Abstract
Plasmodium falciparum sporozoites that develop and mature inside an Anopheles mosquito initiate a malaria infection in humans. Here we report the first proteomic comparison of different parasite stages from the mosquito—early and late oocysts containing midgut sporozoites, and the mature, infectious salivary gland sporozoites. Despite the morphological similarity between midgut and salivary gland sporozoites, their proteomes are markedly different, in agreement with their increase in hepatocyte infectivity. The different sporozoite proteomes contain a large number of stage specific proteins whose annotation suggest an involvement in sporozoite maturation, motility, infection of the human host and associated metabolic adjustments. Analyses of proteins identified in the P. falciparum sporozoite proteomes by orthologous gene disruption in the rodent malaria parasite, P. berghei, revealed three previously uncharacterized Plasmodium proteins that appear to be essential for sporozoite development at distinct points of maturation in the mosquito. This study sheds light on the development and maturation of the malaria parasite in an Anopheles mosquito and also identifies proteins that may be essential for sporozoite infectivity to humans.
Highlights
The life cycle of human malaria parasite Plasmodium falciparum within the mosquito vector begins when gametocytes are taken up in an infected blood meal; after forming gametes and fertilisation, the resulting zygote differentiates into a motile ookinete that traverses the midgut epithelium and transforms within 36– 48 hours into an oocyst (OOC) between the midgut epithelial cells and the basal lamina
Mosquito stage proteome Protein samples derived from infected mosquito midguts and salivary glands were analyzed by nano–liquid chromatography tandem mass spectrometry essentially as previously described [15]
The MS/MS spectra were searched against a combined database of all possible predicted tryptic peptides derived from all P. falciparum, human, and mosquito (Anopheles gambiae) proteins
Summary
The life cycle of human malaria parasite Plasmodium falciparum within the mosquito vector begins when gametocytes are taken up in an infected blood meal; after forming gametes and fertilisation, the resulting zygote differentiates into a motile ookinete that traverses the midgut epithelium and transforms within 36– 48 hours into an oocyst (OOC) between the midgut epithelial cells and the basal lamina. The oocyst is an asexually replicating form of the parasite, which produces up to 2000–4000 sporozoites in about two weeks. Rupture of mature oocysts releases oocystderived sporozoites (ODS) into the hemocoel of the mosquito. The movement of the hemolymph brings the ODS in contact with the salivary glands, which they invade. The sporozoites mature inside the salivary glands and are stored ready for transmission to the mammalian host upon the blood meal. A limited number of the salivary gland sporozoites (SGS) are injected during a mosquito bite and only a few of these complete the necessary migration from the skin to the liver to establish an infection inside hepatocytes. The sporozoite has to complete a number of functions and metabolic readjustments both before and after injection into a mammalian host. The sporozoite has to be capable of actively exiting an oocyst, travelling through the hemolymph (the mosquito circulatory system), and Author Summary
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