Sequential recruitment of SAGA and TFIID in a genomic response to DNA damage in Saccharomyces cerevisiae

Mol Cell Biol. 2011 Jan;31(1):190-202. doi: 10.1128/MCB.00317-10. Epub 2010 Oct 18.

Abstract

Eukaryotic genes respond to their environment by changing the expression of selected genes. The question we address here is whether distinct transcriptional responses to different environmental signals elicit distinct modes of assembly of the transcription machinery. In particular, we examine transcription complex assembly by the stress-directed SAGA complex versus the housekeeping assembly factor TFIID. We focus on genomic responses to the DNA damaging agent methyl methanesulfonate (MMS) in comparison to responses to acute heat shock, looking at changes in genome-wide factor occupancy measured by chromatin immunoprecipitation-microchip (ChIP-chip) and ChIP-sequencing analyses. Our data suggest that MMS-induced genes undergo transcription complex assembly sequentially, first involving SAGA and then involving a slower TFIID recruitment, whereas heat shock genes utilize the SAGA and TFIID pathways rapidly and in parallel. Also Crt1, the repressor of model MMS-inducible ribonucleotide reductase genes, was found not to play a wider role in repression of DNA damage-inducible genes. Taken together, our findings reveal a distinct involvement of gene and chromatin regulatory factors in response to DNA damage versus heat shock and suggest different implementations of the SAGA and TFIID assembly pathways that may depend upon whether a sustained or transient change in gene expression ensues.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Base Sequence
  • Basic-Leucine Zipper Transcription Factors / metabolism
  • Binding Sites / genetics
  • Chromatin Assembly and Disassembly / genetics
  • Chromatin Immunoprecipitation
  • DNA Damage*
  • DNA, Fungal / genetics
  • DNA, Fungal / metabolism
  • Genome, Fungal
  • Heat-Shock Response
  • Methyl Methanesulfonate / toxicity
  • Promoter Regions, Genetic
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Ribonucleotide Reductases / genetics
  • Ribonucleotide Reductases / metabolism
  • Saccharomyces cerevisiae / drug effects
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae / metabolism*
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*
  • TATA-Box Binding Protein / metabolism*
  • Trans-Activators / metabolism*

Substances

  • Basic-Leucine Zipper Transcription Factors
  • DNA, Fungal
  • GCN4 protein, S cerevisiae
  • RFX1 protein, S cerevisiae
  • Repressor Proteins
  • SAGA complex, S cerevisiae
  • SPT15 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • TATA-Box Binding Protein
  • Trans-Activators
  • Methyl Methanesulfonate
  • Ribonucleotide Reductases