Abstract

PIWI-interacting RNAs (piRNAs) are small noncoding RNAs that bind PIWI family proteins exclusively expressed in the germ cells of mammalian gonads. MIWI2-associated piRNAs are essential for silencing transposons during primordial germ cell development, and MIWI-bound piRNAs are required for normal spermatogenesis during adulthood in mice. Although piRNAs have long been regarded as germ cell-specific, increasing lines of evidence suggest that somatic cells also express piRNA-like RNAs (pilRNAs). Here, we report the detection of abundant pilRNAs in somatic cells, which are similar to MIWI-associated piRNAs mainly expressed in pachytene spermatocytes and round spermatids in the testis. Based on small RNA deep sequencing and quantitative PCR analyses, pilRNA expression is dynamic and displays tissue specificity. Although pilRNAs are similar to pachytene piRNAs in both size and genomic origins, they have a distinct ping-pong signature. Furthermore, pilRNA biogenesis appears to utilize a yet to be identified pathway, which is different from all currently known small RNA biogenetic pathways. In addition, pilRNAs appear to preferentially target the 3'-UTRs of mRNAs in a partially complementary manner. Our data suggest that pilRNAs, as an integral component of the small RNA transcriptome in somatic cell lineages, represent a distinct population of small RNAs that may have functions similar to germ cell piRNAs.

Highlights

  • Germ cells exclusively express PIWI-interacting small RNAs for transposon and gene regulation

  • PiRNAs have long been regarded as germ cell-specific, increasing lines of evidence suggest that somatic cells express PIWI-interacting RNAs (piRNAs)-like RNAs

  • Identification of piRNA-like RNAs (pilRNAs) in Somatic Cells/Tissues—We initially searched for pilRNAs from sequence reads of three small noncoding RNA libraries prepared using murine Sertoli cells purified from postnatal day 6 testes, ICCs of the murine gastrointestinal tract, and small intestine based on criteria described previously [16]

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Summary

Background

Germ cells exclusively express PIWI-interacting small RNAs for transposon and gene regulation. We report the detection of abundant pilRNAs in somatic cells, which are similar to MIWIassociated piRNAs mainly expressed in pachytene spermatocytes and round spermatids in the testis. Our data suggest that pilRNAs, as an integral component of the small RNA transcriptome in somatic cell lineages, represent a distinct population of small RNAs that may have functions similar to germ cell piRNAs. PIWI-interacting RNAs (piRNAs) were discovered by virtue of their ability to bind to PIWI proteins, which are exclusively. During male germ cell development, repetitive sequence-derived piRNAs are mainly expressed in primordial germ cells in fetal testes, whereas nonrepetitive sequence-derived piRNAs are predominantly expressed in pachytene spermatocytes and round spermatids in adult testes [9].

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