Molecular Mechanism of DNA Topoisomerase I-Dependent rDNA Silencing: Sir2p Recruitment at Ribosomal Genes

J Mol Biol. 2016 Dec 4;428(24 Pt B):4905-4916. doi: 10.1016/j.jmb.2016.10.032. Epub 2016 Nov 5.

Abstract

Saccharomyces cerevisiae sir2Δ or top1Δ mutants exhibit similar phenotypes involving ribosomal DNA, including (i) loss of transcriptional silencing, resulting in non-coding RNA hyperproduction from cryptic RNA polymerase II promoters; (ii) alterations in recombination; and (iii) a general increase in histone acetylation. Given the distinct enzymatic activities of Sir2 and Top1 proteins, a histone deacetylase and a DNA topoisomerase, respectively, we investigated whether genetic and/or physical interactions between the two proteins could explain the shared ribosomal RNA genes (rDNA) phenotypes. We employed an approach of complementing top1Δ cells with yeast, human, truncated, and chimeric yeast/human TOP1 constructs and of assessing the extent of non-coding RNA silencing and histone H4K16 deacetylation. Our findings demonstrate that residues 115-125 within the yeast Top1p N-terminal domain are required for the complementation of the top1∆ rDNA phenotypes. In chromatin immunoprecipitation and co-immunoprecipitation experiments, we further demonstrate the physical interaction between Top1p and Sir2p. Our genetic and biochemical studies support a model whereby Top1p recruits Sir2p to the rDNA and clarifies a structural role of DNA topoisomerase I in the epigenetic regulation of rDNA, independent of its known catalytic activity.

Keywords: DNA topoisomerase I; Sir2p; histone acetylation; rDNA; transcriptional silencing.

MeSH terms

  • Chromatin Immunoprecipitation
  • DNA Topoisomerases, Type I / genetics
  • DNA Topoisomerases, Type I / metabolism*
  • DNA, Ribosomal / metabolism*
  • Gene Deletion
  • Gene Expression Regulation, Fungal*
  • Genetic Complementation Test
  • Protein Binding
  • RNA, Ribosomal / biosynthesis*
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism*
  • Silent Information Regulator Proteins, Saccharomyces cerevisiae / metabolism*
  • Sirtuin 2 / metabolism*
  • Transcription, Genetic

Substances

  • DNA, Ribosomal
  • RNA, Ribosomal
  • Silent Information Regulator Proteins, Saccharomyces cerevisiae
  • SIR2 protein, S cerevisiae
  • Sirtuin 2
  • DNA Topoisomerases, Type I