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When Small Rnas Become Smaller: Emerging Functions of Snornas and Their Derivatives Anna M

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When Small Rnas Become Smaller: Emerging Functions of Snornas and Their Derivatives Anna M Vol. 63, No 4/2016 601–607 https://doi.org/10.18388/abp.2016_1330 Review When small RNAs become smaller: emerging functions of snoRNAs and their derivatives Anna M. Mleczko and Kamilla Bąkowska-Żywicka* Institute of Bioorganic Chemistry Polish Academy of Sciences, Poznań, Poland Small nucleolar RNAs (snoRNAs) are molecules located tween putative target RNAs and the antisense elements in the cell nucleolus and in Cajal bodies. Many scientif- or the recognition loops within the snoRNA) as well ic reports show that snoRNAs are not only responsible as biochemical identifications of snoRNA targets (e.g. for modifications of other RNAs but also fulfill multiple based on CLASH: crosslinking, ligation, and sequencing other functions such as metabolic stress regulation or of hybrids). However, there are numerous snoRNAs for modulation of alternative splicing. Full-length snoRNAs which no target RNAs have been identified so far. They as well as small RNAs derived from snoRNAs have been are called “orphan snoRNAs”. In multiple cases, orphan implied in human diseases such as cancer or Prader–Willi snoRNAs possess the guide sequences, however, they Syndrome. In this review we describe emerging, non- are not complementary to other canonical RNAs target- canonical roles of snoRNAs and their derivatives with the ed by snoRNAs. emphasis on their role in human diseases. Small nucleolar RNAs were initially discovered in the nucleolus and were thought to exclusively target ribo- Key words: small RNAs, snoRNAs, sdRNAs, microRNAs, regulatory somal RNAs inside this subnuclear compartment. How- RNAs ever, years of research on the snoRNA biology have re- Received: 30 May, 2016; revised: 28 July, 2016; accepted: 08 August, vealed a tremendous number of unexpected discoveries 2016; available on-line: 26 October, 2016 that shed a new light on their functions in processes different than modifications of other RNAs. Small nucle- olar RNAs may take part in the regulation of metabolic INTRODUCTION stress responses, development of some diseases or dis- orders, like cancer or the Prader–Willi syndrome. More- Small nucleolar RNAs (snoRNAs) are one of the over, there is a growing number of evidence that mature most ancient and evolutionarily conserved non-protein snoRNAs undergo further processing into stable shorter coding RNAs. They have been identified in Eukaryotes, fragments, known as snoRNA-derived RNAs (sdRNAs) Archaea and one in the Epstein-Barr virus (Hutzinger et (Falaleeva & Stamm, 2013; Li et al., 2012). Such frag- al., 2009). There are two classes of snoRNAs (C/D and ments are present in many organisms, including mam- H/ACA box) that function as ribonucleoprotein (RNP) mals (Bortolin-Cavaille & Cavaille, 2012; Kishore et al., complexes to guide enzymatic modifications of other 2010; Ender et al., 2008; Bai et al., 2014; Brameier et al., RNAs, mainly ribosomal RNAs (rRNAs). Posttranscrip- 2011; Burroughs et al., 2011), a primitive protozoan Giar- tional rRNA modifications are common for all domains dia lamblia (Saraiya & Wang, 2008), budding yeast Sac- of life; there are three basic types: base methylation, ri- charomyces cerevisiae (Żywicki et al., 2012; Walkowiak et al., bose methylation and pseudouridylation. 2016) and the Epstein-Barr virus (Hutzinger et al., 2009). C/D box snoRNAs take their name from the con- Interestingly, these fragments associate with proteins dif- served sequence elements that they contain, known as ferent than the full-length snoRNAs do, and therefore C/C’ (RUGAUGA, R=purine) and D/D’ (CUGA) box- possibly fulfill distinct cellular functions. Moreover, such es, located near the 5’ and 3’ ends of the snoRNA, re- snoRNA cleavage in yeast cells is most prominent under spectively. C/D box snoRNAs form a ribonucleoprotein non-optimal growth conditions, which include UV irra- complex with 2’-O-methyltransferase fibrillarin and such diation, anaerobic growth, growth in a high or low pH snoRNP complex methylates the target RNAs. A con- served region of 10–21 nucleotides (nt) upstream of the *e-mail: [email protected] D and/or D’ box is complementary to the methylation Abbreviations: 5-HT2CR, 5-hydroxytryptamine receptor 2; Ago, Argonaute protein; CRHR1, corticotropin-releasing hormone recep- site of the target RNA and enables the snoRNA to form tor 1; EBV, Epstein-Barr virus; DPM2, dolichol phosphate-mannose an RNA duplex with the RNA. H/ACA box snoRNAs biosynthesis regulatory protein; HEK293, human embryonic kidney in turn form complexes with the pseudouridine synthase 293 cells; hnRNP, heterogeneous nuclear ribonucleoprotein; HN- dyskerin and perform pseudouridylation. Small nucleolar SCC, head and neck squamous cell carcinomas; MAPK/ERK, mito- gen-activated protein kinases; originally called ERK, extracellular RNAs from this class are built by two stems that form signal-regulated kinases; miRNA, microRNA; mRNA, messenger a pseudouridinilation pocket and two single stranded RNA; ncRNA, non-protein coding RNA; NGS, next generation se- regions that enclose the H (ANANNA) and ACA ele- quencing, NSCLC, non-small-cell lung carcinoma; PBRM1, protein ments. polybromo-1; PCR, polymerase chain reaction; PWS, Prader–Willi syndrome; qRT-PCR, quantitative real-time reverse transcriptase Many studies have investigated snoRNA-guided mod- PCR; RALGPS1, Ral GEF with PH domain and SH3 binding motif ifications. As a result, some features characterizing the 1 protein; RNP, ribonucleoprotein complex; rRNA, ribosomal RNA; functional snoRNA-target site interactions have been sdRNA, small RNA derived from snoRNA; SL-RT-PCR, stem-loop inferred and are used in the computational prediction reverse transcription combined with polymerase chain reaction; snoRNA, small nucleolar RNA; TAF1, transcription initiation factor of snoRNA targets (e.g. sequence complementarity be- TFIID subunit 1; TGF-β, transforming growth factor β 602 A. M. Mleczko and K. Bąkowska-Żywicka 2016 medium or growth in a medium with no amino acids SNORD44 (RNU44) – 71.4% of all nucleolar sdRNAs. or sugars (Żywicki et al., 2012; Tyczewska et al., 2016). Few of the sdRNAs were detected in the cytoplasmic Such response to changing environment may therefore fraction, which could suggest their functional potential indicate that snoRNA processing may play a crucial role in processes different than those in which the mature in the stress-dependent metabolism regulation, similar precursors act (since full-length snoRNAs are localized as in case of tRNA processing (Mleczko et al., 2014). In and perform their function in the nucleolus). The list of this article, we highlight the current state of the art con- discovered snoRNA-derived small RNAs is presented in cerning non-canonical roles of snoRNAs and their deriv- Table 1. atives, sdRNAs, with emphasis on their role in human Concerning the function of sdRNAs in the cells, the disorders. first and breakthrough functional study came from the Meister group. It demonstrated the miRNA-like activity PROCESSING OF snoRNAs TO sdRNAs – of an sdRNA originating from ACA45 snoRNA (Ender DISCOVERING NOVEL FUNCTIONS OF KNOWN RNAs et al., 2008). This particular sdRNA was identified in the Ago-associated RNA library. Importantly, the sequencing reads were found to be conserved in mammals, suggest- In 2008, an unbiased sequencing study (aimed at ing that they are, indeed, specific processing products. In capturing all potential human small RNAs in a range terms of both, processing and function, ACA45 sdRNA of 19–40 nt) led to the observation of specific pro- was similar to miRNAs. Firstly, this sdRNA was pro- cessing and accumulation of small RNAs originating duced in the HEK293 cells in a Dicer-dependent man- from well-characterized non-coding RNAs, including ner. Secondly, an endogenous target RNA has been snoRNAs (Kawai et al., 2008). In the next year, by sys- identified (CDC2L6 – a component of the mediator tematic analyses of deep-sequencing libraries from diverse complex) and experimentally confirmed. ACA45 sdRNA eukaryotic organisms, Taft and coworkers (2009) revealed was able to inhibit the activity of a CDC2L6 target in that small RNAs with evolutionarily conserved size and a miRNA-like pattern. Notably, the same authors identi- position, are derived from the vast majority of snoRNA fied seven additional sdRNAs with miRNA-like process- loci in animals (human, mouse, chicken, fruit fly), thale ing features in the follow-up experiments. Parallel NGS cress and fission yeast. Later on, a comparison of hu- studies of the small transcriptome in mice revealed the man small RNA deep sequencing data sets revealed that presence of snoRNA-originating miRNA-like molecules box C/D sdRNA accumulation patterns are conserved in embryonic stem cells and demonstrated that sdRNAs across multiple cell types (Scott et al., 2012). Recently, in 2014, Laiho and coworkers performed deep sequencing exhibit tissue specific expression (Babiarz et al., 2008; Ba- biarz et al., 2011). of small RNomes in subcellular compartments of the At the same time, two functional snoRNA-originat- HeLa cells (Bai et al., 2014). The nucleolar small RNAs were predominantly represented by 19–20 nt and 25 nt ing miRNA-like RNAs were described in the protozo- reads and 93% of them were mapping to the box C/D an Giardia lamblia, a unicellular parasite whose genome snoRNAs. The most abundantly represented locus does not encode Drosha: miRNA2 (Saraiya & Wang, 2008) and miRNA5 (Li et al., 2011). These miRNA-like among the sdRNA reads in the nucleolar fraction was sdRNAs associated with the Ago
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