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Splicing noncoding RNAs from the inside out

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Eukaryotic precursor‐messenger RNAs (pre‐mRNAs) undergo splicing to remove intragenic regions (introns) and ligate expressed regions (exons) together. Unlike exons in the mature messenger RNAs (mRNAs) that are used for translation, introns that are spliced out of pre‐mRNAs were generally believed to lack function and to be degraded. However, recent studies have revealed that a large group of spliced introns can escape complete degradation and are processed to generate noncoding RNAs (ncRNAs), including different types of small RNAs, long‐noncoding RNAs, and circular RNAs. Strikingly, exonic sequences can be also back‐spliced from pre‐mRNAs to form stable circular RNAs. Together, the findings that ncRNAs can be spliced out of mRNA precursors not only expand the ever‐growing repertoire of ncRNAs that originate from different genomic regions, but also reveal the unexpected transcriptomic complexity and functional capacity of eukaryotic genomes. WIREs RNA 2015, 6:651–660. doi: 10.1002/wrna.1307

This article is categorized under:

  • RNA Evolution and Genomics > Computational Analyses of RNA
  • RNA Processing > Splicing Regulation/Alternative Splicing
  • Regulatory RNAs/RNAi/Riboswitches > Regulatory RNAs
MicroRNAs (MiRNAs) are processed from spliced introns. (a) Eukaryotic precursor RNAs (pre‐RNAs) undergo splicing (dash lines) to remove introns (lines) and ligate exons (bars) together to form either mature mRNAs that are subsequently translated or noncoding RNAs. After splicing, intron lariats are generally debranched and ultimately degraded. ss, splice site. BP, branchpoint. (b) Drosha/DGCR8‐dependent model of canonical mirtron processing. (c) Splicing‐dependent model of mirtron processing. Notably, some mirtrons that derive from small introns have the hairpin exactly ending at the splice sites to resemble pre‐miRNAs, thus do not need to be trimmed by exonucleases.
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Two types of circular RNAs are processed from excised introns or exons. (a) Circular intronic RNAs (CiRNAs) are processed from excised introns. CiRNAs fail to be debranched after splicing, leading to a covalent circle with 2′,5′‐phosphodiester bond between 5′ splice donor site and the branchpoint site. The formation of ciRNAs depends on a consensus RNA motif containing a 7‐nt GU rich element near 5′ splice site (magenta bar) and an 11‐nt C‐rich element near branchpoint (yellow bar). (b) Back‐spliced circular RNAs (CircRNAs) are processed from excised exons. Different from canonical splicing (dashed lines in black), which ligates an upstream 5′ splice site (5′ ss) with a downstream 3′ splice site (3′ ss) to form a linear RNA (top), back‐splicing (dashed line in red) connects downstream a 5′ ss reversely with an upstream 3′ ss to yield a circular RNA with normal 3′,5′‐phosphodiester bond and an alternatively spliced linear RNA with exon exclusion (bottom). Both complementary sequences and protein factors can facilitate back‐splicing by bridging downstream 5′ ss close to upstream 3′ ss. See text for details.
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Small nucleolar RNAs (SnoRNAs) and snoRNA‐ended long‐noncoding RNAs (sno‐lncRNAs) are processed from spliced introns. (a) SnoRNAs are processed from spliced introns. During splicing and exonucleolytic trimming from debranched introns, the assembly of snoRNA with the snoRNA‐associated proteins (snoRNPs, blue spheres) protects it from further exonucleolytic degradation and leads to the formation of mature snoRNPs. (b) Sno‐lncRNAs are processed from spliced introns and flanked with snoRNAs at both ends. Introns containing two snoRNAs are processed from their ends by the snoRNP machinery (blue spheres) and the intronic sequences between these two snoRNAs are protected, thus leading to the formation of lncRNAs with snoRNA ends.
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