Unique cistrome defined as CsMBE is strictly required for Nrf2-sMaf heterodimer function in cytoprotection

Free Radical Biology and Medicine

Volumn 91, Issue , 2016, Pages 45-57

  Otsuki, Akihito ^a   Suzuki, Mikiko ^a   Katsuoka, Fumiki ^b   Tsuchida, Kouhei ^a   Suda, Hiromi ^a   Morita, Masanobu ^a   Shimizu, Ritsuko ^a   Yamamoto, Masayuki ^a,b  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

CsMBE; Maf; MARE; Nrf2

Indexed keywords

ALANINE; CNC SMAF BINDING ELEMENT; HOMODIMER; NUCLEOTIDE; PARACETAMOL; SMALL MAF PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MAF; TRANSCRIPTION FACTOR NRF2; TYROSINE; UNCLASSIFIED DRUG; ANALGESIC AGENT; MAFG PROTEIN, MOUSE; MENADIONE; NFE2L2 PROTEIN, MOUSE; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR MAFG;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CELL PROTECTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING; DNA SEQUENCE; GENE MUTATION; GENE TARGETING; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; RNA SEQUENCE; STIMULATION; STRESS; SUBSTITUTION REACTION; AMINO ACID SEQUENCE; ANIMAL; CELL CULTURE; CELL SURVIVAL; CONSERVED SEQUENCE; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; FEMALE; MALE; METABOLISM; NUCLEOTIDE SEQUENCE; PERITONEUM MACROPHAGE; PHYSIOLOGY; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE;

ACETAMINOPHEN; AMINO ACID SEQUENCE; ANALGESICS, NON-NARCOTIC; ANIMALS; BASE SEQUENCE; BINDING SITES; CELL SURVIVAL; CELLS, CULTURED; CONSERVED SEQUENCE; CYTOPROTECTION; FEMALE; MACROPHAGES, PERITONEAL; MAFG TRANSCRIPTION FACTOR; MALE; MICE; MICE, TRANSGENIC; NF-E2-RELATED FACTOR 2; REPRESSOR PROTEINS; RESPONSE ELEMENTS; TRANSCRIPTIONAL ACTIVATION; VITAMIN K 3;

EID: 84954167103     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.12.005     Document Type: Article

References (60)

1. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, M. Yamamoto, and Y. Nabeshima An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236 1997 313 322
2. K. Taguchi, H. Motohashi, and M. Yamamoto Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution Genes Cells 16 2011 123 140
3. H. Motohashi, F. Katsuoka, J.D. Engel, and M. Yamamoto Small Maf proteins serve as transcriptional cofactors for keratinocyte differentiation in the Keap1-Nrf2 regulatory pathway Proc. Natl. Acad. Sci. U.S.A. 101 2004 6379 6384
4. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J.D. Engel, and M. Yamamoto Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev. 13 1999 76 86
5. A. Kobayashi, M.I. Kang, H. Okawa, M. Ohtsuji, Y. Zenke, T. Chiba, K. Igarashi, and M. Yamamoto Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2 Mol. Cell. Biol. 24 2004 7130 7139
6. K. Igarashi, K. Kataoka, K. Itoh, N. Hayashi, M. Nishizawa, and M. Yamamoto Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Maf proteins Nature 367 1994 568 572
7. K. Itoh, K. Igarashi, N. Hayashi, M. Nishizawa, and M. Yamamoto Cloning and characterization of a novel erythroid cell-derived CNC family transcription factor heterodimerizing with the small Maf family proteins Mol. Cell. Biol. 15 1995 4184 4193
8. O. Johnsen, N. Skammelsrud, L. Luna, M. Nishizawa, H. Prydz, and A.B. Kolstø Small Maf proteins interact with the human transcription factor TCF11/Nrf1/LCR-F1 Nucleic Acids Res. 24 1996 4289 4297
9. T. Oyake, K. Itoh, H. Motohashi, N. Hayashi, H. Hoshino, M. Nishizawa, M. Yamamoto, and K. Igarashi Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site Mol. Cell. Biol. 16 1996 6083 6095
10. T.H. Rushmore, M.R. Morton, and C.B. Pickett The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity J. Biol. Chem. 266 1991 11632 11639
11. Y. Hirotsu, F. Katsuoka, R. Funayama, T. Nagashima, Y. Nishida, K. Nakayama, J.D. Engel, and M. Yamamoto Nrf2-MafG heterodimers contribute globally to antioxidant and metabolic networks Nucleic Acids Res. 40 2012 10228 10239
12. R.S. Friling, A. Bensimon, Y. Tichauer, and V. Daniel Xenobiotic-inducible expression of murine glutathione S-transferase Ya subunit gene is controlled by an electrophile-responsive element Proc. Natl. Acad. Sci. U.S.A. 87 1990 6258 6262
13. V. Mignotte, J.F. Eleouet, N. Raich, and P.H. Romeo Cis- and trans-acting elements involved in the regulation of the erythroid promoter of the human porphobilinogen deaminase gene Proc. Natl. Acad. Sci. U.S.A. 86 1989 6548 6552
14. K. Kataoka, M. Noda, and M. Nishizawa Maf nuclear oncoprotein recognizes sequences related to an AP-1 site and forms heterodimers with both Fos and Jun Mol. Cell. Biol. 14 1994 700 712
15. K. Kataoka, K.T. Fujiwara, M. Noda, and M. Nishizawa MafB, a new Maf family transcription activator that can associate with Maf and Fos but not with Jun Mol. Cell. Biol. 14 1994 7581 7591
16. T.K. Kerppola, and T. Curran A conserved region adjacent to the basic domain is required for recognition of an extended DNA binding site by Maf/Nrl family proteins Oncogene 9 1994 3149 3158
17. T. Yamamoto, M. Kyo, T. Kamiya, T. Tanaka, J.D. Engel, H. Motohashi, and M. Yamamoto Predictive base substitution rules that determine the binding and transcriptional specificity of Maf recognition elements Genes Cells 11 2006 575 591
18. H. Kurokawa, H. Motohashi, S. Sueno, M. Kimura, H. Takagawa, Y. Kanno, M. Yamamoto, and T. Tanaka Structural basis of alternative DNA recognition by Maf transcription factors Mol. Cell. Biol. 29 2009 6232 6244
19. H. Kusunoki, H. Motohashi, F. Katsuoka, A. Morohashi, M. Yamamoto, and T. Tanaka Solution structure of the DNA-binding domain of MafG Nat. Struct. Biol. 9 2002 252 256
20. C.e.S. Consortium Genome sequence of the nematode C. elegans: a platform for investigating biology Science 282 1998 2012 2018
21. M.A. Li, J.D. Alls, R.M. Avancini, K. Koo, and D. Godt The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila Nat. Cell Biol. 5 2003 994 1000
22. M.M. Rahman, G.P. Sykiotis, M. Nishimura, R. Bodmer, and D. Bohmann Declining signal dependence of Nrf2-MafS-regulated gene expression correlates with aging phenotypes Aging Cell 12 2013 554 562
23. Y. Takagi, M. Kobayashi, L. Li, T. Suzuki, K. Nishikawa, and M. Yamamoto MafT, a new member of the small Maf protein family in zebrafish Biochem. Biophys. Res. Commun. 320 2004 62 69
24. T.K. Blackwell, B. Bowerman, J.R. Priess, and H. Weintraub Formation of a monomeric DNA binding domain by Skn-1 bZIP and homeodomain elements Science 266 1994 621 628
25. N. McGinnis, E. Ragnhildstveit, A. Veraksa, and W. McGinnis A cap''n' collar protein isoform contains a selective Hox repressor function Development 125 1998 4553 4564
26. M. Kobayashi, K. Itoh, T. Suzuki, H. Osanai, K. Nishikawa, Y. Katoh, Y. Takagi, and M. Yamamoto Identification of the interactive interface and phylogenic conservation of the Nrf2-Keap1 system Genes Cells 7 2002 807 820
27. A.R. Timme-Laragy, S.I. Karchner, D.G. Franks, M.J. Jenny, R.C. Harbeitner, J.V. Goldstone, A.G. McArthur, and M.E. Hahn Nrf2b, novel zebrafish paralog of oxidant-responsive transcription factor NF-E2-related factor 2 (NRF2) J. Biol. Chem. 287 2012 4609 4627
28. M. Kimura, T. Yamamoto, J. Zhang, K. Itoh, M. Kyo, T. Kamiya, H. Aburatani, F. Katsuoka, H. Kurokawa, T. Tanaka, H. Motohashi, and M. Yamamoto Molecular basis distinguishing the DNA binding profile of Nrf2-Maf heterodimer from that of Maf homodimer J. Biol. Chem. 282 2007 33681 33690
29. M. Dlakić, A.V. Grinberg, D.A. Leonard, and T.K. Kerppola DNA sequence-dependent folding determines the divergence in binding specificities between Maf and other bZIP proteins EMBO J. 20 2001 828 840
30. D. Mashiko, Y. Fujihara, Y. Satouh, H. Miyata, A. Isotani, and M. Ikawa Generation of mutant mice by pronuclear injection of circular plasmid expressing Cas9 and single guided RNA Sci. Rep. 3 2013 3355
31. L. Cong, F.A. Ran, D. Cox, S. Lin, R. Barretto, N. Habib, P.D. Hsu, X. Wu, W. Jiang, L.A. Marraffini, and F. Zhang Multiplex genome engineering using CRISPR/Cas systems Science 339 2013 819 823
32. T. Ishii, K. Itoh, S. Takahashi, H. Sato, T. Yanagawa, Y. Katoh, S. Bannai, and M. Yamamoto Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages J. Biol. Chem. 275 2000 16023 16029
33. A. Maruyama, S. Tsukamoto, K. Nishikawa, A. Yoshida, N. Harada, K. Motojima, T. Ishii, A. Nakane, M. Yamamoto, and K. Itoh Nrf2 regulates the alternative first exons of CD36 in macrophages through specific antioxidant response elements Arch. Biochem. Biophys. 477 2008 139 145
34. F. Katsuoka, J. Yokozawa, K. Tsuda, S. Ito, X. Pan, M. Nagasaki, J. Yasuda, and M. Yamamoto An efficient quantitation method of next-generation sequencing libraries by using MiSeq sequencer Anal. Biochem. 466 2014 27 29
35. B. Langmead, and S.L. Salzberg Fast gapped-read alignment with Bowtie 2 Nat. Methods 9 2012 357 359
36. H. Thorvaldsdóttir, J.T. Robinson, and J.P. Mesirov Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration Brief. Bioinform. 14 2013 178 192
37. Y. Zhang, T. Liu, C.A. Meyer, J. Eeckhoute, D.S. Johnson, B.E. Bernstein, C. Nusbaum, R.M. Myers, M. Brown, W. Li, and X.S. Liu Model-based analysis of ChIP-Seq (MACS) Genome Biol. 9 2008 R137
38. P. Machanick, and T.L. Bailey MEME-ChIP: motif analysis of large DNA datasets Bioinformatics 27 2011 1696 1697
39. C. Trapnell, L. Pachter, and S.L. Salzberg TopHat: discovering splice junctions with RNA-Seq Bioinformatics 25 2009 1105 1111
40. C. Trapnell, B.A. Williams, G. Pertea, A. Mortazavi, G. Kwan, M.J. van Baren, S.L. Salzberg, B.J. Wold, and L. Pachter Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation Nat. Biotechnol. 28 2010 511 515
41. A. Subramanian, P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, E.S. Lander, and J.P. Mesirov Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles Proc. Natl. Acad. Sci. U.S.A. 102 2005 15545 15550
42. J.D. Hayes, and A.T. Dinkova-Kostova The Nrf2 regulatory network provides an interface between redox and intermediary metabolism Trends Biochem. Sci. 39 2014 199 218
43. R. Edgar, M. Domrachev, and A.E. Lash Gene Expression Omnibus: NCBI gene expression and hybridization array data repository Nucleic Acids Res. 30 2002 207 210
44. L.G. Higgins, M.O. Kelleher, I.M. Eggleston, K. Itoh, M. Yamamoto, and J.D. Hayes Transcription factor Nrf2 mediates an adaptive response to sulforaphane that protects fibroblasts in vitro against the cytotoxic effects of electrophiles, peroxides and redox-cycling agents Toxicol. Appl. Pharmacol. 237 2009 267 280
45. Y. Yang, J. Fear, J. Hu, I. Haecker, L. Zhou, R. Renne, D. Bloom, and L.M. McIntyre Leveraging biological replicates to improve analysis in ChIP-seq experiments Comput. Struct. Biotechnol. J. 9 2014 e201401002
46. P. Nioi, M. McMahon, K. Itoh, M. Yamamoto, and J.D. Hayes 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 2003 337 348
47. W.W. Wasserman, and W.E. Fahl Functional antioxidant responsive elements Proc. Natl. Acad. Sci. U.S.A. 94 1997 5361 5366
48. F. Katsuoka, H. Motohashi, J.D. Engel, and M. Yamamoto Nrf2 transcriptionally activates the mafG gene through an antioxidant response element J. Biol. Chem. 280 2005 4483 4490
49. L.V. Favreau, and C.B. Pickett The rat quinone reductase antioxidant response element. Identification of the nucleotide sequence required for basal and inducible activity and detection of antioxidant response element-binding proteins in hepatoma and non-hepatoma cell lines J. Biol. Chem. 270 1995 24468 24474
50. K. Itoh, M. Mochizuki, Y. Ishii, T. Ishii, T. Shibata, Y. Kawamoto, V. Kelly, K. Sekizawa, K. Uchida, and M. Yamamoto Transcription factor Nrf2 regulates inflammation by mediating the effect of 15-deoxy-Delta(12,14)-prostaglandin j(2) Mol. Cell. Biol. 24 2004 36 45
51. E. Kobayashi, T. Suzuki, and M. Yamamoto Roles nrf2 plays in myeloid cells and related disorders Oxid. Med. Cell. Longev. 2013 2013 529219
52. J.H. An, and T.K. Blackwell SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response Genes Dev. 17 2003 1882 1893
53. A.S. Carroll, D.E. Gilbert, X. Liu, J.W. Cheung, J.E. Michnowicz, G. Wagner, T.E. Ellenberger, and T.K. Blackwell SKN-1 domain folding and basic region monomer stabilization upon DNA binding Genes Dev. 11 1997 2227 2238
54. T. Takeuchi, T. Kudo, K. Ogata, M. Hamada, M. Nakamura, K. Kito, Y. Abe, N. Ueda, M. Yamamoto, J.D. Engel, and S. Takahashi Neither MafA/L-Maf nor MafB is essential for lens development in mice Genes Cells 14 2009 941 947
55. C. Zhang, T. Moriguchi, M. Kajihara, R. Esaki, A. Harada, H. Shimohata, H. Oishi, M. Hamada, N. Morito, K. Hasegawa, T. Kudo, J.D. Engel, M. Yamamoto, and S. Takahashi MafA is a key regulator of glucose-stimulated insulin secretion Mol. Cell. Biol. 25 2005 4969 4976
56. M. Nakamura, M. Hamada, K. Hasegawa, M. Kusakabe, H. Suzuki, D.R. Greaves, T. Moriguchi, T. Kudo, and S. Takahashi c-Maf is essential for the F4/80 expression in macrophages in vivo Gene 445 2009 66 72
57. N. Wakabayashi, K. Itoh, J. Wakabayashi, H. Motohashi, S. Noda, S. Takahashi, S. Imakado, T. Kotsuji, F. Otsuka, D.R. Roop, T. Harada, J.D. Engel, and M. Yamamoto Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation Nat. Genet. 35 2003 238 245
58. K. Taguchi, J.M. Maher, T. Suzuki, Y. Kawatani, H. Motohashi, and M. Yamamoto Genetic analysis of cytoprotective functions supported by graded expression of Keap1 Mol. Cell. Biol. 30 2010 3016 3026
59. H. Motohashi, F. Katsuoka, J.A. Shavit, J.D. Engel, and M. Yamamoto Positive or negative MARE-dependent transcriptional regulation is determined by the abundance of small Maf proteins Cell 103 2000 865 875
60. M. Ohtsuji, F. Katsuoka, A. Kobayashi, H. Aburatani, J.D. Hayes, and M. Yamamoto Nrf1 and Nrf2 play distinct roles in activation of antioxidant response element-dependent genes J. Biol. Chem. 283 2008 33554 33562