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piRNA processing by a trimeric Schlafen-domain nuclease

Author

Listed:
  • Nadezda Podvalnaya

    (Institute of Molecular Biology
    Epigenetics & Genome Stability)

  • Alfred W. Bronkhorst

    (Institute of Molecular Biology)

  • Raffael Lichtenberger

    (Vienna Biocenter Campus (VBC)
    University of Vienna)

  • Svenja Hellmann

    (Institute of Molecular Biology)

  • Emily Nischwitz

    (Epigenetics & Genome Stability
    Institute of Molecular Biology)

  • Torben Falk

    (Vienna Biocenter Campus (VBC)
    University of Vienna)

  • Emil Karaulanov

    (Institute of Molecular Biology)

  • Falk Butter

    (University of Vienna
    Friedrich Loeffler Institute)

  • Sebastian Falk

    (Vienna Biocenter Campus (VBC)
    University of Vienna)

  • René F. Ketting

    (Institute of Molecular Biology
    Johannes Gutenberg University)

Abstract

Transposable elements are genomic parasites that expand within and spread between genomes1. PIWI proteins control transposon activity, notably in the germline2,3. These proteins recognize their targets through small RNA co-factors named PIWI-interacting RNAs (piRNAs), making piRNA biogenesis a key specificity-determining step in this crucial genome immunity system. Although the processing of piRNA precursors is an essential step in this process, many of the molecular details remain unclear. Here, we identify an endoribonuclease, precursor of 21U RNA 5′-end cleavage holoenzyme (PUCH), that initiates piRNA processing in the nematode Caenorhabditis elegans. Genetic and biochemical studies show that PUCH, a trimer of Schlafen-like-domain proteins (SLFL proteins), executes 5′-end piRNA precursor cleavage. PUCH-mediated processing strictly requires a 7-methyl-G cap (m7G-cap) and a uracil at position three. We also demonstrate how PUCH interacts with PETISCO, a complex that binds to piRNA precursors4, and that this interaction enhances piRNA production in vivo. The identification of PUCH concludes the search for the 5′-end piRNA biogenesis factor in C. elegans and uncovers a type of RNA endonuclease formed by three SLFL proteins. Mammalian Schlafen (SLFN) genes have been associated with immunity5, exposing a molecular link between immune responses in mammals and deeply conserved RNA-based mechanisms that control transposable elements.

Suggested Citation

  • Nadezda Podvalnaya & Alfred W. Bronkhorst & Raffael Lichtenberger & Svenja Hellmann & Emily Nischwitz & Torben Falk & Emil Karaulanov & Falk Butter & Sebastian Falk & René F. Ketting, 2023. "piRNA processing by a trimeric Schlafen-domain nuclease," Nature, Nature, vol. 622(7982), pages 402-409, October.
  • Handle: RePEc:nat:nature:v:622:y:2023:i:7982:d:10.1038_s41586-023-06588-2
    DOI: 10.1038/s41586-023-06588-2
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    Cited by:

    1. Gangming Zhang & Chunwei Zheng & Yue-he Ding & Craig Mello, 2024. "Casein kinase II promotes piRNA production through direct phosphorylation of USTC component TOFU-4," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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