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The world according to Maf.

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  • 1. Institute of Basic Medical Sciences and Center for TARA, University of Tsukuba, Tsukuba 305, Japan.
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    • Motohashi H 1
    (1 author)

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Nucleic Acids Research, 01 Aug 1997, 25(15):2953-2959
https://doi.org/10.1093/nar/25.15.2953 PMID: 9224592 PMCID: PMC146842

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Abstract 

Maf family proteins are so named because of their structural similarity to the founding member, the oncoprotein v-Maf. The small Maf proteins (MafF, MafG and MafK), as do all family members, include a characteristic basic region linked to a leucine zipper (b-Zip) domain which mediate DNA binding and subunit dimerization respectively. The small Maf proteins form homodimers or heterodimers with other b-Zip proteins present in the cell and bind to Maf recognition elements (MARE) in DNA. Since they lack known transcriptional activation domains, the small Maf proteins function either as obligatory heterodimeric partner molecules with numerous large subunits, discussed below, or alternatively as homo- or heterodimeric transcriptional repressors. The three small Maf proteins are expressed in a number of overlapping tissues, but their expression profiles nonetheless appear to be under meticulous tissue- and developmental stage-specific control. The MARE bears a striking resemblance to the NF-E2 binding sequence. NF-E2 binding sites in the human beta-globin locus control region have been directly implicated as integral components in the circuitry required for eliciting changes in chromatin structure that precede globin gene activation. While the NF-E2 DNA sequence has been shown to be important for erythroid-specific gene regulation, a growing list of other genes may also be regulated through the same, or very similar, cis elements in non-erythroid cells. Taken together, these observations argue that comprehensive analysis of the activities of the small Maf proteins may provide a unique perspective for expanding our understanding of transcriptional regulation that can be elicited through interacting transcription factor networks.

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Nucleic Acids Res. 1997 Aug 1; 25(15): 2953–2959.
PMCID: PMC146842
PMID: 9224592

The world according to Maf.

H Motohashi, J A Shavit, K Igarashi, M Yamamoto, and J D Engel
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Abstract

Maf family proteins are so named because of their structural similarity to the founding member, the oncoprotein v-Maf. The small Maf proteins (MafF, MafG and MafK), as do all family members, include a characteristic basic region linked to a leucine zipper (b-Zip) domain which mediate DNA binding and subunit dimerization respectively. The small Maf proteins form homodimers or heterodimers with other b-Zip proteins present in the cell and bind to Maf recognition elements (MARE) in DNA. Since they lack known transcriptional activation domains, the small Maf proteins function either as obligatory heterodimeric partner molecules with numerous large subunits, discussed below, or alternatively as homo- or heterodimeric transcriptional repressors. The three small Maf proteins are expressed in a number of overlapping tissues, but their expression profiles nonetheless appear to be under meticulous tissue- and developmental stage-specific control. The MARE bears a striking resemblance to the NF-E2 binding sequence. NF-E2 binding sites in the human beta-globin locus control region have been directly implicated as integral components in the circuitry required for eliciting changes in chromatin structure that precede globin gene activation. While the NF-E2 DNA sequence has been shown to be important for erythroid-specific gene regulation, a growing list of other genes may also be regulated through the same, or very similar, cis elements in non-erythroid cells. Taken together, these observations argue that comprehensive analysis of the activities of the small Maf proteins may provide a unique perspective for expanding our understanding of transcriptional regulation that can be elicited through interacting transcription factor networks.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Hunter T. Oncoprotein networks. Cell. 1997 Feb 7;88(3):333–346. [Abstract] [Google Scholar]
  • Nishizawa M, Kataoka K, Goto N, Fujiwara KT, Kawai S. v-maf, a viral oncogene that encodes a "leucine zipper" motif. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7711–7715. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kataoka K, Nishizawa M, Kawai S. Structure-function analysis of the maf oncogene product, a member of the b-Zip protein family. J Virol. 1993 Apr;67(4):2133–2141. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kataoka K, Noda M, Nishizawa M. Maf nuclear oncoprotein recognizes sequences related to an AP-1 site and forms heterodimers with both Fos and Jun. Mol Cell Biol. 1994 Jan;14(1):700–712. [Europe PMC free article] [Abstract] [Google Scholar]
  • Swaroop A, Xu JZ, Pawar H, Jackson A, Skolnick C, Agarwal N. A conserved retina-specific gene encodes a basic motif/leucine zipper domain. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):266–270. [Europe PMC free article] [Abstract] [Google Scholar]
  • Fujiwara KT, Kataoka K, Nishizawa M. Two new members of the maf oncogene family, mafK and mafF, encode nuclear b-Zip proteins lacking putative trans-activator domain. Oncogene. 1993 Sep;8(9):2371–2380. [Abstract] [Google Scholar]
  • Kataoka K, Igarashi K, Itoh K, Fujiwara KT, Noda M, Yamamoto M, Nishizawa M. Small Maf proteins heterodimerize with Fos and may act as competitive repressors of the NF-E2 transcription factor. Mol Cell Biol. 1995 Apr;15(4):2180–2190. [Europe PMC free article] [Abstract] [Google Scholar]
  • Andrews NC, Kotkow KJ, Ney PA, Erdjument-Bromage H, Tempst P, Orkin SH. 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 U S A. 1993 Dec 15;90(24):11488–11492. [Europe PMC free article] [Abstract] [Google Scholar]
  • Igarashi K, Kataoka K, Itoh K, Hayashi N, Nishizawa M, Yamamoto M. Regulation of transcription by dimerization of erythroid factor NF-E2 p45 with small Maf proteins. Nature. 1994 Feb 10;367(6463):568–572. [Abstract] [Google Scholar]
  • Sieweke MH, Tekotte H, Frampton J, Graf T. MafB is an interaction partner and repressor of Ets-1 that inhibits erythroid differentiation. Cell. 1996 Apr 5;85(1):49–60. [Abstract] [Google Scholar]
  • Cordes SP, Barsh GS. The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell. 1994 Dec 16;79(6):1025–1034. [Abstract] [Google Scholar]
  • Ho IC, Hodge MR, Rooney JW, Glimcher LH. The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell. 1996 Jun 28;85(7):973–983. [Abstract] [Google Scholar]
  • Kurschner C, Morgan JI. The maf proto-oncogene stimulates transcription from multiple sites in a promoter that directs Purkinje neuron-specific gene expression. Mol Cell Biol. 1995 Jan;15(1):246–254. [Europe PMC free article] [Abstract] [Google Scholar]
  • Fraser P, Pruzina S, Antoniou M, Grosveld F. Each hypersensitive site of the human beta-globin locus control region confers a different developmental pattern of expression on the globin genes. Genes Dev. 1993 Jan;7(1):106–113. [Abstract] [Google Scholar]
  • Bungert J, Davé U, Lim KC, Lieuw KH, Shavit JA, Liu Q, Engel JD. Synergistic regulation of human beta-globin gene switching by locus control region elements HS3 and HS4. Genes Dev. 1995 Dec 15;9(24):3083–3096. [Abstract] [Google Scholar]
  • Wijgerde M, Grosveld F, Fraser P. Transcription complex stability and chromatin dynamics in vivo. Nature. 1995 Sep 21;377(6546):209–213. [Abstract] [Google Scholar]
  • Jiménez G, Griffiths SD, Ford AM, Greaves MF, Enver T. Activation of the beta-globin locus control region precedes commitment to the erythroid lineage. Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10618–10622. [Europe PMC free article] [Abstract] [Google Scholar]
  • Ney PA, Sorrentino BP, McDonagh KT, Nienhuis AW. Tandem AP-1-binding sites within the human beta-globin dominant control region function as an inducible enhancer in erythroid cells. Genes Dev. 1990 Jun;4(6):993–1006. [Abstract] [Google Scholar]
  • Ney PA, Sorrentino BP, Lowrey CH, Nienhuis AW. Inducibility of the HS II enhancer depends on binding of an erythroid specific nuclear protein. Nucleic Acids Res. 1990 Oct 25;18(20):6011–6017. [Europe PMC free article] [Abstract] [Google Scholar]
  • Talbot D, Grosveld F. The 5'HS2 of the globin locus control region enhances transcription through the interaction of a multimeric complex binding at two functionally distinct NF-E2 binding sites. EMBO J. 1991 Jun;10(6):1391–1398. [Europe PMC free article] [Abstract] [Google Scholar]
  • Strauss EC, Orkin SH. In vivo protein-DNA interactions at hypersensitive site 3 of the human beta-globin locus control region. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5809–5813. [Europe PMC free article] [Abstract] [Google Scholar]
  • Andrews NC, Erdjument-Bromage H, Davidson MB, Tempst P, Orkin SH. Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature. 1993 Apr 22;362(6422):722–728. [Abstract] [Google Scholar]
  • Stamatoyannopoulos JA, Goodwin A, Joyce T, Lowrey CH. NF-E2 and GATA binding motifs are required for the formation of DNase I hypersensitive site 4 of the human beta-globin locus control region. EMBO J. 1995 Jan 3;14(1):106–116. [Europe PMC free article] [Abstract] [Google Scholar]
  • Mignotte V, Wall L, deBoer E, Grosveld F, Romeo PH. Two tissue-specific factors bind the erythroid promoter of the human porphobilinogen deaminase gene. Nucleic Acids Res. 1989 Jan 11;17(1):37–54. [Europe PMC free article] [Abstract] [Google Scholar]
  • Taketani S, Inazawa J, Nakahashi Y, Abe T, Tokunaga R. Structure of the human ferrochelatase gene. Exon/intron gene organization and location of the gene to chromosome 18. Eur J Biochem. 1992 Apr 1;205(1):217–222. [Abstract] [Google Scholar]
  • Kumar R, Chen S, Scheurer D, Wang QL, Duh E, Sung CH, Rehemtulla A, Swaroop A, Adler R, Zack DJ. The bZIP transcription factor Nrl stimulates rhodopsin promoter activity in primary retinal cell cultures. J Biol Chem. 1996 Nov 22;271(47):29612–29618. [Abstract] [Google Scholar]
  • Rehemtulla A, Warwar R, Kumar R, Ji X, Zack DJ, Swaroop A. The basic motif-leucine zipper transcription factor Nrl can positively regulate rhodopsin gene expression. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):191–195. [Europe PMC free article] [Abstract] [Google Scholar]
  • Toki T, Itoh J, Kitazawa J, Arai K, Hatakeyama K, Akasaka J, Igarashi K, Nomura N, Yokoyama M, Yamamoto M, et al. Human small Maf proteins form heterodimers with CNC family transcription factors and recognize the NF-E2 motif. Oncogene. 1997 Apr 24;14(16):1901–1910. [Abstract] [Google Scholar]
  • Igarashi K, Itoh K, Motohashi H, Hayashi N, Matuzaki Y, Nakauchi H, Nishizawa M, Yamamoto M. Activity and expression of murine small Maf family protein MafK. J Biol Chem. 1995 Mar 31;270(13):7615–7624. [Abstract] [Google Scholar]
  • Motohashi H, Igarashi K, Onodera K, Takahashi S, Ohtani H, Nakafuku M, Nishizawa M, Engel JD, Yamamoto M. Mesodermal- vs. neuronal-specific expression of MafK is elicited by different promoters. Genes Cells. 1996 Feb;1(2):223–238. [Abstract] [Google Scholar]
  • Itoh K, Igarashi K, Hayashi N, Nishizawa M, Yamamoto M. Cloning and characterization of a novel erythroid cell-derived CNC family transcription factor heterodimerizing with the small Maf family proteins. Mol Cell Biol. 1995 Aug;15(8):4184–4193. [Europe PMC free article] [Abstract] [Google Scholar]
  • Oyake T, Itoh K, Motohashi H, Hayashi N, Hoshino H, Nishizawa M, Yamamoto M, Igarashi K. 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. 1996 Nov;16(11):6083–6095. [Europe PMC free article] [Abstract] [Google Scholar]
  • Ney PA, Andrews NC, Jane SM, Safer B, Purucker ME, Weremowicz S, Morton CC, Goff SC, Orkin SH, Nienhuis AW. Purification of the human NF-E2 complex: cDNA cloning of the hematopoietic cell-specific subunit and evidence for an associated partner. Mol Cell Biol. 1993 Sep;13(9):5604–5612. [Europe PMC free article] [Abstract] [Google Scholar]
  • Chan JY, Han XL, Kan YW. Isolation of cDNA encoding the human NF-E2 protein. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11366–11370. [Europe PMC free article] [Abstract] [Google Scholar]
  • Caterina JJ, Donze D, Sun CW, Ciavatta DJ, Townes TM. Cloning and functional characterization of LCR-F1: a bZIP transcription factor that activates erythroid-specific, human globin gene expression. Nucleic Acids Res. 1994 Jun 25;22(12):2383–2391. [Europe PMC free article] [Abstract] [Google Scholar]
  • Chan JY, Han XL, Kan YW. Cloning of Nrf1, an NF-E2-related transcription factor, by genetic selection in yeast. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11371–11375. [Europe PMC free article] [Abstract] [Google Scholar]
  • Moi P, Chan K, Asunis I, Cao A, Kan YW. Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9926–9930. [Europe PMC free article] [Abstract] [Google Scholar]
  • Chui DH, Tang W, Orkin SH. cDNA cloning of murine Nrf 2 gene, coding for a p45 NF-E2 related transcription factor. Biochem Biophys Res Commun. 1995 Apr 6;209(1):40–46. [Abstract] [Google Scholar]
  • Mohler J, Vani K, Leung S, Epstein A. Segmentally restricted, cephalic expression of a leucine zipper gene during Drosophila embryogenesis. Mech Dev. 1991 Mar;34(1):3–9. [Abstract] [Google Scholar]
  • Johnsen O, Skammelsrud N, Luna L, Nishizawa M, Prydz H, Kolstø AB. Small Maf proteins interact with the human transcription factor TCF11/Nrf1/LCR-F1. Nucleic Acids Res. 1996 Nov 1;24(21):4289–4297. [Europe PMC free article] [Abstract] [Google Scholar]
  • Engel JD. Meticulous AP-1 factors. Nature. 1994 Feb 10;367(6463):516–517. [Abstract] [Google Scholar]
  • Armstrong JA, Emerson BM. NF-E2 disrupts chromatin structure at human beta-globin locus control region hypersensitive site 2 in vitro. Mol Cell Biol. 1996 Oct;16(10):5634–5644. [Europe PMC free article] [Abstract] [Google Scholar]
  • Dorn R, Krauss V, Reuter G, Saumweber H. The enhancer of position-effect variegation of Drosophila, E(var)3-93D, codes for a chromatin protein containing a conserved domain common to several transcriptional regulators. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11376–11380. [Europe PMC free article] [Abstract] [Google Scholar]
  • Farkas G, Gausz J, Galloni M, Reuter G, Gyurkovics H, Karch F. The Trithorax-like gene encodes the Drosophila GAGA factor. Nature. 1994 Oct 27;371(6500):806–808. [Abstract] [Google Scholar]
  • Albagli O, Dhordain P, Deweindt C, Lecocq G, Leprince D. The BTB/POZ domain: a new protein-protein interaction motif common to DNA- and actin-binding proteins. Cell Growth Differ. 1995 Sep;6(9):1193–1198. [Abstract] [Google Scholar]
  • Yamasaki H, Fibach E, Nudel U, Weinstein IB, Rifkind RA, Marks PA. Tumor promoters inhibit spontaneous and induced differentiation of murine erythroleukemia cells in culture. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3451–3455. [Europe PMC free article] [Abstract] [Google Scholar]
  • Cheng X, Reginato MJ, Andrews NC, Lazar MA. The transcriptional integrator CREB-binding protein mediates positive cross talk between nuclear hormone receptors and the hematopoietic bZip protein p45/NF-E2. Mol Cell Biol. 1997 Mar;17(3):1407–1416. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kotkow KJ, Orkin SH. Complexity of the erythroid transcription factor NF-E2 as revealed by gene targeting of the mouse p18 NF-E2 locus. Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3514–3518. [Europe PMC free article] [Abstract] [Google Scholar]
  • Igarashi K, Itoh K, Hayashi N, Nishizawa M, Yamamoto M. Conditional expression of the ubiquitous transcription factor MafK induces erythroleukemia cell differentiation. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7445–7449. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kotkow KJ, Orkin SH. Dependence of globin gene expression in mouse erythroleukemia cells on the NF-E2 heterodimer. Mol Cell Biol. 1995 Aug;15(8):4640–4647. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kataoka K, Fujiwara KT, Noda M, Nishizawa M. MafB, a new Maf family transcription activator that can associate with Maf and Fos but not with Jun. Mol Cell Biol. 1994 Nov;14(11):7581–7591. [Europe PMC free article] [Abstract] [Google Scholar]
  • Pouponnot C, Nishizawa M, Calothy G, Pierani A. Transcriptional stimulation of the retina-specific QR1 gene upon growth arrest involves a Maf-related protein. Mol Cell Biol. 1995 Oct;15(10):5563–5575. [Europe PMC free article] [Abstract] [Google Scholar]
  • Shivdasani RA, Rosenblatt MF, Zucker-Franklin D, Jackson CW, Hunt P, Saris CJ, Orkin SH. Transcription factor NF-E2 is required for platelet formation independent of the actions of thrombopoietin/MGDF in megakaryocyte development. Cell. 1995 Jun 2;81(5):695–704. [Abstract] [Google Scholar]
  • Chan K, Lu R, Chang JC, Kan YW. NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13943–13948. [Europe PMC free article] [Abstract] [Google Scholar]
  • Farmer SC, Sun CW, Winnier GE, Hogan BL, Townes TM. The bZIP transcription factor LCR-F1 is essential for mesoderm formation in mouse development. Genes Dev. 1997 Mar 15;11(6):786–798. [Abstract] [Google Scholar]
  • Martin DI, Fiering S, Groudine M. Regulation of beta-globin gene expression: straightening out the locus. Curr Opin Genet Dev. 1996 Aug;6(4):488–495. [Abstract] [Google Scholar]
  • Distel RJ, Spiegelman BM. Protooncogene c-fos as a transcription factor. Adv Cancer Res. 1990;55:37–55. [Abstract] [Google Scholar]
  • Vogt PK, Bos TJ. jun: oncogene and transcription factor. Adv Cancer Res. 1990;55:1–35. [Abstract] [Google Scholar]
  • Luna L, Johnsen O, Skartlien AH, Pedeutour F, Turc-Carel C, Prydz H, Kolstø AB. Molecular cloning of a putative novel human bZIP transcription factor on chromosome 17q22. Genomics. 1994 Aug;22(3):553–562. [Abstract] [Google Scholar]
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