Ookinete destruction within the mosquito midgut lumen explains Anopheles albimanus refractoriness to Plasmodium falciparum (3D7A) oocyst infection

Baton, Luke Anthony; Ranford-Cartwright, Lisa

doi:10.1016/j.ijpara.2011.12.005

Cited by 22 publications

(30 citation statements)

References 71 publications

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“…Intriguingly, the activation of female gametocytes, fertilization, and generation of ookinetes were drastically reduced for PbATPβKO parasites in vivo (i.e., within the mosquito gut). The mosquito gut is a harsh environment for parasites (11,49), and the sole purpose of the highly motile ookinetes phase is to escape the gut and establish the new parasite generation in the insect hemocoel so it can produce sporozoites to accumulate in the salivary glands for transmission to new vertebrate hosts (35,50). Rescue experiments demonstrated that as little as 10 h in the mosquito gut was detrimental to ookinete viability in our PbATPβKO parasites.…”

Section: Discussionmentioning

confidence: 96%

Mitochondrial ATP synthase is dispensable in blood-stage Plasmodium berghei rodent malaria but essential in the mosquito phase

Sturm

Mollard

Cozijnsen

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

102

115

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Mitochondrial ATP synthase is driven by chemiosmotic oxidation of pyruvate derived from glycolysis. Blood-stage malaria parasites eschew chemiosmosis, instead relying almost solely on glycolysis for their ATP generation, which begs the question of whether mitochondrial ATP synthase is necessary during the blood stage of the parasite life cycle. We knocked out the mitochondrial ATP synthase β subunit gene in the rodent malaria parasite, Plasmodium berghei, ablating the protein that converts ADP to ATP. Disruption of the β subunit gene of the ATP synthase only marginally reduced asexual blood-stage parasite growth but completely blocked mouse-to-mouse transmission via Anopheles stephensi mosquitoes. Parasites lacking the β subunit gene of the ATP synthase generated viable gametes that fuse and form ookinetes but cannot progress beyond this stage. Ookinetes lacking the β subunit gene of the ATP synthase had normal motility but were not viable in the mosquito midgut and never made oocysts or sporozoites, thereby abrogating transmission to naive mice via mosquito bite. We crossed the self-infertile ATP synthase β subunit knockout parasites with a male-deficient, self-infertile strain of P. berghei, which restored fertility and production of oocysts and sporozoites, which demonstrates that mitochondrial ATP synthase is essential for ongoing viability through the female, mitochondrion-carrying line of sexual reproduction in P. berghei malaria. Perturbation of ATP synthase completely blocks transmission to the mosquito vector and could potentially be targeted for disease control. malaria | ATP synthase | ookinetes | mitochondrial endosymbiosis | aerobic respiration

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Section: Discussionmentioning

confidence: 96%

Mitochondrial ATP synthase is dispensable in blood-stage Plasmodium berghei rodent malaria but essential in the mosquito phase

Sturm

Mollard

Cozijnsen

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

102

115

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“…For example, both a laboratory P. falciparum line of putative African origin (NF54) and a clone from this line (3D7) have low infectivity in or fail to infect New World vectors such as A. albimanus and Anopheles darlingi (7,29). Furthermore, A. gambiae mosquitoes (African malaria vectors) are infected more efficiently with African P. falciparum isolates than with isolates from Thailand (37).…”

Section: Evidence Of Plasmodium Adaptation To Mosquito Vectorsmentioning

confidence: 99%

Mosquito Vectors and the Globalization of Plasmodium falciparum Malaria

et al. 2016

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Plasmodium falciparum malaria remains a devastating public health problem. Recent discoveries have shed light on the origin and evolution of Plasmodium parasites and their interactions with their vertebrate and mosquito hosts. P. falciparum malaria originated in Africa from a single horizontal transfer between an infected gorilla and a human, and became global as the result of human migration. Today, P. falciparum malaria is transmitted worldwide by more than 70 different anopheline mosquito species. Recent studies indicate that the mosquito immune system can be a barrier to malaria transmission and that the P. falciparum Pfs47 gene allows the parasite to evade mosquito immune detection. Here, we review the origin and globalization of P. falciparum and integrate this history with analysis of the biology, evolution, and dispersal of the main mosquito vectors. This new perspective broadens our understanding of P. falciparum population structure and the dispersal of important parasite genetic traits. 20.1

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“…P. falciparum parasites are transmitted by more than 70 different anopheline species worldwide (3), but compatibilities differ between specific vector-parasite combinations (5). For example, P. falciparum NF54 (Pf NF54), of putative African origin, effectively infects Anopheles gambiae, the main malaria vector in sub-Saharan Africa; but A. albimanus is highly refractory to this strain (6)(7)(8); whereas Asian P. falciparum isolates infect Anopheles stephensi (Nijmegen strain), a major vector in India, more effectively than A. gambiae (9). Similar differences in compatibility have been reported between Plasmodium vivax and different anopheline species (10,11).…”

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confidence: 99%

Plasmodium evasion of mosquito immunity and global malaria transmission: The lock-and-key theory

Molina-Cruz

Canepa

Kamath

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

113

167

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Plasmodium falciparum malaria originated in Africa and became global as humans migrated to other continents. During this journey, parasites encountered new mosquito species, some of them evolutionarily distant from African vectors. We have previously shown that the Pfs47 protein allows the parasite to evade the mosquito immune system of Anopheles gambiae mosquitoes. Here, we investigated the role of Pfs47-mediated immune evasion in the adaptation of P. falciparum to evolutionarily distant mosquito species. We found that P. falciparum isolates from Africa, Asia, or the Americas have low compatibility to malaria vectors from a different continent, an effect that is mediated by the mosquito immune system. We identified 42 different haplotypes of Pfs47 that have a strong geographic population structure and much lower haplotype diversity outside Africa. Replacement of the Pfs47 haplotypes in a P. falciparum isolate is sufficient to make it compatible to a different mosquito species. Those parasites that express a Pfs47 haplotype compatible with a given vector evade antiplasmodial immunity and survive. We propose that Pfs47-mediated immune evasion has been critical for the globalization of P. falciparum malaria as parasites adapted to new vector species. Our findings predict that this ongoing selective force by the mosquito immune system could influence the dispersal of Plasmodium genetic traits and point to Pfs47 as a potential target to block malaria transmission. A new model, the "lock-and-key theory" of P. falciparum globalization, is proposed, and its implications are discussed. malaria globalization | immune evasion | anopheles immunity | Plasmodium selection | Pfs47

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Ookinete destruction within the mosquito midgut lumen explains Anopheles albimanus refractoriness to Plasmodium falciparum (3D7A) oocyst infection

Cited by 22 publications

References 71 publications

Mitochondrial ATP synthase is dispensable in blood-stage Plasmodium berghei rodent malaria but essential in the mosquito phase

Mitochondrial ATP synthase is dispensable in blood-stage Plasmodium berghei rodent malaria but essential in the mosquito phase

Mosquito Vectors and the Globalization of Plasmodium falciparum Malaria

Plasmodium evasion of mosquito immunity and global malaria transmission: The lock-and-key theory

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