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Bombyx Vasa sequesters transposon mRNAs in nuage via phase separation requiring RNA binding and self-association

Author

Listed:
  • Hiroya Yamazaki

    (The University of Tokyo)

  • Yurika Namba

    (The University of Tokyo)

  • Shogo Kuriyama

    (The University of Tokyo)

  • Kazumichi M. Nishida

    (The University of Tokyo)

  • Asako Kajiya

    (The University of Tokyo
    Kyoto University)

  • Mikiko C. Siomi

    (The University of Tokyo)

Abstract

Bombyx Vasa (BmVasa) assembles non-membranous organelle, nuage or Vasa bodies, in germ cells, known as the center for Siwi-dependent transposon silencing and concomitant Ago3-piRISC biogenesis. However, details of the body assembly remain unclear. Here, we show that the N-terminal intrinsically disordered region (N-IDR) and RNA helicase domain of BmVasa are responsible for self-association and RNA binding, respectively, but N-IDR is also required for full RNA-binding activity. Both domains are essential for Vasa body assembly in vivo and droplet formation in vitro via phase separation. FAST-iCLIP reveals that BmVasa preferentially binds transposon mRNAs. Loss of Siwi function derepresses transposons but has marginal effects on BmVasa-RNA binding. This study shows that BmVasa assembles nuage by phase separation via its ability to self-associate and bind newly exported transposon mRNAs. This unique property of BmVasa allows transposon mRNAs to be sequestered and enriched in nuage, resulting in effective Siwi-dependent transposon repression and Ago3-piRISC biogenesis.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37634-2
    DOI: 10.1038/s41467-023-37634-2
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    References listed on IDEAS

    as
    1. 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.
    2. Song Xue & Fan Zhou & Tian Zhao & Huimin Zhao & Xuewei Wang & Long Chen & Jin-ping Li & Shi-Zhong Luo, 2022. "Phase separation on cell surface facilitates bFGF signal transduction with heparan sulphate," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    3. 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.
    4. Mylene C. Ferrolino & Diana M. Mitrea & J. Robert Michael & Richard W. Kriwacki, 2018. "Compositional adaptability in NPM1-SURF6 scaffolding networks enabled by dynamic switching of phase separation mechanisms," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
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