Molecular mechanisms of <i>Plasmodium</i> development in male and female <i>Anopheles</i> mosquitoes

Haraguchi, Asako; Takano, Makoto; Hakozaki, Jun; Nakayama, Kazuhiko; Nakamura, S.; Yoshikawa, Yasunaga; Fukumoto, Shinya; Kusakisako, Kodai; Ikadai, Hiromi

doi:10.1101/2022.01.27.477980

Cited by 4 publications

(4 citation statements)

References 28 publications

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“…Furthermore, Saglin is not secreted at detectable levels in the hemolymph where it could potentially serve as a chemotactic attractant for sporozoites. In addition, a recent study has shown that sporozoites do invade the salivary glands of male Anopheles mosquitoes [43] although saglin expression is female-specific [18,19]. Taken together, these observations indicate that Saglin is unlikely to be a determinant for sporozoite invasion of the salivary glands as sporozoites should not come in contact with this protein before reaching the lumen of salivary glands.…”

Section: Discussionmentioning

confidence: 99%

The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites

et al. 2023

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Malaria is caused by the unicellular parasite Plasmodium which is transmitted to humans through the bite of infected female Anopheles mosquitoes. To initiate sexual reproduction and to infect the midgut of the mosquito, Plasmodium gametocytes are able to recognize the intestinal environment after being ingested during blood feeding. A shift in temperature, pH change and the presence of the insect-specific compound xanthurenic acid have been shown to be important stimuli perceived by gametocytes to become activated and proceed to sexual reproduction. Here we report that the salivary protein Saglin, previously proposed to be a receptor for the recognition of salivary glands by sporozoites, facilitates Plasmodium colonization of the mosquito midgut, but does not contribute to salivary gland invasion. In mosquito mutants lacking Saglin, Plasmodium infection of Anopheles females is reduced, resulting in impaired transmission of sporozoites at low infection densities. Interestingly, Saglin can be detected in high amounts in the midgut of mosquitoes after blood ingestion, possibly indicating a previously unknown host-pathogen interaction between Saglin and midgut stages of Plasmodium. Furthermore, we were able to show that saglin deletion has no fitness cost in laboratory conditions, suggesting this gene would be an interesting target for gene drive approaches.

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Section: Discussionmentioning

confidence: 99%

The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites

et al. 2023

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“…Classical fundamental studies have identified the midgut of vectors as the main arena for development of ookinetes and oocysts of hemosporidian parasites (Valkiunas, 2004;Hajkazemian et al, 2021). Few additional studies suggest that development of oocysts is possible also in posterior parts of the dipteran digestive tract, such as the hindgut and the rectum, however without indications of completion of this development or effects on the number of produced sporozoites (Haraguchi et al, 2022). We find that the sections of the hippoboscid digestive tract after the midgut appear to contain more parasites than the midgut itself.…”

Section: Discussionmentioning

confidence: 99%

Genetic infrapopulation sizes in blood parasites: a pilot quantification of the bottleneck in louse fly vectors

Fischer,

Chakarov

2024

Front. Ecol. Evol.

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IntroductionBottleneck events are crucial for the strength of genetic drift, selection and speed of evolution. They are believed to play a particularly prominent role for parasitic infrapopulations, inhabiting single host individuals, which are often established by very few parasite individuals during transmission. In vector-borne pathogens, the bottlenecking effects can even be serialized through repeated filtering of parasitic stages at different tissues and organs of the vector. Using qPCR we aimed to quantify the number of potentially transmittable sporozoites of the hemosporidian blood parasite Haemoproteus columbae in the specialized vector louse flies Pseudolynchia canariensis which transmit these parasites between house pigeon hosts Columba livia.ResultsBased on qPCR measurements of organ-derived DNA of individual louse flies, we estimate that the midgut of these vectors contains on average 20 parasites, the hindgut and other intestines ca. 50 parasites and the salivary glands ca. 5 parasite cells. Nearly one third of all vector individuals appeared to lack parasite DNA, despite having only infected hosts as blood meal sources. The magnitude of parasite numbers in midgut and salivary glands tended to correlate positively.DiscussionOur results indicate, potential severe bottlenecking of parasite populations during individual transmission events and a probable effect of individual vector immunity on this variable. However, this may be partly alleviated by the coloniality of house pigeons, the frequency of louse flies and their daily feeding events in most populations, leading to repeated transmission opportunities, decreased quasi-vertical transmission between parents and offspring and probable panmixia of Haemoproteus columbae lineages. Many of these mechanisms might not apply in other host-vector systems. We propose several additional molecular and microscopical tools to improve the accuracy of estimating parasite population sizes in vectors and call for more estimations in different vector species to better understand the co-evolution between malaria-like blood parasites and their avian and insect hosts.

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“…In agreement with the hypothesis that Saglin may not contribute to salivary gland invasion by sporozoites. A recent study has shown that sporozoites do invade the salivary glands of male Anopheles mosquitoes (Haraguchi et al ., 2022) while saglin is female-specific (Arcà et al ., 2005; Klug et al ., 2021). Taken together, these observations indicate that Saglin is unlikely to be a determinant for sporozoite invasion as sporozoites should not come in contact with this protein before reaching the luminal side of salivary glands.…”

Section: Discussionmentioning

confidence: 99%

The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites

Klug

Gautier

Calvo

et al. 2022

Preprint

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Malaria is caused by the unicelullar parasite Plasmodium which is transmitted to humans through the bite of infected female Anopheles mosquitoes. To initiate sexual reproduction and to infect the midgut of the mosquito, Plasmodium gametocytes are able to recognize the intestinal environment after being ingested during blood feeding. A shift in temperature, pH change and the presence of the insect-specific compound xanthurenic acid have been shown to be important stimuli perceived by gametocytes to become activated and proceed to sexual reproduction. Here we report that the salivary protein Saglin, previously proposed to be a receptor for the recognition of salivary glands by sporozoites, facilitates Plasmodium colonization of the mosquito midgut, but does not contribute to salivary gland invasion. In mosquito mutants lacking Saglin, Plasmodium infection of Anopheles females is greatly reduced, resulting in impaired transmission of sporozoites at low infection densities. Interestingly, our results suggest that Saglin, present in mosquito saliva, must be ingested with the blood meal to affect Plasmodium development, indicating a previously unknown host-pathogen interaction. Furthermore, we were able to show that saglin deletion has no fitness cost in laboratory conditions, suggesting this gene would be an interesting target for gene drive approaches.

show abstract

Molecular mechanisms of Plasmodium development in male and female Anopheles mosquitoes

Cited by 4 publications

References 28 publications

The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites

The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites

Genetic infrapopulation sizes in blood parasites: a pilot quantification of the bottleneck in louse fly vectors

The salivary protein Saglin facilitates efficient midgut colonization of Anopheles mosquitoes by malaria parasites

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