H3 lysine 4 di- and tri-methylation deposited by cryptic transcription attenuates promoter activation

Pinskaya, Marina; Gourvennec, S.; Morillon, Antonin

doi:10.1038/emboj.2009.108

Cited by 148 publications

(191 citation statements)

References 57 publications

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“…2B), supporting the transcriptional memory of GAL1. Previous reports showed that Set1 repressed GAL1 transcription in galactose-containing medium plus 0.5% glucose (11) or GAL1 induction from raffinose to galactose culture (21). We found that SET1 deletion had a minor effect on the induction kinetics of GAL1 from long-term glucose to galactose culture, especially within the first 3 h in galactose culture (Fig.…”

Section: Elimination Of Di-and Trimethylation Of H3k4 Greatly Increassupporting

confidence: 61%

“…It was shown that Set1 is required for silencing of Ty1 retrotransposons GAL1 and PHO84 (6,11), subsequently found to be noncoding RNA-mediated (21, 29 -31). Recently, scientists (21,32) provided evidence that H3K4me2/3 recruits the Rpd3S complex to GAL1 as well as many other inducible genes that show cryptic transcription. In the case of PHO5, our recent study showed that H3K4 methylation recruits the Rpd3L complex, rather than the Rpd3S complex, to the PHO5 promoter and suppresses the aberrant chromatin remodeling at the PHO5 promoter (13).…”

Section: Discussionmentioning

confidence: 99%

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Recent Transcription-induced Histone H3 Lysine 4 (H3K4) Methylation Inhibits Gene Reactivation

Zhou

2011

Journal of Biological Chemistry

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Recent transcription of GAL genes transiently leaves an H3K4 methylation mark at their promoters, providing an epigenetic memory for the recent transcriptional activity. However, the physiological significance of this mark is enigmatic. In our study, we show that the transient H3K4 di-and trimethylation at recently transcribed GAL1 inhibited the reinduction of GAL1. The H3K4 methylation functioned by recruiting the Isw1 ATPase onto GAL1 and thereby limiting the action of RNA polymerase II during GAL1 reactivation. Strikingly, the H3K4 methylation was also observed at the promoters of inositol-and fatty acid-responsive genes after recent transcription and played a negative role in their reinduction. Taken together, our data present a new mechanism by which H3K4 methylation regulates gene transcription.Chromatin, the physiological template of all eukaryotic genetic information, is made of repeating nucleosomes. Each nucleosome consists of 147-bp DNA wrapping around a histone octamer, including two each of H2A, H2B, H3, and H4 (1). In the process of gene transcription, chromatin structure can be modulated at several levels, such as ATP-dependent chromatin remodeling (2), histone modifications (3), and nucleosome disassembly and reassembly (4).Histone H3K4 methylation is one of the major histone modifications conserved in eukaryotes. Set1 is the catalytic subunit of a large complex named COMPASS (5), which is responsible for mono-, di-, and trimethylation observed in yeast (6). Set1-dependent methylation requires histone ubiquitination of lysine 123 of histone H2B via the ubiquitin-conjugating Rad6-Bre1 complex (7). Also, it is regulated by the COMPASS subunits (8). Set1-mediated H3K4 methylation positively regulates the activation of a subset of euchromatic genes, such as RAM2, HAS1, INO1, PPH3, and MET16 (9, 10), but negatively regulates the activation of PHO5 and GAL1 (11). Histone H3K4 methylation, especially trimethylation, is usually associated with active transcription (12). However, our recent study shows that H3K4 trimethylation also associates with the repressed PHO5 gene and remains essentially unchanged during PHO5 activation and inactivation (13).In the case of GAL genes, Set1-mediated H3K4 methylation is absent from their promoters under repressed conditions. During galactose induction, Set1 is co-transcriptionally recruited by the elongating RNA polymerase II (RNAPII) 2 and methylates the corresponding genes. Interestingly, hypermethylation of H3K4 persists after transcriptional inactivation for considerable time (ϳ5 h), constituting a molecular memory within the mRNA coding region for recent transcriptional activity (14). It seems unlikely that such a robust and highly specific phenomenon occurring in living wild-type cells has no biological meaning. In this study, we confirm the post-transcriptional histone H3K4 methylation at the promoters of GAL1 and GAL10. We further show that, after recent transcription, H3K4 was hypermethylated not only at the promoters but also across the ORF regions of GAL1/1...

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Section: Elimination Of Di-and Trimethylation Of H3k4 Greatly Increassupporting

confidence: 61%

Section: Discussionmentioning

confidence: 99%

Recent Transcription-induced Histone H3 Lysine 4 (H3K4) Methylation Inhibits Gene Reactivation

Zhou

2011

Journal of Biological Chemistry

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“…103 Repression URA2 Pyrimidine biogenesis YES usDCI1. 104 Repression DCI1 Fatty acid metabolism YES GAL10 lncRNA 47,48,105 Repression GAL genes Galactose metabolism YES GAL10/GAL10s lncRNAs. 52,53 Promotes induction GAL genes Galactose metabolism YES KCS1 lncRNAs 106 Translational interference KCS1 Inositol hexa/hepta bisphosphate kinase YES SUT719 30,35 Repression SUR7 Plasma membrane protein YES CDC28 AS RNA 29 Promotes induction CDC28 Cell cycle regulator NO RTL.…”

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confidence: 99%

LncRNAs: Bridging environmental sensing and gene expression

2016

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The survival of all organisms is dependent on complex, coordinated responses to environmental cues. Non-coding RNAs have been identified as major players in regulation of gene expression, with recent evidence supporting roles for long non-coding (lnc)RNAs in both transcriptional and post-transcriptional control. Evidence from our laboratory shows that lncRNAs have the ability to form hybridized structures called R-loops with specific DNA target sequences in S. cerevisiae, thereby modulating gene expression. In this Point of View, we provide an overview of the nature of lncRNA-mediated control of gene expression in the context of our studies using the GAL gene cluster as a model for controlling the timing of transcription.

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“…Additional genomic elements have been discovered that are able to regulate transcription of nearby genes through the generation of noncoding RNAs (e.g., see Hongay et al 2006;Houseley et al 2008;Pinskaya et al 2009;Gelfand et al 2011;van Werven et al 2012;Castelnuovo et al 2013), and, based on the finding that noncoding RNA synthesis appears to be a widespread phenomenon in budding yeast (David et al 2006;Neil et al 2009;Xu et al 2009), many more such regulatory examples are likely to be identified in the future.…”

Section: S Cerevisiae Genome Organizationmentioning

confidence: 99%

Budding Yeast for Budding Geneticists: A Primer on the Saccharomyces cerevisiae Model System

2014

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The budding yeast Saccharomyces cerevisiae is a powerful model organism for studying fundamental aspects of eukaryotic cell biology. This Primer article presents a brief historical perspective on the emergence of this organism as a premier experimental system over the course of the past century. An overview of the central features of the S. cerevisiae genome, including the nature of its genetic elements and general organization, is also provided. Some of the most common experimental tools and resources available to yeast geneticists are presented in a way designed to engage and challenge undergraduate and graduate students eager to learn more about the experimental amenability of budding yeast. Finally, a discussion of several major discoveries derived from yeast studies highlights the far-reaching impact that the yeast system has had and will continue to have on our understanding of a variety of cellular processes relevant to all eukaryotes, including humans.

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H3 lysine 4 di- and tri-methylation deposited by cryptic transcription attenuates promoter activation

Cited by 148 publications

References 57 publications

Recent Transcription-induced Histone H3 Lysine 4 (H3K4) Methylation Inhibits Gene Reactivation

Recent Transcription-induced Histone H3 Lysine 4 (H3K4) Methylation Inhibits Gene Reactivation

LncRNAs: Bridging environmental sensing and gene expression

Budding Yeast for Budding Geneticists: A Primer on the Saccharomyces cerevisiae Model System

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