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Alterations in erythrocyte membrane phospholipid organization due to the intracellular growth of the human malaria parasite, Plasmodium falciparum

Published online by Cambridge University Press:  06 April 2009

P. A. Maguire
Affiliation:
Department of Biology, University of California, Riverside, California 92521, USA
J. Prudhomme
Affiliation:
Department of Biology, University of California, Riverside, California 92521, USA
I. W. Sherman
Affiliation:
Department of Biology, University of California, Riverside, California 92521, USA

Summary

The asymmetric distribution of phospholipids in the erythrocyte membrane during the intracellular development of the human malaria parasite Plasmodium falciparum was studied. Infected cells of high parasitaemia were treated with phospholipase A2 or sphingomyelinase C, followed by isolation of the host red cell membrane using the Affigel (731) bead method. Additionally, phosphatidylserine on the surface of infected cells was probed using a phosphatidylserine-sensitive prothrombinase assay. Trophozoite-infected cells showed an increase in phosphatidylethanolamine and phosphatidylserine and a decrease in phosphatidylcholine in the outer leaflet. In addition to the changes already present in trophozoite-infected cells, schizont-infected cells showed a decrease in sphingomyelin as well as a further increase in phosphatidylserine in the outer leaflet. The results are discussed with respect to possible mechanisms and consequences of these changes.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

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References

REFERENCES

Abdalla, S. H. (1987). Opsonizing and agglutinating antibodies against Plasmodium falciparum schizont-infected erythrocytes in Gambian sera. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 214–18.CrossRefGoogle ScholarPubMed
Allen, T., Williamson, P. & Schlegel, R. (1988). Phosphatidylserine as a determinant of reticuloendothelial recognition of liposome models of the erythrocyte surface. Proceedings of the National Academy of Sciences, USA 85, 8067–71.CrossRefGoogle Scholar
Arduini, A., Stern, A., Storto, S., Belfiglio, M., Mancinelli, G., Scurti, R. & Federici, G. (1989). Effect of oxidative stress on membrane phospholipid and protein organization in human erythrocytes. Archives of Biochemistry and Biophysics 273, 112–20.CrossRefGoogle ScholarPubMed
Beaumelle, B., Vial, H. & BienvenÜe, A. (1988). Enhanced transbilayer mobility of phospholipids in malaria-infected monkey erythrocytes: a spin-label study. Journal of Cellular Physiology 135, 94100.CrossRefGoogle ScholarPubMed
Bergmann, W. L., Dressler, V., Haest, C. W. M. & Deuticke, B. (1984). Crosslinking of SH-groups in the erythrocyte membrane enhances transbilayer reorientation of phospholipids. Evidence for a limited access of phospholipids to the reorientation sites. Biochimica et Biophysica Acta 769, 390–8.CrossRefGoogle Scholar
Bligh, E. G. & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–17.CrossRefGoogle ScholarPubMed
Celada, A., Cruchaud, A. & Perrin, L. H. (1983). Phagocytosis of Plasmodium falciparum parasitized erythrocytes by human polymorphonuclear leukocytes. Journal of Parasitology 69, 4953.CrossRefGoogle ScholarPubMed
Chandra, R., Joshi, P. C., Bajpai, V. K. & Gupta, C. M. (1987). Membrane phospholipid organization in calcium-loaded human erythrocytes. Biochimica et Biophysica Acta 902, 253–62.CrossRefGoogle ScholarPubMed
Classen, J., Haest, C. W. M., Tournois, H. & Deuticke, B. (1987). Gramicidin-induced enhancement of transbilayer reorientation of lipids in the erythrocyte membrane. Biochemistry 26, 6604–12.CrossRefGoogle ScholarPubMed
Connor, J., Bucana, C., Fidler, I. & Schroit, A. (1989). Differentiation-dependent expression of phosphatidylserine in mammalian plasma membranes: quantitative assessment of outer-leaflet lipid by prothrombinase complex formation. Proceedings of the National Academy of Sciences, USA 86, 3184–8.CrossRefGoogle Scholar
Connor, J., Gillum, K. & Schroit, A. J. (1990). Maintenance of lipid asymmetry in red blood cells and ghosts: effect of divalent cations and serum albumin on the transbilayer distribution of phosphatidylserine. Biochimica et Biophysica Act 1025, 82–6.CrossRefGoogle ScholarPubMed
Connor, J. & Schroit, A. J. (1990). Aminophospholipid translocation in erythrocytes: evidence for the involvement of a specific transporter and an endofacial protein. Biochemistry 29, 3743.CrossRefGoogle Scholar
Devaux, P. (1988). Review letter: phospholipid flippases. FEBS Letters 234, 812.CrossRefGoogle Scholar
Dressler, V., Haest, C. W. M., Plasa, G., Deuticke, B. & Erusalimsky, J. D. (1984). Stabilizing factors of phospholipid asymmetry in the erythrocyte membrane. Biochimica et Biophysica Acta 775, 189–96.CrossRefGoogle ScholarPubMed
Franck, P. F. H., Chiu, D. T.-Y., Op Den Kamp, J. A. F., Lubin, B., Van Deenen, L. L. M. & Roelofsen, B. (1983). Accelerated transbilayer movement of phosphatidylcholine in sickled erythrocytes – a reversible process. Journal of Biological Chemistry 258, 8435–42.CrossRefGoogle ScholarPubMed
Franck, P. F. H., Op Den Kamp, J. A. F., Roelofson, B. & Van Deenen, L. L. M. (1986). Does diamide treatment of intact erythrocytes cause a loss of phospholipid asymmetry? Biochimica et Biophysica Acta 857, 127–30.CrossRefGoogle Scholar
Gupta, C. M. (1987). Stabilization mechanisms of transbilayer phospholipid asymmetry in erythrocyte membrane. Current Science 23, 1201–9.Google Scholar
Gupta, C. M. & Mishra, G. (1981). Transbilayer phospholipid asymmetry in Plasmodium knowlesi-infected host cell membrane. Science 212, 1047–8.CrossRefGoogle ScholarPubMed
Haest, C., Plasa, G., Camp, D. & Deuticke, B. (1978). Spectrin as a stabilizer of the phospholipid asymmetry in the human erythrocyte membrane. Biochimica et Biophysica Acta 509, 2132.CrossRefGoogle ScholarPubMed
Halbhuber, K. J., Zimmerman, N., Oehring, H., Stibenz, D. & Linss, W. (1987 a). Red blood cell aging – membrane skeleton alteration and IgG receptor expression. Folia Histochemica et Cytobiologica 25, 137–42.Google ScholarPubMed
Halbhuber, K. J., Stibenz, D., Meyer, H. W., Zimmerman, N., Linss, W., Oehring, H. & Brox, D. (1987 b). Membrane skeleton alteration – a factor promoting IgG receptor expression in the erythrocyte membrane. Biomedica et Biochimica Acta 46, S88–S92.Google ScholarPubMed
Haldar, K., De Amorim, A. & Cross, G. (1989). Transport of fluorescent phospholipid analogues from the erythrocyte membrane to the parasite in Plasmodium falciparum-infected cells. Journal of Cell Biology 108, 2183–92.CrossRefGoogle Scholar
Herrmann, A., Clague, M., Puri, A., Morris, S., Blumenthal, R. & Grimaldi, S. (1990). Effect of erythrocyte transbilayer phospholipid distribution on fusion with vesicular stomatitis virus. Biochemistry 29, 4054–8.CrossRefGoogle ScholarPubMed
Jain, K. (1989). The neonatal erythrocyte and its oxidative susceptibility. Seminars in Hematology 26, 286300.Google ScholarPubMed
Joshi, P., Dutta, G. & Gupta, C. (1987). An intracellular simian malarial parasite (Plasmodium knowlesi) induces stage-dependent alterations in membrane phospholipid organization of its host erythrocyte. The Biochemical Journal 246, 103–8.CrossRefGoogle ScholarPubMed
Joshi, P. & Gupta, C. (1988). Abnormal membrane phospholipid organization in Plasmodium falciparum-infected human erythrocytes. British Journal of Haematology 68, 255–9.CrossRefGoogle ScholarPubMed
Lambros, C. & Vanderberg, J. P. (1980). Synchronization of Plasmodium falciparum erythrocyte stages in culture. Journal of Parasitology 65, 418–20.CrossRefGoogle Scholar
Lubin, B., Kuypers, F. & Chiu, D. (1989). Lipid alterations and cellular properties of sickle red cells. Annals of the New York Academy of Sciences 565, 8695.CrossRefGoogle ScholarPubMed
Maguire, P. A. & Sherman, I. W. (1990). Phospholipid composition, cholesterol content and cholesterol exchange in Plasmodium falciparum infected red cells. Molecular and Biochemical Parasitology 38, 105–12.CrossRefGoogle ScholarPubMed
Middelkoop, E., Lubin, B. H., Bevers, E. M., Op Den Kamp, J. A. F., Comfurius, P., Chiu, T. T.-Y., Zwaal, R. F. A., Van Deenen, L. L. M. & Roelofsen, B. (1988). Studies on sickled erythrocytes provide evidence that the asymmetric distribution of phosphatidylserine in the red cell membrane is maintained by both ATP-dependent translocation and interaction with membrane skeletal proteins. Biochimica et Biophysica Acta 937, 281–8.CrossRefGoogle ScholarPubMed
Middlekoop, E., Van Der Hoek, E., Bevers, E., Comfurius, P., Slotboom, A., Op Den Kamp, J., Lubin, B., Zwaal, R. & Roelofsen, B. (1989). Involvement of ATP-dependent aminophospholipid translocation in maintaining phospholipid asymmetry in diamidetreated human erythrocytes. Biochimica et Biophysica Acta 981, 151–60.CrossRefGoogle ScholarPubMed
Moll, G., Vial, H., Bevers, E., Ancelin, M., Roelofsen, B., Confurius, P., Slotboom, A., Zwaal, R. F. A., Op Den Kamp, J. A. F. & Van Deenen, L. L. M. (1990). Phospholipid asymmetry in the plasma membrane of malaria infected erythrocytes. Biochemistry and Cell Biology 68, 579–85.CrossRefGoogle ScholarPubMed
Nakornchai, S., Chiraporn, S., Chongchirasiri, S. & Yuthavong, Y. (1983). Mechanism of enhanced fusion capacity of mouse red cells infected with Plasmodium berghei. Journal of Cell Science 63, 147–54.CrossRefGoogle ScholarPubMed
Op Den Kamp, J. A. F. (1979). Lipid asymmetry in membranes. Annual Review of Biochemistry 48, 4771.CrossRefGoogle ScholarPubMed
Op Den Kamp, J. A. F. (1981). The asymmetric architecture of membranes. In New Comprehensive Biochemistry (ed. Fineau, J. B. & Michell, R. H.), pp. 83126. Amsterdam: Elsevier.Google Scholar
Pasvol, G., Wilson, R. J. M., Smalley, M. E. & Brown, J. (1978). Separation of viable schizont-infected red cells of Plasmodium falciparum from human blood. Annals of Tropical Medicine and Parasitology 721, 87–8.CrossRefGoogle Scholar
Pradhan, D., Weiser, M., Lumley-SAPANSKI, K., Frazier, D., Kemper, S., Williamson, P. & Schlegel, R. (1990). Peroxidation-induced perturbations of erythrocyte lipid organization. Biochimica et Biophysica Acta 1023, 398404.CrossRefGoogle ScholarPubMed
Schwartz, R. W., Olsen, J. A., Raventos-SUAREZ, C., Yee, M., Heath, R. H., Lubin, B. & Nagel, R. L. (1987). Altered plasma membrane phospholipid organization in Plasmodium falciparum-infected human erythrocytes. Blood 69, 401–7.CrossRefGoogle ScholarPubMed
Schwartz, R., Tanaka, Y., Fidler, I., Chiu, D., Lubin, B. & Schroit, A. (1985). Adherence of sickled and phosphatidylserine-enriched human erythrocytes to cultured human peripheral blood monocytes. Journal of Clinical Investigation 75, 1965–72.CrossRefGoogle ScholarPubMed
Sherman, I. & Valdez, E. (1989). In vitro cytoadherence of Plasmodium falciparum-infected erythrocytes to melanoma cells: factors affecting adhesion. Parasitology 98, 359–69.CrossRefGoogle ScholarPubMed
Shinar, E. & Rachmilewitz, E. (1990). Oxidative denaturation of red blood cells in thalassemia. Seminars in Hematology 27, 7082.Google ScholarPubMed
Slotte, J., HedstrÖm, G., RannstrÖm, S. & Ekman, S. (1989). Effects of sphingomyelin degradation on cell cholesterol oxidizability and steady-state distribution between the cell surface and the cell interior. Biochimica et Biophysica Acta 985, 90–6.CrossRefGoogle ScholarPubMed
Tanabe, K., Matsumoto, T., Furasawa, M. & Takada, S. (1982). An increase in Sendai virus-induced cell fusion of erythrocytes infected with P. chabaudi. Experientia 38, 342–4.CrossRefGoogle Scholar
Tanaka, Y. & Schroit, A. (1983). Insertion of fluorescent phosphatidylserine into the membrane of red blood cells. Recognition of autologous macrophages. Journal of Biological Chemistry 258, 11335–43.CrossRefGoogle ScholarPubMed
Trager, W. & Jensen, J. B. (1976). Human malaria parasites in continuous culture. Science 193, 673–5.CrossRefGoogle ScholarPubMed
Tullius, E., Williamson, P. & Schlegel, R. (1989). Effect of transbilayer phospholipid distribution on erythrocyte fusion. Bioscience Reports 9, 623–33.CrossRefGoogle ScholarPubMed
Van Der Schaft, P., Beaumelle, B., Vial, H., Roelofsen, B., Op Den Kamp, J. & Van Deenen, L. (1987). Phospholipid organization in monkey erythrocytes upon Plasmodium knowlesi infection. Biochimica et Biophysica Acta 901, 114.CrossRefGoogle ScholarPubMed
Wali, R., Jaffe, S., Kumar, D. & Kalra, V. (1988). Alterations in organization of phospholipids in erythrocytes as a factor in adherence to endothelial cells in diabetes mellitus. Diabetes 37, 104–11.CrossRefGoogle ScholarPubMed
Wallach, D. F., Mikkelsen, R. B. & Schmidt-ULLRICH, R. (1981). Plasmodial modifications of erythrocyte surfaces. Ciba Foundation Symposium 80, 220–33.Google ScholarPubMed
Zachowski, A., Fellman, P. & Devaux, P. F. (1985). Absence of transbilayer diffusion of spin-labeled sphingomyelin on human erythrocytes. Comparison with the diffusion of several spin-labeled glycerophospholipids. Biochimica et Biophysica Acta 815, 510–14.CrossRefGoogle ScholarPubMed
Zipser, Y., Shachar, R., Goldfarb, A., Rachmilewitz, E. & Kosower, N. A. (1988). Organization of membrane phospholipids in β-thalassemia red cells. The 4th International Congress of Cell Biology, Montreal, Canada (Abstract).Google Scholar
Zwaal, R. F. A., Bevers, E. M., Comfurius, P., Rosing, J., Tilly, R. H. J. & Verhallen, P. F. J. (1989). Loss of membrane phospholipid asymmetry during activation of blood platelets and sickled red cells; mechanisms and physiological significance. Molecular and Cellular Biochemistry 91, 2331.CrossRefGoogle ScholarPubMed