Corepressor-directed preacetylation of histone H3 in promoter chromatin primes rapid transcriptional switching of cell-type-specific genes in yeast

Alec M. DeSimone, Jeffrey D Laney

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Switching between alternate states of gene transcription is fundamental to a multitude of cellular regulatory pathways, including those that govern differentiation. In spite of the progress in our understanding of such transitions in gene activity, a major unanswered question is how cells regulate the timing of these switches. Here, we have examined the kinetics of a transcriptional switch that accompanies the differentiation of yeast cells of one mating type into a distinct new cell type. We found that cell-type-specific genes silenced by the α2 repressor in the starting state are derepressed to establish the new mating-type-specific gene expression program coincident with the loss of α2 from promoters. This rapid derepression does not require the preloading of RNA polymerase II or a preinitiation complex but instead depends upon the Gcn5 histone acetyltransferase. Surprisingly, Gcn5-dependent acetylation of nucleosomes in the promoters of mating-typespecific genes requires the corepressor Ssn6-Tup1 even in the repressed state. Gcn5 partially acetylates the amino-terminal tails of histone H3 in repressed promoters, thereby priming them for rapid derepression upon loss of α2. Thus, Ssn6-Tup1 not only efficiently represses these target promoters but also functions to initiate derepression by creating a chromatin state poised for rapid activation.

Original languageEnglish (US)
Pages (from-to)3342-3356
Number of pages15
JournalMolecular and Cellular Biology
Volume30
Issue number13
DOIs
StatePublished - Jul 2010
Externally publishedYes

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Co-Repressor Proteins
Histones
Chromatin
Yeasts
Genes
Histone Acetyltransferases
Nucleosomes
RNA Polymerase II
Acetylation
Cell Differentiation
Gene Expression

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

Cite this

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abstract = "Switching between alternate states of gene transcription is fundamental to a multitude of cellular regulatory pathways, including those that govern differentiation. In spite of the progress in our understanding of such transitions in gene activity, a major unanswered question is how cells regulate the timing of these switches. Here, we have examined the kinetics of a transcriptional switch that accompanies the differentiation of yeast cells of one mating type into a distinct new cell type. We found that cell-type-specific genes silenced by the α2 repressor in the starting state are derepressed to establish the new mating-type-specific gene expression program coincident with the loss of α2 from promoters. This rapid derepression does not require the preloading of RNA polymerase II or a preinitiation complex but instead depends upon the Gcn5 histone acetyltransferase. Surprisingly, Gcn5-dependent acetylation of nucleosomes in the promoters of mating-typespecific genes requires the corepressor Ssn6-Tup1 even in the repressed state. Gcn5 partially acetylates the amino-terminal tails of histone H3 in repressed promoters, thereby priming them for rapid derepression upon loss of α2. Thus, Ssn6-Tup1 not only efficiently represses these target promoters but also functions to initiate derepression by creating a chromatin state poised for rapid activation.",
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