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Crystal structure of Drosophila Piwi

Author

Listed:
  • Sonomi Yamaguchi

    (The University of Tokyo)

  • Akira Oe

    (The University of Tokyo)

  • Kazumichi M. Nishida

    (The University of Tokyo)

  • Keitaro Yamashita

    (The University of Tokyo)

  • Asako Kajiya

    (The University of Tokyo)

  • Seiichi Hirano

    (The University of Tokyo)

  • Naoki Matsumoto

    (The University of Tokyo)

  • Naoshi Dohmae

    (RIKEN Center for Sustainable Resource Science)

  • Ryuichiro Ishitani

    (The University of Tokyo)

  • Kuniaki Saito

    (Invertebrate Genetics Laboratory, National Institute of Genetics)

  • Haruhiko Siomi

    (Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku)

  • Hiroshi Nishimasu

    (The University of Tokyo)

  • Mikiko C. Siomi

    (The University of Tokyo)

  • Osamu Nureki

    (The University of Tokyo)

Abstract

PIWI-clade Argonaute proteins associate with PIWI-interacting RNAs (piRNAs), and silence transposons in animal gonads. Here, we report the crystal structure of the Drosophila PIWI-clade Argonaute Piwi in complex with endogenous piRNAs, at 2.9 Å resolution. A structural comparison of Piwi with other Argonautes highlights the PIWI-specific structural features, such as the overall domain arrangement and metal-dependent piRNA recognition. Our structural and biochemical data reveal that, unlike other Argonautes including silkworm Siwi, Piwi has a non-canonical DVDK tetrad and lacks the RNA-guided RNA cleaving slicer activity. Furthermore, we find that the Piwi mutant with the canonical DEDH catalytic tetrad exhibits the slicer activity and readily dissociates from less complementary RNA targets after the slicer-mediated cleavage, suggesting that the slicer activity could compromise the Piwi-mediated co-transcriptional silencing. We thus propose that Piwi lost the slicer activity during evolution to serve as an RNA-guided RNA-binding platform, thereby ensuring faithful co-transcriptional silencing of transposons.

Suggested Citation

  • Sonomi Yamaguchi & Akira Oe & Kazumichi M. Nishida & Keitaro Yamashita & Asako Kajiya & Seiichi Hirano & Naoki Matsumoto & Naoshi Dohmae & Ryuichiro Ishitani & Kuniaki Saito & Haruhiko Siomi & Hiroshi, 2020. "Crystal structure of Drosophila Piwi," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-14687-1
    DOI: 10.1038/s41467-020-14687-1
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    Cited by:

    1. Birgit Stallmeyer & Clara Bühlmann & Rytis Stakaitis & Ann-Kristin Dicke & Farah Ghieh & Luisa Meier & Ansgar Zoch & David MacKenzie MacLeod & Johanna Steingröver & Özlem Okutman & Daniela Fietz & Adr, 2024. "Inherited defects of piRNA biogenesis cause transposon de-repression, impaired spermatogenesis, and human male infertility," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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