Heme regulates gene expression by triggering Crm1-dependent nuclear export of Bach1

EMBO Journal

Volumn 23, Issue 13, 2004, Pages 2544-2553

  Suzuki, Hiroshi ^a,e   Tashiro, Satoshi ^a   Hira, Shusuke ^b   Sun, Jiying ^a   Yamazaki, Chikara ^a   Zenke, Yukari ^a   Ikeda Saito, Masao ^b   Yoshida, Minoru ^c,d   Igarashi, Kazuhiko ^a,d  

^a HIROSHIMA UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

^c RIKEN   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Globin; Heme; Heme oxygenase; Maf; Oxidative stress

Indexed keywords

CADMIUM; EXPORTIN 1; HEME; HEME OXYGENASE 1; HEMIN; MUTANT PROTEIN; PROTEIN; PROTEIN BACH1; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR MAFK; UNCLASSIFIED DRUG;

ARTICLE; CELL LINE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TARGETING; SIGNAL TRANSDUCTION; WILD TYPE;

ACTIVE TRANSPORT, CELL NUCLEUS; ALANINE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL LINE; CELL NUCLEUS; CHROMATIN IMMUNOPRECIPITATION; DIMERIZATION; DNA-BINDING PROTEINS; ERYTHROID-SPECIFIC DNA-BINDING FACTORS; ESCHERICHIA COLI; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; FIBROBLASTS; GENE EXPRESSION REGULATION; GENES, REPORTER; GLOBINS; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEINS; HEME; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HEMIN; HUMANS; IMMUNOHISTOCHEMISTRY; KARYOPHERINS; LEUCINE ZIPPERS; MAFK TRANSCRIPTION FACTOR; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PLASMIDS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; SPECTROPHOTOMETRY; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; ZINC FINGERS;

NES;

EID: 3342905184     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600248     Document Type: Article

References (47)

1. Alam J, Shibahara S, Smith A (1989) Transcriptional activation of the heme oxygenase gene by heme and cadmium in mouse hepatoma cells. J Biol Chem 264: 6371-6375
2. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL (1999) Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 274: 26071-26078
3. Alam J, Wicks C, Stewart D, Gong P, Touchard C, Otterbein S, Choi AMK, Burow ME, Tou J (2000) Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells. Role of p38 kinase and Nrf2 transcription factor. J Biol Chem 275: 27694-27702
4. Andrews NC, Erdjument-Bromage H, Davidson MB, Tempst P, Orkin SH (1993a) Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature 362: 722-728
5. Andrews NC, Kotkow KJ, Ney PA, Erdjument-Bromage H, Tempst P, Orkin SH (1993b) The ubiquitous subunit of erythroid transcription factor NF-E2 is a small basic-leucine zipper protein related to the v-maf oncogene. Proc Natl Acad Sci USA 90: 11488-11492
6. Atamna H, Killilea DW, Killilea AN, Ames BN (2002) Heme deficiency may be a factor in the mitochondrial and neuronal decay of aging. Proc Natl Acad Sci USA 99: 14807-14812
7. Brand M, Ranish JA, Kummer NT, Hamilton J, Igarashi K, Francastel C, Chi TH, Crabree GR, Aebersold R, Groudine M (2004) Dynamic changes in transcription factors complexes during erythroid differentiation revealed by quantitative proteomics. Nat Struct Mol Biol 11: 73-80
8. Charnay P, Maniatis T (1983) Transcriptional regulation of globin gene expression in the human erythroid cell line K562. Science 220: 1281-1283
9. Dioum EM, Rutter J, Tuckerman JR, Gonzalez G, Gilles-Gonzalez M, McKnight SL (2002) NPAS2: a gas-responsive transcription factor. Science 298: 2385-2387
10. Fischer U, Huber J, Mattaj IW, Luhrmann R (1995) The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 82: 475-483
11. Han AP, Yu C, Lu L, Fujiwara Y, Browne C, Chin G, Fleming M, Leboulch P, Orkin SH, Chen JJ (2001) Heme-regulated elF2alpha (HRI) is required for translational regulation and survival of erythroid precursors in iron deficiency. EMBO J 20: 6909-6918
12. Hoshino H, Kobayashi A, Yoshida M, Kudo N, Oyake T, Motohashi H, Hayashi N, Yamamoto M, Igarashi K (2000) Oxidative stress abolishes leptomycin B-sensitive nuclear export of transcription represser Bach2 that counteracts activation of Maf recognition element. J Biol Chem 275: 15370-15376
13. Igarashi K, Hoshino H, Muto A, Suwabe N, Nishikawa S, Nakauchi H, Yamamoto M (1998) Multivalem 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
14. Igarashi K, Itoh K, Hayashi N, Nishizawa M, Yamamoto M (1995) Conditional expression of the ubiquitous transcription factor MafK induces erythroleukemia cell differentiation. Proc Natl Acad Sci USA 92: 7445-7449
15. Igarashi K, Kataoka K, Itoh K, Hayashi N, Nishizawa M, Yamamoto M (1994) Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Maf proteins. Nature 367: 568-572
16. Inamdar NM, Ahn YI, 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
17. Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, Katoh Y, Bannai S, Yamamoto M (2000) Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem 275: 16023-16029
18. Kataoka K, Handa H, Nishizawa M (2001) Induction of cellular antioxidative stress genes through heterodimeric transcription factor Nrf2/small Maf by antirheumatic gold(I) compounds. J Biol Chem 276: 34074-34081
19. Kataoka K, Noda M, Nishizawa M (1994) Maf nuclear oncoprotein recognizes sequences related to an AP-1 site and forms heterodimers with both Fos and Jun. Mol Cell Biol 14: 700-712
20. Keyse SM, Tyrrell RM (1989) Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA 86: 99-103
21. Kudo N, Matsumori N, Taoka H, Fujiwara D, Schreiner EP, Wolff B, Yoshida M, Horinouchi S (1999a) Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cystein residue in the central conserved region. Proc Natl Acad Sci USA 96: 9112-9117
22. Kudo N, Taoka H, Toda T, Yoshida M, Horinouchi S (1999b) A novel nuclear export signal sensitive to oxidative stress in the fission yeast transcription factor Pap1. J Biol Chem 274: 15151-15158
23. Lathrop JT, Timko MP (1993) Regulation by heme of mitochondrial protein transport through a conserved aminoacid motif. Science 259: 522-525
24. Monson EK, Weinstein M, Ditta GS, Helinski DR (1992) The FixL protein of Rhizobium meliloti can be separated into a heme-binding oxygen-sensing domain and a functional C-terminal kinase domain. Proc Natl Acad Sci USA 89: 4280-4284
25. Muto A, Tashiro S, Tsuchiya H, Kume A, Kanno M, Ito E, Yamamoto M, Igarashi K (2002) Activation of Maf/AP-1 represser Bach2 promotes apoptosis and its interaction with PML nuclear bodies. J Biol Chem 277: 20724-20733
26. Ney PA, Sorrentino BP, Lowrey CH, Nienhuis AW (1990a) Inducibility of the HS II enhancer depends on binding of an erythroid specific nuclear protein. Nucleic Acids Res 18: 6011-6017
27. Ney PA, Sorrentino BP, McDonagh KT, Nienhuis AW (1990b) Tandem AP-1-binding sites within the human b-globin dominant control region functions as an inducible enhancer in erythroid cells. Genes Dev 4: 993-1006
28. Ogawa K, Sun J, Taketani S, Nakajima O, Nishitani C, Sassa S, Hayashi N, Yamamoto M, Shibahara S, Fujita H, Igarashi K (2001) Heme mediates de-repression of Maf recognition element through direct binding to transcription represser Bach1. EMBO J 20: 2835-2843
29. Otterbein LE, Soares MP, Yamashita K, Bach FH (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24: 449-455
30. Oyake T, Itoh K, Motohashi H, Hayashi N, Hoshino H, Nishizawa M, Yamamoto M, Igarashi K (1996) 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: 6083-6095
31. Poss KD, Tonegawa S (1997) Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci USA 94: 10925-10930
32. Qi Z, Hamza I, O'Brian MR (1999) Heme is an effector molecule for iron-dependent degradation of the bacterial iron response regulator (Irr) protein. Proc Natl Acad Sci USA 96: 13056-13061
33. Shibahara S, Kitamuro T, Takahashi K (2002) Heme degradation and human diseases: diversity in the soul of life. Antioxidants Redox Signaling 4: 593-602
34. Shibahara S, Muller R, Taguchi H, Yoshida T (1985) Cloning and expression of cDNA for rat heme oxygenase. Proc Natl Acad Sci USA 82: 7865-7869
35. Shibahara S, Muller RM, Taguchi H (1987) Transcriptional control of rat heme oxygenase by heat shock. J Biol Chem 262: 12889-12892
36. Shibahara S, Yoshida T, Kikuchi G (1978) Induction of heme oxygenase by hemin in cultured pig alveolar macrophages. Arch Biochem Biophys 188: 243-250
37. Sun J, Brand M, Zenke Y, Tashiro S, Groudine M, Igarashi K (2004) Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription network. Proc Natl Acad Sci USA 101: 1461-1466
38. Sun J, Hoshino H, Takaku K, Nakajima O, Muto A, Suzuki H, Tashiro S, Takahashi S, Shibahara S, Alam J, Taketo MM, Yamamoto M, Igarashi K (2002) Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J 21: 5216-5224
39. Suzuki H, Tashiro S, Sun J, Doi H, Satomi S, Igarashi K (2003) Cadmium induces nuclear export of Bach1, a transcriptional represser of heme oxygenase-1 gene. J Biol Chem 278: 49246-49253
40. Taketani S, Kohno H, Yoshinaga T, Tokunaga R (1989) The human 32-kDa stress protein induced by exposure to arsenite and cadmium ions is heme oxygenase. FEBS Lett 245: 173-176
41. Tang SC, Koch S, Papaefthymiou GC, Foner S, Frankel RB, Ibers JA, Holm RH (1976) Axial ligation modes in iron(III) Porphyrins. Models for the oxidized reaction states of cytochrome P-450 enzymes and the molecular structure of iron(III) protoporphyrin IX dimethyl ester p-nitrobenzenethiolate. J Am Chem Soc 98: 2114-2434
42. Tenhunen R, Marver HS, Schmid R (1970) The enzymatic catabolism of hemoglobin: stimulation of microsomal heme oxygenase by hemin. J Lab Clin Med 75: 410-421
43. Wagener FA, van Beurden HE, von den Hoff JW, Adema GJ, Figdor CG (2003) The heme-heme oxygenase system: a molecular switch in wound healing. Blood 102: 521-528
44. Wen W, Meinkoth JL, Tsien RY, Taylor SS (1995) Identification of a signal for rapid export of proteins from the nucleus. Cell 82: 463-473
45. Yachie A, Niida Y, Wata T, Igarashi N, Kaneda H, Toma T, Ohta K, Kasahara Y, Koizumi S (1999) Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J Clin Investig 103: 129-135
46. Yoshida C, Tokumasu F, Hohmura KI, Bungert J, Hayashi N, Nagasawa T, Engel JD, Yamamoto M, Takeyasu K, Igarashi K (1999) Long range interaction of cis-DNA elements mediated by architectural transcription factor Bach1. Genes Cells 4: 643-655
47. Zhang L, Guarente L (1995) Heme binds to a short sequence that serves a regulatory function in diverse proteins. EMBO J 14: 313-320