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Cytoadherence-related neoantigens on Plasmodium falciparum (human malaria)-infected human erythrocytes result from the exposure of normally cryptic regions of the band 3 protein

Published online by Cambridge University Press:  06 April 2009

I. Crandall  and
I. W. Sherman
I. Crandall
Affiliation:
University of California, Riverside, California 92521, USA
I. W. Sherman
Affiliation:
University of California, Riverside, California 92521, USA
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Summary

Murine monoclonal antibodies (Mabs) were produced by vaccination of Balb/c mice with live Plasmodium falciparum infected red cells (iRBC). The iRBC Mabs recognized altered forms of the human erythrocyte membrane protein band 3; however, these Mabs did not recognize the band 3 molecule in uninfected or ring-infected red cells. The location of epitopes was determined by studying the binding of the iRBC Mabs after selective proteolysis of band 3 as well as by the reactivity of these Mabs to synthetic peptides that corresponded to putative exofacial regions of band 3. Treatment of uninfected red cell membranes with trypsin under low ionic strength conditions resulted in exposure of cryptic epitopes of band 3 which were recognized by the iRBC Mabs. Several of the anti-iRBC Mabs (two of which were described previously) inhibited the in vitro adherence of infected erythrocytes to C32 amelanotic melanoma cells. A mouse polyclonal serum against a synthetic peptide based on an amino acid sequence motif of band 3 reacted (by immunostaining) only with the surface of iRBC and blocked adhesion. Thus, it appears that cryptic residues of the band 3 protein become exposed upon parasitization, and their presence contributes to the increased adhesiveness of the P. falciparum-infected red cell.

Keywords

band 3 proteinPlasmodium falciparummonoclonal antibodyhuman malariacytoadherenceerythrocyte
Type
Research Article
Information
Parasitology , Volume 108 , Issue 3 , April 1994 , pp. 257 - 267
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Aikawa, M. (1977). Variations in structure and function during the life-cycle of malaria parasites. Bulletin of the World Health Organization 55, 139–56.Google Scholar
Aikawa, M., Iseki, M., Barnwell, J. W., Taylor, D., Oo, M. M. & Howard, R. J. (1990). The pathology of human cerebral malaria. American Journal of Tropical Medicine and Hygiene 43, 30–7.CrossRefGoogle ScholarPubMed
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
Bignami, A. & Bastianelli, G. (1890). Osservazioni sulle febbri malariche estive autunnali. La Riforma Medica 223, 1334.Google Scholar
Blake, M. S., Johnston, K. H., Russell-Jones, C. J. & Gotschich, E. C. (1984). A rapid, sensitive method for detection of alkaline phosphase-conjugated antibody on Western blots. Analytical Biochemistry 136, 175–9.CrossRefGoogle ScholarPubMed
Cabantchik, Z. I. & Rothstein, A. (1974). Membrane proteins related to anion permeability of human red blood cells. Journal of Membrane Biology 15, 207–26.CrossRefGoogle ScholarPubMed
Crandall, I., Collins, W. E., Gysin, J. & Sherman, I. W. (1993). Synthetic peptides based on motifs present in human band 3 protein inhibit cytoadherence/sequestration of Plasmodium falciparum (human malaria). Proceedings of the National Academy of Sciences, USA 90, 4703–7.CrossRefGoogle Scholar
Crandall, I. & Sherman, I. W. (1991). Plasmodium falciparum (human malaria) – induced modifications in human erythrocyte band 3 protein. Parasitology 102, 335–40.CrossRefGoogle ScholarPubMed
Crandall, I., Smith, H. J. & Sherman, I. W. (1991). Plasmodium falciparum: the effect of pH and Ca2+ concentration on the in vitro cytoadherence of infected erythrocytes to amelanotic melanoma cells. Experimental Parasitology 73, 362–8.CrossRefGoogle ScholarPubMed
England, B. J., Gunn, R. B. & Steck, T. (1980). An immunological study of band 3, the anion transport protein of the human red cell membrane. Biochimica et Biophysica Acta 623, 171–82.CrossRefGoogle Scholar
Freemount, H. N. & Miller, L. H. (1975). Deep vascular schizogony in Plasmodium fragile: organ distribution and ultrastructure of erythrocytes adherent to vascular endothelium. American Journal of Tropical Medicine and Hygiene 24, 1–8.CrossRefGoogle Scholar
Howard, R. J. (1988). Malarial proteins at the membrane of Plasmodium falciparum-infected erythrocytes and their involvement in cytoadherence to endothelial cells. Progress in Allergy 41, 98–147.Google ScholarPubMed
Jenkins, R. E. & Tanner, M. J. A. (1977). Ionic-strength-dependent changes in the structure of the major protein of the human erythrocyte protein. The Biochemical Journal 161, 131–8.CrossRefGoogle Scholar
Jennings, M. L. & Passow, H. (1979). Anion transport across the erythrocyte membrane, in situ proteolysis of band 3 protein, and cross-linking of proteolytic fragments by 4, 4′-diisothiocyano dihydrostilbene-2, 2′ disulfonate. Biochimica et Biophysica Acta 554, 498–519.CrossRefGoogle ScholarPubMed
Kay, M. M. B. (1984). Localization of senescent cell antigen on band 3. Proceedings of the National Academy of Sciences, USA 81, 5733–57.CrossRefGoogle ScholarPubMed
Kay, M. M. B., Marchalonis, J. J., Hughes, J., Watanabe, K. & Schluter, S. F. (1990). Definition of a physiologic aging autoantigen by using synthetic peptides of membrane protein band 3: localization of the active antigenic sites. Proceedings of the National Academy of Sciences, USA 87, 5734–8.CrossRefGoogle ScholarPubMed
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227, 680–5.CrossRefGoogle ScholarPubMed
Lambros, C. & Vanderberg, J. P. (1980). Synchronization of Plasmodium falciparum erythrocytic stages in culture. Journal of Parasitology 65, 418–20.CrossRefGoogle Scholar
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
Luse, S. A. & Miller, L. H. (1971). Plasmodium falciparum malaria: ultrastructure of parasitized erythrocytes in cardiac vessels. American Journal of Tropical Medicine and Hygiene 20, 655–60.CrossRefGoogle ScholarPubMed
Lux, S. E., John, K. M., Kopito, R. R. & Lodish, H. F. (1989). Cloning and characterization of band 3, the human erythrocyte anion exchange protein (AE-1). Proceedings of the National Academy of Sciences USA 86, 9089–93.CrossRefGoogle Scholar
Markowitz, S. & Marchesi, V. (1981). The carboxylterminal domain of human erythrocyte band 3. Journal of Biological Chemistry 256, 6463–8.CrossRefGoogle ScholarPubMed
Miller, L. H. (1972). The ultrastructure of red cells infected by Plasmodium falciparum in man. Transactions of the Royal Society of Tropical Medicine Hygiene 66, 459–62.CrossRefGoogle ScholarPubMed
Pasvol, G., Wilson, R. J. M., Smalley, M. E. & Brown, J. (1978). Separation of viable schizont-infected cells of Plasmodium falciparum from human blood. Annals of Tropical Medicine and Parasitology 65, 87–8.CrossRefGoogle Scholar
Pongponratn, E., Riganti, M., Punpoowong, B. & Aikawa, M. (1991). Microvascular sequestration of parasitized erythrocytes in human falciparum malaria: a pathological study. American Journal of Tropical Medicine and Hygiene 44, 168–75.CrossRefGoogle ScholarPubMed
Raida, M., Wendel, J., Kojro, E., Fahrenholz, F., Fashold, H., Legrum, B. & Passow, H. (1989). Major proteolytic fragments of the murine band 3 protein as obtained after in situ proteolysis. Biochimica et Biophysica Acta 980, 291–8.CrossRefGoogle ScholarPubMed
Steck, T. L., Ramos, B. & Strapazon, E. (1976). Proteolytic dissection of band 3, the predominant transmembrane polypeptide of the human erythrocyte membrane. Biochemistry 15, 1154–61.CrossRefGoogle ScholarPubMed
Tanner, M. J. A., Martin, P. G. & High, S. (1988). The complete amino acid sequence of the human erythrocyte membrane anion-transport protein deduced from the cDNA sequence. The Biochemical Journal 256, 703–12.CrossRefGoogle ScholarPubMed
Towbin, H., Staehelin, T. & Gordon, J. (1974). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences, USA 76, 4350–4.CrossRefGoogle Scholar
Trager, W. & Jensen, J. B. (1976). Human malaria parasites in continuous culture. Science 193, 673–5.CrossRefGoogle ScholarPubMed
Warrell, D. A. (1987). Pathophysiology of severe falciparum malaria in man. Parasitology 94, S53–S76.CrossRefGoogle ScholarPubMed
Winograd, E. & Sherman, I. W. (1989). Characterization of a modified red cell membrane protein expressed on erythrocytes infected with the human malaria parasite Plasmodium falciparum: possible role as a cytoadherent mediating protein. Journal of Cell Biology 108, 23–30.CrossRefGoogle ScholarPubMed
Zola, H. & Brooks, D. (1982). Techniques for the production and characterization of monoclonal hybridoma antibodies. In Monoclonal Hybridoma Antibodies: Techniques and Applications (ed. Hurrell, J. G. R.), pp. 1–57. Boca Raton, FL: CRC Press Inc.Google Scholar