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An intracellular simian malarial parasite (Plasmodium knowlesi) induces stage-dependent alterations in membrane phospholipid organization of its host erythrocyte.

ABSTRACT: The membrane phospholipid organization in monkey erythrocytes harbouring different developmental stages of the simian malarial parasite Plasmodium knowlesi was studied using phospholipase A2 from two different sources and Merocyanine 540 as the external-membrane probes. Experiments were done to confirm that the phospholipases did not penetrate into the infected cells or hydrolyse phospholipids during membrane isolation. The parasite-free erythrocyte membrane was isolated by differential centrifugation or by using the cationic beads Affi-Gel 731. The purity of the membranes was established by optical and electron microscopy, and by assaying the parasite-specific enzyme glutamate dehydrogenase. About 10% of the phosphatidylethanolamine and none of phosphatidylserine were hydrolysed by the phospholipases in intact normal monkey erythrocytes. However, accessibility of these aminophospholipids to the enzymes was significantly enhanced in the infected cells under identical conditions. The degree of this enhancement depended on the developmental stage of the intracellular parasite, but not on the parasitaemia levels in the infected monkeys, and increased with the parasite growth inside the cells. Analogously, Merocyanine 540 was found to label the trophozoite- or schizont-infected erythrocytes, but not the ring-infected or normal cells. These results demonstrate that the intracellular malarial parasite produces stage-dependent alterations in the membrane phospholipid organization of its host erythrocyte.

SUBMITTER: Joshi P

PROVIDER: S-EPMC1148245 | biostudies-other | 1987 Aug

REPOSITORIES: biostudies-other

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Project description:BACKGROUND:Human blood cells (erythrocytes) serve as hosts for the malaria parasite Plasmodium falciparum during its 48-h intraerythrocytic developmental cycle (IDC). Established in vitro protocols allow for the study of host-parasite interactions during this phase and, in particular, high-resolution metabolomics can provide a window into host-parasite interactions that support parasite development. METHODS:Uninfected and parasite-infected erythrocyte cultures were maintained at 2% haematocrit for the duration of the IDC, while parasitaemia was maintained at 7% in the infected cultures. The parasite-infected cultures were synchronized to obtain stage-dependent information of parasite development during the IDC. Samples were collected in quadruplicate at six time points from the uninfected and parasite-infected cultures and global metabolomics was used to analyse cell fractions of these cultures. RESULTS:In uninfected and parasite-infected cultures during the IDC, 501 intracellular metabolites, including 223 lipid metabolites, were successfully quantified. Of these, 19 distinct metabolites were present only in the parasite-infected culture, 10 of which increased to twofold in abundance during the IDC. This work quantified approximately five times the metabolites measured in previous studies of similar research scope, which allowed for more detailed analyses. Enrichment in lipid metabolism pathways exhibited a time-dependent association with different classes of lipids during the IDC. Specifically, enrichment occurred in sphingolipids at the earlier stages, and subsequently in lysophospholipid and phospholipid metabolites at the intermediate and end stages of the IDC, respectively. In addition, there was an accumulation of 18-, 20-, and 22-carbon polyunsaturated fatty acids, which produce eicosanoids and promote gametocytogenesis in infected erythrocyte cultures. CONCLUSIONS:The current study revealed a number of heretofore unidentified metabolic components of the host-parasite system, which the parasite may exploit in a time-dependent manner to grow over the course of its development in the blood stage. Notably, the analyses identified components, such as precursors of immunomodulatory molecules, stage-dependent lipid dynamics, and metabolites, unique to parasite-infected cultures. These conclusions are reinforced by the metabolic alterations that were characterized during the IDC, which were in close agreement with those known from previous studies of blood-stage infection.

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An intracellular simian malarial parasite (Plasmodium knowlesi) induces stage-dependent alterations in membrane phospholipid organization of its host erythrocyte.

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