Somatic Primary piRNA Biogenesis Driven by cis-Acting RNA Elements and trans-Acting Yb

Hirotsugu Ishizu; Yuka W. Iwasaki; Shigeki Hirakata; Haruka Ozaki; Wataru Iwasaki; Haruhiko Siomi; Mikiko C. Siomi

doi:10.1016/j.celrep.2015.06.035

Somatic Primary piRNA Biogenesis Driven by cis-Acting RNA Elements and trans-Acting Yb

Hirotsugu Ishizu, Yuka W. Iwasaki, Shigeki Hirakata, Haruka Ozaki, Wataru Iwasaki, Haruhiko Siomi, Mikiko C. Siomi

Department of Molecular Biology

Research output: Contribution to journal › Article › peer-review

57 Citations (Scopus)

Abstract

Primary piRNAs in Drosophila ovarian somatic cells arise from piRNA cluster transcripts and the 3' UTRs of a subset of mRNAs, including Traffic jam (Tj) mRNA. However, it is unclear how these RNAs are determined as primary piRNA sources. Here, we identify a cis-acting 100-nt fragment in the Tj 3' UTR that is sufficient for producing artificial piRNAs from unintegrated DNA. These artificial piRNAs were effective in endogenous gene transcriptional silencing. Yb, a core component of primary piRNA biogenesis center Yb bodies, directly bound the Tj-cis element. Disruption of this interaction markedly reduced piRNA production. Thus, Yb is the trans-acting partner of the Tj-cis element. Yb-CLIP revealed that Yb binding correlated with somatic piRNA production but Tj-cis element downstream sequences produced few artificial piRNAs. We thus propose that Yb determines primary piRNA sources through two modes of action: primary binding to cis elements to specify substrates and secondary binding to downstream regions to increase diversity in piRNA populations.

Original language	English
Pages (from-to)	429-440
Number of pages	12
Journal	Cell Reports
Volume	12
Issue number	3
DOIs	https://doi.org/10.1016/j.celrep.2015.06.035
Publication status	Published - 2015 Jul 21

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology(all)

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10.1016/j.celrep.2015.06.035

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title = "Somatic Primary piRNA Biogenesis Driven by cis-Acting RNA Elements and trans-Acting Yb",

abstract = "Primary piRNAs in Drosophila ovarian somatic cells arise from piRNA cluster transcripts and the 3' UTRs of a subset of mRNAs, including Traffic jam (Tj) mRNA. However, it is unclear how these RNAs are determined as primary piRNA sources. Here, we identify a cis-acting 100-nt fragment in the Tj 3' UTR that is sufficient for producing artificial piRNAs from unintegrated DNA. These artificial piRNAs were effective in endogenous gene transcriptional silencing. Yb, a core component of primary piRNA biogenesis center Yb bodies, directly bound the Tj-cis element. Disruption of this interaction markedly reduced piRNA production. Thus, Yb is the trans-acting partner of the Tj-cis element. Yb-CLIP revealed that Yb binding correlated with somatic piRNA production but Tj-cis element downstream sequences produced few artificial piRNAs. We thus propose that Yb determines primary piRNA sources through two modes of action: primary binding to cis elements to specify substrates and secondary binding to downstream regions to increase diversity in piRNA populations.",

author = "Hirotsugu Ishizu and Iwasaki, {Yuka W.} and Shigeki Hirakata and Haruka Ozaki and Wataru Iwasaki and Haruhiko Siomi and Siomi, {Mikiko C.}",

note = "Funding Information: We thank the other members of the M.C.S. laboratories for their discussions and comments on the manuscript. We also thank T. Fukunaga for bioinformatics assistance. This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan to H.I., Y.W.I., W.I., H.S., and M.C.S. Publisher Copyright: {\textcopyright} 2015 The Authors.",

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AU - Ishizu, Hirotsugu

AU - Iwasaki, Yuka W.

AU - Hirakata, Shigeki

AU - Ozaki, Haruka

AU - Iwasaki, Wataru

AU - Siomi, Haruhiko

AU - Siomi, Mikiko C.

N1 - Funding Information: We thank the other members of the M.C.S. laboratories for their discussions and comments on the manuscript. We also thank T. Fukunaga for bioinformatics assistance. This work was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan to H.I., Y.W.I., W.I., H.S., and M.C.S. Publisher Copyright: © 2015 The Authors.

PY - 2015/7/21

Y1 - 2015/7/21

N2 - Primary piRNAs in Drosophila ovarian somatic cells arise from piRNA cluster transcripts and the 3' UTRs of a subset of mRNAs, including Traffic jam (Tj) mRNA. However, it is unclear how these RNAs are determined as primary piRNA sources. Here, we identify a cis-acting 100-nt fragment in the Tj 3' UTR that is sufficient for producing artificial piRNAs from unintegrated DNA. These artificial piRNAs were effective in endogenous gene transcriptional silencing. Yb, a core component of primary piRNA biogenesis center Yb bodies, directly bound the Tj-cis element. Disruption of this interaction markedly reduced piRNA production. Thus, Yb is the trans-acting partner of the Tj-cis element. Yb-CLIP revealed that Yb binding correlated with somatic piRNA production but Tj-cis element downstream sequences produced few artificial piRNAs. We thus propose that Yb determines primary piRNA sources through two modes of action: primary binding to cis elements to specify substrates and secondary binding to downstream regions to increase diversity in piRNA populations.

AB - Primary piRNAs in Drosophila ovarian somatic cells arise from piRNA cluster transcripts and the 3' UTRs of a subset of mRNAs, including Traffic jam (Tj) mRNA. However, it is unclear how these RNAs are determined as primary piRNA sources. Here, we identify a cis-acting 100-nt fragment in the Tj 3' UTR that is sufficient for producing artificial piRNAs from unintegrated DNA. These artificial piRNAs were effective in endogenous gene transcriptional silencing. Yb, a core component of primary piRNA biogenesis center Yb bodies, directly bound the Tj-cis element. Disruption of this interaction markedly reduced piRNA production. Thus, Yb is the trans-acting partner of the Tj-cis element. Yb-CLIP revealed that Yb binding correlated with somatic piRNA production but Tj-cis element downstream sequences produced few artificial piRNAs. We thus propose that Yb determines primary piRNA sources through two modes of action: primary binding to cis elements to specify substrates and secondary binding to downstream regions to increase diversity in piRNA populations.

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Somatic Primary piRNA Biogenesis Driven by cis-Acting RNA Elements and trans-Acting Yb

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