BRG1 Interacts with Nrf2 to Selectively Mediate HO-1 Induction in Response to Oxidative Stress

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 2006 Aug 23

PMID 16923960

Citations 102

Authors

Jianyong Zhang

Tsutomu Ohta

Atsushi Maruyama

Tomonori Hosoya

Keizo Nishikawa

Jonathan M Maher

Shigeki Shibahara

Ken Itoh

Masayuki Yamamoto

Affiliations

Soon will be listed here.

Abstract

NF-E2-related factor 2 (Nrf2) regulates antioxidant-responsive element-mediated induction of cytoprotective genes in response to oxidative stress. The purpose of this study was to determine the role of BRG1, a catalytic subunit of SWI2/SNF2-like chromatin-remodeling complexes, in Nrf2-mediated gene expression. Small interfering RNA knockdown of BRG1 in SW480 cells selectively decreased inducible expression of the heme oxygenase 1 (HO-1) gene after diethylmaleate treatment but did not affect other Nrf2 target genes, such as the gene encoding NADPH:quinone oxidoreductase 1 (NQO1). Chromatin immunoprecipitation analysis revealed that Nrf2 recruits BRG1 to both HO-1 and NQO1 regulatory regions. However, BRG1 knockdown selectively decreased the recruitment of RNA polymerase II to the HO-1 promoter but not to the NQO1 promoter. HO-1, but not other Nrf2-regulated genes, harbors a sequence of TG repeats capable of forming Z-DNA with BRG1 assistance. Similarly, replacement of the TG repeats with an alternative Z-DNA-forming sequence led to BRG1-mediated activation of HO-1. These results thus demonstrate that BRG1, through the facilitation of Z-DNA formation and subsequent recruitment of RNA polymerase II, is critical in Nrf2-mediated inducible expression of HO-1.

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References

Rich A, Zhang S . Timeline: Z-DNA: the long road to biological function. Nat Rev Genet. 2003; 4(7):566-72. DOI: 10.1038/nrg1115. View

Murphy D, Hardy S, Engel D . Human SWI-SNF component BRG1 represses transcription of the c-fos gene. Mol Cell Biol. 1999; 19(4):2724-33. PMC: 84065. DOI: 10.1128/MCB.19.4.2724. View

Alam J, Cook J . Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des. 2003; 9(30):2499-511. DOI: 10.2174/1381612033453730. View

Pal S, Yun R, Datta A, Lacomis L, Erdjument-Bromage H, Kumar J . mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol Cell Biol. 2003; 23(21):7475-87. PMC: 207647. DOI: 10.1128/MCB.23.21.7475-7487.2003. View

Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, Takahashi S . Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet. 2003; 35(3):238-45. DOI: 10.1038/ng1248. View

Zhang L, Fogg D, Waisman D . RNA interference-mediated silencing of the S100A10 gene attenuates plasmin generation and invasiveness of Colo 222 colorectal cancer cells. J Biol Chem. 2003; 279(3):2053-62. DOI: 10.1074/jbc.M310357200. View

Sun J, Brand M, Zenke Y, Tashiro S, Groudine M, Igarashi K . Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network. Proc Natl Acad Sci U S A. 2004; 101(6):1461-6. PMC: 341742. DOI: 10.1073/pnas.0308083100. View

Debril M, Gelman L, Fayard E, Annicotte J, Rocchi S, Auwerx J . Transcription factors and nuclear receptors interact with the SWI/SNF complex through the BAF60c subunit. J Biol Chem. 2004; 279(16):16677-86. DOI: 10.1074/jbc.M312288200. View

Kowenz-Leutz E, Leutz A . A C/EBP beta isoform recruits the SWI/SNF complex to activate myeloid genes. Mol Cell. 2000; 4(5):735-43. DOI: 10.1016/s1097-2765(00)80384-6. View

10.

Yamada N, Yamaya M, Okinaga S, Nakayama K, Sekizawa K, Shibahara S . Microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with susceptibility to emphysema. Am J Hum Genet. 2000; 66(1):187-95. PMC: 1288325. DOI: 10.1086/302729. View

11.

Herbert A, Rich A . Left-handed Z-DNA: structure and function. Genetica. 2000; 106(1-2):37-47. DOI: 10.1023/a:1003768526018. View

12.

de la Serna I, Carlson K, Hill D, Guidi C, Stephenson R, Sif S . Mammalian SWI-SNF complexes contribute to activation of the hsp70 gene. Mol Cell Biol. 2000; 20(8):2839-51. PMC: 85505. DOI: 10.1128/MCB.20.8.2839-2851.2000. View

13.

Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, Katoh Y . Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem. 2000; 275(21):16023-9. DOI: 10.1074/jbc.275.21.16023. View

14.

DiRenzo J, Shang Y, Phelan M, Sif S, Myers M, Kingston R . BRG-1 is recruited to estrogen-responsive promoters and cooperates with factors involved in histone acetylation. Mol Cell Biol. 2000; 20(20):7541-9. PMC: 86306. DOI: 10.1128/MCB.20.20.7541-7549.2000. View

15.

Kadam S, McAlpine G, Phelan M, Kingston R, Jones K, Emerson B . Functional selectivity of recombinant mammalian SWI/SNF subunits. Genes Dev. 2000; 14(19):2441-51. PMC: 316972. DOI: 10.1101/gad.828000. View

16.

Wong A, Shanahan F, Chen Y, Lian L, Ha P, Hendricks K . BRG1, a component of the SWI-SNF complex, is mutated in multiple human tumor cell lines. Cancer Res. 2000; 60(21):6171-7. View

17.

Agalioti T, Lomvardas S, Parekh B, Yie J, Maniatis T, Thanos D . Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter. Cell. 2000; 103(4):667-78. DOI: 10.1016/s0092-8674(00)00169-0. View

18.

Havas K, Flaus A, Phelan M, Kingston R, Wade P, Lilley D . Generation of superhelical torsion by ATP-dependent chromatin remodeling activities. Cell. 2001; 103(7):1133-42. DOI: 10.1016/s0092-8674(00)00215-4. View

19.

Liu R, Liu H, Chen X, Kirby M, Brown P, Zhao K . Regulation of CSF1 promoter by the SWI/SNF-like BAF complex. Cell. 2001; 106(3):309-18. DOI: 10.1016/s0092-8674(01)00446-9. View

20.

Sawado T, Igarashi K, Groudine M . Activation of beta-major globin gene transcription is associated with recruitment of NF-E2 to the beta-globin LCR and gene promoter. Proc Natl Acad Sci U S A. 2001; 98(18):10226-31. PMC: 56943. DOI: 10.1073/pnas.181344198. View