Possible basis for membrane changes in nonparasitized erythrocytes of malaria-infected animals

Joshi, Prince; Alam, Asrar; Chandra, Ramesh; Puri, Sunil K.; Gupta, C. M.

doi:10.1016/0005-2736(86)90486-4

Cited by 17 publications

(9 citation statements)

References 12 publications

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“…Only 5-14% of the PS and 18-25% of the PE were accessible to the phospholipases in the intact cells. This abnormality in the non-parasitized cells has, however, recently been shown not to originate from the presence of malarial parasite in the blood but primarily to arise from the malaria-induced secondary complications (Joshi et al, 1986). It may therefore be suggested that the observed abnormalities in the ring-infected cells are not solely due to the-contamination with the non-parasitized erythrocytes.…”

Section: Resultsmentioning

confidence: 99%

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

Joshi

Dutta²,

Gupta

1987

Biochemical Journal

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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.

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Section: Resultsmentioning

confidence: 99%

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

Joshi

Dutta²,

Gupta

1987

Biochemical Journal

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“…Gupta et al (9,10) indicated that erythrocyte phospholipid organization was altered in both infected and uninfected cells from monkeys infected with P. knowlesi, with PS exposed on the outer leaflet, and PC tranported to the exoplasmic face of the cell. A subsequent report (13) indicated that the observed changes in the phospholipid asymmetry of uninfected erythrocytes was not a consistent change because of infection, and was limited to cells obtained from chronically infected splenectomized animals. It is unclear whether this is a consequence of direct action of the spleen on the phospholipid asymmetry of red cells, or selective clearance of cells containing exofacial PS in the nonsplenectomized animals.…”

Section: Discussionmentioning

confidence: 97%

Transport of fluorescent phospholipid analogues from the erythrocyte membrane to the parasite in Plasmodium falciparum-infected cells.

Haldar

Amorim

Cross

1989

The Journal of Cell Biology

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Abstract. The asexual development of the human malaria parasite Plasmodium falciparum is largely intraerythrocytic. When 1-palmitoyl-2-[6-[(7-nitro-2-1,3-benzoxadiazole-4-yl)amino]caproyl] phosphatidylcholine (NBD-PC) was incorporated into infected and uninfected erythrocyte membranes at 0°C, it remained at the cell surface. At 10°C, the lipid was rapidly internalized in infected erythrocytes at all stages of parasite growth. Our results indicate that the internalization of NBD-PC was not because of endocytosis but rapid transbilayer lipid flip-flop at the infected erythrocyte membrane, followed by monomer diffusion to the parasite. Internalization of the lipid was inhibited by (a) depleting cellular ATP levels; (b) pretreating the cells with N-ethyl maleimide or diethylpyrocarbonate; and (c) 10 mM L-a-glycerophosphorylcholine. The evidence suggests protein-mediated and energy dependent transmembrane movement of the PC analogue.The conditions for the internalization of another phospholipid analogue N-4-nitrobenzo-2-oxa-l,3-diazoledipalmitoyl phosphatidylethanolamine (N-NBD-PE) were distinct from that of NBD-PC and suggest the presence of additional mechanism(s) of parasitemediated lipid transport in the infected host membrane. In spite of the lack of bulk, constitutive endocytosis at the red cell membrane, the uptake of Lucifer yellow by mature infected cells suggests that microdomains of pinocytotic activity are induced by the intracellular parasite. The results indicate the presence of parasite-induced mechanisms of lipid transport in infected erythrocyte membranes that modify host membrane properties and may have important implications on phospholipid asymmetry in these membranes.URING its intraerythrocytic development, the human malaria parasite Plasmodium falciparum induces changes in both lipid and protein components of the infected erythrocyte membrane. Several parasite proteins are introduced into the erythrocyte membrane (4, 11,12,18,24,31,36,38); its morphology, rigidity, and permeability are markedly altered (5, 8, 17); and there is increased disorder in phospholipid packing of the bilayer (33). The distribution of phospholipids in P. falciparum and P. knowlesi-infected erythrocyte membranes may be altered in contrast to uninfected cells (9,26), and an increased uptake and exchangeability of phospholipids is reported between P. knowlesi-infected erythrocyte membranes and synthetic phospholipids (20, 37). However, little is known about the molecular basis of these changes in parasitized erythrocytes.Membrane phospholipid asymmetry is an intrinsic property of cellular membranes. Altering the distribution of phospholipids across the plasma membrane (for example, increasing phosphatidylserine on the exoplasmic leaflet of the Portions of this work were presented at the Fed. Eur. Biochem. Soc. Advanced Course on Lipid Flow at Maria Aim, Austria, March 1988. plasma membrane) can lead to clearance of the cell from circulation (25,32). Rapid transbilayer phospholipid movement across biological membranes app...

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“…Lipid asymmetry of the membrane, maintained by an aminophospholipid translocase activity, is reduced in aged erythrocytes 41 or erythrocytes under oxidative stress. 42 Altered membrane PL organization, particularly a greater PS exposure on the outer surface of the membrane, has been reported in both IRBCs 2,43,44 and URBCs, 45,46 although not confirmed by others. 29,47 Oxidative stress induced by P falciparum might contribute to the loss of PS by changing the transbilayer organization of the membrane phospholipids and enhancing PS exposure on the outer surface.…”

Section: Discussionmentioning

confidence: 99%

Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum

Omodeo‐Salè

Motti

Basilico

et al. 2003

Blood

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Red blood cells infected with Plasmodium falciparum (IRBCs) undergo changes primarily in their membrane composition that contribute to malaria pathogenesis. However, all manifestations (eg, anemia) cannot be accounted for by IRBCs alone. Uninfected erythrocytes (URBCs) may play a role, but they have been underresearched. We wanted to document changes in the erythrocyte membrane that could contribute to URBC reduced life span and malaria-associated anemia. Human erythrocytes were cultured with P falciparum and washed at the trophozoite stage. IRBCs and URBCs were separated on Percoll density gradient, thus obtaining erythrocyte fractions of different densities/ages. IRBC-and URBCpurified membranes were analyzed and compared with control normal erythrocytes (NRBCs) of the same age, from the same donor, kept in the same conditions. P falciparum accelerated aging of both IRBCs and URBCs, causing a significant shift in the cell population toward the denser (old) fraction. Protein, phospholipid, and cholesterol content were reduced in IRBCs and young URBCs. Young and medium uninfected fractions had higher levels of lipid peroxidation and phospholipid saturation (because of the loss of polyunsaturated fatty acids, PUFAs) and lower phosphatidylserine. In IRBCs, thiobarbituric reactive substances (TBARSs) were higher, and PUFAs and phosphatidylserine lower than in NRBCs and URBCs. In comparison, trophozoite membranes had lower phospholipid (particularly sphingomyelin and phosphatidylserine) and cholesterol content and a higher degree of saturation. Parasiteinduced peroxidative damage might account for these modifications. In summary, we demonstrated that membrane damage leading to accelerated senescence of both infected and uninfected erythrocytes will likely contribute to malaria anemia. (Blood. 2003;102:705-711)

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Possible basis for membrane changes in nonparasitized erythrocytes of malaria-infected animals

Cited by 17 publications

References 12 publications

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

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

Transport of fluorescent phospholipid analogues from the erythrocyte membrane to the parasite in Plasmodium falciparum-infected cells.

Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum

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