Histone H3 lysine 4 hypermethylation prevents aberrant nucleosome remodeling at the PHO5 promoter

Mol Cell Biol. 2011 Aug;31(15):3171-81. doi: 10.1128/MCB.05017-11. Epub 2011 Jun 6.

Abstract

Recent studies have highlighted the histone H3K4 methylation (H3K4me)-dependent transcriptional repression in Saccharomyces cerevisiae; however, the underlying mechanism remains inexplicit. Here, we report that H3K4me inhibits the basal PHO5 transcription under high-phosphate conditions by suppressing nucleosome disassembly at the promoter. We found that derepression of the PHO5 promoter by SET1 deletion resulted in a labile chromatin structure, allowing more binding of RNA polymerase II (Pol II) but not the transactivators Pho2 and Pho4. We further showed that Pho23 and Cti6, two plant homeodomain (PHD)-containing proteins, cooperatively anchored the large Rpd3 (Rpd3L) complex to the H3K4-methylated PHO5 promoter. The deacetylation activity of Rpd3 on histone H3 was required for the function of Set1 at the PHO5 promoter. Taken together, our data suggest that Set1-mediated H3K4me suppresses nucleosome remodeling at the PHO5 promoter so as to reduce basal transcription of PHO5 under repressive conditions. We propose that the restriction of aberrant nucleosome remodeling contributes to strict control of gene transcription by the transactivators.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Acid Phosphatase / genetics*
  • Acid Phosphatase / metabolism
  • Carrier Proteins / metabolism
  • Chromatin / genetics
  • Chromatin / metabolism
  • Chromatin Immunoprecipitation
  • DNA-Binding Proteins / antagonists & inhibitors
  • Fluorescent Antibody Technique
  • Histone Deacetylases / metabolism
  • Histone-Lysine N-Methyltransferase / biosynthesis
  • Histone-Lysine N-Methyltransferase / genetics
  • Histone-Lysine N-Methyltransferase / metabolism
  • Histones / metabolism*
  • Homeodomain Proteins / antagonists & inhibitors
  • Methylation
  • Nuclear Proteins / metabolism
  • Nucleosomes / metabolism*
  • Organisms, Genetically Modified
  • Promoter Regions, Genetic*
  • RNA Polymerase II / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Saccharomyces cerevisiae / enzymology
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins / antagonists & inhibitors
  • Saccharomyces cerevisiae Proteins / biosynthesis
  • Saccharomyces cerevisiae Proteins / genetics*
  • Saccharomyces cerevisiae Proteins / metabolism
  • Transcription, Genetic

Substances

  • Carrier Proteins
  • Chromatin
  • Cti6 protein, S cerevisiae
  • DNA-Binding Proteins
  • Histones
  • Homeodomain Proteins
  • Nuclear Proteins
  • Nucleosomes
  • PHO2 protein, S cerevisiae
  • PHO4 protein, S cerevisiae
  • Pho23 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Histone-Lysine N-Methyltransferase
  • SET1 protein, S cerevisiae
  • RNA Polymerase II
  • Acid Phosphatase
  • PHO5 protein, S cerevisiae
  • RPD3 protein, S cerevisiae
  • Histone Deacetylases