Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-24T12:27:07.728Z Has data issue: false hasContentIssue false
  • English
  • Français

Cytoadherence-related homologous motifs in Plasmodium falciparum antigen Pf155/RESA and erythrocyte band 3 protein

Published online by Cambridge University Press:  06 April 2009

J. Iqbal ,
A. B. Siddique ,
N. Ahlborg ,
P. Perlmann  and
K. Berzins
J. Iqbal
Affiliation:
Department of Immunology, Stockholm University, S-106 91 Stockholm, Sweden
A. B. Siddique
Affiliation:
Department of Immunology, Stockholm University, S-106 91 Stockholm, Sweden
N. Ahlborg
Affiliation:
Department of Immunology, Stockholm University, S-106 91 Stockholm, Sweden
P. Perlmann
Affiliation:
Department of Immunology, Stockholm University, S-106 91 Stockholm, Sweden
K. Berzins
Affiliation:
Department of Immunology, Stockholm University, S-106 91 Stockholm, Sweden
Get access Rights & Permissions [Opens in a new window]

Summary

Cytoadherence of Plasmodium falciparum-infected erythrocytes plays an important role in the pathogenesis of cerebral malaria. The identity of cell surface molecules on parasitized erythrocytes involved in cytoadherence is of great interest to understand the molecular basis of this mechanism. Peptide sequences derived from exofacial loops of the erythrocyte antigen band 3 from parasitized erythrocytes have previously been shown to inhibit cytoadherence. We now report that a non-repeated region of Pf155/RESA (residues 213–218) contains a hexapeptide motif being highly homologous to cytoadherence inhibitory sequences from band 3. Synthetic peptides containing the hexapeptide motif of Pf155/RESA inhibited the binding of P.falciparum-infected erythrocytes to melanoma cells in vitro. Furthermore, individuals residing in malaria-endemic areas have antibodies reactive with epitopes involving these motifs in band 3 and in Pf155/RESA.

Keywords

Plasmodium falciparumPf155/RESAband 3 proteincytoadherencesynthetic peptides
Type
Research Article
Information
Parasitology , Volume 110 , Issue 5 , June 1995 , pp. 503 - 511
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aikawa, M. (1988). Human cerebral malaria. American Journal of Tropical Medicine and Hygiene 39, 3–10.CrossRefGoogle ScholarPubMed
Aikawa, M., Torii, M., Sjölander, A., Berzins, K., Perlmann, P. & Miller, L. H. (1990). Pf155/RESA antigen is localized in dense granules of Plasmodium falciparum merozoites. Experimental Parasitology 71, 326–9.Google Scholar
Anders, R. F., Barzaga, N., Shi, P-T., Scanlon, D. B., Brown, L. E., Thomas, L. M., Brown, G. V., Stahl, H. D., Coppel, R. L. & Kemp, D. J. (1987). Repetitive sequences in malaria antigens. In Molecular Strategies of Parasitic Invasion, (ed. Agabian, N., Goodman, H. & Nogueira, N.), pp. 333–342. New York: Alan R. Liss, Inc.Google Scholar
Berzins, K., Perlmann, H., Wåhlin, B., Carlsson, J., Wahlgren, M., Udomsangpetch, R., Björkman, A., Patarroyo, M. E. & Perlmann, P. (1986). Rabbit and human antibodies to a repeated amino acid sequence of a Plasmodium falciparum antigen, Pf155, react with the native protein and inhibit merozoite invasion. Proceedings of the National Academy of Sciences, USA 83, 1065–9.Google Scholar
Berzins, K. (1991). Pf155/RESA is not a surface antigen of Plasmodium falciparum infected erythrocytes. Parasitology Today 7, 193–4.CrossRefGoogle Scholar
Biggs, B. A., Goozé, L., Wycherley, K., Wollish, W., Southwell, B., Leech, J. H. & Brown, G. V. (1991). Antigenic variation in Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 88, 9171–4.CrossRefGoogle ScholarPubMed
Cappai, R., Schravendijk, Van M. R., Anders, R. F., Peterson, M. G., Thomas, L. M., Cowman, A. F. & Kemp, D. J. (1989). Expression of the RESA gene in Plasmodium falciparum isolate FCR3 is prevented by a subtelomeric deletion. Molecular and Cellular Biology 9, 3584–7.Google ScholarPubMed
Carlsson, J., Berzins, K., Perlmann, H. & Perlmann, P. (1991). Studies on Pf155/RESA and other soluble antigens from in vitro cultured Plasmodium falciparum. Parasitology Research 77, 27–32.Google Scholar
Cheung, A., Leban, J., Shaw, A. R., Merkli, B., Stocker, J., Chizzolini, C., Sander, C. & Perrin, L. H. (1986). Immunization with synthetic peptides of a Plasmodium falciparum surface antigen induces anti-merozoite antibodies. Proceedings of the National Academy of Sciences, USA 83, 8328–32.CrossRefGoogle Scholar
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 the malaria parasite Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 90, 4703–7.CrossRefGoogle ScholarPubMed
Crandall, I. & Sherman, I. W. (1991). Plasmodium falciparum (human malaria)-induced modifications in human erythrocyte band 3 protein. Parasitology 102, 335–40.Google Scholar
Crandall, I. & Sherman, I. W. (1994). Cytoadherence-related neoantigens on Plasmodium falciparum (human malaria)-infected human erythrocytes result from the exposure of normally cryptic regions of the band 3 protein. Parasitology 108, 257–67.Google Scholar
Damian, R. T. (1989). Molecular mimicry: Parasite evasion and host defence. Current Topics in Microbiology and Immunology 145, 101–15.Google Scholar
Deloron, P., le Bras, J., Savel, J. & Coulaud, J. P. (1987). Antibodies to the Pf155 antigen of Plasmodium falciparum: measurement by cell-ELISA and correlation with expected immune protection. American Journal of Tropical Medicine and Hygiene 37, 22–6.Google Scholar
Favaloro, J. M., Coppel, R. L., Corcoran, L. M., Foote, S. J., Brown, G. V., Anders, R. F. & Kemp, D. J. (1986). Structure of the RESA gene of Plasmodium falciparum. Nucleic Acids Research 14, 8265–77.Google Scholar
Foley, M., Tilley, L., Sawyer, W. H. & Anders, R. F. (1991). The ring-infected erythrocyte surface antigen of Plasmodium falciparum associates with spectrin in the erythrocyte membrane. Molecular and Biochemical Parasitology 46, 137–48.CrossRefGoogle ScholarPubMed
Geysen, H. M., Rodda, S. J., Mason, T. J., Tribbick, G. & Schoofs, P. G. (1987). Strategies for epitope analysis using peptide synthesis. Journal of Immunological Methods 102, 259–74.Google Scholar
Greenwood, B. M., Bradley, A. K. & Greenwood, A. M. (1987). Mortality and morbidity from malaria among children in a rural area of The Gambia, West Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 478–86.CrossRefGoogle Scholar
Houghten, R. A. (1985). General method for the rapid solid-phase synthesis of large numbers of peptides: specificity of antigen-antibody interaction at the level of individual amino acids. Proceedings of the National Academy of Sciences, USA 82, 5131–5.Google Scholar
Howard, R. J. (1988). Malaria proteins at the membrane of Plasmodium falciparum-infected erythrocytes and their involvement in cytoadherence to endothelial cells. Progress in Allergy 41, 98–147.Google Scholar
Kay, M. M. B. (1991). Band 3 in aging and neurological disease. Annals of the New York Academy of Sciences 621, 179–205.CrossRefGoogle ScholarPubMed
Kay, M. M. B. (1992). Molecular mapping of human band 3 aging antigenic sites and active amino acids using synthetic peptides. Journal of Protein Chemistry 11, 595–602.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-exchanger protein (AE1). Proceedings of the National Academy of Sciences, USA 86, 9089–93.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 Scholar
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.Google Scholar
Mattei, D. & Scherf, A. (1991). Cross-reacting epitopes shared between Plasmodium falciparum and its host: the origin of autoreactive antibodies? Research in Immunology 40, 698–703.Google Scholar
Nguyen-Dinh, P., Berzins, K., Collins, W. E., Wahlgren, M., Udomsangpetch, R. & Perlmann, P. (1987). Antibodies to Pf155, a major antigen of Plasmodium falciparum: longitudinal studies in humans. American Journal of Tropical Medicine and Hygiene 37, 501–5.CrossRefGoogle Scholar
Oo, M. M., Aikawa, M., Than, T., Aye, T. M., Myint, P. T., Igarashi, I. & Schoene, W. C. (1987). Human cerebral malaria: a pathological study. Journal of Neuropathology and Experimental Neurology 46, 223–31.Google Scholar
Perlmann, H., Perlmann, P., Berzins, K., Wåhlin, B., Troye-Blomberg, M., Hagstedt, M., Andersson, I., Högh, B., Petersen, E. & Björkman, A. (1989). Dissection of the human antibody response to the malaria antigen Pf155/RESA into epitope specific components. Immunological Reviews 112, 115–32.Google Scholar
Petersen, E., Hogh, B., Marbiah, N. T., Perlmann, H., Willcox, M., Dolopaie, E., Björkman, A., Hanson, A. P. & Perlmann, P. (1990). A longitudinal study of Pf155/RESA antibodies and malaria infection in adult Liberians. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 339–45.CrossRefGoogle ScholarPubMed
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.Google Scholar
Reithmeier, A. F. R. (1993). The erythrocyte anion transporter (band 3). Current Biology 3, 515–23.Google Scholar
Riganti, M., Pongponratn, E., Tegoshi, T., Looareesuwan, S., Punpoowong, B. & Aikawa, M. (1990). Human cerebral malaria in Thailand: a clinico-pathological correlation. Immunology Letters 25, 199–206.Google Scholar
Ruangjirachuporn, W., Udomsangpetch, R., Carlsson, J., Drenckhahn, D., Perlmann, P. & Berzins, K. (1991). Plasmodium falciparum: analysis of the interaction of antigen Pf155/RESA with the erythrocyte membrane. Experimental Parasitology 73, 62–72.Google Scholar
Sällberg, M., Ruden, U., Magnius, L. O., Norrby, E. & Wahren, B. (1991). Rapid ‘tea-bag’ peptide synthesis using 9-fluorenylmethoxycarbonyl (Fmoc) protected amino acids applied for antigenic mapping of viral proteins. Immunology Letters 30, 59–68.Google Scholar
Sherman, I. W. & Valdez, E. L. (1989). In vitro cytoadherence of Plasmodium falciparum-infected erythrocytes to melanoma cells: factors affecting adhesion. Parasitology 98, 359–69.CrossRefGoogle ScholarPubMed
Trager, W. & Jensen, J. B. (1976). Human malaria parasites in continuous culture. Science 193, 673–5.CrossRefGoogle ScholarPubMed
Udeinya, I. J., Graves, P. M., Carter, R., Aikawa, M. & Miller, L. H. (1983). Plasmodium falciparum: effect of time in continuous culture on binding to human endothelial cells and amelanotic melanoma cells. Experimental Parasitology 56, 207–14.Google Scholar
Udomsangpetch, R., Aikawa, M., Berzins, K., Wahlgren, M. & Perlmann, P. (1989). Cytoadherence of knobless Plasmodium falciparum infected erythrocytes and its inhibition by a human monoclonal antibody. Nature, London 338, 763–5.Google Scholar
Udomsangpetch, R., Webster, H. K., Pattanapanyasat, K., Pitchayangkul, S. & Thaithong, S. (1992). Cytoadherence characteristics of rosette-forming Plasmodium falciparum. Infection and Immunity 60, 4483–90.CrossRefGoogle ScholarPubMed
Wahlgren, M., Björkman, A., Perlmann, H., Berzins, K. & Perlmann, P. (1986). Anti-Plasmodium falciparum antibodies acquired by residents in a holoendemic area of Liberia during development of clinical immunity. American Journal of Tropical Medicine and Hygiene 35, 22–9.Google Scholar
Wåhlin, B., Wahlgren, M., Perlmann, H., Berzins, K., Björkman, A., Patarroyo, M. E. & Perlmann, P. (1984). Human antibodies to a Mr 155,000 Plasmodium falciparum antigen efficiently inhibit merozoite invasion. Proceedings of the National Academy of Sciences, USA 81, 7912–16.Google Scholar
Wåhlin, B., Sjölander, A., Ahlborg, N., Udomsangpetch, R., Scherp, A., Mattei, D., Berzins, K. & Perlmann, P. (1992). Involvement of Pf155/RESA and cross-reactive antigens in Plasmodium falciparum merozoite invasion in vitro. Injection and Immunity 60, 443–9.CrossRefGoogle ScholarPubMed
Wesseling, J. G., de Ree, J. M., Ponnudurai, T., Smits, M. A. & Schoenmakers, J. G. G. (1988). Nucleotide sequence and deduced amino acid sequence of a Plasmodium falciparum actin gene. Molecular and Biochemical Parasitology 27, 313–20.Google Scholar
Winograd, E., Greenan, J. R. T. & Sherman, I. W. (1987). Expression of senescent antigen on erythrocytes infected with a knobby variant of the human malaria parasite Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 84, 1931–5.Google Scholar
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.Google Scholar