Molecular mechanisms that distinguish TFIID housekeeping from regulatable SAGA promoters

Jonge, Wim J. de; O’Duibhir, Eoghan; Lijnzaad, Philip; Leenen, Dik van; Koerkamp, Marian J. A. Groot; Kemmeren, Patrick; Holstege, Frank C.P.

doi:10.15252/embj.201695621

Cited by 54 publications

(74 citation statements)

References 84 publications

(185 reference statements)

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“…Paired‐end 125‐bp reads were aligned with Bowtie 2. Nucleosome dyads were found by taking the middle of each paired read of insert size between 95 and 225 bp (or 140 and 225 bp) and were smoothed with a 31‐bp window, as described in de Jonge et al (). Data are deposited in GEO with accession number: GSE116337.…”

Section: Methodsmentioning

confidence: 99%

Live‐cell imaging reveals the interplay between transcription factors, nucleosomes, and bursting

et al. 2019

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Transcription factors show rapid and reversible binding to chromatin in living cells, and transcription occurs in sporadic bursts, but how these phenomena are related is unknown. Using a combination of in vitro and in vivo single‐molecule imaging approaches, we directly correlated binding of the Gal4 transcription factor with the transcriptional bursting kinetics of the Gal4 target genes GAL3 and GAL10 in living yeast cells. We find that Gal4 dwell time sets the transcriptional burst size. Gal4 dwell time depends on the affinity of the binding site and is reduced by orders of magnitude by nucleosomes. Using a novel imaging platform called orbital tracking, we simultaneously tracked transcription factor binding and transcription at one locus, revealing the timing and correlation between Gal4 binding and transcription. Collectively, our data support a model in which multiple RNA polymerases initiate transcription during one burst as long as the transcription factor is bound to DNA, and bursts terminate upon transcription factor dissociation.

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Section: Methodsmentioning

confidence: 99%

Live‐cell imaging reveals the interplay between transcription factors, nucleosomes, and bursting

et al. 2019

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“…In yeast, SAGA predominates at more regulated nonhousekeeping genes (de Jonge et al 2017) and are preferentially used by those with TATA boxes, including those associated with stress (Basehoar et al 2004;Huisinga and Pugh 2004). A more comprehensive genome-wide analysis of all viable SAGA deletion mutants suggests that different modules regulate different sets of genes (Helmlinger et al 2011).…”

Section: Dub and Hat Module Subunits Control Expression Of A Subset Omentioning

confidence: 99%

Enzymatic modules of the SAGA chromatin-modifying complex play distinct roles in Drosophila gene expression and development

Seidel

Szerszen

et al. 2017

Genes Dev.

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The Spt-Ada-Gcn5-acetyltransferase (SAGA) chromatin-modifying complex is a transcriptional coactivator that contains four different modules of subunits. The intact SAGA complex has been well characterized for its function in transcription regulation and development. However, little is known about the roles of individual modules within SAGA and whether they have any SAGA-independent functions. Here we demonstrate that the two enzymatic modules of Drosophila SAGA are differently required in oogenesis. Loss of the histone acetyltransferase (HAT) activity blocks oogenesis, while loss of the H2B deubiquitinase (DUB) activity does not. However, the DUB module regulates a subset of genes in early embryogenesis, and loss of the DUB subunits causes defects in embryogenesis. ChIP-seq (chromatin immunoprecipitation [ChIP] combined with high-throughput sequencing) analysis revealed that both the DUB and HAT modules bind most SAGA target genes even though many of these targets do not require the DUB module for expression. Furthermore, we found that the DUB module can bind to chromatin and regulate transcription independently of the HAT module. Our results suggest that the DUB module has functions within SAGA and independent functions.

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“…Many studies suggest that there are at least two broad classes of genes: housekeeping and highly-regulated genes (de Jonge et al, 2016; Eisenberg and Levanon, 2013; Huisinga and Pugh, 2004; Mencía et al, 2002; Ohtsuki et al, 1998; Zabidi and Stark, 2016). These two gene classes differ in their response to transcription activators, chromatin organization and modifications, and in promoter sequence elements.…”

Section: Introductionmentioning

confidence: 99%

Transcription of Nearly All Yeast RNA Polymerase II-Transcribed Genes Is Dependent on Transcription Factor TFIID

et al. 2017

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SUMMARY Previous studies suggested that expression of most yeast mRNAs is dominated by either transcription factor TFIID or SAGA. We reexamined the role of TFIID by rapid depletion of S. cerevisiae TFIID subunits and measurement of changes in nascent transcription. We find that transcription of nearly all mRNAs is strongly dependent on TFIID function. Degron-dependent depletion of Tafs 1,2,7,11, and 13 showed similar transcription decreases for genes in the Taf1-depleted, Taf1-enriched, TATA-containing and TATA-less gene classes. The magnitude of TFIID-dependence varies with growth conditions, although this variation is similar genome-wide. Many studies have suggested differences in gene regulatory mechanisms between TATA and TATA-less genes and these differences have been attributed in part to differential dependence on SAGA or TFIID. Our work indicates that TFIID participates in expression of nearly all yeast mRNAs and that differences in regulation between these two gene categories is due to other properties.

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Molecular mechanisms that distinguish TFIID housekeeping from regulatable SAGA promoters

Cited by 54 publications

References 84 publications

Live‐cell imaging reveals the interplay between transcription factors, nucleosomes, and bursting

Live‐cell imaging reveals the interplay between transcription factors, nucleosomes, and bursting

Enzymatic modules of the SAGA chromatin-modifying complex play distinct roles in Drosophila gene expression and development

Transcription of Nearly All Yeast RNA Polymerase II-Transcribed Genes Is Dependent on Transcription Factor TFIID

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