Malaria oocysts require circumsporozoite protein to evade mosquito immunity

Feng Zhu, Hong Zheng, Suilin Chen, Kun Zhang, Xin Qin, Jingru Zhang, Taiping Liu, Yongling Fan, Liting Wang, Xiaoxu Li, Jian Zhang () and Wenyue Xu ()
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Feng Zhu: Army Medical University (Third Military Medical University)
Hong Zheng: Army Medical University (Third Military Medical University)
Suilin Chen: Army Medical University (Third Military Medical University)
Kun Zhang: Army Medical University (Third Military Medical University)
Xin Qin: Army Medical University (Third Military Medical University)
Jingru Zhang: Army Medical University (Third Military Medical University)
Taiping Liu: Army Medical University (Third Military Medical University)
Yongling Fan: Army Medical University (Third Military Medical University)
Liting Wang: Army Medical University (Third Military Medical University)
Xiaoxu Li: Ministry of Education of China
Jian Zhang: Army Medical University (Third Military Medical University)
Wenyue Xu: Army Medical University (Third Military Medical University)

Nature Communications, 2022, vol. 13, issue 1, 1-14

Abstract: Abstract Malaria parasites are less vulnerable to mosquito immune responses once ookinetes transform into oocysts, facilitating parasite development in the mosquito. However, the underlying mechanisms of oocyst resistance to mosquito defenses remain unclear. Here, we show that circumsporozoite protein (CSP) is required for rodent malaria oocysts to avoid mosquito defenses. Mosquito infection with CSPmut parasites (mutation in the CSP pexel I/II domains) induces nicotinamide adenine dinucleotide phosphate (NADPH) oxidase 5 (NOX5)-mediated hemocyte nitration, thus activating Toll pathway and melanization of mature oocysts, upregulating hemocyte TEP1 expression, and causing defects in the release of sporozoites from oocysts. The pre-infection of mosquitoes with the CSPmut parasites reduces the burden of infection when re-challenged with CSPwt parasites by inducing hemocyte nitration. Thus, we demonstrate why oocysts are invisible to mosquito immunity and reveal an unknown role of CSP in the immune evasion of oocysts, indicating it as a potential target to block malaria transmission.

Date: 2022
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DOI: 10.1038/s41467-022-30988-z

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