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Plasmodium falciparum: regional differences in lectin and cationized ferritin binding to the surface of the malaria-infected human erythrocyte

Published online by Cambridge University Press:  06 April 2009

I. W. Sherman  and
Jane R. T. Greenan
I. W. Sherman
Affiliation:
Department of Biology, University of California, Riverside, CA 92521
Jane R. T. Greenan
Affiliation:
Department of Biology, University of California, Riverside, CA 92521
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Summary

The distribution of anionic residues on the surface of erythrocytes infected with Plasmodium falciparum was studied using cationized ferritin (CF) and transmission electron microscopy. CF staining of uninfected erythrocytes or erythrocytes infected with a knobless variant resulted in a dense and uniform distribution of ferritin particles; however, when red cells infected with a knob-inducing variant were exposed to CF, aggregates of ferritin particles were observed in the region of membrane elevation. Lectin binding to the erythrocyte surface was visualized by transmission electron microscopy using ferritin-conjugated lectins and lectin-fetuin-gold. No differences were observed in the lectin-binding patterns of malaria-infected or uninfected erythrocytes using WGA (wheat-germ agglutinin), RCA (ricin), and Limax flavus lectin. In distinct contrast to the uniform distribution of ferritin particles seen with these lectins was the appearance of clusters of ferritin-ConA over the knobby regions. Localized aggregates of ConA were not seen in knob-free areas or on the surface of red cells infected with a knobless variant. No significant differences were found in the agglutination reactions of normal and infected cells with the Cancer antennarius lectin specific for O-acylated sialic acids.

Type
Research Article
Information
Parasitology , Volume 93 , Issue 1 , August 1986 , pp. 17 - 32
Copyright
Copyright © Cambridge University Press 1986

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References

Ackerman, G. A. (1975). Surface differentiation of hemopoietic cells demonstrated ultrastructurally with cationized ferritin. Cell and Tissue Research 159, 23–37.CrossRefGoogle ScholarPubMed
Aikawa, M. (1977). Variations in structure and function during the life cycle of malarial parasites. Bulletin of the World Health Organization 55, 139–56.Google ScholarPubMed
Aikawa, M. & Miller, L. (1983). Structural alterations of the erythrocyte membrane during malarial parasite invasion and intraerythrocytic development. Ciba Foundation Symposium 94, 45–59.Google ScholarPubMed
Allred, D. R., Sterling, C. & Morse, P. (1983). Increased fluidity of Plasmodium berghei-infected mouse red blood cell membranes detected by electron spin resonance spectroscopy. Molecular and Biochemical Parasitology 7, 27–39.CrossRefGoogle ScholarPubMed
Allred, D., Gruenberg, J. & Sherman, I. (1986). Dynamic rearrangements of erythrocyte membrane internal architecture induced by infection with Plasmodium falciparum. Journal of Cell Science (in the Press).CrossRefGoogle ScholarPubMed
Burry, R. W. & Wood, J. G. (1979). Contributions of lipids and proteins to the surface charge of membranes. An electron microscopy study with cationized and anionized ferritin. Journal of Cell Biology 82, 726–41.Google Scholar
Clark, L., Chan, L., Powars, D. & Baker, R. F. (1981). Negative charge distribution and density on the surface of oxygenated normal and sickle red cells. Blood 57, 675–8.CrossRefGoogle ScholarPubMed
Danon, D., Goldstein, L., Marikovsky, Y. & Skutelsky, E. (1972). Use of cationized ferritin as a label of negative charges on cell surfaces.Journal of Ultrastructure Research 38, 500–10.CrossRefGoogle ScholarPubMed
David, P. H., Hommel, M. & Oligino, L. (1981). Interactions of Plasmodium falciparum infected erythrocytes with ligand-coated agarose beads. Molecular and Biochemical Parasitology 4, 195–204.CrossRefGoogle ScholarPubMed
Etkin, N. L. & Eaton, J. W. (1975). Malaria induced erythrocyte oxidant sensitivity. In Erythrocyte Structure and Metabolism (ed. Brewer, G. J.), pp. 219–32. New York: A. Liss Inc.Google Scholar
Frank, P., Berers, E., Lubin, B., Comfurius, P., Op den Kamp, J., Zwaal, R., Van Deenen, L. & Roelofsen, B. (1985). Uncoupling of the membrane skeleton from the lipid bilayer. The cause of accelerated phospholipid flip-flop leading to an enhanced procoagulant activity of sickled cells. Journal of Clinical Investigation 75, 183–90.CrossRefGoogle Scholar
Frens, G. (1973). Controlled nucleation for the regulation of the particle size in monodisperse gold solutions. Nature Physical Science 241, 20.Google Scholar
Friedman, M., Roth, E., Nagel, R. & Trager, W. (1979). Plasmodium falciparum: Physiological interactions with the human sickle cell. Experimental Parasitology 47, 73–80.CrossRefGoogle ScholarPubMed
Gruenberg, J., Allred, D. & Sherman, I. W. (1983). Scanning electron microscope analysis of the protrusions (knobs) present on the surface of Plasmodium falciparum-infected erythrocytes. Journal of Cell Biology 97, 795–802.CrossRefGoogle ScholarPubMed
Gupta, C. M., Alm, A., Mathur, P. & Dutta, G. (1982). A new look at non-parasitized red cells of malaria-infected monkeys. Nature, London 299, 259–61.CrossRefGoogle Scholar
Gupta, C. M. & Mishra, G. C. (1981). Transbilayer phospholipid asymmetry in Plasmodium knowlesi-infected host cell membrane. Science 212, 1047–9.CrossRefGoogle ScholarPubMed
Hebbel, R., Yamada, O., Moldow, C., Jacob, H., White, J. & Eaton, J. (1980). Abnormal adherence of sickle erythrocytes to cultured vascular endothelium. Journal of Clinical Investigation 65, 154–60.Google Scholar
Howard, R. J. & Day, K. P. (1981). Plasmodium berghei: Modification of sialic acid on red cells from infected mouse blood. Experimental Parasitology 51, 95–103.CrossRefGoogle ScholarPubMed
Howard, R. J. & Sawyer, W. H. (1980). Changes in the membrane microviscosity of mouse red blood cells infected with Plasmodium berghei detected using nonyl(9-anthroyloxy) fatty acid fluorescent probes. Parasitology 80, 331–42.CrossRefGoogle Scholar
Johnson, G., Allen, D., Cadman, S., Fairbank, J., White, J., Lampkin, B. & Kaplan, M. (1979). Red cell membrane polypeptide aggregates in glucose-6-phosphate dehydrogenase mutants with chronic hemolytic disease. New England Journal of Medicine 301, 512–27.CrossRefGoogle ScholarPubMed
Kahane, I., Ben-Chetrit, E., Shifter, A. & Rachmilewitz, E. A. (1980). The erythrocyte membranes in β-thalassemia. Lower sialic acid levels in glycophorin. Biochimica et Biophysica Acta 596, 10–17.CrossRefGoogle ScholarPubMed
Kilejian, A. & Olson, J. (1979). Proteins and glycoproteins from human erythrocytes infected with Plasmodium falciparum. Bulletin of the World Health Organization 57, 101–7.Google ScholarPubMed
Krungkrai, J. & Yuthavong, Y. (1983). Enhanced Ca2+ uptake by mouse erythrocytes in malarial (Plasmodium berghei) infection. Molecular and Biochemical Parasitology 7, 227–36.Google Scholar
Langreth, S. G. & Reese, R. T. (1979). Antigenicity of the infected erythrocyte and merozoite surface in falciparum malaria. Journal of Experimental Medicine 150, 1241–54.Google Scholar
Leech, J. H., Barnwell, J. W., Miller, L. H. & Howard, R. J. (1984). Indentification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. Journal of Experimental Medicine 159, 1567–75.CrossRefGoogle Scholar
Lubin, B., Chin, D., Bastacky, J., Roelofson, B. & Van Deenen, L. (1981). Abnormalities in membrane phospholipid organization in sickled erythrocytes. Journal of Clinical Investigation 67, 1643–9.CrossRefGoogle ScholarPubMed
Luse, S. A. & Miller, L. H. (1971). Plasmodium falciparum: Ultrastructure of parasitized erythrocytes in cardiac vessels. American Journal of Tropical Medicine and Hygiene 20, 655–60.CrossRefGoogle ScholarPubMed
Macpherson, G. G., Warrell, M. J., White, N. J., Looareesuwan, S. & Warrell, D. A. (1985). Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. American Journal of Pathology 119, 385–401.Google ScholarPubMed
Miller, L., Cooper, G., Chien, S. & Freemount, H. N. (1972). Surface charge on Plasmodium knowlesi- and P. coatneyi-infected red cells of Macaca mullatta. Experimental Parasitology 32, 86–95.CrossRefGoogle Scholar
Orr, G. & Rando, R. (1978). Synthetic concanavalin A receptors and erythrocyte agglutination. Nature, London 272, 722–5.CrossRefGoogle ScholarPubMed
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
Raventos-Suarez, C., Kaul, D. K., Macaluso, F. & Nagel, R. (1985). Membrane knobs are required for the microcirculatory obstruction induced by Plasmodium falciparum-infected erythrocytes. Proceedings of the National Academy of Sciences, USA 82, 3829–33.CrossRefGoogle ScholarPubMed
Ravindranath, M., Higa, H., Cooper, E. & Paulson, J. (1985). Purification and characterization of an o–acetylsialic acid-specific lectin from a marine crab Cancer antennarius. Journal of Biological Chemistry 260, 8850–6.CrossRefGoogle ScholarPubMed
Roffman, E., Spiegel, Y. & Wilchek, M. (1980). Ferritin hydrazide, a novel covalent electron dense reagent for the ultrastructural localization of glycoconjugates. Biochemical and Biophysical Research Communication 97, 1192–8.Google Scholar
Roth, J., Lucocq, J. & Charest, P. (1984). Light and electron microscopic demonstration of sialicacid residues with the lectin from Limax flavus: A cytochemical affinity technique with the use of fetuin–gold complexes. Journal of Histology and Cytochemistry 32, 1167–76.CrossRefGoogle Scholar
Sauberman, N., Fortier, N., Joshi, W., Piotrowski, J. & Snyder, L. (1983). Spectrin-hemoglobin crosslinkages associated with in vitro oxidant hypersensitivity in pathologic and artificially dehydrated cells. British Journal of Haematology 54, 15–28.Google Scholar
Schnebli, H. & Bachi, T. (1975). Reaction of lectins with human erythrocytes. Factors governing the agglutination reaction. Experimental Cell Research 91, 175–83.Google Scholar
Shakespeare, P., Trigg, P. & Tappenden, L. (1979). Some properties of membranes in the simian malaria parasite. Annals of Tropical Medicine and Parasitology 73, 333–43.Google Scholar
Sharon, N. & Lis, H. (1975). Use of lectins for the study of membranes. In Methods in Membrane Biology, vol. 3 (ed. Korn, E.), pp. 147–200. New York: Plenum.Google Scholar
Sherman, I. W. & Greenan, J. (1984). Malarial infection alters red cell membrane fluidity. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 641–4.CrossRefGoogle ScholarPubMed
Snyder, L. M., Leb, L., Piotrowski, J., Sauberman, N., Lius, S. & Fortier, N. (1983). Irreversible spectrin-haemoglobin crosslinking in vivo: a marker for red cell senecence. British Journal of Haematology 53, 379–84.Google Scholar
Takahashi, Y., Sherman, I. W. (1978). Plasmodium lophurae: Cationized ferritin staining, an electron microscope cytochemical method of differentiating malarial parasite and host cell membranes. Experimental Parasitology 44, 145–54.CrossRefGoogle Scholar
Takahashi, Y. & Sherman, I. W. (1980). Plasmodium lophurae: Lectin mediated agglutination of malaria-infected red cells and fine-structure cytochemical detection of lectin binding sites on plasmodial and host cell membranes. Experimental Parasitology 49, 233–47.CrossRefGoogle Scholar
Tanabe, K., Mikkelson, R. & Wallach, D. (1982). Calcium transport of Plasmodium chabaudi infected erythrocytes. Journal of Cell Biology 93, 680–4.CrossRefGoogle ScholarPubMed
Trager, W. & Jensen, J. B. (1976). Human malaria parasites in continuous culture. Science 193, 673–5.Google Scholar
Vincent, H. M. & Wilson, R. J. M. (1980). Reduced lectin binding on erythrocytes of monkeys infected with malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 449–55.CrossRefGoogle ScholarPubMed
Walker, D. (1981). Cationic ferritin binding sites and surface charge densities of transformed cells. Journal of Histology and Cytochemistry 29, 255–65.CrossRefGoogle ScholarPubMed
Wassef, N., Richardson, E. & Alving, C. R. (1985). Specific binding of concanavalin A to free inositol and liposomes containing phosphatidylinositol. Biochemical and Biophysical Research Communications 130, 76–83.Google Scholar
Wise, G. E., Shienvold, F. L. & Rubin, R. W. (1978). Effects of pronase and concanavalin A upon the freeze-etch morphology of cell membranes of intact human erythrocytes. Journal of Cell Science 30, 63–76.CrossRefGoogle ScholarPubMed
Zweig, S. E., Tokuyasu, K. T. & Singer, S. J. (1981). Member-associated changes during erythro-poiesis. On the mechanism of maturation of reticulocytes to erythrocytes. Journal of Supramolecular Structure and Cellular Biochemistry 17, 163–81.Google Scholar