Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-24T04:34:50.647Z Has data issue: false hasContentIssue false

Characterization of the modes of action of anti-Pbs21 malaria transmission-blocking immunity: ookinete to oocyst differentiation in vivo

Published online by Cambridge University Press:  06 April 2009

G. R. R. Ranawaka
Affiliation:
Molecular and Cellular Parasitology Research Group, Department of Biology, Imperial College, London SW7 2BB
S. L. Fleck
Affiliation:
Molecular and Cellular Parasitology Research Group, Department of Biology, Imperial College, London SW7 2BB
A. R. Alejo Blanco
Affiliation:
Molecular and Cellular Parasitology Research Group, Department of Biology, Imperial College, London SW7 2BB
R. E. Sinden
Affiliation:
Molecular and Cellular Parasitology Research Group, Department of Biology, Imperial College, London SW7 2BB

Summary

The impact of immune sera, and peripheral blood cells (PBC) from mice immunized with Plasmodium berghei ookinetes; and of purified immunoglobulin or Fab fragments from anti-Pbs21 monoclonal antibody 13.1, upon establishment of oocyst infections in the mosquito was studied. Infections were initiated either from gametocyte-infected mice, or membrane feeders which contained either gametocytes or mature ookinetes. PBC from ookinete-immunized mice presented with non-immune serum failed to show any transmission-blocking activity. Anti-ookinete serum, intact anti-Pbs21 monoclonal antibody 13.1 or its Fab fragments, all inhibited oocyst formation significantly. When gametocyte-infected mice or gametocytes in membrane feeds were used, inhibition did not directly correlate with antibody concentration. In membrane feeders that contained ookinetes and antibody, concentration-dependent inhibition usually occurred. The efficacy of purified 13.1 IgG was dependent upon the ookinete concentration. The ookinete plasmalemma and cytoplasm were significantly disturbed after 12h in bloodmeals that contained antibody 13.1, but not in the isotype controls. These changes may have caused the observed failure of the ookinete to migrate as rapidly as the controls from the destructive environment of the bloodmeal.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1994

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., Rener, J., Carter, R. & Miller, L. H. (1981). An electron microscopical study of the interaction of monoclonal antibodies with gametes of the malarial parasite Plasmodium gallinaceum. Journal of Protozoology 28, 383–8.CrossRefGoogle ScholarPubMed
Barr, P. J., Green, K. M., Gibson, H. L., Bathurst, I. C., Quakyi, I. A. & Kaslow, D. C. (1991). Recombinant Pfs25 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in experimental animals. Journal of Experimental Medicine 174, 1203–8.CrossRefGoogle ScholarPubMed
Canning, E. U. & Sinden, H. E. (1973). The organization of the ookinete and observations on nuclear division in oocysts of Plasmodium berghei. Parasitology 67, 2940.CrossRefGoogle ScholarPubMed
Carter, R. & Chen, D. H. (1976). Malaria transmission blocked by immunization with gametes of the malaria parasite. Nature, London 236, 5760.CrossRefGoogle Scholar
Carter, R., Graves, P. M., Keister, D. B. & Quakyi, I. A. (1990). Properties of epitopes of Pfs 48/45, a target of transmission blocking monoclonal antibodies, on gametes of different isolates of Plasmodium falciparum. Parasite Immunology 12, 587603.CrossRefGoogle ScholarPubMed
Carter, R., Kumar, N., Quakyi, I., Good, M., Mendis, K., Graves, P. & Miller, L. (1988). Immunity to sexual stages of malaria parasites. Progress in Allergy 41, 193214.Google ScholarPubMed
Duffy, P. E., Pimenta, P. & Kaslow, D. C. (1993). Pgs28 belongs to a family of epidermal growth factor like antigens that are targets of malaria transmission-blocking antibodies. Journal of Experimental Medicine 177, 505–10.CrossRefGoogle ScholarPubMed
Gass, R. F. (1977). Influences of blood digestion on the development of Plasmodium gallinaceum (Brumpt) in the midgut of Aedes aegypti (L.). Acta Tropica 34, 127–40.Google ScholarPubMed
Gass, R. F. & Yeates, R. A. (1979). In vitro damage of cultured ookinetes of Plasmodium gallinaceum by digestive proteinases from susceptible Aedes aegypti. Acta Tropica 36, 243–52.Google ScholarPubMed
Gwadz, R. W. (1976). Malaria: successful immunization against sexual stages of Plasmodium gallinaceum. Science 193, 1150–1.CrossRefGoogle ScholarPubMed
Harte, P. G., Rogers, N. C. & Targett, G. A. T. (1985). Role of T cells in preventing transmission of rodent malaria. Immunology 56, 17.Google ScholarPubMed
Kaslow, D. C., Bathurst, I. C. & Barr, P. J. (1992). Malaria transmission-blocking vaccines. Trends in Biotechnology 10, 388–91.CrossRefGoogle ScholarPubMed
Matsuoka, H., Paton, M. G., Barker, G. C., Alejo Blanco, A. R. & Sinden, R. E. (1994). Studies on the immunogenicity of a recombinant ookinete surface antigen Pbs21 from Plasmodium berghei expressed in Escherichia coli. Parasite Immunology 16, 2734.CrossRefGoogle ScholarPubMed
Medley, G. F., Sinden, R. E., Fleck, S. L., Billingsley, P. F., Tirawanchai, N. & Rodriguez, M. H. (1993). Heterogeneity in patterns of malarial oocyst infections in the mosquito vector. Parasitology 106, 441–9.CrossRefGoogle ScholarPubMed
Muller, H.-M., Crampton, J. M., Della Torre, A., Sinden, R. B. & Crisanti, A. (1993). Members of a trypsin gene family in Anopheles gambiae are induced in the gut by bloodmeal. EMBO Journal 12, 2891–900.CrossRefGoogle Scholar
Ozaki, L. S., Gwadz, R. W. & Godson, G. N. (1984). Simple centrifugation method for rapid separation of sporozoites from mosquitoes. Journal of Parasitology 70, 831–3.CrossRefGoogle ScholarPubMed
Ponnudurai, T., Gemert, G. V. A. N., Bensink, T., Lensen, A. H. W. & Meuwissen, J. H. E. T. (1987). Transmission blockade of Plasmodium falciparum: its variability with gametocyte numbers and concentration of antibody. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 491–3.CrossRefGoogle ScholarPubMed
Ranawaka, C., Alejo Blanco, R. & Sinden, R. E. (1993). The effect of transmission-blocking antibody ingested in primary and secondary bloodfeeds, upon the development of Plasmodium berghei in the mosquito vector. Parasitology 107, 225–31.CrossRefGoogle ScholarPubMed
Ranawaka, G. R. R., Alejo Blanco, A. R. & Sinden, R. E. (1994). Characterization of the effector mechanisms of a transmission-blocking antibody upon differentiation of Plasmodium berghei gametocytes into ookinetes in vitro. Parasitology 109, 1117.CrossRefGoogle ScholarPubMed
Rosenberg, R., Wirtz, R. A., Schneider, I. & Burce, R. (1990). An estimation of the number of malaria sporozoites ejected by a feeding mosquito. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 209–12.CrossRefGoogle ScholarPubMed
Rutlege, L. C., Gould, D. J. & Tantichareon, B. (1969). Factors affecting the infection of anophelines with human malaria in Thailand. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 613–19.CrossRefGoogle Scholar
Sieber, K.-P., Huber, M., Kaslow, D., Banks, S. M., Torii, M., Aikawa, M. & Miller, L. H. (1991). The peritrophic membrane as a barrier: its penetration by Plasmodium gallinaceum and the effect of a monoclonal antibody to ookinetes. Experimental Parasitology 72, 145–56.CrossRefGoogle ScholarPubMed
Simonetti, A. B., Billingsley, P. F., Winger, L. A. & Sinden, R. E. (1993). Kinetics and expression of two major Plasmodium berghei antigens in the mosquito vector Anopheles stephensi. Journal of Eukaryotic Microbiology 40, 569–76.CrossRefGoogle ScholarPubMed
Sinden, R. E. (1984). The biology of Plasmodium in the mosquito. Experientia 40, 1330–43.CrossRefGoogle ScholarPubMed
Sinden, R. E. & Smalley, M. J. (1976). Gametocytes of Plasmodium falciparum: phagocytosis by leucocytes in vivo and in vitro. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 344–5.CrossRefGoogle ScholarPubMed
Stewart, M. J., Nawrot, R. J., Schulman, S. & Vanderberg, J. P. (1986). Plasmodium berghei sporozoite invasion is blocked in vitro by sporozoite-immobilizing antibodies. Infection and Immunity 51, 859–64.CrossRefGoogle ScholarPubMed
Suhrbier, A., Winger, L., O'dowd, C., Hodivala, K. & Sinden, R. E. (1990). An antigen specific to the liver stage of rodent malaria recognized by a monoclonal antibody. Parasite Immunology 12, 473–81.CrossRefGoogle Scholar
Tirawanchai, N., Winger, L. A., Nicholas, J. & Sinden, R. E. (1991). Analysis of immunity induced by the affinity-purified 21-kilodalton zygote–ookinete surface antigen of Plasmodium berghei. Infection and Immunity 59, 3644.CrossRefGoogle ScholarPubMed
Vermeulen, A. N., Ponnudurai, T., Beckers, P. J. A., Verhave, J. P., Smits, M. A. & Meuwissen, J. H. E. T. (1985). Sequential expression of antigens on sexual stages of Plasmodium falciparum accessible to transmission blocking antibodies in the mosquito. Journal of Experimental Medicine 162, 1460–76.CrossRefGoogle ScholarPubMed
Winger, L. A., Tirawanchai, N., Nicholas, J., Carter, H. E., Smith, J. E. & Sinden, R. E. (1988). Ookinete antigens of Plasmodium berghei. Appearance on the zygote surface of an M r 21 kD determinant identified by transmission-blocking monoclonal antibodies. Parasite Immunology 10, 193207.CrossRefGoogle Scholar
Wirtz, R. A., Duncan, J. F., Njelesani, E. K., Schneider, I., Brown, A. E., Oster, C. N., Were, J. Bo. & Webster, H. K. (1989). ELISA method for detecting Plasmodium falciparum circumsporozoite antibody. Bulletin of the World Health Organization 67, 535–42.Google ScholarPubMed