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Siwi cooperates with Par-1 kinase to resolve the autoinhibitory effect of Papi for Siwi-piRISC biogenesis

Author

Listed:
  • Hiromi Yamada

    (The University of Tokyo)

  • Kazumichi M. Nishida

    (The University of Tokyo)

  • Yuka W. Iwasaki

    (Keio University School of Medicine
    Precursory Research for Embryonic Science and Technology)

  • Yosuke Isota

    (The University of Tokyo)

  • Lumi Negishi

    (The University of Tokyo)

  • Mikiko C. Siomi

    (The University of Tokyo)

Abstract

Bombyx Papi acts as a scaffold for Siwi-piRISC biogenesis on the mitochondrial surface. Papi binds first to Siwi via the Tudor domain and subsequently to piRNA precursors loaded onto Siwi via the K-homology (KH) domains. This second action depends on phosphorylation of Papi. However, the underlying mechanism remains unknown. Here, we show that Siwi targets Par-1 kinase to Papi to phosphorylate Ser547 in the auxiliary domain. This modification enhances the ability of Papi to bind Siwi-bound piRNA precursors via the KH domains. The Papi S547A mutant bound to Siwi, but evaded phosphorylation by Par-1, abrogating Siwi-piRISC biogenesis. A Papi mutant that lacked the Tudor and auxiliary domains escaped coordinated regulation by Siwi and Par-1 and bound RNAs autonomously. Another Papi mutant that lacked the auxiliary domain bound Siwi but did not bind piRNA precursors. A sophisticated mechanism by which Siwi cooperates with Par-1 kinase to promote Siwi-piRISC biogenesis was uncovered.

Suggested Citation

  • Hiromi Yamada & Kazumichi M. Nishida & Yuka W. Iwasaki & Yosuke Isota & Lumi Negishi & Mikiko C. Siomi, 2022. "Siwi cooperates with Par-1 kinase to resolve the autoinhibitory effect of Papi for Siwi-piRISC biogenesis," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29193-9
    DOI: 10.1038/s41467-022-29193-9
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    References listed on IDEAS

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    1. Kazumichi M. Nishida & Kazuhiro Sakakibara & Yuka W. Iwasaki & Hiromi Yamada & Ryo Murakami & Yukiko Murota & Takeshi Kawamura & Tatsuhiko Kodama & Haruhiko Siomi & Mikiko C. Siomi, 2018. "Hierarchical roles of mitochondrial Papi and Zucchini in Bombyx germline piRNA biogenesis," Nature, Nature, vol. 555(7695), pages 260-264, March.
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    Cited by:

    1. Hiroya Yamazaki & Yurika Namba & Shogo Kuriyama & Kazumichi M. Nishida & Asako Kajiya & Mikiko C. Siomi, 2023. "Bombyx Vasa sequesters transposon mRNAs in nuage via phase separation requiring RNA binding and self-association," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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    1. Hiroya Yamazaki & Yurika Namba & Shogo Kuriyama & Kazumichi M. Nishida & Asako Kajiya & Mikiko C. Siomi, 2023. "Bombyx Vasa sequesters transposon mRNAs in nuage via phase separation requiring RNA binding and self-association," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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