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Noncoding RNAs and the borders of heterochromatin

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Eukaryotic genomes contain long stretches of repetitive DNA sequences, which are the preferred sites for the assembly of heterochromatin structures. The formation of heterochromatin results in highly condensed chromosomal domains that limit the accessibility of DNA to the transcription and recombination machinery to maintain genome stability. Heterochromatin has the tendency to spread, and the formation of boundaries that block heterochromatin spreading is required to maintain stable gene expression patterns. Recent work has suggested that noncoding RNAs (ncRNAs) are involved in regulating boundary formation in addition to their well‐established roles in chromatin regulation. Here, we present a review of our current understanding of the involvement of ncRNA at the boundaries of heterochromatin, highlighting their mechanisms of action in different settings. WIREs RNA 2014, 5:835–847. doi: 10.1002/wrna.1249 This article is categorized under: Regulatory RNAs/RNAi/Riboswitches > Regulatory RNAs
The establishment and spreading of heterochromatin. (a) In fission yeast and other organisms, specific DNA sequences (in orange) recruit heterochromatin‐associated histone‐modifying enzymes, such as histone methyltransferases (HMTs) that preferentially methylate histone H3K9, and histone deacetylases (HDACs). These enzymes act on histones at the nucleation site to establish heterochromatic modifications. (b) H3K9me is recognized by chromodomain‐containing HP1 (Swi6 in fission yeast). (c) HP1/Swi6 recruits HMTs and HDACs to adjacent nucleosomes to reiterate the process of H3K9me and HP1/Swi6 binding, continuous cycles of which lead to the long‐range spreading of heterochromatin.
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Noncoding RNAs (ncRNAs) and heterochromatin boundaries. (a) Many known or predicted heterochromatin boundary elements, like the SINE and tRNA genes, are sites of ncRNA transcription. Transcription‐mediated histone modifications and histone turn over might contribute to heterochromatin boundary formation at these elements. (b) In fission yeast, BORDERLINE evicts Swi6 in cis from chromatin by directly binding to Swi6 and interfering with its ability to interact with H3K9me, thus halting Swi6‐dependent spreading. (c) In Drosophila, ncRNAs serve a scaffolding function to mediate the clustering of insulator bodies. (d) In mammals, ncRNAs directly regulate the binding of CTCF to insulator DNA sequences.
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Noncoding RNAs and heterochromatin chromatin assembly. (a) RNA interference (RNAi)‐mediated heterochromatin assembly in fission yeast. Repetitive DNA elements are transcribed and processed by the RNAi pathway into siRNAs, which are used by effector protein complex RITS to target histone methyltransferase CLRC to nascent transcripts. (b) Small interfering RNAs (siRNAs) might mediate the clustering of distant loci, such as telomeres, at the nuclear envelope. (c) Xist interacts directly with PRC2 through a repeat (RepA) and recruits PRC2 to initiate inactivation of the X chromosome. (d) HOTAIR binds both LSD1 and PRC2 via different sequences on the RNA, acting as a scaffold for histone‐modifying enzymes to coordinate their activities.
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Heterochromatin boundaries. (a) The transitions between heterochromatin and euchromatin are marked by DNA sequences termed boundary elements (orange) that prevent heterochromatin (green) from spreading into neighboring euchromatin regions (red). (b) One mode of boundary function is the recruitment of euchromatin‐associated histone‐modifying enzymes, such as histone acetyltransferases (HATs) and histone demethylases (HDM) to the boundary region to antagonize the addition of heterochromatin‐associated histone modifications to block heterochromatin spreading. (c) Another mechanism by which boundaries function is to spatially separate heterochromatin and euchromatin domains through specific protein complexes that interact with nuclear structures.
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