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Nuclear-localized tiny RNAs are associated with transcription initiation and splice sites in metazoans

ABSTRACT: We have recently shown that transcription initiation RNAs (tiRNAs) are derived from sequences downstream of transcription start sites. Here we report the identification of a second class of nuclear-specific ~17-18 nucleotide small RNA whose 3’ ends map precisely to the splice donor site of internal exons in animals. These splice-site RNAs (spliRNAs) are associated with highly expressed genes, and show evidence of developmental stage- and region-specific expression. We also confirm that tiRNAs are nuclear localized, enriched at chromatin marks associated with transcription initiation, and possess a 3’ nucleotide bias. Additionally, we find that microRNA-offset RNAs (moRNAs), the oncogenic miR-15/16 cluster and most snoRNA-derived small RNAs (sdRNAs) are enriched in the nucleus, whereas most miRNAs and two H/ACA sdRNAs are cytoplasmically enriched. We propose that nuclear localized tiny RNAs are involved in epigenetic regulation of gene expression.

ORGANISM(S): Homo sapiens

PROVIDER: GSE20664 | GEO | 2010/07/01

SECONDARY ACCESSION(S): PRJNA124917

REPOSITORIES: GEO

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Project description:Pervasive transcription in the mammalian genome produces thousands of long noncoding RNAs (lncRNAs) and promoter- or enhancer-associated unstable transcripts. They preferentially locate to chromatin, at which some regulate chromatin structure, transcription and RNA processing. While several RNA sequences responsible for nuclear localization have been identified, such as repeats in the lncRNA Xist and Alu-like elements for long RNAs, how lncRNAs as a class are enriched on chromatin remains elusive. To screen for cis-elements that contribute to RNA-chromatin localization, we developed a high-throughput method named RNA elements for subcellular localization by sequencing (REL-seq), and discovered a U1 small nuclear ribonucleoprotein (snRNP)-recognition motif being critical for chromatin localization of reporter RNAs. Across the genome, chromatin-bound lncRNAs, which are enriched with 5’ splice sites and depleted of 3’ splice sites, exhibit high levels of U1 snRNA binding compared to cytoplasm-localized protein-coding mRNAs. Acute depletion of U1 snRNA, or U1 snRNP protein component SNRNP70, drastically reduces the chromatin association of hundreds of lncRNAs and unstable transcripts without altering the overall transcription rate in cells. In addition, rapid degradation of SNRNP70 reduces the localization of both nascent and polyadenylated lncRNA transcripts to chromatin, and disrupts the nuclear-speckles and genome-wide localization of Malat1, a highly conserved and abundant lncRNA. Moreover, chromatin-bound U1 snRNP interacts with transcriptionally engaged RNA polymerase (Pol) II. Together, these results demonstrate that U1 snRNP acts widely to tether and mobilize lncRNAs to chromatin in a Pol II transcription-dependent manner. Our findings uncover a novel role of U1 snRNP beyond pre-mRNA processing and provide molecular insights into how lncRNAs are recruited to Pol II-transcribed genes and have a propensity for chromatin-associated functions.

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Nuclear-localized tiny RNAs are associated with transcription initiation and splice sites in metazoans

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