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The emerging landscape of small nucleolar RNAs in cell biology.

Dupuis-Sandoval F, Poirier M, Scott MS - Wiley Interdiscip Rev RNA (2015)

Bottom Line: As a family, they have been well characterized as playing a central role in ribosome biogenesis, guiding either the sequence-specific chemical modification of pre-rRNA (ribosomal RNA) or its processing.In recent years, thanks in great part to advances in sequencing methodologies, we have seen many examples of the diversity that exists in the snoRNA family on multiple levels.Under the deluge of novel features and functions that have recently come to light, snoRNAs emerge as a central, dynamic, and highly versatile group of small regulatory RNAs.

View Article: PubMed Central - PubMed

Affiliation: Biochemistry Department, Faculty of Medicine and Health Sciences, University of Sherbrooke, Sherbrooke, Canada.

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Extent and diversity of box C/D small nucleolar RNA (snoRNA)-like molecules. While box C/D snoRNAs typically range between 60 and 90 nucleotides in length (a), mini-snoRNAs, binding the same interaction partners as classical snoRNAs, but lacking boxes C′ and D′ have been detected by sequencing (b). At the other end of the spectrum, snoRNA-lncRNA (long noncoding RNA) consisting of two box C/D snoRNAs and the intronic sequence separating them have also been reported (c). Many studies have also detected stable snoRNA-derived RNAs (sdRNAs) likely generated by the action of endonucleases or exonucleases. Some sdRNAs are miRNA-like37–39 while others are longer products40 (d). Boxes C/C′ and D/D′ are represented, respectively, by orange and cyan colored boxes.
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fig02: Extent and diversity of box C/D small nucleolar RNA (snoRNA)-like molecules. While box C/D snoRNAs typically range between 60 and 90 nucleotides in length (a), mini-snoRNAs, binding the same interaction partners as classical snoRNAs, but lacking boxes C′ and D′ have been detected by sequencing (b). At the other end of the spectrum, snoRNA-lncRNA (long noncoding RNA) consisting of two box C/D snoRNAs and the intronic sequence separating them have also been reported (c). Many studies have also detected stable snoRNA-derived RNAs (sdRNAs) likely generated by the action of endonucleases or exonucleases. Some sdRNAs are miRNA-like37–39 while others are longer products40 (d). Boxes C/C′ and D/D′ are represented, respectively, by orange and cyan colored boxes.

Mentions: While the mammalian complement of both box C/D and box H/ACA snoRNAs has been extensively probed using both experimental and computational approaches (see, e.g., Refs 12–14, 34, and 35), deep sequencing is still identifying potential new members of these classes. Recent photoreactive nucleotide-enhanced cross-linking and immunoprecipitation (PAR-CLIP) of core snoRNA-associated proteins followed by sequencing of the bound RNA has allowed the detection of dozens of novel human snoRNAs, some of which have also been detected by northern blot and/or are likely copies or homologs of known snoRNA identified in human or in other organisms.36 Deep sequencing is also revealing the existence of very small and very large snoRNA-like molecules (Figure 2). Mini-snoRNAs of type box C/D with boxes C and D but lacking boxes C′ and D′ were detected by deep sequencing of HEK293 cells and were detected bound to core-associated proteins.36 Such mini-snoRNAs can be as short as 27 nucleotides in length and would not be long enough to hold two guide sequences.36 In parallel, long noncoding RNAs with snoRNA ends (sno-lncRNAs) were identified by deep sequencing of the nonpolyadenylated transcriptomes of HeLa and human embryonic stem cells and, in a later study, in rhesus and mouse embryonic stem cells.41,42 Sno-lncRNAs are produced from loci containing two snoRNAs within the same intron. While they are believed to be processed by the canonical snoRNP machinery, they also bind the splicing factor RBFOX2 and have been proposed to act as molecular sinks, titrating RBFOX2 in specific cell types, resulting in splicing alteration.41 The small number of pairs of snoRNAs encoded in the same host intron appears to limit the number of possible sno-lncRNAs; although one example of a sno-lncRNA produced from snoRNAs in neighboring introns has been described in mouse, its expression proposed to be regulated by alternative splicing.42 Overall, the snoRNA count is likely to continue to increase over the next few years, although newly discovered members are expected to be of decreasing abundance, highly cell-type specific, or highly noncanonical.


The emerging landscape of small nucleolar RNAs in cell biology.

Dupuis-Sandoval F, Poirier M, Scott MS - Wiley Interdiscip Rev RNA (2015)

Extent and diversity of box C/D small nucleolar RNA (snoRNA)-like molecules. While box C/D snoRNAs typically range between 60 and 90 nucleotides in length (a), mini-snoRNAs, binding the same interaction partners as classical snoRNAs, but lacking boxes C′ and D′ have been detected by sequencing (b). At the other end of the spectrum, snoRNA-lncRNA (long noncoding RNA) consisting of two box C/D snoRNAs and the intronic sequence separating them have also been reported (c). Many studies have also detected stable snoRNA-derived RNAs (sdRNAs) likely generated by the action of endonucleases or exonucleases. Some sdRNAs are miRNA-like37–39 while others are longer products40 (d). Boxes C/C′ and D/D′ are represented, respectively, by orange and cyan colored boxes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4696412&req=5

fig02: Extent and diversity of box C/D small nucleolar RNA (snoRNA)-like molecules. While box C/D snoRNAs typically range between 60 and 90 nucleotides in length (a), mini-snoRNAs, binding the same interaction partners as classical snoRNAs, but lacking boxes C′ and D′ have been detected by sequencing (b). At the other end of the spectrum, snoRNA-lncRNA (long noncoding RNA) consisting of two box C/D snoRNAs and the intronic sequence separating them have also been reported (c). Many studies have also detected stable snoRNA-derived RNAs (sdRNAs) likely generated by the action of endonucleases or exonucleases. Some sdRNAs are miRNA-like37–39 while others are longer products40 (d). Boxes C/C′ and D/D′ are represented, respectively, by orange and cyan colored boxes.
Mentions: While the mammalian complement of both box C/D and box H/ACA snoRNAs has been extensively probed using both experimental and computational approaches (see, e.g., Refs 12–14, 34, and 35), deep sequencing is still identifying potential new members of these classes. Recent photoreactive nucleotide-enhanced cross-linking and immunoprecipitation (PAR-CLIP) of core snoRNA-associated proteins followed by sequencing of the bound RNA has allowed the detection of dozens of novel human snoRNAs, some of which have also been detected by northern blot and/or are likely copies or homologs of known snoRNA identified in human or in other organisms.36 Deep sequencing is also revealing the existence of very small and very large snoRNA-like molecules (Figure 2). Mini-snoRNAs of type box C/D with boxes C and D but lacking boxes C′ and D′ were detected by deep sequencing of HEK293 cells and were detected bound to core-associated proteins.36 Such mini-snoRNAs can be as short as 27 nucleotides in length and would not be long enough to hold two guide sequences.36 In parallel, long noncoding RNAs with snoRNA ends (sno-lncRNAs) were identified by deep sequencing of the nonpolyadenylated transcriptomes of HeLa and human embryonic stem cells and, in a later study, in rhesus and mouse embryonic stem cells.41,42 Sno-lncRNAs are produced from loci containing two snoRNAs within the same intron. While they are believed to be processed by the canonical snoRNP machinery, they also bind the splicing factor RBFOX2 and have been proposed to act as molecular sinks, titrating RBFOX2 in specific cell types, resulting in splicing alteration.41 The small number of pairs of snoRNAs encoded in the same host intron appears to limit the number of possible sno-lncRNAs; although one example of a sno-lncRNA produced from snoRNAs in neighboring introns has been described in mouse, its expression proposed to be regulated by alternative splicing.42 Overall, the snoRNA count is likely to continue to increase over the next few years, although newly discovered members are expected to be of decreasing abundance, highly cell-type specific, or highly noncanonical.

Bottom Line: As a family, they have been well characterized as playing a central role in ribosome biogenesis, guiding either the sequence-specific chemical modification of pre-rRNA (ribosomal RNA) or its processing.In recent years, thanks in great part to advances in sequencing methodologies, we have seen many examples of the diversity that exists in the snoRNA family on multiple levels.Under the deluge of novel features and functions that have recently come to light, snoRNAs emerge as a central, dynamic, and highly versatile group of small regulatory RNAs.

View Article: PubMed Central - PubMed

Affiliation: Biochemistry Department, Faculty of Medicine and Health Sciences, University of Sherbrooke, Sherbrooke, Canada.

Show MeSH