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

Pengge Qian, Xu Wang, Cuirong Guan, Xin Fang, Mengya Cai, Chuan-qi Zhong, Yong Cui, Yanbin Li, Luming Yao, Huiting Cui (), Kai Jiang () and Jing Yuan ()
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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

Nature Communications, 2022, vol. 13, issue 1, 1-23

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41467-022-35270-w

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