Abstract
To date, the vast majority of known virus-encoded microRNAs (miRNAs) are derived from polymerase II transcripts encoded by DNA viruses. A recent demonstration that the bovine leukemia virus, a retrovirus, uses RNA polymerase III to directly transcribe the pre-miRNA hairpins to generate viral miRNAs further supports the common notion that the canonical pathway of miRNA biogenesis does not exist commonly among RNA viruses. Here, we show that an exogenous virus-specific region, termed the E element or XSR, of avian leukosis virus subgroup J (ALV-J), a member of avian retrovirus, encodes a novel miRNA, designated E (XSR) miRNA, using the canonical miRNA biogenesis pathway. Detection of novel microRNA species derived from the E (XSR) element, a 148-nucleotide noncoding RNA with hairpin structure, showed that the E (XSR) element has the potential to function as a microRNA primary transcript, demonstrating a hitherto unknown function with possible roles in myeloid leukosis associated with ALV-J.
Highlights
To date, the vast majority of known virus-encoded microRNAs are derived from polymerase II transcripts encoded by DNA viruses
During miRNA profiling of an avian leukosis virus subgroup J (ALV-J)-transformed turkey macrophage cell line IAH30 [25] by deep-sequence analysis on an Illumina GAIIx platform, we observed the presence of two distinct small RNA sequences that mapped perfectly to the E (XSR) element in the 3= untranslated region (UTR) of the HPRS-103 genome (GenBank accession number Z46390.1)
The 5= arm of the stem-loop sequence is the most abundant species present in the IAH30 library (Fig. 1C). These results strongly suggested that we had identified a premiRNA encoded within the E (XSR) element of avian leukosis virus (ALV)-J
Summary
The vast majority of known virus-encoded microRNAs (miRNAs) are derived from polymerase II transcripts encoded by DNA viruses. The retroviral genome includes a number of cis-acting elements [3] One such element is the 148-nucleotide exogenous virus-specific region (E or XSR) identified in the SR-A and Pr-C strains of RSV at the 5= and the 3= sides of the src gene, respectively [4, 5]. RNA viruses are generally thought not to contain pre-miRNA structures to avoid endonuclease-mediated cleavage of the genome, antigenome, and mRNAs. retroviruses have not been widely documented to exploit the miRNA pathway [21], a recent demonstration of a conserved cluster of RNA polymerase III (Pol III)-transcribed miRNAs from the bovine leukemia virus (BLV) genome [22, 23] showed the potential of retroviruses to encode miRNAs. The E (XSR) element sequences from ALV-J strains show hairpin-like structures suggestive of miRNA precursors the existence of any mature miRNA has not been demonstrated in ALV-J-infected/transformed cells. Using a deepsequencing approach on one of the ALV-J-transformed cell lines, we identified a novel small-RNA population encoded from within the E (XSR) element
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