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Retrotransposons and pseudogenes regulate mRNAs and lncRNAs via the piRNA pathway in the germline.

ABSTRACT: The eukaryotic genome has vast intergenic regions containing transposons, pseudogenes, and other repetitive sequences. They produce numerous long noncoding RNAs (lncRNAs) and Piwi-interacting RNAs (piRNAs), yet the functions of the vast intergenic regions remain largely unknown. Mammalian piRNAs are abundantly expressed from the spermatocyte to round spermatid stage, coinciding with the widespread expression of lncRNAs in these cells. Here, we show that piRNAs derived from transposons and pseudogenes mediate the degradation of a large number of mRNAs and lncRNAs in mouse late spermatocytes. In particular, they have a large impact on the lncRNA transcriptome, as a quarter of lncRNAs expressed in late spermatocytes are up-regulated in mice deficient in the piRNA pathway. Furthermore, our genomic and in vivo functional analyses reveal that retrotransposon sequences in the 3' UTR of mRNAs are targeted by piRNAs for degradation. Similarly, the degradation of spermatogenic cell-specific lncRNAs by piRNAs is mediated by retrotransposon sequences. Moreover, we show that pseudogenes regulate mRNA stability via the piRNA pathway. The degradation of mRNAs and lncRNAs by piRNAs requires PIWIL1 (also known as MIWI) and, at least in part, depends on its slicer activity. Together, these findings reveal the presence of a highly complex and global RNA regulatory network mediated by piRNAs with retrotransposons and pseudogenes as regulatory sequences.

SUBMITTER: Watanabe T

PROVIDER: S-EPMC4352877 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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Retrotransposons and pseudogenes regulate mRNAs and lncRNAs via the piRNA pathway in the germline.

Watanabe Toshiaki T Cheng Ee-chun EC Zhong Mei M Lin Haifan H

Genome research 20141205 3

The eukaryotic genome has vast intergenic regions containing transposons, pseudogenes, and other repetitive sequences. They produce numerous long noncoding RNAs (lncRNAs) and Piwi-interacting RNAs (piRNAs), yet the functions of the vast intergenic regions remain largely unknown. Mammalian piRNAs are abundantly expressed from the spermatocyte to round spermatid stage, coinciding with the widespread expression of lncRNAs in these cells. Here, we show that piRNAs derived from transposons and pseudo ...[more]

PMID: 25480952

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Project description:BACKGROUND:Piwi-interacting RNAs (piRNAs) are a special class of small RNAs that provide defense against transposable elements in animal germline cells. In Drosophila, germline piRNAs are thought to be processed at a unique perinuclear structure, the nuage, that houses piRNA pathway proteins including the Piwi clade of Argonaute family proteins, along with several Tudor domain proteins, RNA helicases and nucleases. We previously demonstrated that Tudor domain protein Tejas (Tej), an ortholog of vertebrate Tdrd5, is an important component of the piRNA pathway. RESULTS:In the current study, we identified the paralog of the Drosophila tej gene, tapas (tap), which is an ortholog of vertebrate Tdrd7. Like Tej, Tap is localized at the nuage. Alone, tap loss leads to a mild increase in transposon expression and decrease in piRNAs targeting transposons expressed in the germline. The tap gene genetically interacts with other piRNA pathway genes and we also show that Tap physically interacts with piRNA pathway components, such as Piwi family proteins Aubergine and Argonaute3 and the RNA helicases Spindle-E and Vasa. Together with tej, tap is required for survival of germline cells during early stages and for polarity formation. We further observed that loss of tej and tap together results in more severe defects in the piRNA pathway in germline cells compared to single mutants: the double-mutant ovaries exhibit mis-localization of piRNA pathway components and significantly greater reduction of piRNAs against transposons predominantly expressed in germline compared to single mutants. The single or double mutants did not have any reduction in piRNAs mapping to transposons predominantly expressed in gonadal somatic cells or those derived from unidirectional clusters such as flamenco. Consistently, the loss of both tej and tap function resulted in mis-localization of Piwi in germline cells, whereas Piwi remained localized to the nucleus in somatic cells. CONCLUSIONS:Our observations suggest that tej and tap work together for germline maintenance. tej and tap also function in a synergistic manner to maintain examined piRNA components at the perinuclear nuage and for piRNA production in Drosophila germline cells.

Dataset Information

Retrotransposons and pseudogenes regulate mRNAs and lncRNAs via the piRNA pathway in the germline.

Publications

Retrotransposons and pseudogenes regulate mRNAs and lncRNAs via the piRNA pathway in the germline.

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