Home LiteratureArticle Details
PMID: 10364158 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Cell cycle-regulated histone acetylation required for expression of the yeast HO gene.

Genes & development ·Vol. 13 ·No. 11 ·1999-06-01 ·Pages 1412-21

Krebs JE, Kuo MH, Allis CD, Peterson CL

Abstract

Expression of the yeast HO gene in late G1 of the cell cycle requires the SWI/SNF chromatin remodeling complex, the Gcn5p histone acetyltransferase, and two different sequence-specific transcriptional activators, Swi5p and Swi4p/Swi6p. We have used chromatin immunoprecipitation assays to investigate the role of each of these trans-acting factors in establishing a cell cycle-regulated domain of histone acetylation surrounding the HO upstream regulatory region. We detect a approximately 1-kb domain of H3 and H4 acetylation that is established in mid-G1, prior to and independent of HO transcription, which then declines with kinetics similar to inactivation of HO. This cell cycle burst of histone acetylation requires Gcn5p, SWI/SNF, and the Swi5p activator, but occurs in the absence of the Swi4p activator. We also find that inactivation of the Sin3p/Rpd3p deacetylase complex leads to a high level of acetylation at the HO locus throughout the cell cycle. We propose a sequential model for activation of HO in which the Swi5p-dependent recruitment of the Gcn5p acetyltransferase requires chromatin remodeling events by the SWI/SNF complex.

MeSH Terms
Acetylation Cell Cycle Cell Cycle Proteins DNA-Binding Proteins Deoxyribonucleases, Type II Site-Specific/genetics Fungal Proteins/metabolism G1 Phase Gene Expression Regulation, Fungal Genes, Fungal Histone Deacetylases/metabolism Histones/metabolism Nucleosomes Promoter Regions, Genetic Protein Kinases/metabolism Repressor Proteins S Phase Saccharomyces cerevisiae/enzymology,genetics Saccharomyces cerevisiae Proteins Transcription Factors/metabolism
Chemicals
Cell Cycle Proteins DNA-Binding Proteins Fungal Proteins Histones Nucleosomes Repressor Proteins SIN3 protein, S cerevisiae SWI5 protein, S cerevisiae Saccharomyces cerevisiae Proteins Transcription Factors Protein Kinases HO protein, S cerevisiae SCEI protein, S cerevisiae Deoxyribonucleases, Type II Site-Specific RPD3 protein, S cerevisiae Histone Deacetylases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Krebs J E
Program in Molecular Medicine and Department of Biochemistry and Molecular Biology, University of Massachusetts Medical Center, Worcester, Massachusetts 01605, USA.
Kuo M H
Allis C D
Peterson C L
References (61)
61 references, click to expand
  1. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  2. Mutations in chromatin components suppress a defect of Gcn5 protein in Saccharomyces cerevisiae.
    Mol Cell Biol. 1998 Feb;18(2):1049-54 PMID: 9448002
  3. 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
  4. 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
  5. SWI5 instability may be necessary but is not sufficient for asymmetric HO expression in yeast.
    Genes Dev. 1993 Mar;7(3):517-28 PMID: 8449406
  6. Regulating the HO endonuclease in yeast.
    Curr Opin Genet Dev. 1993 Apr;3(2):286-94 PMID: 8504254
  7. Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins.
    Cell. 1993 Sep 24;74(6):993-1007 PMID: 8402888
  8. 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
  9. Epistasis analysis of suppressor mutations that allow HO expression in the absence of the yeast SW15 transcriptional activator.
    Genetics. 1994 Mar;136(3):781-8 PMID: 8005433
  10. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex.
    Science. 1994 Jul 1;265(5168):53-60 PMID: 8016655
  11. Facilitated binding of TATA-binding protein to nucleosomal DNA.
    Nature. 1994 Aug 11;370(6489):481-5 PMID: 8047170
  12. Role of yeast SNF and SWI proteins in transcriptional activation.
    Cold Spring Harb Symp Quant Biol. 1993;58:257-63 PMID: 7956037
  13. Genetic interactions between SIN3 mutations and the Saccharomyces cerevisiae transcriptional activators encoded by MCM1, STE12, and SWI1.
    Mol Gen Genet. 1994 Dec 15;245(6):675-85 PMID: 7830715
  14. Cdc6 is an unstable protein whose de novo synthesis in G1 is important for the onset of S phase and for preventing a 'reductional' anaphase in the budding yeast Saccharomyces cerevisiae.
    EMBO J. 1995 Aug 1;14(15):3788-99 PMID: 7641697
  15. Switching transcription on and off during the yeast cell cycle: Cln/Cdc28 kinases activate bound transcription factor SBF (Swi4/Swi6) at start, whereas Clb/Cdc28 kinases displace it from the promoter in G2.
    Genes Dev. 1996 Jan 15;10(2):129-41 PMID: 8566747
  16. Binding to the yeast SwI4,6-dependent cell cycle box, CACGAAA, is cell cycle regulated in vivo.
    Nucleic Acids Res. 1996 Feb 15;24(4):558-65 PMID: 8604294
  17. 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
  18. Mother cell-specific HO expression in budding yeast depends on the unconventional myosin myo4p and other cytoplasmic proteins.
    Cell. 1996 Mar 8;84(5):687-97 PMID: 8625407
  19. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells.
    Cell. 1996 Mar 8;84(5):699-709 PMID: 8625408
  20. Identification of asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene.
    Cell. 1996 Mar 8;84(5):711-22 PMID: 8625409
  21. EGT2 gene transcription is induced predominantly by Swi5 in early G1.
    Mol Cell Biol. 1996 Jul;16(7):3264-74 PMID: 8668141
  22. Multiple SWItches to turn on chromatin?
    Curr Opin Genet Dev. 1996 Apr;6(2):171-5 PMID: 8722173
  23. Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines.
    Nature. 1996 Sep 19;383(6597):269-72 PMID: 8805705
  24. The transcription factor Swi5 regulates expression of the cyclin kinase inhibitor p40SIC1.
    Mol Cell Biol. 1996 Oct;16(10):5701-7 PMID: 8816483
  25. SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast.
    Genes Dev. 1997 Jan 1;11(1):83-93 PMID: 9000052
  26. The Swi5 transcription factor of Saccharomyces cerevisiae has a role in exit from mitosis through induction of the cdk-inhibitor Sic1 in telophase.
    Genetics. 1997 Jan;145(1):85-96 PMID: 9017392
  27. Histone acetyltransferase activity and interaction with ADA2 are critical for GCN5 function in vivo.
    EMBO J. 1997 Feb 3;16(3):555-65 PMID: 9034338
  28. Histone acetyltransferase activity of yeast Gcn5p is required for the activation of target genes in vivo.
    Genes Dev. 1998 Mar 1;12(5):627-39 PMID: 9499399
  29. Critical residues for histone acetylation by Gcn5, functioning in Ada and SAGA complexes, are also required for transcriptional function in vivo.
    Genes Dev. 1998 Mar 1;12(5):640-53 PMID: 9499400
  30. SWI-SNF complex participation in transcriptional activation at a step subsequent to activator binding.
    Mol Cell Biol. 1998 Apr;18(4):1774-82 PMID: 9528749
  31. Five SWI genes are required for expression of the HO gene in yeast.
    J Mol Biol. 1984 Oct 5;178(4):853-68 PMID: 6436497
  32. Cell cycle control of the yeast HO gene: cis- and trans-acting regulators.
    Cell. 1987 Feb 13;48(3):389-97 PMID: 3542227
  33. Activation of the yeast HO gene by release from multiple negative controls.
    Cell. 1987 Feb 27;48(4):567-77 PMID: 3545494
  34. Both positive and negative regulators of HO transcription are required for mother-cell-specific mating-type switching in yeast.
    Cell. 1987 Feb 27;48(4):579-87 PMID: 3028642
  35. Swi5 controls a novel wave of cyclin synthesis in late mitosis.
    Mol Biol Cell. 1998 Apr;9(4):945-56 PMID: 9529390
  36. Perturbation of nucleosome core structure by the SWI/SNF complex persists after its detachment, enhancing subsequent transcription factor binding.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):4947-52 PMID: 9560208
  37. Essential and redundant functions of histone acetylation revealed by mutation of target lysines and loss of the Gcn5p acetyltransferase.
    EMBO J. 1998 Jun 1;17(11):3155-67 PMID: 9606197
  38. The C-terminal domain of Sin1 interacts with the SWI-SNF complex in yeast.
    Mol Cell Biol. 1998 Jul;18(7):4157-64 PMID: 9632800
  39. A subset of TAF(II)s are integral components of the SAGA complex required for nucleosome acetylation and transcriptional stimulation.
    Cell. 1998 Jul 10;94(1):45-53 PMID: 9674426
  40. Transcriptional activators direct histone acetyltransferase complexes to nucleosomes.
    Nature. 1998 Jul 30;394(6692):498-502 PMID: 9697775
  41. Targeted recruitment of the Sin3-Rpd3 histone deacetylase complex generates a highly localized domain of repressed chromatin in vivo.
    Mol Cell Biol. 1998 Sep;18(9):5121-7 PMID: 9710596
  42. SWI/SNF complexes and facilitation of TATA binding protein:nucleosome interactions.
    Methods. 1998 Aug;15(4):303-14 PMID: 9740718
  43. Identification and analysis of yeast nucleosomal histone acetyltransferase complexes.
    Methods. 1998 Aug;15(4):315-21 PMID: 9740719
  44. Loss of transcriptional activity of a transgene is accompanied by DNA methylation and histone deacetylation and is prevented by insulators.
    Genes Dev. 1998 Sep 15;12(18):2852-62 PMID: 9744862
  45. Alteration of nucleosome structure as a mechanism of transcriptional regulation.
    Annu Rev Biochem. 1998;67:545-79 PMID: 9759497
  46. Purified histone acetyltransferase complexes stimulate HIV-1 transcription from preassembled nucleosomal arrays.
    Proc Natl Acad Sci U S A. 1998 Oct 27;95(22):12924-9 PMID: 9789016
  47. Chromatin remodeling: a marriage between two families?
    Bioessays. 1998 Sep;20(9):771-80 PMID: 9819566
  48. Functional organization of the yeast SAGA complex: distinct components involved in structural integrity, nucleosome acetylation, and TATA-binding protein interaction.
    Mol Cell Biol. 1999 Jan;19(1):86-98 PMID: 9858534
  49. Activation domain-specific and general transcription stimulation by native histone acetyltransferase complexes.
    Mol Cell Biol. 1999 Jan;19(1):855-63 PMID: 9858608
  50. The core histone N-terminal domains are required for multiple rounds of catalytic chromatin remodeling by the SWI/SNF and RSC complexes.
    Biochemistry. 1999 Feb 23;38(8):2514-22 PMID: 10029546
  51. Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter.
    Cell. 1999 Apr 30;97(3):299-311 PMID: 10319811
  52. The determination of mother cell-specific mating type switching in yeast by a specific regulator of HO transcription.
    EMBO J. 1987 Jan;6(1):243-8 PMID: 15981333
  53. 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
  54. SWI/SNF stimulates the formation of disparate activator-nucleosome complexes but is partially redundant with cooperative binding.
    J Biol Chem. 1997 May 9;272(19):12642-9 PMID: 9139720
  55. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex.
    Genes Dev. 1997 Jul 1;11(13):1640-50 PMID: 9224714
  56. The yeast SWI-SNF complex facilitates binding of a transcriptional activator to nucleosomal sites in vivo.
    Mol Cell Biol. 1997 Aug;17(8):4811-9 PMID: 9234737
  57. A large protein complex containing the yeast Sin3p and Rpd3p transcriptional regulators.
    Mol Cell Biol. 1997 Aug;17(8):4852-8 PMID: 9234741
  58. Essential functional interactions of SAGA, a Saccharomyces cerevisiae complex of Spt, Ada, and Gcn5 proteins, with the Snf/Swi and Srb/mediator complexes.
    Genetics. 1997 Oct;147(2):451-65 PMID: 9335585
  59. Role for ADA/GCN5 products in antagonizing chromatin-mediated transcriptional repression.
    Mol Cell Biol. 1997 Nov;17(11):6212-22 PMID: 9343382
  60. Catalytic activity of the yeast SWI/SNF complex on reconstituted nucleosome arrays.
    EMBO J. 1997 Nov 17;16(22):6772-82 PMID: 9362491
  61. The role of phosphorylation and the CDC28 protein kinase in cell cycle-regulated nuclear import of the S. cerevisiae transcription factor SWI5.
    Cell. 1991 Aug 23;66(4):743-58 PMID: 1652372
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
1999-06-01
Pages
1412-21
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC316758
Subset
IM
Grants
NIGMS NIH HHS · R01 GM049650 · United States
NIGMS NIH HHS · R37 GM049650 · United States
NIGMS NIH HHS · GM49650 · United States
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: [email protected]