Abstract
BackgroundSmall nucleolar RNAs (snoRNAs) are mid-size non-coding RNAs required for ribosomal RNA modification, implying a ubiquitous tissue distribution linked to ribosome synthesis. However, increasing numbers of studies identify extra-ribosomal roles of snoRNAs in modulating gene expression, suggesting more complex snoRNA abundance patterns. Therefore, there is a great need for mapping the snoRNome in different human tissues as the blueprint for snoRNA functions.ResultsWe used a low structure bias RNA-Seq approach to accurately quantify snoRNAs and compare them to the entire transcriptome in seven healthy human tissues (breast, ovary, prostate, testis, skeletal muscle, liver, and brain). We identify 475 expressed snoRNAs categorized in two abundance classes that differ significantly in their function, conservation level, and correlation with their host gene: 390 snoRNAs are uniformly expressed and 85 are enriched in the brain or reproductive tissues. Most tissue-enriched snoRNAs are embedded in lncRNAs and display strong correlation of abundance with them, whereas uniformly expressed snoRNAs are mostly embedded in protein-coding host genes and are mainly non- or anticorrelated with them. Fifty-nine percent of the non-correlated or anticorrelated protein-coding host gene/snoRNA pairs feature dual-initiation promoters, compared to only 16% of the correlated non-coding host gene/snoRNA pairs.ConclusionsOur results demonstrate that snoRNAs are not a single homogeneous group of housekeeping genes but include highly regulated tissue-enriched RNAs. Indeed, our work indicates that the architecture of snoRNA host genes varies to uncouple the host and snoRNA expressions in order to meet the different snoRNA abundance levels and functional needs of human tissues.
Highlights
Small nucleolar RNAs are mid-size non-coding RNAs required for ribosomal RNA modification, implying a ubiquitous tissue distribution linked to ribosome synthesis
Most expressed human snoRNAs are produced from intron-embedded genes To determine the tissue distribution of snoRNAs and their relative abundance within the human transcriptome, we sequenced total ribodepleted fragmented RNA from seven healthy human tissues
The majority of box H/ACA snoRNAs (50%) are the only snoRNA embedded within their host genes (HGs) (Fig. 1A middle panel, mono-intronic HG), while the majority of box C/D snoRNAs (78%) are encoded with multiple snoRNAs in separate introns of the same HG (Fig. 1A right panel, multi-intronic HG)
Summary
Small nucleolar RNAs (snoRNAs) are mid-size non-coding RNAs required for ribosomal RNA modification, implying a ubiquitous tissue distribution linked to ribosome synthesis. Small nucleolar RNAs (snoRNAs) are a conserved family of mid-size non-coding RNA best characterized as guides for the chemical modification of nascent ribosomal RNA (rRNA) [1,2,3]. Functional snoRNAs are a part of larger ribonucleoprotein complexes (snoRNPs) composed of core proteins required for snoRNA stability that represent an enzymatic moiety needed for the RNA modification reaction [2, 4,5,6]. A small number of box C/D snoRNAs have been shown to guide the acetylation of rRNA [9, 10]. Other snoRNAs have no known target in rRNA or snRNAs and are referred to as “orphan” snoRNAs [8]
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