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In vitro cytoadherence of Plasmodium falciparum-infected erythrocytes to melanoma cells: factors affecting adhesion

Published online by Cambridge University Press:  06 April 2009

I. W. Sherman
Affiliation:
Department of Biology, University of California, Riverside, California 92521
Esther Valdez
Affiliation:
Department of Biology, University of California, Riverside, California 92521

Summary

A reproducible and standardized assay for measuring the cytoadherence of knobby Plasmodium falciparum-infected red cells to amelanotic melanoma cells was developed. Adhesion was dependent on temperature, haematocrit, and parasitaemia. Addition of EDTA to the binding medium reduced adhesion. Removal of protease-sensitive molecules on the surface of the infected cell abolished cytoadherence, whereas removal of carbohydrate residues by treatment of cells with neuraminidase or galactosidase promoted adhesion. Calcium, magnesium, fibrinogen or fibronectin in the medium had no effect on adhesion nor was there any enhancement of adhesion by pre-loading infected cells with calcium. Serum was essential for good adhesion. Adhesion was species specific for target cells; human endothelial or amelanotic melanoma cells were suitable target cells whereas bovine cells were not. The amelanotic melanoma cell could be formalin-fixed and still retain its adhesion properties. The binding properties of formalin-fixed amelanotic melanoma cells were not identical to those of endothelial or unfixed target cells.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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References

REFERENCES

Aikawa, M., Rabbege, J. R., Udeinya, I. & Miller, L. H. (1983). Electron microscopy of knobs in Plasmodium falciparum-infected erythrocytes. Journal of Parasitology 69, 435–7.CrossRefGoogle ScholarPubMed
Aley, A. B., Sherwood, J. A. & Howard, R. J. (1984). Knob-positive and knob-negative Plasmodium falciparum differ in expression of a strain-specific malarial antigen on the surface of infected erythrocytes. Journal of Experimental Medicine 160, 1585–90.CrossRefGoogle ScholarPubMed
Aley, S. B., Barnwell, J. W., Daniel, W. A. & Howard, R. J. (1984). Identification of parasite proteins in a membrane preparation enriched for the surface membrane of erythrocytes infected with Plasmodium knowlesi. Molecular and Biochemical Parasitology 12, 6984.CrossRefGoogle Scholar
Barnwell, J. W., Howard, R. J. & Miller, L. H. (1983). Influence of the spleen on the expression of surface antigens on parasitized erythrocytes. Ciba Foundation Symposium 94, 117–36.Google ScholarPubMed
David, P. H., Hommel, M., Miller, L. H., Udeinya, I. J. & Oligino, L. D. (1983). Parasite sequestration in Plasmodium falciparum malaria: spleen and antibody modulation of cytoadherence of infected erythrocytes. Proceedings of the National Academy of Sciences, USA 80, 5075–9.CrossRefGoogle ScholarPubMed
Fukuda, M. N., Fukuda, M. & Hakomori, S.-I. (1979). Cell surface modification by endo-β-galactosidase. Change of blood group activities and release of oligosaccharides from glycoproteins and cyclosphingolipids of human erythrocytes. Journal of Biological Chemistry 254(12), 5488–65.CrossRefGoogle ScholarPubMed
Gruenberg, J., Allred, D. R. & 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, 795802.CrossRefGoogle ScholarPubMed
Harlan, J. M. (1985). Leukocyte-endothelial interactions. Blood 65(3), 513–25.CrossRefGoogle ScholarPubMed
Hoover, R. L. & Karnovsky, M. J. (1984). Adhesive interactions between polymorphonuclear leukocytes and endothelium. In Biology of Endothelial Cells (ed. Jaffe, E. A.), pp. 277–85. Boston: Martinus Nijhoff.CrossRefGoogle Scholar
Howard, R. J., Kaushal, D. & Carter, R. (1982). Plasmodium gallinaceum: radioiodination of parasite antigens with l,3,4,6-tetrachloro)-3α,6α-diphenylglycoluril (Iodogen). Studies with zygotes of P. gallinaceum. Journal of Protozoology 29, 114–17.CrossRefGoogle Scholar
Jaffe, E. A., Nachman, R. L., Becker, C. G. & Minick, C. R. (1973). Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. Journal of Clinical Investigation 52, 2745–56.CrossRefGoogle ScholarPubMed
Lambros, C. & Vanderberg, J. P. (1980). Synchronization of Plasmodium falciparum erythrocytic stages in culture. Journal of Parasitology 65, 418–20.CrossRefGoogle Scholar
Langreth, S. G., Jensen, J. B., Reese, R. T. & Trager, W. (1978). Fine structure of human malaria in vitro. Journal of Protozoology 25, 443–52.CrossRefGoogle ScholarPubMed
Langreth, S. G., Motyl, M. R. & Trager, W. (1979). Plasmodium falciparum: loss of knobs on the infected erythrocyte surface after long term cultivation. Experimental Parasitology 48, 213–19.CrossRefGoogle ScholarPubMed
Leech, J. H., Barnwell, J. W., Miller, L. H. & Howard, R. J. (1984). Identification of a strain-specific malarial antigen exposed on the surface of Plasmodium falciparum-infected erythrocytes. Journal of Experimental Medicine 159, 1567–75.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, 385401.Google ScholarPubMed
Marsh, K., Marsh, V. M., Brown, J., Whittle, H. C. & Greenwood, B. M. (1988). Plasmodium falciparum: the behavior of clinical isolates in an in vitro model of infected red blood cell sequestration. Experimental Parasitology 65, 202–8.CrossRefGoogle Scholar
Mohandas, N. & Evans, E. (1984). Adherence of sickle erythrocytes to vascular endothelial cells: requirement for both cell membrane changes and plasma factors. Blood 64, 282–7.CrossRefGoogle ScholarPubMed
Ockenhouse, C. F. & Chulay, J. D. (1988). Plasmodium falciparum sequestration: OKM5 antigen (DC36) mediates cytoadherence of parasitized erythrocytes to a myelomonocytic cell line. Journal of Infectious Diseases 157(3), 584–8.CrossRefGoogle Scholar
Pasvol, G., Wilson, 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 72, 87–8.CrossRefGoogle ScholarPubMed
Pongponratn, E., Riganti, M., Harinasuta, T. & Bunnag, D. (1985). Electron microscopy of the human brain in cerebral malaria. Southeast Asian Journal of Tropical Medicine and Public Health 16(2), 219–27.Google ScholarPubMed
Raventos-Suarez, C., Kaul, D. K., Maculuso, F. & Nagel, R. L. (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
Roberts, D. D., Sherwood, J. A., Spitalnik, S. L., Panton, L. J., Howard, R. J., Dixit, V. M., Frazier, W. A., Miller, L. H. & Ginsburg, V. (1985). Thrombospondin binds falciparum malaria parasitized erythrocytes and may mediate cytoadherence. Nature, London 318, 64–6.CrossRefGoogle ScholarPubMed
Schlegel, R. A., Prendergast, T. W. & Williamson, P. (1985). Membrane phospholipid asymmetry as a factor in erythrocyte-endothelial cell interactions. Journal of Cellular Physiology 123, 215–18.CrossRefGoogle ScholarPubMed
Schmidt, J. A., Udeinya, I. J., Leech, J. H., Hay, R. J., Aikawa, M., Barnwell, J., Green, I. & Miller, L. H. (1982). Plasmodium falciparum malaria: an amelanotic melanoma cell line bears receptors for the knob ligand on infected erythrocytes. Journal of Clinical Investigation 70, 379–86.CrossRefGoogle ScholarPubMed
Shepro, D., Batbouta, J. C., Robblee, L. S., Carson, M. P. & Belamarich, F. A. (1975). Serotonin transport by cultured bovine aortic endothelium. Circulation Research 36, 799806.CrossRefGoogle ScholarPubMed
Sherman, I. (1985). Membrane structure and function of malaria parasites and the infected erythrocyte. Parasitology 91, 609–45.CrossRefGoogle ScholarPubMed
Sherman, I. W. & Greenan, J. R. T. (1986). Plasmodium falciparum: regional differences in lectin and cationized ferritin binding to the surface of the malaria-infected human erythrocyte. Parasitology 93, 1732.CrossRefGoogle Scholar
Sherwood, J. A., Roberts, D. D., Marsh, K., Harvery, E. B., Spitalnik, S. L., Miller, L. H. & Howard, R. J.(1987). Thrombospondin binding by parasitized erythrocyte isolates in falciparum malaria. American Journal of Tropical Medicine and Hygiene 36(2), 228–33.CrossRefGoogle ScholarPubMed
Singh, B., Monsigny, M. & Hommel, M. (1987). Amino-sugars inhibit the in vitro cytoadherence of Plasmodium falciparum-infected erythrocytes to melanoma cells. Molecular and Biochemical Parasitology 23, 4753.CrossRefGoogle ScholarPubMed
Trager, W. & Jensen, J. B. (1976). Human malaria parasites in continuous culture. Science 193, 673–5.CrossRefGoogle ScholarPubMed
Trager, W., Tershakovec, M., Lyandvert, L., Stanley, H., Lanners, N. & Gubert, E. (1981). Clones of the malaria parasite Plasmodium falciparum obtained by microscopic selection – their characterization with regard to knobs, chloroquine sensitivity, and formation of gametocytes. Proceedings of the National Academy of Sciences, USA 78, 6527–30.CrossRefGoogle ScholarPubMed
Udeinya, I. J., Graves, P. M., Carter, R. & Aikawa, M. (1983). Plasmodium falciparum: effect of time in continuous culture on binding to human endothelial cells and amelanotic melonoma cells. Experimental Parasitology 56, 207–14.CrossRefGoogle Scholar
Udeinya, I. J., Leech, J., Aikawa, M. & Miller, L. H. (1985). An in vitro assay for sequestration: binding of Plasmodium falciparum-infected erythrocytes to formalin-fixed endothelial cells and amelanotic melanoma cells. Journal of Protozoology 32(1), 8890.CrossRefGoogle Scholar
Udeinya, I. J., Schmidt, J. A., Aikawa, M., Miller, L. H. & Green, I. (1981). Falciparum malaria-infected erythrocytes specifically bind to cultured human endothelial cells. Science 213, 555–7.CrossRefGoogle ScholarPubMed
Warrell, D. A. (1987). Pathophysiology of severe falciparum malaria in man. Parasitology 94, S53S76.CrossRefGoogle ScholarPubMed
Wautier, J. L., Pintigny, D., Wautier, M. P., Paton, R. C., Galacteros, F., Passa, P. & Caen, J. P. (1983). Fibrinogen, a modulator of erythrocyte adhesion to vascular endothelium. Journal of Laboratory and Clinical Medicine 101(6), 911–20.Google ScholarPubMed
Wickramasinghe, S. N., Phillips, R. E., Looareesuwan, S., Warrell, D. A. & Hughes, M. (1987). The bone marrow in human cerebral malaria: parasite sequestration within sinusoids. British Journal of Haematology 66, 295306.CrossRefGoogle ScholarPubMed