Rapid activity-induced transcription of Arc and other IEGs relies on poised RNA polymerase II

Saha, Ramendra N.; Wissink, Erin M.; Bailey, Emma R.; Zhao, Mei; Fargo, David C.; Hwang, Ji-Yeon; Daigle, Kelly R; Fenn, J. Daniel; Adelman, Karen; Dudek, Serena M.

doi:10.1038/nn.2839

Cited by 152 publications

(200 citation statements)

References 46 publications

(57 reference statements)

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“…5C). The additional recruitment of Pol II around the TSS of ZC3H12c is similar to the activation of some Pol IIpoised genes reported previously (Hargreaves et al 2009;Saha et al 2011) and is likely to support the multiple rounds of RNA synthesis because preassociated Pol II was insufficient. For both CXCL3 and ZC3H12c, knockdown of either JMJD3 or KIAA1718 significantly reduced Pol II distribution throughout the gene body while having no impact on Pol II enrichment at TSSs (Fig.…”

Section: Jmjd3 and Kiaa1718 Regulate Target Gene Transcriptional Elonsupporting

confidence: 79%

The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation

et al. 2012

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The histone H3 Lys 27 (H3K27) demethylase JMJD3 has been shown to play important roles in transcriptional regulation and cell differentiation. However, the mechanism underlying JMJD3-mediated transcriptional regulation remains incompletely understood. Here we show that JMJD3 is associated with KIAA1718, whose substrates include dimethylated H3K27 (H3K27me2), and proteins involved in transcriptional elongation. JMJD3 and KIAA1718 directly bind to and regulate the expression of a plethora of common target genes in both a demethylase activity-dependent and -independent manner in the human promyelocytic leukemia cell line HL-60. We found that JMJD3 and KIAA1718 collaborate to demethylate trimethylated H3K27 (H3K27me3) on a subset of their target genes, some of which are bivalently marked by H3K4me3 and H3K27me3 and associated with promoter-proximal, paused RNA polymerase II (Pol II) before activation. Reduction of either JMJD3 or KIAA1718 diminishes Pol II traveling along the gene bodies of the affected genes while having no effect on the promoter-proximal Pol II. Furthermore, JMJD3 and KIAA1718 also play a role in localizing elongation factors SPT6 and SPT16 to the target genes. Our results support the model whereby JMJD3 activates bivalent gene transcription by demethylating H3K27me3 and promoting transcriptional elongation. Taken together, these findings provide new insight into the mechanisms by which JMJD3 regulates gene expression.

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Section: Jmjd3 and Kiaa1718 Regulate Target Gene Transcriptional Elonsupporting

confidence: 79%

The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation

et al. 2012

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“…The Pol II signal is maximal from mid-to late morning (ZT6-ZT10), which slightly anticipates the maximal transcription times of core circadian genes like per and tim (So and Rosbash 1997;Menet et al 2010). Most Pol II signals are promoter-proximal and may reflect poised Pol II complexes often found on genes that respond quickly to environmental stimuli (Rougvie and Lis 1988;Kim et al 2005;Muse et al 2007;Saha et al 2011).…”

Section: Discussionmentioning

confidence: 96%

Drosophila CLOCK target gene characterization: implications for circadian tissue-specific gene expression

Abruzzi¹,

Rodriguez²,

Menet³

et al. 2011

Genes Dev.

160

142

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CLOCK (CLK) is a master transcriptional regulator of the circadian clock in Drosophila. To identify CLK direct target genes and address circadian transcriptional regulation in Drosophila, we performed chromatin immunoprecipitation (ChIP) tiling array assays (ChIP–chip) with a number of circadian proteins. CLK binding cycles on at least 800 sites with maximal binding in the early night. The CLK partner protein CYCLE (CYC) is on most of these sites. The CLK/CYC heterodimer is joined 4–6 h later by the transcriptional repressor PERIOD (PER), indicating that the majority of CLK targets are regulated similarly to core circadian genes. About 30% of target genes also show cycling RNA polymerase II (Pol II) binding. Many of these generate cycling RNAs despite not being documented in prior RNA cycling studies. This is due in part to different RNA isoforms and to fly head tissue heterogeneity. CLK has specific targets in different tissues, implying that important CLK partner proteins and/or mechanisms contribute to gene-specific and tissue-specific regulation.

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“…Activation of IEGs corresponds to the first genomic response given within minutes of a stimulus. Recently, Saha et al (Saha et al, 2011) were able to categorize IEGs into two groups depending on their expression time. For rapid IEGs, which are expressed within a few minutes, DNA polymerase II (Pol II) stalling was seen in the promoter region of these genes, whereas delayed IEGs, which are expressed within an hour of the stimulus, largely lacked this poised Pol II (Saha and Dudek, 2013;Saha et al, 2011).…”

Section: Reviewmentioning

confidence: 99%

“…Recently, Saha et al (Saha et al, 2011) were able to categorize IEGs into two groups depending on their expression time. For rapid IEGs, which are expressed within a few minutes, DNA polymerase II (Pol II) stalling was seen in the promoter region of these genes, whereas delayed IEGs, which are expressed within an hour of the stimulus, largely lacked this poised Pol II (Saha and Dudek, 2013;Saha et al, 2011). This mechanism of stalling was shown to be pertinent in regulating the timing and dynamics of gene responses, as mRNA accumulation was not affected (Saha et al, 2011).…”

Section: Reviewmentioning

confidence: 99%

“…This mechanism of stalling is itself an example of an epigenetic mechanism, because it retains permissive epigenetic marks on promoters, making the chromatin accessible to polymerases and therefore allowing a robust transcription. In addition to Pol II having its largest subunit (RPB1) phosphorylated on serine-5 residues of the C-terminus, the promoter region is enriched with histones with high levels of H3K4me3 methylation (Saha et al, 2011;Telese et al, 2013). ncRNA ncRNA genes produce several classes of functional RNA molecules that are highly integrated into the molecular circuitry, making them important players in the regulation of gene expression through various mechanisms, such as RNA interference and gene silencing (Bernstein and Allis, 2005;Qureshi and Mehler, 2012).…”

Section: Histone Modificationsmentioning

confidence: 99%

See 1 more Smart Citation

Neurogenomic mechanisms of social plasticity

Cardoso

Teles

Oliveira

2015

Journal of Experimental Biology

102

116

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Group-living animals must adjust the expression of their social behaviour to changes in their social environment and to transitions between life-history stages, and this social plasticity can be seen as an adaptive trait that can be under positive selection when changes in the environment outpace the rate of genetic evolutionary change. Here, we propose a conceptual framework for understanding the neuromolecular mechanisms of social plasticity. According to this framework, social plasticity is achieved by rewiring or by biochemically switching nodes of a neural network underlying social behaviour in response to perceived social information. Therefore, at the molecular level, it depends on the social regulation of gene expression, so that different genomic and epigenetic states of this brain network correspond to different behavioural states, and the switches between states are orchestrated by signalling pathways that interface the social environment and the genotype. Different types of social plasticity can be recognized based on the observed patterns of inter-versus intra-individual occurrence, time scale and reversibility. It is proposed that these different types of social plasticity rely on different proximate mechanisms at the physiological, neural and genomic level.

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Rapid activity-induced transcription of Arc and other IEGs relies on poised RNA polymerase II

Cited by 152 publications

References 46 publications

The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation

The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation

Drosophila CLOCK target gene characterization: implications for circadian tissue-specific gene expression

Neurogenomic mechanisms of social plasticity

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