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Characterization of surface proteins and glycoproteins on red blood cells from mice infected with haemosporidia: Plasmodium berghei infections of BALB/c mice

Published online by Cambridge University Press:  06 April 2009

R. J. Howard ,
Patricia M. Smith  and
G. F. Mitchell
R. J. Howard
Affiliation:
The Laboratory of Immunoparasitology, The Walter and Eliza Hall Institute of Medical Research, Royal Melbourne Hospital P.O., Victoria 3050, Australia
Patricia M. Smith
Affiliation:
The Laboratory of Immunoparasitology, The Walter and Eliza Hall Institute of Medical Research, Royal Melbourne Hospital P.O., Victoria 3050, Australia
G. F. Mitchell
Affiliation:
The Laboratory of Immunoparasitology, The Walter and Eliza Hall Institute of Medical Research, Royal Melbourne Hospital P.O., Victoria 3050, Australia
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Summary

The surface proteins and glycoproteins of red cells from Plasmodium berghei-infected blood have been radio-isotope labelled and compared with those of normal mouse erythrocytes using the following protein labelling probes: lactoperoxidase-catalysed radio-iodination of tyrosyl residues, periodate oxidation and NaB3H4 reduction of sialic acid and oxidation of galactosyl/N-acetylgalactosaminyl residues by galactose oxidase with subsequent NaB3H4 reduction. During P. berghei infection, new tyrosyl-labelled proteins with apparent molecular weights (Mr) of 60000, 54000, 40000 and 27500 appeared on the surface of most, if not all, red cells in the blood. Purified multinucleate cells (mostly reticulocytes) differed only in that they also had a surface protein with Mr of 83000. However, this molecule is thought to be specific to mouse reticulocytes rather than derived from parasites. In contrast to the relatively minor changes detected with radio-iodination, striking changes in glycoprotein radio-isotope labelling resulted from infection. All of the red cells in infected blood of greater than 20% parasitaemia lost their periodate-sensitive glycoprotein sialic acid. With some samples there was little change in glycoprotein labelling by the galactose oxidase method, provided neuraminidase was also added. Modification of the exocyclic hydroxyls of sialic acid is postulated to account for this. Other blood samples exhibited a dramatic loss of galactose oxidase-dependent labelling. It is suggested that these observations may relate to the excessive red cell destruction of uninfected as well as infected cells which has been inferred in many haemosporidial infections, including malaria.

Type
Research Article
Information
Parasitology , Volume 81 , Issue 2 , October 1980 , pp. 273 - 298
Copyright
Copyright © Cambridge University Press 1980

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References

REFERENCES

Aikawa, M., Hepler, P. K., Huff, C. G. & Spriuz, H. (1966). The feeding mechanism of avian malarial parasites. Journal of Cell Biology 28, 355–73.CrossRefGoogle ScholarPubMed
Aminoff, D., Bell, W. C., Fulton, I. & Ingerbrigsten, N. (1976). Effect of sialidase on the viability of erythrocytes in circulation. American Journal of Hematology 1, 419–32.CrossRefGoogle ScholarPubMed
Aminoff, D., Vorder, Bruegge W. F., Bell, W. C., Sarpolis, K. & Williams, R. (1977). Role of sialic acid in survival of erythrocytes in the circulation: interaction of neuraminidase-treated and untreated erythrocytes with spleen and liver at the cellular level. Proceedings of the National Academy of Sciences, USA 74, 1521–4.CrossRefGoogle ScholarPubMed
Bodammer, J. E. & Bahr, G. F. (1973). The initiation of a metabolic window in the surface of host erythrocytes by Plasmodium berghei NYU-2. Laboratory Investigation 28, 708–18.Google ScholarPubMed
Boonpucknavig, S., Boonpucknavig, V. & Bhamarapravati, N. (1972). Immunpathological studies of Plasmodium berghei-infected mice. Immune complex nephritis. Archives of Pathology 94, 322–30.Google Scholar
Brown, I. N. (1969). Immunological aspects of malaria infection. Advances in Immunology 11, 267–349.CrossRefGoogle ScholarPubMed
Brown, K. N., Brown, I. N. & Hills, C. A. (1970). Immunity to malaria. I. Protection against Plasmodium knowlesi shown by monkeys sensitized with drug-suppressed infections or by dead parasites in Freund's adjuvant. Experimental Parasitology 28, 304–17.CrossRefGoogle ScholarPubMed
Cook, L., Grant, P. T. & Kermack, W. O. (1961). Proteolytic enzymes of the erythrocytic forms of rodent and simian species of malarial plasmodia. Experimental Parasitology 11, 372–9.CrossRefGoogle Scholar
Cohen, S., Butcher, G. A. & Crandall, R. B. (1969). Action of malarial antibody in vitro. Nature, London 223, 368–71.CrossRefGoogle ScholarPubMed
Corwin, R. M. & McGhee, R. B. (1966). Anemia in ducklings treated with malarious plasma. Experimental Parasitology 18, 281–9.CrossRefGoogle Scholar
Corwin, R. M., McGhee, R. B. & Sloan, B. L. (1965). Anemia in ducklings injected with malarious plasma. Journal of Parasitology 51, (Suppl.) 36.Google Scholar
Cox, H. W. (1966). A factor associated with anemia and immunity in Plasmodium knowlesi infections. Military Medicine 131 (Suppl.) 1195–200.CrossRefGoogle ScholarPubMed
Czop, J. K., Fearon, D. T. & Austen, K. F. (1978). Membrane sialic acid on target particles modulates their phagocytosis by a trypsin-sensitive mechanism on human monocytes. Proceedings of the National Academy of Sciences, USA 75, 3831–5.CrossRefGoogle ScholarPubMed
Dodge, J. T., Mitchell, C. & Hanahan, D. J. (1963). The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes. Archives of Biochemistry and Biophysics 100, 119–30.CrossRefGoogle ScholarPubMed
Dunn, M. J. (1969 a). Alterations of red blood cell sodium transport during malarial infection. Journal of Clinical Investigation 48, 674–83.CrossRefGoogle ScholarPubMed
Dunn, M. J. (1969 b). Alterations of red blood cell metabolism in simian malaria: evidence for abnormalities of nonparasitized cells. Military Medicine 134, 1100–5.CrossRefGoogle ScholarPubMed
Durocher, J. R., Payne, R. C. & Conrad, M. E. (1974). Role of sialic acid in erythrocyte survival. Blood 45, 11–20.CrossRefGoogle Scholar
Eaton, M. D. (1939). The soluble malarial antigen in the serum of monkeys infected with Plasmodium knowlesi. Journal of Experimental Medicine 69, 517–32.CrossRefGoogle Scholar
Fairbanks, G., Steck, T. L. & Wallach, D. F. H. (1971). Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry 10, 2606–17.CrossRefGoogle ScholarPubMed
Fearon, D. T. (1978). Regulation by membrane sialic acid of β1H-dependent decay-dissociation of amplification C3 convertase of the alternative complement pathway. Proceedings of the National Academy of Sciences, USA 75, 1971–5.CrossRefGoogle ScholarPubMed
Gahmberg, C. G., Jokinen, M. & Andersson, L. C. (1978). Expression of the major sialoglycoprotein (Glycophorin) on erythroid cells in human bone marrow. Blood 52, 379–87.CrossRefGoogle ScholarPubMed
Gattegno, L., Bladier, D. & Cornillot, P. (1974). The role of sialic acid in the determination of the survival of rabbit erythrocytes in the circulation. Carbohydrate Research 34, 361–9.CrossRefGoogle ScholarPubMed
Gattegno, L., Bladier, D. & Cornillot, P. (1975). Ageing in vivo and neuraminidase treatment of rabbit erythrocytes: influence on half life as assessed by 51Cr labelling. Hoppe Seyler's Zeitschrift für Physiologische Chemie 356, 391–7.CrossRefGoogle ScholarPubMed
Gautam, O. P., Kreier, J. P. & Kreier, R. C. (1970). Antibody coating on erythrocytes of chickens infected with Plasmodium gallinaceum. Indian Journal of Medical Research 58, 529–43.Google ScholarPubMed
Gregoriadis, G., Putman, D., Louis, L. & Neerunjun, D. (1974). Comparative effect and fate of non-entrapped and liposome-entrapped neuraminidase injected into rats. The Biochemical Journal 140, 323–30.CrossRefGoogle ScholarPubMed
Holz, G. G. Jr (1977). Lipids and the malarial parasite. Bulletin of the World Health Organization 55, 235–46.Google ScholarPubMed
Homewood, C. A. & Neame, K. D. (1974). Malaria and the permeability of the host erythrocyte. Nature, London 252, 718–19.CrossRefGoogle ScholarPubMed
Howard, R. J. & Day, K. (1980). Plasmodium berghei: modification of sialic acid on red cells from infected mouse blood; a possible role in anemia induced by malaria. Experimental Parasitology, (in the Press.)Google Scholar
Howard, R. J., Mitchell, G. F. & Battye, F. L. (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). 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, 573–6.CrossRefGoogle ScholarPubMed
Howard, R. J., Smith, P. M. & Mitchell, G. F. (1979 a). Identification of several differences between external proteins and glycoproteins of normal mouse (BALB/c) and human erythrocytes. Journal of Membrane Biology 49, 171–98.CrossRefGoogle ScholarPubMed
Howard, R. J., Smith, P. M. & Mitchell, G. F. (1979 b). Optimal conditions for lactoperoxidase catalyzed radioiodination of external proteins on mouse erythrocytes. Australian Journal of Experimental Biology and Medical Science 57, 355–68.CrossRefGoogle ScholarPubMed
Howard, R. J., Smith, P. M. & Mitchell, G. F. (1980 a). Characterization of surface proteins and glycoproteins on red blood cells from mice infected with haemosporidia: Babesia rodhaini infections of BALB/c mice. Parasitology 81, 251–71.CrossRefGoogle ScholarPubMed
Howard, R. J., Smith, P. M. & Mitchell, G. F. (1980 b). Characterization of surface proteins and glycoproteins on red blood cells from mice infected with haemosporidia: Plasmodium yoelii infections of BALB/c mice. Parasitology 81, 299–314.CrossRefGoogle ScholarPubMed
Jancik, J. & Schauer, R. (1974). Sialic acid—a determinant of the life-time of rabbit erythrocytes. Hoppe Seyler's Zeitschrift für Physiologische Chemie 355, 395–400.Google ScholarPubMed
Jancik, J. M., Schauer, R., Andres, K. H. & von Düring, M. (1978). Sequestration of neuraminidase-treated erythrocytes. Studies on its topographic, morphologic and immunologic aspects. Cell and Tissue Research 186, 209–26.CrossRefGoogle Scholar
Jancik, J., Schauer, R. & Streicher, H. J. (1975). Influence of membrane-bound N-acetylneuraminic acid on the survival of erythrocytes in man. Hoppe Seyler's Zeitschrift für Physiologische Chemie 356, 1329–31.Google ScholarPubMed
Kilejian, A., Abati, A. & Trager, W. (1977). Plasmodium falciparum and Plasmodium coatneyi: immunogenicity of ‘knob-like protrusions’ on infected erythrocyte membranes. Experimental Parasitology 42, 75–164.CrossRefGoogle ScholarPubMed
Konigk, B. & Mirtsch, S. (1977). Plasmodium chabaudi-infection of mice: specific activities of erythrocyte membrane-associated enzymes and patterns of proteins and glycoproteins of of erythrocyte membrane preparations. Tropenmedizin und Parasitologie 28, 17–22.Google ScholarPubMed
Kreier, J., Shapiro, H., Dilley, D., Szilvassey, I. P. & Ristic, M. (1966). Autoimmune reactions in rats with Plasmodium berghei infection. Experimental Parasitology 19, 155–62.CrossRefGoogle ScholarPubMed
Lawrence, C. W. & Cenedella, R. (1969). Lipid content of Plasmodium berghei-infected rat red blood cells. Experimental Parasitology 26, 181–6.CrossRefGoogle ScholarPubMed
Levy, M. R. & Chou, S. C. (1973). Activity and some properties of an acid proteinase from normal and Plasmodium berghei-infected red cells. Journal of Parasitology 59, 1064–70.CrossRefGoogle ScholarPubMed
Levy, M. R., Siddiqui, W. A. & Chou, S. C. (1974). Acid protease activity in Plasmodium falciparum and P. knowlesi and ghosts of their respective host cells. Nature, London 247, 546–9.CrossRefGoogle Scholar
Lis, H. & Sharon, N. (1973). The biochemistry of plant lectins (phytohemagglutinins) Annual Review of Biochemistry 42, 541–74.CrossRefGoogle ScholarPubMed
Lustig, H. J., Nussenzweig, V. & Nussenzweig, R. S. (1977). Erythrocyte membrane-associated immunoglobulins during malaria infection of mice. Journal of Immunology 119, 210–16.CrossRefGoogle ScholarPubMed
Marchesi, V. T., Furthmayer, H. & Tomita, M. (1976). The red cell membrane. Annual Review of Biochemistry 45, 667–98.CrossRefGoogle Scholar
McColm, A. A., Shakespeare, P. G. & Trigg, P. I. (1977). Release of protein by erythrocytic stages of Plasmodium knowlesi during cultivation in vitro. Bulletin of the World Health Organization 55, 275–81.Google ScholarPubMed
McCormick, G. J. (1970). Amino acid transport and incorporation in red blood cells of normal and Plasmodium knowlesi infected rhesus monkeys. Experimental Parasitology 27, 143–9.CrossRefGoogle ScholarPubMed
McGregor, I. A., Turner, M. W., Williams, K. & Hall, P. (1968). Soluble antigens in blood of patients with severe Plasmodium falciparum malaria. Lancet 1, 881–4.CrossRefGoogle ScholarPubMed
Miller, L. H. (1977). Hypothesis on the mechanism of erythrocyte invasion by malaria merozoites. Bulletin of the World Health Organization 55, 155–60.Google ScholarPubMed
Miller, L. H., Aikawa, M. & Dvorak, J. A. (1975). Malaria (Plasmodium knowlesi) merozoites: immunity and the surface coat. Journal of Immunology 114, 1237–42.CrossRefGoogle ScholarPubMed
Mitchell, G. F., Handman, E. & Howard, R. J. (1978). Protection of mice against plasmodium and babesia infections: attempts to raise host-protective sera. Australian Journal of Experimental Biology and Medical Science 56, 553–9.CrossRefGoogle ScholarPubMed
Mitchell, G. F., Hogarth-Scott, R. S., Edwards, R. D., Lewers, H. M., Cousins, G. & Moore, T. (1976). Studies on immune responses to parasite antigens in mice. I. Ascaris suum larvae numbers and antiphosphorylcholine responses in infected mice of various strains and in hypothymic nu/nu mice. International Archives of Allergy and Applied Immunology 52, 64–78.CrossRefGoogle ScholarPubMed
Ohtomo, H. & Katori, M. (1972). Reliable evidence of involvement of the kinin system in mouse malaria. Japanese Journal of Pharmacology 22, 493–509.CrossRefGoogle Scholar
Onabanjo, A. O. & Maegraith, B. G. (1970). Kallikrein as a pathogenic agent in Plasmodium knowlesi infection in Mucaca mulatta. British Journal of Experimental Pathology 51, 523–33.Google Scholar
Onabanjo, A. O., Bhabani, A. R. & Maegraith, B. G. (1970). The significance of kinin-destroying enzymes activity in Plasmodium knowlesi malarial infections. British Journal of Experimental Pathology 51, 534–40.Google Scholar
Poels, L. G., Van Niekerk, C. C., Franken, M. A. M. & Van Elven, E. H. (1977). P1asmodium berghei: selective release of ‘protective antigens’. Experimental Parasitology 42, 182–93.CrossRefGoogle ScholarPubMed
Poels, L. G., Van Niekerk, C. C. & Franken, M. A. M. (1978). Plasmodial antigens exposed on the surface of infected reticulocytes: their role in induction of protective immunity in mice. Israel Journal of Medical Science 14, 575–81.Google ScholarPubMed
Potempa, L. A. & Garvin, J. E. (1976). A third form for the major glycoprotein of the human erythrocyte membrane in sodium dodecyl sulfate: electrophoresis as band PAS-4 at high ionic strength. Biochemical and Biophysical Research Communications 72, 1049–55.CrossRefGoogle ScholarPubMed
Rao, K. N., Subrahmanyam, D. & Pukrash, S. (1970). Plasmodium berghei: lipids of rat red blood cells. Experimental Parasitology 27, 22–7.CrossRefGoogle ScholarPubMed
Roth, R. L. & Herman, R. (1979). Plasmodium berghei: correlation of in vitro erythrophagocytosis with the dynamics of early-onset anemia and reticulocytosis in mice. Experimental Parasitology 47, 169–79.CrossRefGoogle ScholarPubMed
Schauer, R. (1973). Chemistry and biology of the Acylneuraminic acids. Angewandte Chemie International Edition 12, 127–38.CrossRefGoogle ScholarPubMed
Schauer, R., Buscher, H. P. & Casals-Stenzel, J. (1974). Sialic acids: their analysis and enzymic modification in relation to the synthesis of submandibular gland glycoproteins. Biochemical Society Symposia 40, 87–116.Google Scholar
Schauer, R. & Faillard, H. (1968). Das verhalten isomerer N, O-Diacetylneuraminsäuergly-koside im Submaxillarismucin von Pferd und Rind bei Einwirkung bakterieller Neuraminidase. Hoppe Seyler's Zeitschrift für Physiologische Chemie 349, 961–8.CrossRefGoogle ScholarPubMed
Schubert, D. (1970). Immunoglobulin biosynthesis. IV. Carbohydrate attachment to immunoglobulin subunits. Journal of Molecular Biology 51, 287–301.CrossRefGoogle ScholarPubMed
Seitz, H. M. (1972). Demonstration of malarial antigens in the sera of Plasmodium berghei infected mice. Journal of Parasitology 58, 179–80.CrossRefGoogle ScholarPubMed
Sherman, I. W. & Tanigoshi, 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
Sibinovic, K. H., Milar, R., Ristic, M. & Cox, H. W. (1969). In vivo and in Vitro effects of serum antigens of babesial infection and their antibodies on parasitized and normal erythrocytes. Annals of Tropical Medicine and Parasitology 63, 327–36.CrossRefGoogle ScholarPubMed
Topley, E., Knight, R. & Woodruff, A. W. (1973). The direct antiglobin test and immunoconglutinin titers in patients with malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 67, 51–4.CrossRefGoogle Scholar
Trigg, P. I., Hirst, S. I., Shakespeare, P. G. & Tappenden, L. (1977). Labelling of membrane glycoprotein in erythrocytes infected with Plasmodium knowlesi. Bulletin of the World Health Organization 55, 203–7.Google 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
Ward, P. A. & Kibukamusoke, J. W. (1969). Evidence for soluble immune complexes in the pathogenesis of the glomerulonephritis of quartan malaria. Lancet 1, 283–5.CrossRefGoogle ScholarPubMed
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
Wilson, R. J. M., McGregor, I. A. & Williams, K. (1975). Occurrence of S-antigens in serum of Plasmodium falciparum infections in man. Transactions of the Royal Society of Tropical Medicine and Hygiene 69, 453–9.CrossRefGoogle ScholarPubMed
Wilson, R. J. M., McGregor, I. A. & Hall, P. J. (1975). Persistence and recurrence of S-antigens in Plasmodium falciparum infections in man. Transactions of the Royal Society of Tropical Medicine and Hygiene 69, 460–7.CrossRefGoogle ScholarPubMed
Zimmerman, B. & Chapman, M. L. (1977). Fractionation of lymphocyte surface antigens. I. Rapid method for eliminating labelled lipid from cell surface antigens iodinated by the lactoperoxidase catalyzed reaction. Journal of Immunological Methods 15, 183–92.CrossRefGoogle Scholar
Zuckerman, A. (1964). Autoimmunization and other types of indirect damage to host cells as factors in certain protozoan diseases. Experimental Parasitology 15, 138–83.CrossRefGoogle ScholarPubMed