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A subpellicular microtubule dynein transport machinery regulates ookinete morphogenesis for mosquito transmission of Plasmodium yoelii

Author

Listed:
  • Bing Liu

    (Xiamen University)

  • Cong Liu

    (University of South China)

  • Zhenkui Li

    (University of South China)

  • Wenjia Liu

    (Xiamen University)

  • Huiting Cui

    (Xiamen University)

  • Jing Yuan

    (Xiamen University)

Abstract

The cortical cytoskeleton of subpellicular microtubules (SPMTs) supports the Plasmodium ookinete morphogenesis during mosquito transmission of malaria. SPMTs are hypothesized to function as the cytoskeletal tracks in motor-driven cargo transport for apical organelle and structure assembly in ookinetes. However, the SPMT-based transport motor has not been identified in the Plasmodium. The cytoplasmic dynein is the motor moving towards the minus end of microtubules (MTs) and likely be responsible for cargo transport to the apical part in ookinetes. Here we screen 7 putative dynein heavy chain (DHC) proteins in the P. yoelii and identify DHC3 showing peripheral localization in ookinetes. DHC3 is localized at SPMTs throughout ookinete morphogenesis. We also identify five other dynein subunits localizing at SPMTs. DHC3 disruption impairs ookinete development, shape, and gliding, leading to failure in mosquito infection of Plasmodium. The DHC3-deficient ookinetes display defective formation or localization of apical organelles and structures. Rab11A and Rab11B interact with DHC3 at SPMTs in a DHC3-dependent manner, likely functioning as the receptors for the cargoes driven by SPMT-dynein. Disturbing Rab11A or Rab11B phenocopies DHC3 deficiency in ookinete morphogenesis. Our study reveals an SPMT-based dynein motor driving the transport of Rab11A- and Rab11B-labeled cargoes in the ookinete morphogenesis of Plasmodium.

Suggested Citation

  • Bing Liu & Cong Liu & Zhenkui Li & Wenjia Liu & Huiting Cui & Jing Yuan, 2024. "A subpellicular microtubule dynein transport machinery regulates ookinete morphogenesis for mosquito transmission of Plasmodium yoelii," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52970-7
    DOI: 10.1038/s41467-024-52970-7
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    References listed on IDEAS

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    1. Josie L. Ferreira & Vojtěch Pražák & Daven Vasishtan & Marc Siggel & Franziska Hentzschel & Annika M. Binder & Emma Pietsch & Jan Kosinski & Friedrich Frischknecht & Tim W. Gilberger & Kay Grünewald, 2023. "Variable microtubule architecture in the malaria parasite," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Xiangli Wang & Yong Fu & Wandy L. Beatty & Meisheng Ma & Alan Brown & L. David Sibley & Rui Zhang, 2021. "Publisher Correction: Cryo-EM structure of cortical microtubules from human parasite Toxoplasma gondii identifies their microtubule inner proteins," Nature Communications, Nature, vol. 12(1), pages 1-1, December.
    3. Shaojun Long & Bryan Anthony & Lisa L. Drewry & L. David Sibley, 2017. "A conserved ankyrin repeat-containing protein regulates conoid stability, motility and cell invasion in Toxoplasma gondii," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    4. Melissa A. Gee & John E. Heuser & Richard B. Vallee, 1997. "An extended microtubule-binding structure within the dynein motor domain," Nature, Nature, vol. 390(6660), pages 636-639, December.
    5. Pengge Qian & Xu Wang & Cuirong Guan & Xin Fang & Mengya Cai & Chuan-qi Zhong & Yong Cui & Yanbin Li & Luming Yao & Huiting Cui & Kai Jiang & Jing Yuan, 2022. "Apical anchorage and stabilization of subpellicular microtubules by apical polar ring ensures Plasmodium ookinete infection in mosquito," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    6. Xiangli Wang & Yong Fu & Wandy L. Beatty & Meisheng Ma & Alan Brown & L. David Sibley & Rui Zhang, 2021. "Cryo-EM structure of cortical microtubules from human parasite Toxoplasma gondii identifies their microtubule inner proteins," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
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