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PMID: 9372928 Published · ppublish English Journal Article

Sin mutations of histone H3: influence on nucleosome core structure and function.

Molecular and cellular biology ·Vol. 17 ·No. 12 ·1997-12-00 ·Pages 6953-69

Kurumizaka H, Wolffe AP

Abstract

Sin mutations in Saccharomyces cerevisiae alleviate transcriptional defects that result from the inactivation of the yeast SWVI/SNF complex. We have investigated the structural and functional consequences for the nucleosome of Sin mutations in histone H3. We directly test the hypothesis that mutations in histone H3 leading to a SWI/SNF-independent (Sin) phenotype in yeast lead to nucleosomal destabilization. In certain instances this is shown to be true; however, nucleosomal destabilization does not always occur. Topoisomerase I-mediated relaxation of minichromosomes assembled with either mutant histone H3 or wild-type H3 together with histones H2A, H2B, and H4 indicates that DNA is constrained into nucleosomal structures containing either mutant or wild-type proteins. However, nucleosomes containing particular mutant H3 molecules (R116-H and T118-I) are more accessible to digestion by micrococcal nuclease and do not constrain DNA in a precise rotational position, as revealed by digestion with DNase I. This result establishes that Sin mutations in histone H3 located close to the dyad axis can destabilize histone-DNA contacts at the periphery of the nucleosome core. Other nucleosomes containing a distinct mutant H3 molecule (E105-K) associated with a Sin phenotype show very little change in nucleosome structure and stability compared to wild-type nucleosomes. Both mutant and wild-type nucleosomes continue to restrict the binding of either TATA-binding protein/transcription factor IIA (TFIIA) or the RNA polymerase III transcription machinery. Thus, different Sin mutations in histone H3 alter the stability of histone-DNA interactions to various extents in the nucleosome while maintaining the fundamental architecture of the nucleosome and contributing to a common Sin phenotype.

MeSH Terms
Animals Chickens Chromatin/chemistry,genetics DNA, Fungal/metabolism DNA-Binding Proteins/metabolism Fungal Proteins/chemistry,genetics,metabolism Histones/chemistry,genetics,metabolism In Vitro Techniques Mutation Nucleosomes/chemistry,metabolism Phenotype Plasmids/metabolism RNA Polymerase III/metabolism Recombinant Proteins/chemistry,genetics,metabolism Saccharomyces cerevisiae/genetics,metabolism TATA-Box Binding Protein Transcription Factor TFIIA Transcription Factors/metabolism Xenopus laevis
Chemicals
Chromatin DNA, Fungal DNA-Binding Proteins Fungal Proteins Histones Nucleosomes Recombinant Proteins TATA-Box Binding Protein Transcription Factor TFIIA Transcription Factors RNA Polymerase III
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Kurumizaka H
Laboratory of Molecular Embryology, National Institute of Child Health and Human Development, Bethesda, Maryland 20892-5431, USA.
Wolffe A P
References (104)
104 references, click to expand
  1. RPD1 (SIN3/UME4) is required for maximal activation and repression of diverse yeast genes.
    Mol Cell Biol. 1991 Dec;11(12):6306-16 PMID: 1944290
  2. RPD3 encodes a second factor required to achieve maximum positive and negative transcriptional states in Saccharomyces cerevisiae.
    Mol Cell Biol. 1991 Dec;11(12):6317-27 PMID: 1944291
  3. The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10148-52 PMID: 1946434
  4. Nucleosome positioning is determined by the (H3-H4)2 tetramer.
    Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10596-600 PMID: 1961726
  5. Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription.
    Cell. 1992 Feb 7;68(3):573-83 PMID: 1339306
  6. Histones H2A/H2B inhibit the interaction of transcription factor IIIA with the Xenopus borealis somatic 5S RNA gene in a nucleosome.
    Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1229-33 PMID: 1741376
  7. Structure of DNA in a nucleosome core at high salt concentration and at high temperature.
    Biochemistry. 1993 Mar 2;32(8):1895-8 PMID: 8383529
  8. The yeast SNF2/SWI2 protein has DNA-stimulated ATPase activity required for transcriptional activation.
    Genes Dev. 1993 Apr;7(4):583-91 PMID: 8458575
  9. Histone-DNA contacts in a nucleosome core containing a Xenopus 5S rRNA gene.
    Biochemistry. 1993 Jul 13;32(27):6810-4 PMID: 8334114
  10. Preferential and asymmetric interaction of linker histones with 5S DNA in the nucleosome.
    Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6415-9 PMID: 8341648
  11. A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor.
    EMBO J. 1993 Nov;12(11):4279-90 PMID: 8223438
  12. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription.
    Nature. 1993 Nov 11;366(6451):170-4 PMID: 8232556
  13. Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA.
    Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10489-93 PMID: 8248135
  14. Role of the histone amino termini in facilitated binding of a transcription factor, GAL4-AH, to nucleosome cores.
    Mol Cell Biol. 1994 Feb;14(2):970-81 PMID: 8289837
  15. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor.
    Nature. 1994 Feb 10;367(6463):525-32 PMID: 8107823
  16. Nucleosome structural changes due to acetylation.
    J Mol Biol. 1994 Feb 25;236(3):685-90 PMID: 8114086
  17. A multisubunit complex containing the SWI1/ADR6, SWI2/SNF2, SWI3, SNF5, and SNF6 gene products isolated from yeast.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1950-4 PMID: 8127913
  18. A role for histones H2A/H2B in chromatin folding and transcriptional repression.
    Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2339-43 PMID: 8134397
  19. Five SWI/SNF gene products are components of a large multisubunit complex required for transcriptional enhancement.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):2905-8 PMID: 8159677
  20. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex.
    Science. 1994 Jul 1;265(5168):53-60 PMID: 8016655
  21. Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex.
    Nature. 1994 Aug 11;370(6489):477-81 PMID: 8047169
  22. Facilitated binding of TATA-binding protein to nucleosomal DNA.
    Nature. 1994 Aug 11;370(6489):481-5 PMID: 8047170
  23. The establishment of active promoters in chromatin.
    Bioessays. 1994 Aug;16(8):541-7 PMID: 8086003
  24. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p.
    Science. 1996 Apr 19;272(5260):408-11 PMID: 8602529
  25. Repression domain of the yeast global repressor Tup1 interacts directly with histones H3 and H4.
    Genes Dev. 1996 May 15;10(10):1247-59 PMID: 8675011
  26. Acetylation of histone H4 plays a primary role in enhancing transcription factor binding to nucleosomal DNA in vitro.
    EMBO J. 1996 May 15;15(10):2508-18 PMID: 8665858
  27. Thermodynamic studies of the core histones: pH and ionic strength effects on the stability of the (H3-H4)/(H3-H4)2 system.
    Biochemistry. 1996 Feb 13;35(6):2037-46 PMID: 8639689
  28. Regulation of gene expression by nucleosomes.
    Curr Opin Genet Dev. 1996 Apr;6(2):164-70 PMID: 8722172
  29. A p300/CBP-associated factor that competes with the adenoviral oncoprotein E1A.
    Nature. 1996 Jul 25;382(6589):319-24 PMID: 8684459
  30. Differential association of HMG1 and linker histones B4 and H1 with dinucleosomal DNA: structural transitions and transcriptional repression.
    EMBO J. 1996 Sep 16;15(18):4959-69 PMID: 8890169
  31. Functional domains for assembly of histones H3 and H4 into the chromatin of Xenopus embryos.
    Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):12780-5 PMID: 8917496
  32. The transcriptional coactivators p300 and CBP are histone acetyltransferases.
    Cell. 1996 Nov 29;87(5):953-9 PMID: 8945521
  33. RSC, an essential, abundant chromatin-remodeling complex.
    Cell. 1996 Dec 27;87(7):1249-60 PMID: 8980231
  34. Folding of the DNA double helix in chromatin-like structures from simian virus 40.
    Proc Natl Acad Sci U S A. 1975 May;72(5):1843-7 PMID: 168578
  35. The organization of histones and DNA in chromatin: evidence for an arginine-rich histone kernel.
    Cell. 1976 Jul;8(3):333-47 PMID: 986252
  36. Action of micrococcal nuclease on chromatin and the location of histone H1.
    J Mol Biol. 1977 Jan 25;109(3):393-404 PMID: 833849
  37. Kinetic analysis of deoxyribonuclease I cleavages in the nucleosome core: evidence for a DNA superhelix.
    J Mol Biol. 1978 Sep 15;124(2):391-420 PMID: 568667
  38. The histone core complex: an octamer assembled by two sets of protein-protein interactions.
    Biochemistry. 1978 Nov 14;17(23):4955-64 PMID: 718868
  39. A nuclear extract of Xenopus laevis oocytes that accurately transcribes 5S RNA genes.
    Cell. 1978 Nov;15(3):1077-86 PMID: 569551
  40. Assembly of newly replicated chromatin.
    Cell. 1978 Nov;15(3):969-77 PMID: 103629
  41. Stable nucleosome positioning and complete repression by the yeast alpha 2 repressor are disrupted by amino-terminal mutations in histone H4.
    Genes Dev. 1992 Mar;6(3):411-25 PMID: 1547940
  42. Mobile nucleosomes--a general behavior.
    EMBO J. 1992 Aug;11(8):2951-9 PMID: 1639066
  43. Yeast SNF2/SWI2, SNF5, and SNF6 proteins function coordinately with the gene-specific transcriptional activators GAL4 and Bicoid.
    Genes Dev. 1992 Sep;6(9):1707-15 PMID: 1516829
  44. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection.
    Trends Genet. 1992 Nov;8(11):387-91 PMID: 1332230
  45. Roles of SWI1, SWI2, and SWI3 proteins for transcriptional enhancement by steroid receptors.
    Science. 1992 Dec 4;258(5088):1598-604 PMID: 1360703
  46. Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure.
    Genes Dev. 1992 Dec;6(12A):2288-98 PMID: 1459453
  47. A positive role for histone acetylation in transcription factor access to nucleosomal DNA.
    Cell. 1993 Jan 15;72(1):73-84 PMID: 8422685
  48. Transcriptional repression in Saccharomyces cerevisiae by a SIN3-LexA fusion protein.
    Mol Cell Biol. 1993 Mar;13(3):1805-14 PMID: 8441414
  49. The SNF/SWI family of global transcriptional activators.
    Curr Opin Cell Biol. 1994 Jun;6(3):396-402 PMID: 7917331
  50. Transcriptional activation. Switched-on chromatin.
    Curr Biol. 1994 Jun 1;4(6):525-8 PMID: 7922373
  51. Yeast histone H4 and H3 N-termini have different effects on the chromatin structure of the GAL1 promoter.
    EMBO J. 1995 Apr 3;14(7):1468-77 PMID: 7729422
  52. Chromatin remodeling by GAGA factor and heat shock factor at the hypersensitive Drosophila hsp26 promoter in vitro.
    EMBO J. 1995 Apr 18;14(8):1727-36 PMID: 7737124
  53. A human protein with homology to Saccharomyces cerevisiae SNF5 interacts with the potential helicase hbrm.
    Nucleic Acids Res. 1995 Apr 11;23(7):1127-32 PMID: 7739891
  54. Nucleosomal anatomy--where are the histones?
    Bioessays. 1995 Feb;17(2):161-70 PMID: 7748166
  55. The SWI-SNF complex: a chromatin remodeling machine?
    Trends Biochem Sci. 1995 Apr;20(4):143-6 PMID: 7770913
  56. Energy-dependent chromatin accessibility and nucleosome mobility in a cell-free system.
    EMBO J. 1995 May 15;14(10):2209-16 PMID: 7774579
  57. A positive role for nucleosome mobility in the transcriptional activity of chromatin templates: restriction by linker histones.
    EMBO J. 1995 Aug 1;14(15):3752-65 PMID: 7641694
  58. The TAF(II)250 subunit of TFIID has histone acetyltransferase activity.
    Cell. 1996 Dec 27;87(7):1261-70 PMID: 8980232
  59. Characterization of monoclonal antibodies raised against p300: both p300 and CBP are present in intracellular TBP complexes.
    J Virol. 1997 Feb;71(2):1726-31 PMID: 8995708
  60. 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
  61. Effects of Sin- versions of histone H4 on yeast chromatin structure and function.
    EMBO J. 1997 Apr 15;16(8):2086-95 PMID: 9155034
  62. Histone acetylation: influence on transcription, nucleosome mobility and positioning, and linker histone-dependent transcriptional repression.
    EMBO J. 1997 Apr 15;16(8):2096-107 PMID: 9155035
  63. Remodeling of regulatory nucleoprotein complexes on the Xenopus hsp70 promoter during meiotic maturation of the Xenopus oocyte.
    EMBO J. 1997 Jul 16;16(14):4361-73 PMID: 9250680
  64. Chromatin reconstituted from tandemly repeated cloned DNA fragments and core histones: a model system for study of higher order structure.
    Cell. 1985 Oct;42(3):799-808 PMID: 2996776
  65. Genomic organization and nucleotide sequence of two distinct histone gene clusters from Xenopus laevis. Identification of novel conserved upstream sequence elements.
    J Mol Biol. 1985 Oct 5;185(3):479-99 PMID: 3863963
  66. A bacteriophage RNA polymerase transcribes through a Xenopus 5S RNA gene transcription complex without disrupting it.
    Cell. 1986 Feb 14;44(3):381-9 PMID: 3943130
  67. Structural analysis of a triple complex between the histone octamer, a Xenopus gene for 5S RNA and transcription factor IIIA.
    EMBO J. 1985 Dec 16;4(13A):3473-82 PMID: 4092686
  68. Suppressors of SNF2 mutations restore invertase derepression and cause temperature-sensitive lethality in yeast.
    Genetics. 1986 Apr;112(4):741-53 PMID: 3514373
  69. 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
  70. Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements.
    EMBO J. 1986 Oct;5(10):2689-96 PMID: 3536481
  71. Structural details of an adenine tract that does not cause DNA to bend.
    Nature. 1988 Feb 4;331(6155):455-7 PMID: 3340190
  72. Changes in histone gene dosage alter transcription in yeast.
    Genes Dev. 1988 Feb;2(2):150-9 PMID: 2834270
  73. Helical repeat and linking number of surface-wrapped DNA.
    Science. 1988 Jul 15;241(4863):323-7 PMID: 3388041
  74. Depletion of histone H4 and nucleosomes activates the PHO5 gene in Saccharomyces cerevisiae.
    EMBO J. 1988 Jul;7(7):2221-8 PMID: 3046934
  75. Extremely conserved histone H4 N terminus is dispensable for growth but essential for repressing the silent mating loci in yeast.
    Cell. 1988 Oct 7;55(1):27-39 PMID: 3048701
  76. Nucleosome loss activates yeast downstream promoters in vivo.
    Cell. 1988 Dec 23;55(6):1137-45 PMID: 2849508
  77. Yeast alpha 2 repressor positions nucleosomes in TRP1/ARS1 chromatin.
    Mol Cell Biol. 1990 May;10(5):2247-60 PMID: 2183026
  78. DNA and protein determinants of nucleosome positioning on sea urchin 5S rRNA gene sequences in vitro.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5724-8 PMID: 2377610
  79. Genetic evidence for an interaction between SIR3 and histone H4 in the repression of the silent mating loci in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1990 Aug;87(16):6286-90 PMID: 2201024
  80. The structure of DNA in a nucleosome.
    Proc Natl Acad Sci U S A. 1990 Oct;87(19):7405-9 PMID: 2170977
  81. The Saccharomyces cerevisiae SIN3 gene, a negative regulator of HO, contains four paired amphipathic helix motifs.
    Mol Cell Biol. 1990 Nov;10(11):5927-36 PMID: 2233725
  82. A functional interaction between the C-terminal domain of RNA polymerase II and the negative regulator SIN1.
    Cell. 1991 Mar 22;64(6):1135-43 PMID: 2004420
  83. Chromatosome positioning on assembled long chromatin. Linker histones affect nucleosome placement on 5 S rDNA.
    J Mol Biol. 1991 Jul 5;220(1):89-100 PMID: 2067021
  84. A negative regulator of HO transcription, SIN1 (SPT2), is a nonspecific DNA-binding protein related to HMG1.
    Mol Cell Biol. 1991 Aug;11(8):4135-46 PMID: 2072912
  85. 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
  86. Role of chromatin and Xenopus laevis heat shock transcription factor in regulation of transcription from the X. laevis hsp70 promoter in vivo.
    Mol Cell Biol. 1995 Nov;15(11):6013-24 PMID: 7565754
  87. Disruption of reconstituted nucleosomes. The effect of particle concentration, MgCl2 and KCl concentration, the histone tails, and temperature.
    J Biol Chem. 1995 Nov 17;270(46):27399-402 PMID: 7499192
  88. Interplay between nucleosomes and transcription factors at the yeast PHO5 promoter.
    Semin Cell Biol. 1995 Aug;6(4):177-83 PMID: 8562909
  89. Amino acid substitutions in the structured domains of histones H3 and H4 partially relieve the requirement of the yeast SWI/SNF complex for transcription.
    Genes Dev. 1995 Nov 15;9(22):2770-9 PMID: 7590252
  90. 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
  91. Steroid hormone receptors: many actors in search of a plot.
    Cell. 1995 Dec 15;83(6):851-7 PMID: 8521509
  92. Purification and properties of an ATP-dependent nucleosome remodeling factor.
    Cell. 1995 Dec 15;83(6):1011-20 PMID: 8521501
  93. RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling.
    Cell. 1996 Jan 26;84(2):235-44 PMID: 8565069
  94. DNA-binding properties of the yeast SWI/SNF complex.
    Nature. 1996 Feb 29;379(6568):844-7 PMID: 8587611
  95. 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
  96. A new procedure for purifying histone pairs H2A + H2B and H3 + H4 from chromatin using hydroxylapatite.
    Nucleic Acids Res. 1979 Feb;6(2):689-96 PMID: 424310
  97. Silver staining of proteins in polyacrylamide gels.
    Anal Biochem. 1981 Nov 15;118(1):197-203 PMID: 6175245
  98. Eukaryotic RNA polymerase II binds to nucleosome cores from transcribed genes.
    Nature. 1983 Feb 10;301(5900):482-8 PMID: 6823327
  99. Structural features of a phased nucleosome core particle.
    Proc Natl Acad Sci U S A. 1983 Jan;80(1):51-5 PMID: 6572008
  100. Iron(II) EDTA used to measure the helical twist along any DNA molecule.
    Science. 1985 Nov 8;230(4726):679-81 PMID: 2996145
  101. Structure of subnucleosomal particles. Tetrameric (H3/H4)2 146 base pair DNA and hexameric (H3/H4)2(H2A/H2B)1 146 base pair DNA complexes.
    Biochemistry. 1985 Jul 30;24(16):4435-50 PMID: 4052408
  102. Histone contributions to the structure of DNA in the nucleosome.
    Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6829-33 PMID: 1650485
  103. The histone core exerts a dominant constraint on the structure of DNA in a nucleosome.
    Biochemistry. 1991 Aug 27;30(34):8434-40 PMID: 1653013
  104. Superhelical stress and nucleosome-mediated repression of 5S RNA gene transcription in vitro.
    EMBO J. 1991 Nov;10(11):3419-28 PMID: 1717265
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1997-12-00
Pages
6953-69
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC232553
Subset
IM
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