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Gender-related secretome of Plasmodium berghei sexual stages

ABSTRACT: Plasmodium, the malaria parasite, undergoes a complex life cycle, which alternates between a vertebrate host and a mosquito vector of the genus Anopheles. In red blood cells of the vertebrate host, Plasmodium multiplies asexually or differentiates into gamete precursors, the male and female gametocytes, responsible for parasite transmission. Sexual stage maturation occurs in the midgut of the mosquito vector, where male and female gametes egress from the host erythrocyte to form a zygote. Gamete egress entails the successive rupture of two membranes surrounding the parasite, the parasitophorous vacuole membrane and the erythrocyte plasma membrane. In this study, we applied a proteomic approach to identify proteins differentially released/secreted by female and male gametocytes of the rodent Plasmodium berghei activated to form gametes. We compared secreted molecules of the wild type gametocytes with those of a transgenic line defective in male gamete maturation and egress. This enabled us to provide a comprehensive dataset of egress-related molecules and their gender specificity. Using specific antibodies, we validated eleven candidate molecules, predicted as either gender-specific or common to both male and female gametocytes. All of them localize to punctuate, vesicle-like structures that relocate to cell periphery upon activation, but only three of them localize to the gametocyte-specific secretory vesicles named osmiophilic bodies. Our results confirm that the egress process involves a tightly coordinated secretory apparatus that includes different types of vesicles and may put the basis for functional studies aimed at designing novel transmission-blocking molecules.

INSTRUMENT(S): LTQ XL

ORGANISM(S): Plasmodium Berghei Anka (ncbitaxon:5823) Mus Musculus (ncbitaxon:10090)

SUBMITTER: FEDERICA FRATINI

PROVIDER: MSV000085650 | MassIVE | Tue Jun 30 09:49:00 BST 2020

REPOSITORIES: MassIVE

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Project description:Plasmodium falciparum gametocyte stages represent a small fraction of the entire parasite biomass that is present during human malaria infection, yet they alone lead to the transmission of this devastating disease. One of the critical gaps in malaria transmission biology and surveillance is our lack of knowledge about gametocyte biology, especially sexual dimorphic development that may influence transmission from the human to the mosquito. Ratios of male and female gametocytes in the peripheral blood can vary significantly; influenced in part by asexual blood stage and gametocyte density as well as vertebrate and invertebrate host factors. Moreover, the role of sex ratios on gametocyte transmission potential to mosquitoes is unknown and dissecting this process has been hampered by the lack of sex-specific protein markers for the circulating, mature stage V gametocytes. The current evidence suggests a high degree of conservation in gametocyte gene complement across Plasmodium, and therefore presumably for sex-specific genes as well. Therefore, to better our understanding of gametocyte development and subsequent infectiousness to mosquitoes, we undertook a two pronged approach. First, we acquired the mixed, male and female stage V gametocyte proteomes of the NF54 isolate and mature stage V female proteome from Dd2, a strain that is defective in producing mature males. Second, we then undertook a Systematic Subtractive Bioinformatic analysis (filtering) approach to identify sex-specific P. falciparum NF54 protein markers based on a comparison with the Dd2 strain and syntenic male and female proteins from the reanalyzed and updated P. berghei (related rodent malaria parasite) gametocyte proteomes. This has produced a short list of putative 174 male- and 258 female-specific P. falciparum stage V proteins. Furthermore, we generated antibodies against three putative female-specific gametocyte stage V proteins in P. falciparum and confirmed sex-specificity for two proteins and also the loss sex-partitioning for a putative female-specific protein in rodent malaria parasites.

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Gender-related secretome of Plasmodium berghei sexual stages

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