RNA polymerase II (RNAP II)-associated factors are recruited to tRNA loci, revealing that RNAP II- and RNAP III-mediated transcriptions overlap in yeast

J Biol Chem. 2019 Aug 16;294(33):12349-12358. doi: 10.1074/jbc.RA119.008529. Epub 2019 Jun 24.

Abstract

In yeast (Saccharomyces cerevisiae), the synthesis of tRNAs by RNA polymerase III (RNAP III) down-regulates the transcription of the nearby RNAP II-transcribed genes by a mechanism that is poorly understood. To clarify the basis of this tRNA gene-mediated (TGM) silencing, here, conducting a bioinformatics analysis of available ChIP-chip and ChIP-sequencing genomic data from yeast, we investigated whether the RNAP III transcriptional machinery can recruit protein factors required for RNAP II transcription. An analysis of 46 genome-wide protein-density profiles revealed that 12 factors normally implicated in RNAP II-mediated gene transcription are more enriched at tRNA than at mRNA loci. These 12 factors typically have RNA-binding properties, participate in the termination stage of the RNAP II transcription, and preferentially localize to the tRNA loci by a mechanism that apparently is based on the RNAP III transcription level. The factors included two kinases of RNAP II (Bur1 and Ctk1), a histone demethylase (Jhd2), and a mutated form of a nucleosome-remodeling factor (Spt6) that have never been reported to be recruited to tRNA loci. Moreover, we show that the expression levels of RNAP II-transcribed genes downstream of tRNA loci correlate with the distance from the tRNA gene by a mechanism that depends on their orientation. These results are consistent with the notion that pre-tRNAs recruit RNAP II-associated factors, thereby reducing the availability of these factors for RNAP II transcription and contributing, at least in part, to the TGM-silencing mechanism.

Keywords: RNA polymerase II; RNA polymerase III; RNA-binding protein; chromatin immunoprecipitation (ChiP); gene regulation; gene silencing; genome-wide transcription; precursor tRNA (pre-tRNA); transcriptomics; transfer RNA (tRNA).

MeSH terms

  • Cyclin-Dependent Kinases* / genetics
  • Cyclin-Dependent Kinases* / metabolism
  • Genetic Loci*
  • Histone Chaperones* / genetics
  • Histone Chaperones* / metabolism
  • Protein Kinases* / genetics
  • Protein Kinases* / metabolism
  • RNA Polymerase II* / genetics
  • RNA Polymerase II* / metabolism
  • RNA, Fungal / biosynthesis
  • RNA, Fungal / genetics
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / genetics
  • RNA, Transfer / genetics*
  • Saccharomyces cerevisiae Proteins* / genetics
  • Saccharomyces cerevisiae Proteins* / metabolism
  • Saccharomyces cerevisiae* / genetics
  • Saccharomyces cerevisiae* / metabolism
  • Transcription, Genetic / physiology*
  • Transcriptional Elongation Factors* / genetics
  • Transcriptional Elongation Factors* / metabolism

Substances

  • CTDK-I protein complex, S cerevisiae
  • Histone Chaperones
  • RNA, Fungal
  • RNA, Messenger
  • SPT6 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • Transcriptional Elongation Factors
  • RNA, Transfer
  • Protein Kinases
  • Cyclin-Dependent Kinases
  • SGV1 protein, S cerevisiae
  • RNA Polymerase II