation, proliferation, and hypertrophy in human airway smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 292: L1543-L1555.
3. Ito, K., S. Lim, G. Caramori, K. F. Chung, P. J. Barnes, and I. M. Adcock. 2001. Cigarette smoking reduces histone deacetylase 2 expression, enhances cytokine expression, and inhibits glucocorticoid actions in alveolar macrophages. FASEB J. 15: 1110-1112.
4. Nakamaru, Y., C. Vuppusetty, H. Wada, J. C. Milne, M. Ito, C. Rossios, M. Elliot, J. Hogg, S. Kharitonov, H. Goto, et al. 2009. A protein deacetylase SIRT1 is a negative regulator of metalloproteinase-9. FASEB J. 23: 2810-2819.
5. Barnes, P. J. 2008. Immunology of asthma and chronic obstructive pulmonary disease. Nat. Rev. Immunol. 8: 183-192.
6. Chung, K. F. 2005. The role of airway smooth muscle in the pathogenesis of airway wall remodeling in chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc. 2: 347-354, discussion 371-372.
7. Itoh, K., T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, 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.
8. McMahon, M., K. Itoh, M. Yamamoto, and J. D. Hayes. 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.
9. Goven, D., A. Boutten, V. Leçon-Malas, J. Marchal-Sommé, N. Amara, B. Crestani, M. Fournier, G. Lesèche, P. Soler, J. Boczkowski, and M. Bonay. 2008. Altered Nrf2/Keap1-Bach1 equilibrium in pulmonary emphysema. Thorax 63: 916-924.
10. Makabe, S., Y. Takahashi, H. Watanabe, M. Murakami, T. Ohba, and H. Ito. 2010. Fluvastatin protects vascular smooth muscle cells against oxidative stress through the Nrf2-dependent antioxidant pathway. Atherosclerosis 213: 377-384.
11. Sykiotis, G. P., and D. Bohmann. 2010. Stress-activated cap'n'collar transcription factors in aging and human disease. Sci. Signal. 3: re3.
12. Yu, S., T. O. Khor, K. L. Cheung, W. Li, T. Y. Wu, Y. Huang, B. A. Foster, Y. W. Kan, and A. N. Kong. 2010. Nrf2 expression is regulated by epigenetic mechanisms in prostate cancer of TRAMP mice. PLoS One 5: e8579.
13. Malhotra, D., R. Thimmulappa, A. Navas-Acien, A. Sandford, M. Elliott, A. Singh, L. Chen, X. Zhuang, J. Hogg, P. Pare, et al. 2008. Decline in NRF2- regulated antioxidants in chronic obstructive pulmonary disease lungs due to loss of its positive regulator, DJ-1. Am. J. Respir. Crit. Care Med. 178: 592-604.
14. Suzuki, M., T. Betsuyaku, Y. Ito, K. Nagai, Y. Nasuhara, K. Kaga, S. Kondo, and M. Nishimura. 2008. Down-regulated NF-E2-related factor 2 in pulmonary macrophages of aged smokers and patients with chronic obstructive pulmonary disease. Am. J. Respir. Cell Mol. Biol. 39: 673-682.
15. Mercado, N., R. Thimmulappa, C. M. Thomas, P. S. Fenwick, K. K. Chana, L. E. Donnelly, S. Biswal, K. Ito, and P. J. Barnes. 2011. Decreased histone deacetylase 2 impairs Nrf2 activation by oxidative stress. Biochem. Biophys. Res. Commun. 406: 292-298.
16. Muller, S., P. Filippakopoulos, and S. Knapp. 2011. Bromodomains as therapeutic targets. Expert Rev. Mol. Med. 13: e29.
17. Wu, S. Y., and C. M. Chiang. 2007. The double bromodomain-containing chromatin adaptor Brd4 and transcriptional regulation. J. Biol. Chem. 282: 13141-13145.
18. Brasier, A. R., B. Tian, M. Jamaluddin, M. K. Kalita, R. P. Garofalo, and M. Lu. 2011. RelA Ser276 phosphorylation-coupled Lys310 acetylation controls transcriptional elongation of inflammatory cytokines in respiratory syncytial virus infection. J. Virol. 85: 11752-11769.
19. Yang, Z., N. He, and Q. Zhou. 2008. Brd4 recruits P-TEFb to chromosomes at late mitosis to promote G1 gene expression and cell cycle progression. Mol. Cell. Biol. 28: 967-976.
20. Zuber, J., J. Shi, E. Wang, A. R. Rappaport, H. Herrmann, E. A. Sison, D. Magoon, J. Qi, K. Blatt, M. Wunderlich, et al. 2011. RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia. Nature 478: 524-528.
21. Jang, M. K., K. Mochizuki, M. Zhou, H. S. Jeong, J. N. Brady, and K. Ozato. 2005. The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol. Cell 19: 523-534.
22. LeRoy, G., B. Rickards, and S. J. Flint. 2008. The double bromodomain proteins Brd2 and Brd3 couple histone acetylation to transcription. Mol. Cell 30: 51-60.
23. Filippakopoulos, P., J. Qi, S. Picaud, Y. Shen, W. B. Smith, O. Fedorov, E. M. Morse, T. Keates, T. T. Hickman, I. Felletar, et al. 2010. Selective inhibition of BET bromodomains. Nature 468: 1067-1073.
24. Zhang, Y., A. Chen, X. M. Yan, and G. Huang. 2012. Disordered epigenetic regulation in MLL-related leukemia. Int. J. Hematol. 96: 428-437.
25. Spiltoir, J. I., M. S. Stratton, M. A. Cavasin, K. Demos-Davies, B. G. Reid, J. Qi, J. E. Bradner, and T. A. McKinsey. 2013. BET acetyl-lysine binding proteins control pathological cardiac hypertrophy. J. Mol. Cell. Cardiol. 63: 175-179.
26. Murdolo, G., M. Piroddi, F. Luchetti, C. Tortoioli, B. Canonico, C. Zerbinati, F. Galli, and L. Iuliano. 2013. Oxidative stress and lipid peroxidation byproducts at the crossroad between adipose organ dysregulation and obesitylinked insulin resistance. Biochimie 95: 585-594.
27. Wang, F., H. Liu, W. P. Blanton, A. Belkina, N. K. Lebrasseur, and G. V. Denis. 2010. Brd2 disruption in mice causes severe obesity without type 2 diabetes. Biochem. J. 425: 71-83.
28. Dhakshinamoorthy, S., A. K. Jain, D. A. Bloom, and A. K. Jaiswal. 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.
29. Kim, S. B., R. K. Pandita, U. Eskiocak, P. Ly, A. Kaisani, R. Kumar, C. Cornelius, W. E. Wright, T. K. Pandita, and J. W. Shay. 2012. Targeting of Nrf2 induces DNA damage signaling and protects colonic epithelial cells from ionizing radiation. Proc. Natl. Acad. Sci. USA 109: E2949-E2955.
30. Denis, G. V., M. E. McComb, D. V. Faller, A. Sinha, P. B. Romesser, and C. E. Costello. 2006. Identification of transcription complexes that contain the double bromodomain protein Brd2 and chromatin remodeling machines. J. Proteome Res. 5: 502-511.
31. Thatcher, T. H., H. M. Hsiao, E. Pinner, M. Laudon, S. J. Pollock, P. J. Sime, and R. P. Phipps. 2013. Neu-164 and Neu-107, two novel antioxidant and antimyeloperoxidase compounds, inhibit acute cigarette smoke-induced lung inflammation. Am. J. Physiol. Lung Cell. Mol. Physiol. 305: L165-L174.
32. Khanduja, K. L., G. Kaushik, S. Khanduja, C. M. Pathak, J. Laldinpuii, and D. Behera. 2011. Corticosteroids affect nitric oxide generation, total free radicals production, and nitric oxide synthase activity in monocytes of asthmatic patients. Mol. Cell. Biochem. 346: 31-37.
33. Apopa, P. L., X. He, and Q. Ma. 2008. Phosphorylation of Nrf2 in the transcription activation domain by casein kinase 2 (CK2) is critical for the nuclear translocation and transcription activation function of Nrf2 in IMR-32 neuroblastoma cells. J. Biochem. Mol. Toxicol. 22: 63-76.
34. Brown, S. L., K. R. Sekhar, G. Rachakonda, S. Sasi, and M. L. Freeman. 2008. Activating transcription factor 3 is a novel repressor of the nuclear factor erythroid-derived 2-related factor 2 (Nrf2)-regulated stress pathway. Cancer Res. 68: 364-368.
35. Sun, Z., Y. E. Chin, and D. D. Zhang. 2009. Acetylation of Nrf2 by p300/CBP augments promoter-specific DNA binding of Nrf2 during the antioxidant response. Mol. Cell. Biol. 29: 2658-2672.
36. Wang, H., K. Liu, M. Geng, P. Gao, X. Wu, Y. Hai, Y. Li, Y. Li, L. Luo, J. D. Hayes, et al. 2013. RXRa inhibits the NRF2-ARE signaling pathway through a direct interaction with the Neh7 domain of NRF2. Cancer Res. 73: 3097-3108.
37. Kwak, M. K., K. Itoh, M. Yamamoto, and T. W. Kensler. 2002. Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Mol. Cell. Biol. 22: 2883-2892.
38. Yang, Z., J. H. Yik, R. Chen, N. He, M. K. Jang, K. Ozato, and Q. Zhou. 2005. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol. Cell 19: 535-545.
39. Rahman, S., M. E. Sowa, M. Ottinger, J. A. Smith, Y. Shi, J. W. Harper, and P. M. Howley. 2011. The Brd4 extraterminal domain confers transcription activation independent of pTEFb by recruiting multiple proteins, including NSD3. Mol. Cell. Biol. 31: 2641-2652.
40. Belkina, A. C., and G. V. Denis. 2012. BET domain co-regulators in obesity, inflammation and cancer. Nat. Rev. Cancer 12: 465-477.
41. Ki, S. H., I. J. Cho, D. W. Choi, and S. G. Kim. 2005. Glucocorticoid receptor (GR)-associated SMRT binding to C/EBPbeta TAD and Nrf2 Neh4/5: role of SMRT recruited to GR in GSTA2 gene repression. Mol. Cell. Biol. 25: 4150-4165.
42. Shang, E., X. Wang, D. Wen, D. A. Greenberg, and D. J. Wolgemuth. 2009. Double bromodomain-containing gene Brd2 is essential for embryonic development in mouse. Dev. Dyn. 238: 908-917.