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Telomeric noncoding RNA: telomeric repeat‐containing RNA in telomere biology

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Abstract Telomeres are nucleoprotein structures that cap the ends of eukaryotic chromosomes, protecting them from degradation and activation of DNA damage response. For this reason, functional telomeres are vital to genome stability. For years, telomeres were assumed to be transcriptionally silent, because of their heterochromatic state. It was only recently shown that, in several organisms, telomeres are transcribed, giving rise to a long noncoding RNA (lncRNA) called telomeric repeat‐containing RNA (TERRA). Several lines of evidence now indicate that TERRA molecules play crucial roles in telomere homeostasis and telomere functions. Recent studies have shown that the expression and regulation of TERRA are dynamically controlled by each chromosome end. TERRA has been involved in the regulation of telomere length, telomerase activity, and heterochromatin formation at telomeres. The correct regulation of the telomeric transcripts may be essential to genome stability, and altered TERRA levels associate with tumorigenesis and cellular senescence. Thus, the study of the molecular mechanisms of TERRA biogenesis and function may advance the understanding of telomere‐related diseases, including cancer and aging. This article is categorized under: Regulatory RNAs/RNAi/Riboswitches > Regulatory RNAs RNA in Disease and Development > RNA in Disease

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Mechanisms involved in regulating telomeric repeat‐containing RNA (TERRA) expression. (a) In budding yeast, the telomere‐binding protein Rap1 inhibits TERRA expression by inducing degradation of TERRA transcripts, via Rat1 exonuclease (1). Rap1 also inhibits TERRA transcription by recruiting Sir and Rif proteins at chromosome ends. The histone deacetylase activity of Sir2 compacts the chromatin at subtelomeric regions, inhibiting RNA polymerase II‐mediated transcription (2). (b) In mammalian cells, TERRA expression is regulated by the presence of post‐translational modifications on telomeric histones (1), as well as by cytosine methylation of subtelomeric CpG islands (2). Binding of CTCF and cohesin at the subtelomeric regions promotes TERRA expression (3).
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Proposed biological functions of telomeric repeat‐containing RNA (TERRA). (a) In budding yeast, telomeric RNA–DNA hybrids (R‐loops) interfere with DNA replication at the subtelomeric regions by inducing replication forks stalling (1). The presence of R‐loops at telomere also impairs telomere length maintenance by promoting 5′‐end resection via Exo1 exonuclease (2). (b) TERRA expression may contribute to the formation of heterochromatin at mammalian telomeres by facilitating the recruitment of the heterochromatic protein HP1α at telomeres, thereby promoting trimethylation of the lysine 9 of the telomeric histone H3. (c) In budding yeast, TERRA transcripts expressed from short telomeres can promote the formation of telomerase clusters T‐Recs. The TERRA‐telomerase complex subsequently relocates to the telomere from which TERRA originates for its elongation.
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RNA in Disease and Development > RNA in Disease
Regulatory RNAs/RNAi/Riboswitches > Regulatory RNAs

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