Genome-wide expression analysis of a new class of lncRNAs driven by SINE B2

•Genome-wide transcription of B2-AS lncRNAs revealed via a B2-AS-specific approach.•B2 loci are related to variable RNA transcripts, including B2-AS lncRNA and B2 RNAs.•B2-AS lncRNA transcripts can be cleaved in vitro by the Dicer1 enzyme into small RNAs.•The presence of B2-AS lncRNAs imply both genome-wide and locus-specific effects.•Dicer1 down-regulation has a genome-wide impact on B2-locus transcription. Repetitive short interspersed elements B2 (SINE B2) have been shown to possess two promoters: polymerase III promoter for producing short B2-S RNAs and polymerase II promoter for driving the expression of long non-coding RNA (B2-AS lncRNAs). Using a B2-antisense (B2-AS) transcript sequence from the SINE B2 resident in mitochondrial translocator protein gene (Tspo) locus, we constructed a B2-AS specific RNA library and identified 96,862 sequences encoding potential B2-mediated lncRNAs, of which 55,592 lncRNAs with more than 390 nt in length possess a feature of potential genomic locus-specific effect. In addition, small RNA-Northern hybridization showed that the new B2-AS lncRNAs are constantly degraded by the Dicer1 enzyme, a finding further confirmed by in vitro Dicer1 enzyme digestion. B2-AS lncRNAs regulate the expression of target genes in a different fashion than B2-S RNAs. Genome-wide cross-comparison with mRNA mapping showed a total of 904 mRNA loci directly targeted by B2-AS lncRNAs, suggesting a locus-specific effect of the B2-AS lncRNAs and a general effect of B2-S RNAs.