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Changes in the membrane microviscosity of mouse red blood cells infected with Plasmodium berghei detected using n-(9-anthroyloxy) fatty acid fluorescent probes

Published online by Cambridge University Press:  06 April 2009

R. J. Howard
Affiliation:
Immunoparasitology Laboratory, The Walter and Eliza Hall Institute of Medical Research, Parkville, Victoria 3052, Australia
W. H. Sawyer
Affiliation:
The Russell Grimwade School of Biochemistry, University of Melbourne, Parkville, Victoria 3052, Australia

Summary

A set of n-(9-anthroyloxy) fatty acids (n = 2, 6, 9, 12, 16) have been used as fluorescent probes to examine the lipid environment at different depths in the outer membrane of normal mouse erythrocytes and red blood cells from Plasmodium berghei-infected blood. Fluorescent polarization experiments with normal mouse erythrocytes have demonstrated a typical gradient in microviscosity from the surface to the centre of the bilayer as a consequence of the motional properties of the C-atoms of the phospholipid acyl chains. The fluorescent probes rotate faster in the membrane of purified pluriparasitized cells (> 90% purity) than with the remaining fraction of red blood cells from infected blood (20–40% immature, infected red cells, and uninfected red cells), or normal mouse erythrocytes. This increase in fluidity with heavily infected cells occurs predominantly at the centre of the lipid bilayer, rather than at the membrane surface. A comparison of the polarization values of intact and lysed infected cells indicates that the fluorescent fatty acids preferentially label the plasma membrane rather than the internal membranes of infected cells. The results suggest that P. berghei infection causes a change in the composition and/or organization of the outer membrane of pluriparasitized cells which produces a decrease in membrane microviscosity.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1980

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References

Angus, M. G. N., Fletcher, K. A. & Maegraith, B. G. (1971). Studies on the lipids of Plasmodium knowlesi-infected rhesus monkeys (Macaca mulatta). IV. Changes in erythrocyte lipids. Annals of Tropical Medicine and Parasitology 65, 429–39.CrossRefGoogle ScholarPubMed
Barenholz, Y., Moore, N. F. & Wagner, R. R. (1976). Enveloped viruses as model membrane systems. Microviscosity of vesicular stomatitis virus and host cell membranes. Biochemistry 15, 3563–70.CrossRefGoogle ScholarPubMed
Bashford, C. L., Morgan, C. S. & Radda, G. K. (1976). Measurement and interpretation of fluorescence polarizations in phospholipid dispersions. Biochimica et biophysica acta 426, 157–72.CrossRefGoogle Scholar
Beach, D. H., Sherman, I. W. & Holz, G. G. Jr. (1977). Lipids of Plasmodium lophurae, and of erythrocytes and plasmas of normal and P. lophurae-infected pekin ducklings. Journal of Parasitology 63, 6275.CrossRefGoogle ScholarPubMed
Bruckdorfer, K. R., Demel, R. A., De Gier, J. & Van Deenen, L. L. M. (1969). The effect of partial replacements of membrane cholesterol by other steroids on the osmotic fragility and glycerol permeability of erythrocytes. Biochimica et biophysica acta 183, 334–45.CrossRefGoogle ScholarPubMed
Cenedella, R. J., Jarrell, J. J. & Saxe, L. H. (1969). Plasmodium berghei: production in vitro of free fatty acids. Experimental Parasitology 24, 130–6.CrossRefGoogle ScholarPubMed
Cooper, R. A. (1978). Increased membrane cholesterol and decreased membrane fluidity in human red blood cells. Journal of Supramolecular Structure (Suppl.) 2, 189.Google Scholar
Cooper, R. A., Arner, E. C., Wiley, J. S. & Shattil, S. J. (1975). Modification of red cell membrane structure by cholesterol-rich lipid dispersions. A model for the primary spur cell defect. Journal of Clinical Investigation 55, 115–26.CrossRefGoogle Scholar
Cooper, R. A., Diloy-Puray, M., Lando, P. & Greenberg, M. S. (1972). An analysis of lipoproteins, bile acids and red cell membranes associated with target cells and spur cells in patients with liver disease. Journal of Clinical Investigation 51, 3182–92.CrossRefGoogle ScholarPubMed
Crumpton, M. J., Marchalonis, J. J., Haustein, D., Atwell, J. J. & Harris, A. W. (1976). Plasma membrane of a murine T cell lymphoma: surface labelling, membrane isolation, separation of membrane proteins and distribution of surface label amongst these proteins. Australian Journal of Experimental Biology and Medical Science 54, 302–16.Google ScholarPubMed
Crumpton, M. J. & Snary, D. (1974). Preparation and properties of lymphocyte plasma membrane. In Contemporary Topics in Molecular Immunology, vol. 3 (ed. Ada, G. L.), pp. 2756. New York: Plenum Publishing.CrossRefGoogle Scholar
Dawson, R. M. C. (1973). The exchange of phospholipids between cell membranes. Subcellular Biochemistry 2, 6989.Google ScholarPubMed
Demel, R. A. & De Kruyff, B. (1976). The function of sterols in membranes. Biochimica et biophysica acta 457, 109–32.CrossRefGoogle ScholarPubMed
Dunn, M. J. (1969 a). Alterations in red blood cell metabolism in simian malaria: evidence for abnormalities of non-parasitized cells. Military Medicine 134 (Suppl.), 110–15.CrossRefGoogle Scholar
Dunn, M. J. (1969 b). Alterations of red blood cell sodium transport during malarial infection. Journal of Clinical Investigation 48, 674–84.CrossRefGoogle ScholarPubMed
Dvorak, J. A., Miller, L. H., Whitehouse, W. C. & Shiroishi, T. (1975). Invasion of erythrocytes by malaria merozoites. Science 187, 748–50.CrossRefGoogle ScholarPubMed
Fogel, B. J., Shields, C. & Von Doenhoff, A. Jr. (1966). The osmotic fragility of erythrocytes in experimental malaria. American Journal of Tropical Medicine and Hygiene 15, 269–75.CrossRefGoogle ScholarPubMed
Ginger, C. (1967). Preliminary studies on the lipid constitution of the malaria parasite. Transactions of the Royal Society for Tropical Medicine and Hygiene 61, 23.Google Scholar
Ginn, F. L., Hochstein, P. & Trump, B. F. (1969). Membrane alterations in hemolysis: internalization of plasmalemma induced by primaquine. Science 164, 843.CrossRefGoogle ScholarPubMed
Haigh, E. A., Thulborn, K. R. & Sawyer, W. H. (1979). Comparison of fluorescence energy transfer and quenching methods to establish the position and orientation of components within the transverse plane of the lipid bilayer. Application to the gramicidin A-bilayer interaction. Biochemistry 18, 3525.CrossRefGoogle Scholar
Hare, F. & Lussan, C. (1977). Variations in microviscosity values induced by different rotational behaviour of fluorescent probes in some aliphatic environments. Biochimica et biophysica acta 467, 262–72.CrossRefGoogle ScholarPubMed
Holz, G. G. Jr. (1977). Lipids and the malaria parasite. Bulletin of the World, Health Organization 55, 235–46.Google Scholar
Holz, G. G. Jr., Beach, D. H. & Sherman, I. W. (1977). Octadecenoic fatty acids and their association with hemolysis in malaria. Journal of Protozoology 24, 566–74.CrossRefGoogle ScholarPubMed
Howard, R. J., Battye, F. L. & Mitchell, G. F. (1979). Plasmodium-infected blood cells analysed and sorted by flow fluorimetry using the deoxyribonucleic acid binding dye 33258 Hoechst. Journal of Histochemistry and Cytochemistry 27, 803–13.CrossRefGoogle ScholarPubMed
Howard, R. J., Smith, P. M. & Mitchell, G. F. (1978 a). External proteins on hemosporidial infected erythrocytes. Journal of Supramolecular Structure (Suppl.) 2, 218.Google Scholar
Howard, R. J., Smith, P. M. & Mitchell, G. F. (1978 b). Removal of leucocytes from red cells in Plasmodium berghei-infected mouse blood and purification of schizont-infected cells. Annals of Tropical Medicine and Parasitology 72, 573–5.CrossRefGoogle ScholarPubMed
Kimelberg, H. K. & Papahadjopoulos, D. (1974). Effects of phospholipid acyl chain fluidity, phase transitions, and cholesterol on (sodium-potassium ion)-stimulated adenosine-tri-phosphatase. Journal of Biological Chemistry 249, 1071–80.CrossRefGoogle Scholar
Königk, E. & Mirtsch, S. (1977). Plasmodium chabaudi infection of mice: specific activities of erythrocyte membrane associated enzymes and patterns of proteins and glycoproteins of erythrocyte membrane preparations. Zeitschrift für Tropenmedizin und Parasitologie 28, 1722.Google ScholarPubMed
Ladda, R., Aikawa, M. & Sprinz, H. (1969). Penetration of erythrocytes by merozoites of mammalian and avian malarial parasites. Journal of Parasitology 65, 633–44.CrossRefGoogle Scholar
Laser, H. (1948). Hemolytic system in the blood of malaria-infected monkeys. Nature, London 161, 560.CrossRefGoogle ScholarPubMed
Laser, H., Kemp, P., Miller, N., Lander, D. & Klein, R. A. (1975 a). Malaria, quinine and red cell lysis. Parasitology 71, 167–81.CrossRefGoogle ScholarPubMed
Laser, H., Klein, R. A., Kemp, P., Lander, D. & Miller, N. G. A. (1975 b). Changes in the neutral lipid content of erythrocytes parasitized by Plasmodium knowlesi. Parasitology 71, v–vi.Google Scholar
Lawrence, C. W. & Cenedella, R. J. (1969). Lipid content of Plasmodium berghei-infected rat red blood cells. Experimental Parasitology 26, 181–6.CrossRefGoogle ScholarPubMed
McLaren, D. J., Bannister, L. H., Trigg, P. I. & Butcher, G. A. (1977). A freeze-fracture study on the parasite-erythrocyte inter-relationship in Plasmodium knowlesi infections. Bulletin of the World-Health Organization 55, 199203.Google Scholar
Miller, L. H. & Chien, S. (1971). Density distribution of red cells infected by Plasmodium knowlesi and Plasmodium coatneyi. Experimental Parasitology 29, 451–6.CrossRefGoogle ScholarPubMed
Neame, K. D. & Homewood, C. A. (1975). Alterations in the permeability of mouse erythrocytes infected with the malaria parasite Plasmodium berghei. International journal for Parasitology 5, 537–40.CrossRefGoogle ScholarPubMed
Pagano, R. E., Ozato, K. & Ruysschaert, F. M. (1977). Intracellular distribution of lipophilic fluorescent probes in mammalian cells. Biochimica et biophysica acta 465, 661–6.CrossRefGoogle ScholarPubMed
Rao, R. N., Subrahmanyam, D. & Prakash, S. (1970). Plasmodium berghei: lipids of rat red-blood cells. Experimental Parasitology 27, 22–7.CrossRefGoogle ScholarPubMed
Rock, R. C. (1971). Incorporation of 14C-labelled fatty acids into lipids of rhesus erythrocytes and Plasmodium knowlesi in vitro. Comparative Biochemistry and Physiology 40, 893906.Google Scholar
Seed, T. M. & Kreier, J. P. (1972). Plasmodium gallinaceum: erythrocyte membrane alterations and associated plasma changes induced by experimental infections. Proceedings of the Helminthological Society of Washington 39 (Special Issue), 387411.Google Scholar
Seelig, A. & Seelig, J. (1974). The dynamic structure of fatty acyl chains in a phospholipid bilayer measured by deuterium magnetic resonance. Biochemistry 13, 4839–45.CrossRefGoogle Scholar
Shaklai, N., Yguerabide, J. & Ranney, H. M. (1977). Interaction of hemoglobin with red blood cell membranes as shown by a fluorescent chromophore. Biochemistry 16, 5585–97.CrossRefGoogle ScholarPubMed
Shattil, S. J. & Cooper, R. A. (1976). Membrane microviscosity and human platelet function. Biochemistry 15, 4832–7.CrossRefGoogle ScholarPubMed
Sherman, I. W. & Tanagoshi, L. (1974). Incorporation of 14C-amino acids by malarial plasmodia (Plasmodium lophurae). VI. Changes in the kinetic constants of amino acid transport during infection. Experimental Parasitology 35, 369–73.CrossRefGoogle Scholar
Shinitzky, M. & Barenholz, Y. (1978). Fluidity parameters of lipid regions determined by fluorescence polarization. Biochimica et biophysica acta 515, 367–94.CrossRefGoogle ScholarPubMed
Siddiqui, W. A., Schnell, J. V. & Geiman, Q. M. (1967). Stearic acid as plasma replacement for intracellular in vitro culture of Plasmodium knowlesi. Science 156, 1623–5.CrossRefGoogle ScholarPubMed
Thulborn, K. R. & Sawyer, W. H. (1978). Properties and locations of a set of fluorescent probes sensitive to the fluidity gradient of the lipid bilayer. Biochimica et biophysica acta 511, 125–40.CrossRefGoogle Scholar
Thulborn, K. R., Treloar, F. E. & Sawyer, W. H. (1978). A microviscosity barrier in the lipid bilayer due to the presence of phospholipids containing unsaturated acyl chains. Biochemical and Biophysical Research Communications 81, 42–9.CrossRefGoogle Scholar
Tilley, L., Thulborn, K. R. & Sawyer, W. H. (1979). An assessment of the fluidity gradient of the lipid bilayer as determined by a set of n–(9-anthroyloxy) fatty acids (n = 2, 6, 9, 12, 16). Journal of Biological Chemistry 254, 2592–4.CrossRefGoogle Scholar
Trigg, P. I. (1968). A new continuous perfusion technique for the cultivation of malaria parasites in vitro. Transactions of the Royal Society of Tropical Medicine and Hygiene 62, 371–8.CrossRefGoogle Scholar
Trigg, P. I., Hirst, S. I., Shakespeare, P. G. & Tappenden, L. (1977). Labelling of membrane glycoproteins in erythrocytes infected with Plasmodium knowlesi. Bulletin of the World Health Organization 55, 203–7.Google ScholarPubMed
Wallace, W. R. (1966). Fatty acid composition of lipid classes in Plasmodium lophurae and Plasmodium berghei. American Journal of Tropical Medicine and Hygiene 15, 811–13.CrossRefGoogle ScholarPubMed
Wallach, D. F. H. & Conley, M. (1977). Altered membrane proteins of monkey erythrocytes infected with simian malaria. Journal of Molecular Medicine 2, 119–36.Google Scholar
Weidekamm, E., Wallach, D. F. H., Lin, P.-S. & Hendricks, J. (1973). Erythrocyte membrane alterations due to infection with Plasmodium berghei. Biochimica et biophysica acta 323, 539–46.CrossRefGoogle ScholarPubMed
Wiley, J. S. & Cooper, R. A. (1975). Inhibition of cation cotransport by cholesterol enrichment of human red cell membranes. Biochimica et biophysica acta 413, 425–31.CrossRefGoogle ScholarPubMed
Wright, B. M., Edwards, A. J. & Jones, V. E. (1974). Use of a cell rupturing pump for the preparation of thymocyte subcellular fractions. Journal of Immunological Methods 1, 281–96.CrossRefGoogle Scholar
Yamamoto, R. S., Crittenden, L. B., Sokoloff, L. & Jay, G. E. Jr. (1963). Genetic variations in plasma lipid content in mice. Journal of Lipid Research 4, 413–18.CrossRefGoogle ScholarPubMed