Hostname: page-component-848d4c4894-nr4z6 Total loading time: 0 Render date: 2024-05-12T22:59:17.125Z Has data issue: false hasContentIssue false

Contrasts in antigen expression in the erythrocytic and exoerythrocytic stages of rodent malaria

Published online by Cambridge University Press:  06 April 2009

A. Suhrbier
Affiliation:
1Molecular and Cellular Parasitology Research Group, Department of Pure and Applied Biology, Imperial College, London SW7 2BB
M. F. Wiser
Affiliation:
2Department of Tropical Medicine and Parasitology, Tulane Medical Center, New Orleans
L. Winger
Affiliation:
1Molecular and Cellular Parasitology Research Group, Department of Pure and Applied Biology, Imperial College, London SW7 2BB
P. Harte
Affiliation:
3Department of Medical Protozoology, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT
M. F. Newton
Affiliation:
1Molecular and Cellular Parasitology Research Group, Department of Pure and Applied Biology, Imperial College, London SW7 2BB
K. J. Hodivala
Affiliation:
1Molecular and Cellular Parasitology Research Group, Department of Pure and Applied Biology, Imperial College, London SW7 2BB
J. Nicholas
Affiliation:
1Molecular and Cellular Parasitology Research Group, Department of Pure and Applied Biology, Imperial College, London SW7 2BB
R. E. Sinden
Affiliation:
1Molecular and Cellular Parasitology Research Group, Department of Pure and Applied Biology, Imperial College, London SW7 2BB

Summary

The time and Site of expression of five antigens, recognized by monoclonal antibodies raised against blood-stage parasites, were studied in the exoerythrocytic stage of Plasmodium berghei using indirect immunofluorescent antibody staining. Two monoclonal antibodies (W 3. 5, I 2. 6), which stain the cytoplasm of infected erythrocytes, did not stain the cytoplasm of the infected liver cell but stained the parasite itself suggesting a difference in the antigenic architecture of the erythrocytic and exoerythrocytic parasites. Another antibody (17. 6. 1) revealed a further difference in the antigenic composition of the blood and liver-stage parasites being expressed almost exclusively in the former. Two others (C139 and 17. 3. 9) showed broadly similar patterns of expression in these two stages of the malarial life-cycle.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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

Aley, S. B., Barnwell, J. W., Bates, M. D., Collins, W. E. & Hollingdale, M. R. (1987). P. vivax: exoerythrocytic schizonts recognized by monoclonal antibodies against blood stage schizonts. Experimental Parasitology 64, 188–94.CrossRefGoogle ScholarPubMed
Coppel, R. L., Favaloro, J. M., Crewther, P. E., Durkot, T. R., Bianco, A. E., Stahl, H. D., Kemp, D. J., Anders, R. F. & Brown, G. V. (1985). A blood stage antigen of P. falciparum shares determinants with the circumsporozoite coat protein. Proceedings of the National Academy of Sciences, USA 82, 5121–5.CrossRefGoogle Scholar
Cox, F. E. G. (1988). Which way for malaria? Nature, London 331, 486.CrossRefGoogle ScholarPubMed
Danforth, H. D., Orjih, A. U. & Nussenzweig, R. S. (1978). Immunofluorescent staining of exoerythrocytic schizonts of P. berghei in fixed liver tissue with stage specific immune serum. Journal of Parasitology 64, 1123–5.CrossRefGoogle ScholarPubMed
Druilhe, P., Puebla, R. M., Miltgen, F., Perrin, L. & Gentillini, M. (1984). Species- and stage-specific antigens in exoerythrocytic stages of P. falciparum. American Journal of Tropical Medicine and Hygiene 33, 336–41.CrossRefGoogle Scholar
Guerin-Marchand, C., Druilhe, P., Galey, B., Londono, A., Patarpotikul, J., Beaudoin, R. L., Dubeaux, C., Tartar, A., Mercereau-Puijalon, O. & Langsley, G. (1987). A liver stage specific antigen of P. falciparum characterized by gene cloning. Nature, London 329, 164–7.CrossRefGoogle ScholarPubMed
Hamilton, A. J., Suhrbier, A., Nicholas, J. & Sinden, R. E. (1988). Immunoelectron microscopic localization of circumsporozoite antigen in the differentiating exoerythrocytic trophozoite of P. berghei. Cell Biology International Reports 12, 123–9.CrossRefGoogle Scholar
Holder, A. A. & Freeman, R. R.. (1984). Characterization of a high molecular weight protective antigen of P. yoelii. Parasitology 88, 211–19.CrossRefGoogle Scholar
Hollingdale, M. R. (1985). Malaria and the liver. Hepatology 5, 327–35.CrossRefGoogle ScholarPubMed
Hollingdale, M. R., Collins, W. E. & Campbell, C. C. (1986). In vitro culture of exoerythrocytic parasites of the North-Korean strain of P. vivax in hepatoma cells. American Journal of Tropical Medicine and Hygiene 35, 275–6.CrossRefGoogle ScholarPubMed
Hollingdale, M. R., Leef, J. L., McCullough, M. & Beaudoin, R. L. (1981). In vitro cultivation of the exoerythrocytic stage of P. berghei from sporozoites. Science 213, 1021–2.CrossRefGoogle ScholarPubMed
Hollingdale, M. R. & Leland, P. (1982). Detection of exoerythrocytic stages of P. berghei in fixed liver tissue and cultured cells by an immunoperoxidase antibody technique. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 624–6.CrossRefGoogle ScholarPubMed
Hollingdale, M. R., Leland, P., Leef, J. L., Leef, M. F. & Beaudoin, R. L. (1983). Serological reactivity of in vitro cultured exoerythrocytic stages of P. berghei in indirect immunofluorescent or immunoperoxidase antibody tests. American Journal of Tropical Medicine and Hygiene 32, 2430.CrossRefGoogle ScholarPubMed
Hollingdale, M. R., Leland, P. & Sigler, C. I. (1985). In vitro cultivation of the exoerythrocytic stage of P. berghei in irradiated hepatoma cells. American Journal of Tropical Medicine and Hygiene 34, 21–3.CrossRefGoogle ScholarPubMed
Hope, I. A., Mackay, M., Hyde, J. E., Gorman, G. & Scaife, J. (1985). The gene for an exported antigen of the malaria parasite P. falciparum cloned and expressed in E. coli. Nucleic acid Research 13, 369–79.CrossRefGoogle Scholar
Howard, J. H. (1986). Malaria: antigens andhost-parasite interactions. Receptors and Ligands-Intercellular Communication (ed. Cinader, B.), vol 7. Parasite Antigens: Towards New Strategies for Vaccines. (ed. Pearson, T. W.), New York and Basel: Marcel Dekker.Google Scholar
Kara, U. A. K., Stenzel, D. J., Ingram, T. L. & Kidson, C. (1988). The parasitophorous vacuole membrane of P. falciparum: demonstration of vesicle formation using an immunoprobe. European Journal of Cell Biology 46, 917.Google Scholar
Krotoski, W. A., Jumper, J. R. & Collins, W. E. (1973). Immunofluorescent staining of exoerythrocytic schizonts of simian plasmodia in fixed tissue. American Journal of Tropical Medicine and Hygiene 22, 159–62.CrossRefGoogle ScholarPubMed
Kumar, S., Miller, L. H., Quakyi, I. A., Keister, D. B., Houghten, R. A., Maloy, W. L., Moss, B., Berzofski, J. A. & Good, M. F. (1988). Cytotoxic T cells specific for the circumsporozoite protein of P. falciparum. Nature, London 334, 258–69.CrossRefGoogle Scholar
Maurice, M., Rogier, E., Cassio, D. & Feldmann, G. (1988). Formation of plasma membrane domains in rat hepatocytes and hepatoma cell lines in culture. Journal of Cell Science 90, 7992.CrossRefGoogle ScholarPubMed
Mazier, D., Landau, I., Druilhe, P., Miltgen, F., Guguen-Guillouzo, C., Baccam, D., Baxter, I., Chigot, J. P. & Gentillini, M. (1984). Cultivation of the liver forms of P. vivax in human hepatocytes. Nature, London 307, 367–9.CrossRefGoogle Scholar
Mazier, D., Miltgen, F., Nudelman, S., Nussler, A., Renia, L., Pied, S., Goma, J. & Gentilini, M. (1988). Pre-erythrocytic stages of plasmodia. Role of specific and non-specific factors. Biology of the Cell 64, 165–72.CrossRefGoogle Scholar
Meis, J. F. G. M., Rijntjes, P. L. M., Verhave, J. P., Ponnudurai, T., Hollingdale, M. R. & Yap, S. H. (1985). Infection of cryopreserved adult human hepatocytes with P. falciparum sporozoites. Cell Biology International Reports 9, 976.CrossRefGoogle Scholar
Meis, J. F. G. M., Verhave, J. P., Yap, S. H., Meuwissen, J. H. E. T H. (1985 a). Transformation of sporozoites of P. berghei into exoerythrocytic forms in the liver of its mammalian host. Cell and Tissue Research 241, 353–60.CrossRefGoogle Scholar
Meis, J. F. G. M., Verhave, J. P., Yap, S. H., Meuwissen, J. H. E. T H. (1985b). Fine structure of exoerythrocytic merozoite formation of P. berghei in the rat liver. Journal of Protozoology 32, 694–9.CrossRefGoogle Scholar
Nussenzweig, V. & Nussenzweig, R. S. (1985). Circumsporozoite proteins of malaria parasites. Cell 42, 401–4.CrossRefGoogle ScholarPubMed
Schofield, L., Villaquirian, J., Ferreira, A., Schellenkens, H., Nussenzweig, R. & Nussenzweig, V. (1987). Gamma interferon, CD8+T cells and antibodies required for immunity to malaria sporozoites. Nature, London 330, 664–6.CrossRefGoogle ScholarPubMed
Suhrbier, A., Hamilton, A. J., Nicholas, J. & Sinden, R. E. (1988). The fate of the circumsporozoite protein during the exoerythrocytic development of P. berghei. European Journal of Cell Biology 46, 2530.Google Scholar
Suhrbier, A., Holder, A. A., Wiser, M. F., Nicholas, J. & Sinden, R. E. (1989). Expression of the precursor of the major merozoite surface antigens during the hepatic stage of malaria. American Journal of Tropical Medicine and Hygiene 40, 351–5.CrossRefGoogle ScholarPubMed
Suhrbier, A., Janse, C., Mons, B., Fleck, S. L., Nicholas, J., Davies, C. S. & Sinden, R. E. (1987). The complete development in vitro of the vertebrate phase of the mammalian malarial parasite P. berghei. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 907–9.CrossRefGoogle Scholar
Szarfman, A., Walliker, D., McBride, J., Lyon, J. A., Quakyi, I. A. & Carter, R. (1988). Allelic forms of gp195, a major blood stage antigen of P. falciparum, are expressed in liver stages. Journal of Experimental Medicine 167, 231–6.CrossRefGoogle Scholar
Townsend, A. R. M. (1987). Recognition of influenza virus proteins by cytotoxic T lymphocytes. Immunology Research 6, 80100.CrossRefGoogle ScholarPubMed
Vermeulen, A. N., Van Deursen, J., Brakenhoff, R. H., Lensen, T. H. W., Ponnudurai, T. & Meuwissen, J. E. th. (1986). Characterization of P. falciparum sexual stage antigens and their biosynthesis in synchronized gametocyte cultures. Molecular and Biochemical Parasitology 20, 155–63.CrossRefGoogle Scholar
Weiss, W. R., Sedegah, M., Beaudoin, R. L., Miller, L. H. & Good, M. F. (1988). CD8+T cells (cytotoxic/ suppressors) are required for protection in mice immunised with malaria sporozoites. Proceedings of the National Academy of Sciences, USA 85, 573–6.CrossRefGoogle ScholarPubMed
Winger, L. A., Tirawanchai, N., Nicholas, J., Carter, H. E., Smith, J. E. & Sinden, R. E. (1987). Ookinete antigens of P. berghei. Appearance on the zygote of a Mr21kDa surface determinant identified by transmission blocking antibodies. Parasite Immunology 10, 193207.CrossRefGoogle Scholar
Wiser, M. F. (1986). Characterization of monoclonal antibodies directed against erythrocytic stage antigens of P. berghei. European Journal of Cell Biology 42, 4551.Google Scholar
Wiser, M. F. (1989). Plasmodial antigens external to the parasite but within the infected erythrocyte. Parasitology Research 75, 206–11.CrossRefGoogle Scholar
World health Organization(1988). Exoerythrocytic and asexual blood stage antigens of human parasites: report of the tenth meeting of the scientific working group on the immunology of malaria. TDR/IMMAL/SWG(10)/88.3.Google Scholar