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Screening of Drosophila microRNA-degradation sequences reveals Argonaute1 mRNA’s role in regulating miR-999

Author

Listed:
  • Peike Sheng

    (University of Florida
    University of Florida)

  • Lu Li

    (University of Florida
    University of Florida)

  • Tianqi Li

    (University of Florida
    University of Florida)

  • Yuzhi Wang

    (University of Florida
    University of Florida)

  • Nicholas M. Hiers

    (University of Florida
    University of Florida)

  • Jennifer S. Mejia

    (University of Florida)

  • Jossie S. Sanchez

    (University of Florida)

  • Lei Zhou

    (University of Florida
    University of Florida
    University of Florida)

  • Mingyi Xie

    (University of Florida
    University of Florida
    University of Florida)

Abstract

MicroRNAs (miRNA) load onto AGO proteins to target mRNAs for translational repression or degradation. However, miRNA degradation can be triggered when extensively base-paired with target RNAs, which induces confirmational change of AGO and recruitment of ZSWIM8 ubiquitin ligase to mark AGO for proteasomal degradation. This target RNA-directed miRNA degradation (TDMD) mechanism appears to be evolutionarily conserved, but recent studies have focused on mammalian systems. Here, we performed AGO1-CLASH in Drosophila S2 cells, with Dora (ortholog of vertebrate ZSWIM8) knockout mediated by CRISPR-Cas9 to identify five TDMD triggers (sequences that can induce miRNA degradation). Interestingly, one trigger in the 3′ UTR of AGO1 mRNA induces miR-999 degradation. CRISPR-Cas9 knockout of the AGO1 trigger in S2 cells and in Drosophila specifically elevates miR-999, with concurrent repression of the miR-999 targets. AGO1 trigger knockout flies respond poorly to hydrogen peroxide-induced stress, demonstrating the physiological importance of this TDMD event.

Suggested Citation

  • Peike Sheng & Lu Li & Tianqi Li & Yuzhi Wang & Nicholas M. Hiers & Jennifer S. Mejia & Jossie S. Sanchez & Lei Zhou & Mingyi Xie, 2023. "Screening of Drosophila microRNA-degradation sequences reveals Argonaute1 mRNA’s role in regulating miR-999," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37819-9
    DOI: 10.1038/s41467-023-37819-9
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    References listed on IDEAS

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    1. Acong Yang & Tie-Juan Shao & Xavier Bofill-De Ros & Chuanjiang Lian & Patricia Villanueva & Lisheng Dai & Shuo Gu, 2020. "AGO-bound mature miRNAs are oligouridylated by TUTs and subsequently degraded by DIS3L2," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    2. Scott M. Hammond & Emily Bernstein & David Beach & Gregory J. Hannon, 2000. "An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells," Nature, Nature, vol. 404(6775), pages 293-296, March.
    3. Hans-Hermann Wessels & Svetlana Lebedeva & Antje Hirsekorn & Ricardo Wurmus & Altuna Akalin & Neelanjan Mukherjee & Uwe Ohler, 2019. "Global identification of functional microRNA-mRNA interactions in Drosophila," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    4. Francesco Ghini & Carmela Rubolino & Montserrat Climent & Ines Simeone & Matteo J. Marzi & Francesco Nicassio, 2018. "Endogenous transcripts control miRNA levels and activity in mammalian cells by target-directed miRNA degradation," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
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