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PMID: 10075929 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The GATA factor AreA is essential for chromatin remodelling in a eukaryotic bidirectional promoter.

The EMBO journal ·Vol. 18 ·No. 6 ·1999-03-15 ·Pages 1584-97

Muro-Pastor MI, Gonzalez R, Strauss J, Narendja F, Scazzocchio C

Abstract

The linked niiA and niaD genes of Aspergillus nidulans are transcribed divergently. The expression of these genes is subject to a dual control system. They are induced by nitrate and repressed by ammonium. AreA mediates derepression in the absence of ammonium and NirA supposedly mediates nitrate induction. Out of 10 GATA sites, a central cluster (sites 5-8) is responsible for approximately 80% of the transcriptional activity of the promoter on both genes. We show occupancy in vivo of site 5 by the AreA protein, even under conditions of repression. Sites 5-8 are situated in a pre-set nucleosome-free region. Under conditions of expression, a drastic nucleosomal rearrangement takes place and the positioning of at least five nucleosomes flanking the central region is lost. Remodelling is strictly dependent on the presence of an active areA gene product, and independent from the NirA-specific and essential transcription factor. Thus, nucleosome remodelling is independent from the transcriptional activation of the niiA-niaD promoter. The results presented cast doubts on the role of NirA as the unique transducer of the nitrate induction signal. We demonstrate, for the first time in vivo, that a GATA factor is involved directly in chromatin remodelling.

MeSH Terms
Aspergillus nidulans/genetics,metabolism Base Sequence Binding Sites Chromatin/genetics,ultrastructure DNA Footprinting DNA, Fungal/chemistry,genetics Fungal Proteins/genetics,metabolism Genes, Reporter Multigene Family Mutagenesis, Site-Directed Nitrate Reductase Nitrate Reductases/genetics,metabolism Nitrite Reductases/genetics,metabolism Promoter Regions, Genetic Recombinant Fusion Proteins/biosynthesis Recombinant Proteins/metabolism Restriction Mapping Transcription Factors/genetics,metabolism Transcription, Genetic Transcriptional Activation Zinc Fingers
Chemicals
AreA protein, Aspergillus nidulans Chromatin DNA, Fungal Fungal Proteins Recombinant Fusion Proteins Recombinant Proteins Transcription Factors NirA protein, Aspergillus nidulans Nitrate Reductases Nitrite Reductases Nitrate Reductase
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Muro-Pastor M I
Institut de Génétique et Microbiologie, Université Paris-Sud, UMR CNRS C8621, 91405 Orsay Cedex, France.
Gonzalez R
Strauss J
Narendja F
Scazzocchio C
References (74)
74 references, click to expand
  1. Transformation by integration in Aspergillus nidulans.
    Gene. 1983 Dec;26(2-3):205-21 PMID: 6368319
  2. Aspergillus nidulans contains a single actin gene which has unique intron locations and encodes a gamma-actin.
    Gene. 1988 Oct 30;70(2):283-93 PMID: 2975248
  3. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR.
    Science. 1989 Nov 10;246(4931):780-6 PMID: 2814500
  4. nit-2, the major nitrogen regulatory gene of Neurospora crassa, encodes a protein with a putative zinc finger DNA-binding domain.
    Mol Cell Biol. 1990 Mar;10(3):1056-65 PMID: 2137552
  5. The regulatory gene areA mediating nitrogen metabolite repression in Aspergillus nidulans. Mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger.
    EMBO J. 1990 May;9(5):1355-64 PMID: 1970293
  6. nit-2, the major positive-acting nitrogen regulatory gene of Neurospora crassa, encodes a sequence-specific DNA-binding protein.
    Proc Natl Acad Sci U S A. 1990 Jul;87(14):5331-5 PMID: 2142530
  7. Interaction between major nitrogen regulatory protein NIT2 and pathway-specific regulatory factor NIT4 is required for their synergistic activation of gene expression in Neurospora crassa.
    Mol Cell Biol. 1998 Jul;18(7):3983-90 PMID: 9632783
  8. Perturbation of nucleosome structure by the erythroid transcription factor GATA-1.
    J Mol Biol. 1998 Jun 12;279(3):529-44 PMID: 9641976
  9. In situ detection of protein-DNA interactions in filamentous fungi by in vivo footprinting.
    Nucleic Acids Res. 1998 Aug 15;26(16):3862-4 PMID: 9685506
  10. The genetics of Aspergillus nidulans.
    Adv Genet. 1953;5:141-238 PMID: 13040135
  11. Droperidol lengthens cardiac repolarization due to block of the rapid component of the delayed rectifier potassium current.
    J Cardiovasc Electrophysiol. 1999 Dec;10(12):1597-604 PMID: 10636190
  12. Regulation of nitrate reduction in Aspergillus nidulans.
    Nature. 1967 Sep 16;215(5107):1234-7 PMID: 6052720
  13. Nitrogen metabolite repression in Aspergillus nidulans.
    Mol Gen Genet. 1973 Nov 2;126(2):111-41 PMID: 4591376
  14. Mutations in nirA gene of Aspergillus nidulans and nitrogen metabolism.
    Nature. 1978 Apr 20;272(5655):732-4 PMID: 347305
  15. Genetic studies of nitrate assimilation in Aspergillus nidulans.
    Biol Rev Camb Philos Soc. 1979 Aug;54(3):291-327 PMID: 389305
  16. Sequence specific cleavage of DNA by micrococcal nuclease.
    Nucleic Acids Res. 1981 Jun 25;9(12):2643-58 PMID: 7279658
  17. Isolation and characterisation of the crnA-niiA-niaD gene cluster for nitrate assimilation in Aspergillus nidulans.
    Gene. 1990 Jun 15;90(2):181-92 PMID: 2205530
  18. Functional elements in the promoter region of the Aspergillus nidulans gpdA gene encoding glyceraldehyde-3-phosphate dehydrogenase.
    Gene. 1990 Sep 1;93(1):101-9 PMID: 2121607
  19. crnA encodes a nitrate transporter in Aspergillus nidulans.
    Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):204-8 PMID: 1986367
  20. Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1.
    Nature. 1991 Jan 17;349(6306):257-60 PMID: 1987478
  21. Molecular cloning and functional characterization of the pathway-specific regulatory gene nirA, which controls nitrate assimilation in Aspergillus nidulans.
    Mol Cell Biol. 1991 Feb;11(2):795-802 PMID: 1990284
  22. A twin-reporter vector for simultaneous analysis of expression signals of divergently transcribed, contiguous genes in filamentous fungi.
    Gene. 1991 Jul 31;104(1):119-22 PMID: 1916271
  23. nirA, the pathway-specific regulatory gene of nitrate assimilation in Aspergillus nidulans, encodes a putative GAL4-type zinc finger protein and contains four introns in highly conserved regions.
    Mol Cell Biol. 1991 Nov;11(11):5746-55 PMID: 1922075
  24. Chromatin as an essential part of the transcriptional mechanism.
    Nature. 1992 Jan 16;355(6357):219-24 PMID: 1731219
  25. Effects of different DNA polymerases in ligation-mediated PCR: enhanced genomic sequencing and in vivo footprinting.
    Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):1021-5 PMID: 1736283
  26. Nitrate reductase and nitrite reductase transcript levels in various mutants of Aspergillus nidulans: confirmation of autogenous regulation.
    Mol Gen Genet. 1992 Feb;231(3):485-8 PMID: 1538701
  27. Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure.
    Genes Dev. 1992 Dec;6(12A):2288-98 PMID: 1459453
  28. GAL4 disrupts a repressing nucleosome during activation of GAL1 transcription in vivo.
    Genes Dev. 1993 May;7(5):857-69 PMID: 8491382
  29. Structural and functional requirements for the chromatin transition at the PHO5 promoter in Saccharomyces cerevisiae upon PHO5 activation.
    J Mol Biol. 1993 Jun 5;231(3):658-67 PMID: 8515443
  30. NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1.
    Science. 1993 Jul 23;261(5120):438-46 PMID: 8332909
  31. Chromatin disruption in the promoter of human immunodeficiency virus type 1 during transcriptional activation.
    EMBO J. 1993 Aug;12(8):3249-59 PMID: 8344262
  32. The erythroid protein cGATA-1 functions with a stage-specific factor to activate transcription of chromatin-assembled beta-globin genes.
    Genes Dev. 1993 Sep;7(9):1796-809 PMID: 8370527
  33. Hypersensitive sites in the 5' promoter region of nit-3, a highly regulated structural gene of Neurospora crassa.
    J Bacteriol. 1993 Nov;175(21):6755-9 PMID: 8226616
  34. Two different, adjacent and divergent zinc finger binding sites are necessary for CREA-mediated carbon catabolite repression in the proline gene cluster of Aspergillus nidulans.
    EMBO J. 1994 Jan 15;13(2):407-15 PMID: 8313886
  35. The molecular genetics of nitrate assimilation in fungi and plants.
    Annu Rev Genet. 1993;27:115-46 PMID: 8122899
  36. Transcription: in tune with the histones.
    Cell. 1994 Apr 8;77(1):13-6 PMID: 8156588
  37. Architectural variations of inducible eukaryotic promoters: preset and remodeling chromatin structures.
    Bioessays. 1994 Mar;16(3):165-70 PMID: 8166669
  38. An early haematopoietic defect in mice lacking the transcription factor GATA-2.
    Nature. 1994 Sep 15;371(6494):221-6 PMID: 8078582
  39. A nucleosome precludes binding of the transcription factor Pho4 in vivo to a critical target site in the PHO5 promoter.
    EMBO J. 1994 Oct 17;13(20):4848-55 PMID: 7957054
  40. The transactivation domain of Pho4 is required for nucleosome disruption at the PHO5 promoter.
    EMBO J. 1994 Oct 17;13(20):4856-62 PMID: 7957055
  41. 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):106-16 PMID: 7828582
  42. Functional synergy and physical interactions of the erythroid transcription factor GATA-1 with the Krüppel family proteins Sp1 and EKLF.
    Mol Cell Biol. 1995 May;15(5):2437-47 PMID: 7739528
  43. Distribution of GAGA protein on Drosophila genes in vivo.
    Genes Dev. 1995 May 1;9(9):1098-110 PMID: 7744251
  44. Sequence-specific DNA binding by NIT4, the pathway-specific regulatory protein that mediates nitrate induction in Neurospora.
    Mol Microbiol. 1995 Mar;15(5):935-42 PMID: 7596294
  45. The negative-acting NMR regulatory protein of Neurospora crassa binds to and inhibits the DNA-binding activity of the positive-acting nitrogen regulatory protein NIT2.
    Biochemistry. 1995 Jul 11;34(27):8861-8 PMID: 7612627
  46. The intergenic region between the divergently transcribed niiA and niaD genes of Aspergillus nidulans contains multiple NirA binding sites which act bidirectionally.
    Mol Cell Biol. 1995 Oct;15(10):5688-99 PMID: 7565720
  47. Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis.
    Nat Genet. 1995 Sep;11(1):40-4 PMID: 7550312
  48. The role of a positioned nucleosome at the Drosophila melanogaster hsp26 promoter.
    EMBO J. 1995 Oct 2;14(19):4738-46 PMID: 7588603
  49. HSF access to heat shock elements in vivo depends critically on promoter architecture defined by GAGA factor, TFIID, and RNA polymerase II binding sites.
    Genes Dev. 1995 Nov 15;9(22):2756-69 PMID: 7590251
  50. Repression and activation by multiprotein complexes that alter chromatin structure.
    Genes Dev. 1996 Apr 15;10(8):905-20 PMID: 8608939
  51. White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein.
    EMBO J. 1996 Apr 1;15(7):1650-7 PMID: 8612589
  52. Tissue-specific factors additively increase the probability of the all-or-none formation of a hypersensitive site.
    EMBO J. 1996 May 15;15(10):2496-507 PMID: 8665857
  53. Nitrogen metabolite signalling involves the C-terminus and the GATA domain of the Aspergillus transcription factor AREA and the 3' untranslated region of its mRNA.
    EMBO J. 1996 Jun 3;15(11):2791-801 PMID: 8654376
  54. Carbon catabolite repression of xylanase I (xyn1) gene expression in Trichoderma reesei.
    Mol Microbiol. 1996 Sep;21(6):1273-81 PMID: 8898395
  55. Remodeling chromatin structures for transcription: what happens to the histones?
    Bioessays. 1996 Nov;18(11):875-84 PMID: 8939065
  56. White collar 2, a partner in blue-light signal transduction, controlling expression of light-regulated genes in Neurospora crassa.
    EMBO J. 1997 Jan 2;16(1):98-109 PMID: 9009271
  57. Transcription factors vs nucleosomes: regulation of the PHO5 promoter in yeast.
    Trends Biochem Sci. 1997 Mar;22(3):93-7 PMID: 9066259
  58. RNA polymerase II holoenzyme recruitment is sufficient to remodel chromatin at the yeast PHO5 promoter.
    Cell. 1997 Apr 4;89(1):55-62 PMID: 9094714
  59. Genetic regulation of nitrogen metabolism in the fungi.
    Microbiol Mol Biol Rev. 1997 Mar;61(1):17-32 PMID: 9106362
  60. Chromatin remodeling by transcriptional activation domains in a yeast episome.
    J Biol Chem. 1997 Apr 25;272(17):11526-34 PMID: 9111067
  61. The distal GATA sequences of the sid1 promoter of Ustilago maydis mediate iron repression of siderophore production and interact directly with Urbs1, a GATA family transcription factor.
    EMBO J. 1997 Apr 1;16(7):1742-50 PMID: 9130718
  62. Subtle hydrophobic interactions between the seventh residue of the zinc finger loop and the first base of an HGATAR sequence determine promoter-specific recognition by the Aspergillus nidulans GATA factor AreA.
    EMBO J. 1997 Jul 1;16(13):3974-86 PMID: 9233807
  63. Transcription factor access to chromatin.
    Nucleic Acids Res. 1997 Sep 15;25(18):3559-63 PMID: 9278473
  64. Nucleosome transactions on the promoters of the yeast GAL and PHO genes.
    J Biol Chem. 1997 Oct 24;272(43):26795-8 PMID: 9341105
  65. end-1 encodes an apparent GATA factor that specifies the endoderm precursor in Caenorhabditis elegans embryos.
    Genes Dev. 1997 Nov 1;11(21):2883-96 PMID: 9353257
  66. A rapid method for chromatin structure analysis in the filamentous fungus Aspergillus nidulans.
    Nucleic Acids Res. 1997 Oct 1;25(19):3955-6 PMID: 9380523
  67. Factors affecting Saccharomyces cerevisiae ADH2 chromatin remodeling and transcription.
    J Biol Chem. 1997 Dec 5;272(49):30828-34 PMID: 9388226
  68. Zinc fingers are sticking together.
    Trends Biochem Sci. 1998 Jan;23(1):1-4 PMID: 9478126
  69. The regulator of nitrate assimilation in ascomycetes is a dimer which binds a nonrepeated, asymmetrical sequence.
    Mol Cell Biol. 1998 Mar;18(3):1339-48 PMID: 9488449
  70. Characterization of the Aspergillus nidulans nmrA gene involved in nitrogen metabolite repression.
    J Bacteriol. 1998 Apr;180(7):1973-7 PMID: 9537404
  71. The solution structure of a fungal AREA protein-DNA complex: an alternative binding mode for the basic carboxyl tail of GATA factors.
    J Mol Biol. 1998 Apr 3;277(3):605-20 PMID: 9533883
  72. The solution structure of the Leu22-->Val mutant AREA DNA binding domain complexed with a TGATAG core element defines a role for hydrophobic packing in the determination of specificity.
    J Mol Biol. 1998 Apr 3;277(3):621-34 PMID: 9533884
  73. High sequence specificity of micrococcal nuclease.
    Nucleic Acids Res. 1981 Jun 25;9(12):2659-73 PMID: 6269057
  74. A method for the selection of deletion mutations in the L-proline catabolism gene cluster of Aspergillus nidulans.
    Genet Res. 1981 Oct;38(2):171-95 PMID: 7035292
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1093/emboj/18.6.1584
Published
1999-03-15
Pages
1584-97
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1171246
Subset
IM
Corrections
ErratumIn
-
External Links
PubMed source DOI: 10.1093/emboj/18.6.1584 PMC Full Text View journal details
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