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Apical anchorage and stabilization of subpellicular microtubules by apical polar ring ensures Plasmodium ookinete infection in mosquito

Author

Listed:
  • Pengge Qian

    (Xiamen University)

  • Xu Wang

    (Xiamen University)

  • Cuirong Guan

    (Wuhan University)

  • Xin Fang

    (Xiamen University)

  • Mengya Cai

    (Xiamen University)

  • Chuan-qi Zhong

    (Xiamen University)

  • Yong Cui

    (Xiamen University)

  • Yanbin Li

    (Xiamen University)

  • Luming Yao

    (Xiamen University)

  • Huiting Cui

    (Xiamen University)

  • Kai Jiang

    (Wuhan University)

  • Jing Yuan

    (Xiamen University)

Abstract

Morphogenesis of many protozoans depends on a polarized establishment of cortical cytoskeleton containing the subpellicular microtubules (SPMTs), which are apically nucleated and anchored by the apical polar ring (APR). In malaria parasite Plasmodium, APR emerges in the host-invading stages, including the ookinete for mosquito infection. So far, the fine structure and molecular components of APR as well as the underlying mechanism of APR-mediated apical positioning of SPMTs are largely unknown. Here, we resolve an unprecedented APR structure composed of a top ring plus approximate 60 radiating spines. We report an APR-localizing and SPMT-binding protein APR2. APR2 disruption impairs ookinete morphogenesis and gliding motility, leading to Plasmodium transmission failure in mosquitoes. The APR2-deficient ookinetes display defective apical anchorage of APR and SPMT due to the impaired integrity of APR. Using protein proximity labeling, we obtain a Plasmodium ookinete APR proteome and validate ten undescribed APR proteins. Among them, APRp2 and APRp4 directly interact with APR2 and also mediate the apical anchorage of SPMTs. This study sheds light on the molecular basis of APR in the organization of Plasmodium ookinete SPMTs.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35270-w
    DOI: 10.1038/s41467-022-35270-w
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    References listed on IDEAS

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    1. Peter Bieling & Liedewij Laan & Henry Schek & E. Laura Munteanu & Linda Sandblad & Marileen Dogterom & Damian Brunner & Thomas Surrey, 2007. "Reconstitution of a microtubule plus-end tracking system in vitro," Nature, Nature, vol. 450(7172), pages 1100-1105, December.
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