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Sialoglycoproteins and sialic acids of Plasmodium knowlesi schizont-infected erythrocytes and normal rhesus monkey erythrocytes

Published online by Cambridge University Press:  06 April 2009

R. J. Howard ,
G. Reuter ,
J. W. Barnwell  and
R. Schauer
R. J. Howard
Affiliation:
Malaria Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA
G. Reuter
Affiliation:
Biochemisches Institut, Christian-Albrechts Universität, D-2300, Kiel 1, West Germany
J. W. Barnwell
Affiliation:
Malaria Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA
R. Schauer
Affiliation:
Malaria Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA
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Summary

The effects of malaria infection on RBC sialic acids and sialoglycoproteins were studied with asexual blood-stage infections of Plasmodium knowlesi in rhesus monkeys. Glycoprotein radio-isotope labelling methods were used to compare the sialoglycoproteins of normal RBC and P. knowlesi schizont-infected RBC (SI-RBC). Tritiation of glycoproteins from SI-RBC with the standard sialidase + galactose oxidase/NaB3H4 method or standard periodate/NaB3H4 method was significantly decreased when compared to normal RBC. However, tritium uptake into glycoproteins was normal when SI-RBC were treated with 5-fold higher concentrations of both enzymes in the first labelling method, or with a 5-fold increase in the molar ratio of periodate to sialic acid in the second method. The mobility of tritiated host cell glycoproteins on SDS–polyacrylamide gels was identical for SI-RBC and normal RBC. New bands, possibly glycoproteins, of 230, 160, 90, 52, and 30 kDa were detected after labelling SI-RBC by the modified periodate/NaB3H4 method. Sialic acid analysis of normal rhesus monkey RBC (62μg/1010 RBC) revealed that 46% of the total sialic acid was N-glycolylneuraminic acid, 33% was N-acetyl-9-O-acetylneuraminic acid, and the remainder N-acetylneuraminic acid. SI-RBC collected either directly from infected monkeys or after in vitro culture of ring-infected RBC in horse serum, had increased total sialic acid (126 or 115μg/1010 RBC, respectively). The sialic acid content of infected RBC must increase during parasite development since RBC infected with ring-stage P. knowlesi had the same content as normal RBC. There was no significant difference in the ratio of the three sialic acids of SI-RBC and normal RBC. In contrast, the uninfected RBC from infected blood of different monkeys showed marked variation in sialic acid composition and generally had a lower sialic acid content than normal RBC.

Type
Research Article
Information
Parasitology , Volume 92 , Issue 3 , June 1986 , pp. 527 - 543
Copyright
Copyright © Cambridge University Press 1986

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References

REFERENCES

Aley, S. B., Barnwell, J. W., Daniel, W. & 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, 69–84.CrossRefGoogle Scholar
Aikawa, M., Miller, L. H. & Rabbege, J. (1975). Caveola-vesicle complexes in the plasmalemma of erythrocytes infected with Plasmodium vivax and P. cynomolgi. American Journal of Pathology 79, 285–94.Google ScholarPubMed
Barnwell, J. W., Howard, R. J., Coon, H. G. & Miller, L. H. (1983). Splenic requirement for antigenic variation and expression of the variant antigen on the erythrocyte membrane in cloned Plasmodium knowlesi malaria. Infection and Immunity 40, 985–94.CrossRefGoogle ScholarPubMed
Blumenfeld, O. O., Gallop, P. M. & Liao, T. H. (1972). Modification and introduction of a specific radioactive label into the erythrocyte membrane sialoglycoproteins. Biochemical and Biophysical Research communications 48, 242–51.CrossRefGoogle ScholarPubMed
Brown, K. N. & Brown, I. N. (1965). Immunity to malaria: antigenic variation in chronic infections of Plasmodium knowlesi. Nature, London 208, 1286–8.CrossRefGoogle ScholarPubMed
Corfield, A. P. & Schauer, R. (1982). Occurrence of sialic acids. In Sialic Acids, Chemistry, Metabolism and Function (ed. Schauer, R.), pp. 5–50Wien and New York: Springer-Verlag.CrossRefGoogle Scholar
Dodge, J. T., Mitchell, C. & Hanahan, D. J. (1963). The preparation and chemical characteristics of hemoglobin-free ghosts of human erythrocytes. Archieves of Biochemistry and Biophysics 100, 119–30.CrossRefGoogle ScholarPubMed
Gahmberg, C. G. (1976). External labelling of human erythrocyte glycoproteins. Studies with galactose oxidase and fluorography. Journal of Biological Chemistry 251, 510–15.CrossRefGoogle ScholarPubMed
Gahmberg, C. G. & Andersson, L. C. (1977). Selective radioactive labelling of cell surface sialo-glycoproteins by periodate-tritiated borohydride. Journal of Biological Chemistry 252, 5888–94.CrossRefGoogle Scholar
Gahmberg, C. G. & Hakomori, S-I. (1973). External labelling of cell surface galactose and galactos-amine in glycolipid and glycoprotein of human erythrocytes. Journal of Biological Chemistry 248, 4311–17.CrossRefGoogle ScholarPubMed
Gahmberg, C. G., Myllyla, G., Leikola, J., Pirkola, A. & Nordling, S. (1976). Absence of the major sialoglycoprotein in the membrane of human En(a-) erythrocytes and increased glycosylation of Band 3. Journal of Biological Chemistry 251, 6108–16.CrossRefGoogle ScholarPubMed
Grant, P. T. & Fulton, J. D. (1957). The catabolism of glucose by strains of Trypanosoma rhodesiense. The Biochemical Journal 66, 242–50.CrossRefGoogle ScholarPubMed
Howard, R. J., Barnwell, J. W. & Kao, V. (1982 a). Tritiation of protein antigens of Plasmodium knowlesi schizont-infected erythrocytes using pyridoxal phosphate-[3H] sodium borohydride. Molecular and Biochemical Parasitology 6, 369–87.CrossRefGoogle Scholar
Howard, R. J., Barnwell, J. W. & Kao, V. (1983). Antigenic variation in Plasmodium knowlesi malaria: identification of the variant antigen on infected erythrocytes. Proceedings of the National Academy of Sciences, USA 80, 4129–33.CrossRefGoogle ScholarPubMed
Howard, R. J., Barnwell, J. W., Kao, V., Daniel, W. A. & Aley, S. B. (1982 b). Radioiodination of new protein antigens on the surface of Plasmodium knowlesi schizont-infected erythrocytes. Molecular and Biochemical Parasitology 6, 343–67.CrossRefGoogle ScholarPubMed
Howard, R. J. & Kao, V. (1981). Comparison of the surface membrane proteins of human and rhesus monkey (Macaca mulatta) erythrocytes labelled with protein and glycoprotein radiolabelling probes. Comparative Biochemistry and Physiology 708b, 767–74.Google Scholar
Howard, R. J., Kao, V. & Barnwell, J. W. (1983). Protein antigens of Plasmodium knowlesi clones of different variant antigen phenotype. Parasitology 88, 221–37.CrossRefGoogle Scholar
Howard, R. J., Rodwell, B. J., Smith, P. M., Callow, L. L. & Mitchell, G. F. (1980). Comparison of the surface proteins and glycoproteins on erythrocytes of calves before and during infection with Babesia bovis. Journal of Protozoology 27, 241–7CrossRefGoogle ScholarPubMed
Howard, R. J., Smith, P. M. & Mitchell, G. F. (1979). Identification of differences between the surface proteins and glycoproteins of normal mouse (BALB/c) and human erythrocytes. Journal of Membrane Biology 49, 171–98.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
Kamerling, J. P. & Vliegenthart, J. F. G. (1982). In Sialic Acids. Chemistry, Metabolism and Function (ed. Schauer, R.), pp. 95–125. Wien, New York: Springer-Verlag.CrossRefGoogle Scholar
Kutner, S., Ginsburg, H. & Cabantchik, Z. I. (1983). Perm-selectivity changes in malaria (Plasmodium falciparum) infected human red blood-cell membranes. Journal of Cellular Physiology 114, 245–51.CrossRefGoogle Scholar
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227, 680–5.CrossRefGoogle ScholarPubMed
Liao, T. H., Gallop, P. M. & Blumenfeld, O. O. (1973). Modification of sialyl residues of sialoglycoprotein(s) of the human erythrocyte surface. Journal of Biological Chemistry 248, 8247–53.CrossRefGoogle ScholarPubMed
Marikovsky, Y. & Danon, D. (1969). Electron microscope analysis of young and old red blood cells stained with celloidal iron for surface charge evaluation. Journal of Cell Biology 43, 1–7.CrossRefGoogle Scholar
Miller, L. H., Cooper, G. W., Chien, S. & Freemount, H. N. (1972). Surface charge on Plasmodium knowlesi and P. coatneyi-infected red cells of Macaca mulatta. Experimental Parasitology 32, 86–95.CrossRefGoogle ScholarPubMed
Reuter, G., Pfeil, R., Stoll, S., Schauer, R., Kamerling, J. P., Versluis, C. & Vliegenthart, J. F. G. (1983). Identification of new sialic acids derived from glycoprotein of bovine submandibular gland. European Journal of Biochemistry 134, 139–43.CrossRefGoogle ScholarPubMed
Reuter, G., Vliegenthart, J. F. G., Wember, M., Schauer, R. & Howard, R. J. (1980). Identification of 9-O-acetyl-N-acetylneuraminic acid on the surface of BALB/c mouse erythrocytes. Biochemical and Biophysical Research Communications 94, 567–72.CrossRefGoogle ScholarPubMed
Schauer, R. (1978). Characterization of sialic acids. Methods in Enzymology 50, 64–89.CrossRefGoogle ScholarPubMed
Schauer, R.Wember, M. & Howard, R. J. (1984). Malaria parasites do not contain or synthesize sialic acids. Hoppe-Seyler's Zeitschrift für Physiologische Chemie 365, 185–94.CrossRefGoogle ScholarPubMed
Shulka, A. K. & Schauer, R. (1982). Analysis of N, O-activated neuraminic acids by high-performance liquid anion-exchange chromatography. Journal of Chromatography 244, 81–9Google 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
Uhlenbruck, G. & Schmitt, J. (1965). Über das Vorkommen von N-Glykolyl-Neuraminsaure bei Affen, Naturwissenschaften 52, 163.CrossRefGoogle Scholar
Veh, R. W., Corfield, A. P., Sander, M. & Schauer, R. (1977). Neuraminic acid-specific modification and tritium labeling of gangliosides. Biochimica et Biophysica Acta 486, 145–60.CrossRefGoogle Scholar