Home LiteratureArticle Details
PMID: 9774346 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Nucleosome structure of the yeast CHA1 promoter: analysis of activation-dependent chromatin remodeling of an RNA-polymerase-II-transcribed gene in TBP and RNA pol II mutants defective in vivo in response to acidic activators.

The EMBO journal ·Vol. 17 ·No. 20 ·1998-10-15 ·Pages 6028-38

Moreira JM, Holmberg S

Abstract

The Saccharomyces cerevisiae CHA1 gene encodes the catabolic L-serine (L-threonine) dehydratase. We have previously shown that the transcriptional activator protein Cha4p mediates serine/threonine induction of CHA1 expression. We used accessibility to micrococcal nuclease and DNase I to determine the in vivo chromatin structure of the CHA1 chromosomal locus, both in the non-induced state and upon induction. Upon activation, a precisely positioned nucleosome (nuc-1) occluding the TATA box and the transcription start site is removed. A strain devoid of Cha4p showed no chromatin alteration under inducing conditions. Five yeast TBP mutants defective in different steps in activated transcription abolished CHA1 expression, but failed to affect induction-dependent chromatin rearrangement of the promoter region. Progressive truncations of the RNA polymerase II C-terminal domain caused a progressive reduction in CHA1 transcription, but no difference in chromatin remodeling. Analysis of swi1, swi3, snf5 and snf6, as well as gcn5, ada2 and ada3 mutants, suggested that neither the SWI/SNF complex nor the ADA/GCN5 complex is involved in efficient activation and/or remodeling of the CHA1 promoter. Interestingly, in a sir4 deletion strain, repression of CHA1 is partly lost and activator-independent remodeling of nuc-1 is observed. We propose a model for CHA1 activation based on promoter remodeling through interactions of Cha4p with chromatin components other than basal factors and associated proteins.

MeSH Terms
Chromatin/genetics,metabolism DNA-Binding Proteins/physiology Fungal Proteins/physiology Genes, Fungal L-Serine Dehydratase/chemistry,genetics,physiology Mutation Nucleosomes/chemistry,genetics,metabolism Promoter Regions, Genetic RNA Polymerase II/deficiency,physiology Saccharomyces cerevisiae Saccharomyces cerevisiae Proteins Serine/metabolism Silent Information Regulator Proteins, Saccharomyces cerevisiae TATA Box/genetics,physiology TATA-Box Binding Protein Threonine Dehydratase/chemistry,genetics,physiology Trans-Activators/physiology Transcription Factors/physiology
Chemicals
CHA4 protein, S cerevisiae Chromatin DNA-Binding Proteins Fungal Proteins Nucleosomes SIR4 protein, S cerevisiae Saccharomyces cerevisiae Proteins Silent Information Regulator Proteins, Saccharomyces cerevisiae TATA-Box Binding Protein Trans-Activators Transcription Factors Serine RNA Polymerase II L-Serine Dehydratase Threonine Dehydratase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Moreira J M
Department of Genetics, Institute of Molecular Biology, University of Copenhagen, Oster Farimagsgade 2A, DK-1353 Copenhagen K, Denmark.
Holmberg S
References (75)
75 references, click to expand
  1. ADA1, a novel component of the ADA/GCN5 complex, has broader effects than GCN5, ADA2, or ADA3.
    Mol Cell Biol. 1997 Jun;17(6):3220-8 PMID: 9154821
  2. A unique structure at the carboxyl terminus of the largest subunit of eukaryotic RNA polymerase II.
    Proc Natl Acad Sci U S A. 1985 Dec;82(23):7934-8 PMID: 2999785
  3. RNA polymerase II carboxy-terminal domain contributes to the response to multiple acidic activators in vitro.
    Genes Dev. 1991 Dec;5(12B):2431-40 PMID: 1752437
  4. 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
  5. SWI2/SNF2 and related proteins: ATP-driven motors that disrupt protein-DNA interactions?
    Cell. 1997 Mar 21;88(6):737-40 PMID: 9118215
  6. Occurrence of a catabolic L-serine (L-threonine) deaminase in Saccharomyces cerevisiae.
    Eur J Biochem. 1982 Apr;123(3):571-6 PMID: 7042346
  7. 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
  8. Architectural specificity in chromatin structure at the TATA box in vivo: nucleosome displacement upon beta-phaseolin gene activation.
    Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4772-7 PMID: 9539814
  9. Identification of native complexes containing the yeast coactivator/repressor proteins NGG1/ADA3 and ADA2.
    J Biol Chem. 1997 Feb 28;272(9):5571-8 PMID: 9038164
  10. Chromatin remodeling during Saccharomyces cerevisiae ADH2 gene activation.
    Mol Cell Biol. 1996 May;16(5):1978-88 PMID: 8628264
  11. A highly conserved domain of RNA polymerase II shares a functional element with acidic activation domains of upstream transcription factors.
    Mol Cell Biol. 1994 Nov;14(11):7507-16 PMID: 7935466
  12. Functional redundancy and structural polymorphism in the large subunit of RNA polymerase II.
    Cell. 1987 Sep 11;50(6):909-15 PMID: 3304659
  13. Binding of general transcription factor TFIIB to an acidic activating region.
    Nature. 1991 Oct 10;353(6344):569-71 PMID: 1922364
  14. A simple method for generating single-stranded DNA probes labeled to high activities.
    Nucleic Acids Res. 1990 Oct 25;18(20):6157-8 PMID: 2235518
  15. Specific interaction between the nonphosphorylated form of RNA polymerase II and the TATA-binding protein.
    Cell. 1992 May 29;69(5):871-81 PMID: 1591781
  16. Transcription-induced nucleosome 'splitting': an underlying structure for DNase I sensitive chromatin.
    EMBO J. 1991 Mar;10(3):607-15 PMID: 2001676
  17. Modifiers of position effect are shared between telomeric and silent mating-type loci in S. cerevisiae.
    Cell. 1991 Sep 20;66(6):1279-87 PMID: 1913809
  18. Stimulation of RNA polymerase II transcription initiation by recruitment of TBP in vivo.
    Nature. 1995 Apr 27;374(6525):822-3 PMID: 7723829
  19. Facilitated binding of TATA-binding protein to nucleosomal DNA.
    Nature. 1994 Aug 11;370(6489):481-5 PMID: 8047170
  20. The TBP-TFIIA interaction in the response to acidic activators in vivo.
    Science. 1995 Jul 7;269(5220):75-8 PMID: 7604282
  21. Binding of transcription factor TFIID to the major late promoter during in vitro nucleosome assembly potentiates subsequent initiation by RNA polymerase II.
    Cell. 1987 Nov 20;51(4):613-22 PMID: 3677170
  22. ADA5/SPT20 links the ADA and SPT genes, which are involved in yeast transcription.
    Mol Cell Biol. 1996 Jun;16(6):3197-205 PMID: 8649430
  23. Role for ADA/GCN5 products in antagonizing chromatin-mediated transcriptional repression.
    Mol Cell Biol. 1997 Nov;17(11):6212-22 PMID: 9343382
  24. Chromatin structure of the yeast FBP1 gene: transcription-dependent changes in the regulatory and coding regions.
    Yeast. 1993 Nov;9(11):1229-40 PMID: 8109172
  25. Molecular genetics of serine and threonine catabolism in Saccharomyces cerevisiae.
    Genetics. 1988 Jul;119(3):527-34 PMID: 2841185
  26. Role of nucleosomal cores and histone H1 in regulation of transcription by RNA polymerase II.
    Science. 1991 Oct 11;254(5029):238-45 PMID: 1718039
  27. A nucleosome-dependent static loop potentiates estrogen-regulated transcription from the Xenopus vitellogenin B1 promoter in vitro.
    EMBO J. 1993 Feb;12(2):423-33 PMID: 8440235
  28. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation.
    Cell. 1996 Mar 22;84(6):843-51 PMID: 8601308
  29. The relationship of regulatory proteins and DNase I hypersensitive sites in the yeast GAL1-10 genes.
    Nucleic Acids Res. 1985 Dec 9;13(23):8409-23 PMID: 3909104
  30. Chromatin remodeling machines: similar motors, ulterior motives.
    Trends Biochem Sci. 1998 Jan;23(1):20-5 PMID: 9478131
  31. Recruiting TATA-binding protein to a promoter: transcriptional activation without an upstream activator.
    Mol Cell Biol. 1995 Oct;15(10):5757-61 PMID: 7565728
  32. Comparative amino acid sequence analysis of the C6 zinc cluster family of transcriptional regulators.
    Nucleic Acids Res. 1996 Dec 1;24(23):4599-607 PMID: 8967907
  33. DNase I sensitivity of the chromatin of the yeast SUC2 gene for invertase.
    Mol Gen Genet. 1986 Dec;205(3):422-7 PMID: 3550382
  34. The amino-terminal tails of the core histones and the translational position of the TATA box determine TBP/TFIIA association with nucleosomal DNA.
    Nucleic Acids Res. 1995 Nov 25;23(22):4557-64 PMID: 8524642
  35. Nuclease hypersensitive regions with adjacent positioned nucleosomes mark the gene boundaries of the PHO5/PHO3 locus in yeast.
    EMBO J. 1986 Oct;5(10):2681-7 PMID: 3023055
  36. RNA polymerase II C-terminal repeat influences response to transcriptional enhancer signals.
    Nature. 1990 Oct 4;347(6292):491-4 PMID: 2215664
  37. Basal components of the transcription apparatus (RNA polymerase II, TATA-binding protein) contain activation domains: is the repetitive C-terminal domain (CTD) of RNA polymerase II a "portable enhancer domain"?
    Mol Reprod Dev. 1994 Oct;39(2):215-25 PMID: 7826625
  38. Nucleoprotein hybridization: a method for isolating active and inactive genes as chromatin.
    Nucleic Acids Res. 1991 Mar 25;19(6):1325-36 PMID: 2030947
  39. Characterization of physical interactions of the putative transcriptional adaptor, ADA2, with acidic activation domains and TATA-binding protein.
    J Biol Chem. 1995 Aug 18;270(33):19337-44 PMID: 7642611
  40. Mechanisms of transcriptional activation in vivo: two steps forward.
    Trends Genet. 1996 Aug;12(8):311-5 PMID: 8783941
  41. Upstream activation sequence-dependent alteration of chromatin structure and transcription activation of the yeast GAL1-GAL10 genes.
    Mol Cell Biol. 1989 Apr;9(4):1721-32 PMID: 2657404
  42. The role of a positioned nucleosome at the Drosophila melanogaster hsp26 promoter.
    EMBO J. 1995 Oct 2;14(19):4738-46 PMID: 7588603
  43. Cha4p of Saccharomyces cerevisiae activates transcription via serine/threonine response elements.
    Genetics. 1996 Oct;144(2):467-78 PMID: 8889513
  44. Direct and selective binding of an acidic transcriptional activation domain to the TATA-box factor TFIID.
    Nature. 1990 Jun 28;345(6278):783-6 PMID: 2193231
  45. Transcriptional activation: a complex puzzle with few easy pieces.
    Cell. 1994 Apr 8;77(1):5-8 PMID: 8156597
  46. Replication and segregation of plasmids containing cis-acting regulatory sites of silent mating-type genes in Saccharomyces cerevisiae are controlled by the SIR genes.
    Mol Cell Biol. 1987 Dec;7(12):4225-37 PMID: 3325822
  47. A functional role for nucleosomes in the repression of a yeast promoter.
    EMBO J. 1991 Feb;10(2):361-8 PMID: 1899374
  48. A new class of activation-defective TATA-binding protein mutants: evidence for two steps of transcriptional activation in vivo.
    Mol Cell Biol. 1996 Aug;16(8):4456-64 PMID: 8754846
  49. Contact with a component of the polymerase II holoenzyme suffices for gene activation.
    Cell. 1995 May 5;81(3):359-68 PMID: 7736588
  50. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection.
    Trends Genet. 1992 Nov;8(11):387-91 PMID: 1332230
  51. Silent information regulator protein complexes in Saccharomyces cerevisiae: a SIR2/SIR4 complex and evidence for a regulatory domain in SIR4 that inhibits its interaction with SIR3.
    Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2186-91 PMID: 9122169
  52. The chromatin structure of specific genes: II. Disruption of chromatin structure during gene activity.
    Cell. 1979 Apr;16(4):807-14 PMID: 455450
  53. Activation domains of stably bound GAL4 derivatives alleviate repression of promoters by nucleosomes.
    Cell. 1991 Feb 8;64(3):533-44 PMID: 1991320
  54. ADA3, a putative transcriptional adaptor, consists of two separable domains and interacts with ADA2 and GCN5 in a trimeric complex.
    Mol Cell Biol. 1995 Mar;15(3):1203-9 PMID: 7862114
  55. Yeast alpha 2 repressor positions nucleosomes in TRP1/ARS1 chromatin.
    Mol Cell Biol. 1990 May;10(5):2247-60 PMID: 2183026
  56. A regulatory element in the CHA1 promoter which confers inducibility by serine and threonine on Saccharomyces cerevisiae genes.
    Mol Cell Biol. 1993 Dec;13(12):7604-11 PMID: 8246977
  57. The presence of nucleosomes on a DNA template prevents initiation by RNA polymerase II in vitro.
    Cell. 1986 Apr 11;45(1):95-104 PMID: 3955658
  58. Protein/DNA architecture of the DNase I hypersensitive region of the Drosophila hsp26 promoter.
    EMBO J. 1988 Jul;7(7):2191-201 PMID: 2901349
  59. A class of activation domains interacts directly with TFIIA and stimulates TFIIA-TFIID-promoter complex assembly.
    Mol Cell Biol. 1995 Nov;15(11):6465-73 PMID: 7565798
  60. Extensive homology among the largest subunits of eukaryotic and prokaryotic RNA polymerases.
    Cell. 1985 Sep;42(2):599-610 PMID: 3896517
  61. The general transcription factors of RNA polymerase II.
    Genes Dev. 1996 Nov 1;10(21):2657-83 PMID: 8946909
  62. Fine analysis of the chromatin structure of the yeast SUC2 gene and of its changes upon derepression. Comparison between the chromosomal and plasmid-inserted genes.
    Nucleic Acids Res. 1987 Sep 11;15(17):6937-56 PMID: 2821486
  63. The basics of basal transcription by RNA polymerase II.
    Cell. 1994 Apr 8;77(1):1-3 PMID: 8156586
  64. Transcriptional activation. Tuning-up transcription.
    Curr Biol. 1995 Jan 1;5(1):43-6 PMID: 7697348
  65. Increased recruitment of TATA-binding protein to the promoter by transcriptional activation domains in vivo.
    Science. 1994 Oct 14;266(5183):280-2 PMID: 7939664
  66. Transcription factors vs nucleosomes: regulation of the PHO5 promoter in yeast.
    Trends Biochem Sci. 1997 Mar;22(3):93-7 PMID: 9066259
  67. Recombinant yeast TFIID, a general transcription factor, mediates activation by the gene-specific factor USF in a chromatin assembly assay.
    Proc Natl Acad Sci U S A. 1990 Dec;87(23):9153-7 PMID: 2251256
  68. Nucleosome loss activates yeast downstream promoters in vivo.
    Cell. 1988 Dec 23;55(6):1137-45 PMID: 2849508
  69. Interaction with RAP74 subunit of TFIIF is required for transcriptional activation by serum response factor.
    Nature. 1995 Feb 16;373(6515):632-5 PMID: 7854423
  70. Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines.
    Nature. 1996 Sep 19;383(6597):269-72 PMID: 8805705
  71. Repression and activation by multiprotein complexes that alter chromatin structure.
    Genes Dev. 1996 Apr 15;10(8):905-20 PMID: 8608939
  72. Structural and functional analysis of yeast putative adaptors. Evidence for an adaptor complex in vivo.
    J Biol Chem. 1996 Mar 1;271(9):5237-45 PMID: 8617808
  73. Nucleosomes inhibit the initiation of transcription but allow chain elongation with the displacement of histones.
    Cell. 1987 Apr 24;49(2):203-10 PMID: 3568125
  74. Histone acetylation and transcriptional regulatory mechanisms.
    Genes Dev. 1998 Mar 1;12(5):599-606 PMID: 9499396
  75. Xenopus TFIIIA gene transcription is dependent on cis-element positioning and chromatin structure.
    Mol Cell Biol. 1998 Jul;18(7):3811-8 PMID: 9632765
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1998-10-15
Pages
6028-38
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170929
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com