Abstract
A search for early response genes that are activated following germ cell induction from mouse embryonic stem cells in vitro led us to the isolation of a long noncoding RNA that contains a SINE (short interspersed element)-B1F motif that was named R53. In situ hybridization and northern blot analyses revealed that the R53 subfragment RNA bears a B1F motif, is processed from the primary transcript, is expressed in adult testis and is predominantly localized in meiotic metaphase chromatin during spermatogenesis. Recent studies of chromosome-associated RNAs have explored novel functions of noncoding RNAs. Specifically, chromosome-bound noncoding RNAs function not only as structural components of chromosome but also as scaffolds that recruit epigenetic modulators for transcriptional regulation, and they are dynamically rearranged during the cell cycle. However, few studies have explored meiotic chromatin; thus, R53 RNA appears to be the first long noncoding RNA to be tightly associated with the metaphase chromatin during spermatogenesis. Furthermore, R53 knockdown using a lentivirus-mediated RNAi injected into mouse testis and organ culture of the fragments revealed a remarkable reduction in postmeiotic cells and irregular up-regulation of several postmeiotic genes, which suggests the possibility that the SINE-B1-derived noncoding RNA R53 plays an indispensable role in the transcriptional regulation of key spermatogenesis genes.
Highlights
Recent investigations have revealed that transposable element (TE) inserts, which account for nearby 50% of most eukaryotic genomes, are not ‘junk’ or ‘parasite’ DNA but rather have great potential to cause drastic changes in the developmental pattern of gene expression by increasing genetic variation and the recombination rate [1,2,3]
The R53 sequence contains a SINE-B1 motif (133 bp) that belongs to the B1F subfamily, which is one of six subfamilies (B1A-F) that are distinguishable at several diagnostic positions [10, 20] (Fig 1A)
Because the sequences in the R53-B1F motif that correspond to the promoter boxes exhibit a remarkable differences relative to the consensus (Fig 1A) and the motif ends without a polyA-stretch, it seems likely that the R53-B1F element itself cannot be transcribed by Pol III and exhibits greatly reduced, if any, transposition activity [24]
Summary
Recent investigations have revealed that transposable element (TE) inserts, which account for nearby 50% of most eukaryotic genomes, are not ‘junk’ or ‘parasite’ DNA but rather have great potential to cause drastic changes in the developmental pattern of gene expression by increasing genetic variation and the recombination rate [1,2,3]. SINEs are one of the major classes of TEs, which include long interspersed elements (LINEs) and retrovirus-. A SINE-B1 RNA associates with meiotic metaphase chromatin like long terminal repeat (LTR). SINEs originate from within small RNAs, such as 7SLRNA (cytoplasmic signal recognition particle), rRNA and tRNA, and unlike LINEs and LTRs, SINEs have their own internal RNA polymerase III (polIII) promoter [6]. Some SINE sequences have been demonstrated to function in gene expression and chromosome organization at the insertion site via the internal binding sites for various transcriptional factors (TFs) and epigenetic modifiers [2, 3, 8,9,10,11,12]
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