HAT–HDAC interplay modulates global histone H3K14 acetylation in gene‐coding regions during stress

Johnsson, Anna; Durand-Dubief, Mickaël; Xue-Franzén, Yongtao; Rönnerblad, Michelle; Ekwall, Karl; Wright, Anthony P. H.

doi:10.1038/embor.2009.127

Cited by 99 publications

(86 citation statements)

References 30 publications

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“…Although Gcn5 is broadly enriched across highly transcribed genes in yeast (49), Gcn5-dependent acetylation patterns differ between gene promoters and coding regions (20,49). For example, both H3K9 and H3K14 acetylation can be catalyzed by Gcn5 in vivo, but high-resolution ChIP-sequencing data show that H3K9 acetylation is narrowly limited to promoter regions (20), whereas H3K14 acetylation spreads across gene bodies as well (49). How can the same enzyme generate different acetylation patterns?…”

Section: Discussionmentioning

confidence: 99%

Nucleosome competition reveals processive acetylation by the SAGA HAT module

Ringel

Cieniewicz

Taverna

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The Spt-Ada-Gcn5 acetyltransferase (SAGA) coactivator complex hyperacetylates histone tails in vivo in a manner that depends upon histone 3 lysine 4 trimethylation (H3K4me3), a histone mark enriched at promoters of actively transcribed genes. SAGA contains a separable subcomplex known as the histone acetyltransferase (HAT) module that contains the HAT, Gcn5, bound to Sgf29, Ada2, and Ada3. Sgf29 contains a tandem Tudor domain that recognizes H3K4me3-containing peptides and is required for histone hyperacetylation in vivo. However, the mechanism by which H3K4me3 recognition leads to lysine hyperacetylation is unknown, as in vitro studies show no effect of the H3K4me3 modification on histone peptide acetylation by Gcn5. To determine how H3K4me3 binding by Sgf29 leads to histone hyperacetylation by Gcn5, we used differential fluorescent labeling of histones to monitor acetylation of individual subpopulations of methylated and unmodified nucleosomes in a mixture. We find that the SAGA HAT module preferentially acetylates H3K4me3 nucleosomes in a mixture containing excess unmodified nucleosomes and that this effect requires the Tudor domain of Sgf29. The H3K4me3 mark promotes processive, multisite acetylation of histone H3 by Gcn5 that can account for the different acetylation patterns established by SAGA at promoters versus coding regions. Our results establish a model for Sgf29 function at gene promoters and define a mechanism governing crosstalk between histone modifications.T he different patterns of histone posttranslational modifications distributed across the genome are proposed to constitute a "histone code" that orchestrates distinct transcriptional programs by recruiting specific effector proteins (1-4). The phenomenon of histone code "crosstalk," whereby one type of histone modification directs the establishment of another, or through which several histone modifications are recognized in tandem, has emerged as an important and widespread mechanism regulating chromatin-templated processes (5, 6). The multifunctional complexes that activate transcription are thought to mediate crosstalk through "reader" domains that recognize particular chromatin marks as well as through catalytic subunits that deposit or remove histone modifications (5,7,8). As a result, distinct combinations of histone posttranslational modifications that correlate with transcriptional output cluster across the genome (9-11). High levels of histone 3 lysine 4 trimethylation (H3K4me3) and histone H3 hyperacetylation are present at the promoters of actively transcribed genes (9,11,12), and multiple lines of evidence support the existence of regulatory mechanisms coupling the two modifications. Studies using tandem mass spectrometry to sequence whole histone tails have shown that H3K4me3 is highly correlated with hyperacetylation of the same H3 tail (13,14). Deleting the yeast Set1 methyltransferase, which trimethylates H3K4, leads to dramatically lower levels of histone H3 tail acetylation overall (13, 15). These results are consistent with ...

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Section: Discussionmentioning

confidence: 99%

Nucleosome competition reveals processive acetylation by the SAGA HAT module

Ringel

Cieniewicz

Taverna

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Given that KAT2A increases histone H3K9/K14 acetylation (H3K9/K14ac) and accessibility of factors promoting transcription (33,41,42), we speculated that KAT2A is recruited to DDIT3⅐phospho-JUN complex via physical interaction with DDIT3 at the AP-1 binding site (Ϫ304/Ϫ298) in the TNFRSF10A promoter region, leading to acetylation of H3K9/ K14 and further enhancement of TNFRSF10A transcription. To verify this hypothesis, we performed ChIP experiments using anti-H3K9/K14ac antibody in the H1792 cell lysates after treatment with TG (1 M) or Tm (1 M) for 12 h. We found that the antibody against H3K9/K14ac captured the AP-1 binding site region of human TNFRSF10A promoter, and the quantity of PCR product containing the AP-1 binding site was increased in cell lysate prepared from TG-or Tm-treated H1792 cells, respectively (Fig.…”

Section: Ddit3 and Tnfrsf10a Expressions Are Up-regulated By Ermentioning

confidence: 99%

DDIT3 and KAT2A Proteins Regulate TNFRSF10A and TNFRSF10B Expression in Endoplasmic Reticulum Stress-mediated Apoptosis in Human Lung Cancer Cells

Lei

et al. 2015

Journal of Biological Chemistry

104

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Background:The mechanisms of transcriptional regulation of TNFRSF10A and TNFRSF10B are not well described. Results: DDIT3 and KAT2A cooperatively up-regulated TNFRSF10A and TNFRSF10B. Conclusion: DDIT3 and KAT2A promote the transcription of TNFRSF10A and TNFRSF10B via the AP-1 and DDIT3 binding sites, respectively. Significance: Our findings offer new insights on the mechanisms of ER stress-mediated apoptosis.

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“…However, recent studies in yeast revealed that only a fraction of bound genes is misregulated upon deletion of SAGA subunits, and, conversely, only a fraction of misregulated genes is bound by the corresponding subunits (Lenstra et al 2011;Venters et al 2011;Lenstra and Holstege 2012). Furthermore, a wider distribution of the complex is suggested by chromatin immunoprecipitation (ChIP) experiments on a few model genes in yeast that also detected SAGA in the coding region and by ChIP-coupled high-throughput sequencing (ChIP-seq) analyses in flies that revealed a colocalization of SAGA with RNA polymerase II (Pol II) in the body of a subset of genes (Govind et al 2007;Johnsson et al 2009;Weake et al 2011). In addition to its gene-specific regulatory role, it has been proposed that SAGA acetylates histones throughout the genome in a global and untargeted manner (Vogelauer et al 2000).…”

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confidence: 99%

The SAGA coactivator complex acts on the whole transcribed genome and is required for RNA polymerase II transcription

Bonnet¹,

Wang²,

Baptista³

et al. 2014

Genes Dev.

192

222

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The SAGA (Spt-Ada-Gcn5 acetyltransferase) coactivator complex contains distinct chromatin-modifying activities and is recruited by DNA-bound activators to regulate the expression of a subset of genes. Surprisingly, recent studies revealed little overlap between genome-wide SAGA-binding profiles and changes in gene expression upon depletion of subunits of the complex. As indicators of SAGA recruitment on chromatin, we monitored in yeast and human cells the genome-wide distribution of histone H3K9 acetylation and H2B ubiquitination, which are respectively deposited or removed by SAGA. Changes in these modifications after inactivation of the corresponding enzyme revealed that SAGA acetylates the promoters and deubiquitinates the transcribed region of all expressed genes. In agreement with this broad distribution, we show that SAGA plays a critical role for RNA polymerase II recruitment at all expressed genes. In addition, through quantification of newly synthesized RNA, we demonstrated that SAGA inactivation induced a strong decrease of mRNA synthesis at all tested genes. Analysis of the SAGA deubiquitination activity further revealed that SAGA acts on the whole transcribed genome in a very fast manner, indicating a highly dynamic association of the complex with chromatin. Thus, our study uncovers a new function for SAGA as a bone fide cofactor for all RNA polymerase II transcription.

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HAT–HDAC interplay modulates global histone H3K14 acetylation in gene‐coding regions during stress

Cited by 99 publications

References 30 publications

Nucleosome competition reveals processive acetylation by the SAGA HAT module

Nucleosome competition reveals processive acetylation by the SAGA HAT module

DDIT3 and KAT2A Proteins Regulate TNFRSF10A and TNFRSF10B Expression in Endoplasmic Reticulum Stress-mediated Apoptosis in Human Lung Cancer Cells

The SAGA coactivator complex acts on the whole transcribed genome and is required for RNA polymerase II transcription

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