Abstract
BackgroundThe development of differentiated sexual stages (gametocytes) within human red blood cells is essential for the propagation of the malaria parasite, since only mature gametocytes will survive in the mosquito’s midgut. Hence gametocytogenesis is a pre-requisite for transmission of the disease. Physiological changes involved in sexual differentiation are still enigmatic. In particular the lipid metabolism—despite being central to cellular regulation and development—is not well explored.MethodsHere the lipid profiles of red blood cells infected with the five different sexual stages of Plasmodium falciparum were analysed by mass spectrometry and compared to those from uninfected and asexual trophozoite infected erythrocytes.ResultsFundamental differences between erythrocytes infected with the different parasite stages were revealed. In mature gametocytes many lipids that decrease in the trophozoite and early gametocyte infected red blood cells are regained. In particular, regulators of membrane fluidity, cholesterol and sphingomyelin, increased significantly during gametocyte maturation. Neutral lipids (serving mainly as caloriometric reserves) increased from 3 % of total lipids in uninfected to 27 % in stage V gametocyte infected red blood cells. The major membrane lipid class (phospholipids) decreased during gametocyte development.ConclusionsThe lipid profiles of infected erythrocytes are characteristic for the particular parasite life cycle and maturity stages of gametocytes. The obtained lipid profiles are crucial in revealing the lipid metabolism of malaria parasites and identifying targets to interfere with this deadly disease.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-016-1130-z) contains supplementary material, which is available to authorized users.
Highlights
The development of differentiated sexual stages within human red blood cells is essential for the propagation of the malaria parasite, since only mature gametocytes will survive in the mosquito’s midgut
New lipid structures appear inside the host cell: the parasite is surrounded by a parasitophorous vacuole membrane [24] and new parasite induced membranous structures (Maurer’s clefts and transport vesicles) emerge, which play an important role in trafficking of parasite virulence factors to the surface of infected red blood cell membranes
Distinct morphological lipid pattern of P. falciparum gametocytes In order to visualize and distinguish the overall changes in the lipid pattern of red blood cells (RBCs) infected with gametocytes compared to uninfected and trophozoite-infected RBCs, the cells were labelled with different lipid probes for cholesterol, neutral lipids and polar lipids and imaged at the same settings
Summary
The development of differentiated sexual stages (gametocytes) within human red blood cells is essential for the propagation of the malaria parasite, since only mature gametocytes will survive in the mosquito’s midgut. In contrast to the 48-hour blood stage life cycle of asexual parasites, it takes 9–12 days for P. falciparum gametocytes to fully develop inside human red blood cells (RBCs). During this time the gametocytes progress through five morphologically. There is enormous demand for lipids due to parasite growth inside the host cell [developing organelles (e.g. nucleus, mitochondria, food vacuoles and apicoplast) surrounded by membranes and accumulating lipids in lipid bodies] and subsequent replication. New lipid structures appear inside the host cell: the parasite is surrounded by a parasitophorous vacuole membrane [24] and new parasite induced membranous structures (Maurer’s clefts and transport vesicles) emerge, which play an important role in trafficking of parasite virulence factors to the surface of infected red blood cell (iRBC) membranes
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