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The DEAD-box RNA helicase PfDOZI imposes opposing actions on RNA metabolism in Plasmodium falciparum

Author

Listed:
  • Hui Min

    (University of South Florida
    China Medical University)

  • Xiaoying Liang

    (University of South Florida)

  • Chengqi Wang

    (University of South Florida)

  • Junling Qin

    (University of South Florida)

  • Rachasak Boonhok

    (University of South Florida
    Walailak University)

  • Azhar Muneer

    (University of South Florida)

  • Awtum M. Brashear

    (University of South Florida)

  • Xiaolian Li

    (University of South Florida)

  • Allen M. Minns

    (Pennsylvania State University)

  • Swamy Rakesh Adapa

    (University of South Florida)

  • Rays H. Y. Jiang

    (University of South Florida)

  • Gang Ning

    (Pennsylvania State University)

  • Yaming Cao

    (China Medical University)

  • Scott E. Lindner

    (Pennsylvania State University)

  • Jun Miao

    (University of South Florida)

  • Liwang Cui

    (University of South Florida)

Abstract

In malaria parasites, the regulation of mRNA translation, storage and degradation during development and life-stage transitions remains largely unknown. Here, we functionally characterized the DEAD-box RNA helicase PfDOZI in P. falciparum. Disruption of pfdozi enhanced asexual proliferation but reduced sexual commitment and impaired gametocyte development. By quantitative transcriptomics, we show that PfDOZI is involved in the regulation of invasion-related genes and sexual stage-specific genes during different developmental stages. PfDOZI predominantly participates in processing body-like mRNPs in schizonts but germ cell granule-like mRNPs in gametocytes to impose opposing actions of degradation and protection on different mRNA targets. We further show the formation of stress granule-like mRNPs during nutritional deprivation, highlighting an essential role of PfDOZI-associated mRNPs in stress response. We demonstrate that PfDOZI participates in distinct mRNPs to maintain mRNA homeostasis in response to life-stage transition and environmental changes by differentially executing post-transcriptional regulation on the target mRNAs.

Suggested Citation

  • Hui Min & Xiaoying Liang & Chengqi Wang & Junling Qin & Rachasak Boonhok & Azhar Muneer & Awtum M. Brashear & Xiaolian Li & Allen M. Minns & Swamy Rakesh Adapa & Rays H. Y. Jiang & Gang Ning & Yaming , 2024. "The DEAD-box RNA helicase PfDOZI imposes opposing actions on RNA metabolism in Plasmodium falciparum," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48140-4
    DOI: 10.1038/s41467-024-48140-4
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    References listed on IDEAS

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    1. Suresh M. Ganesan & Alejandra Falla & Stephen J. Goldfless & Armiyaw S. Nasamu & Jacquin C. Niles, 2016. "Synthetic RNA–protein modules integrated with native translation mechanisms to control gene expression in malaria parasites," Nature Communications, Nature, vol. 7(1), pages 1-10, April.
    2. Jessica L. Bridgford & Stanley C. Xie & Simon A. Cobbold & Charisse Flerida A. Pasaje & Susann Herrmann & Tuo Yang & David L. Gillett & Lawrence R. Dick & Stuart A. Ralph & Con Dogovski & Natalie J. S, 2018. "Artemisinin kills malaria parasites by damaging proteins and inhibiting the proteasome," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    3. Min Zhang & Chengqi Wang & Jenna Oberstaller & Phaedra Thomas & Thomas D. Otto & Debora Casandra & Sandhya Boyapalle & Swamy R. Adapa & Shulin Xu & Katrina Button-Simons & Matthew Mayho & Julian C. Ra, 2021. "The apicoplast link to fever-survival and artemisinin-resistance in the malaria parasite," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
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