Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-23T00:16:24.805Z Has data issue: false hasContentIssue false

The effect of transmission-blocking antibody ingested in primary and secondary bloodfeeds, upon the development of Plasmodium berghei in the mosquito vector

Published online by Cambridge University Press:  06 April 2009

G. Ranawaka
Affiliation:
Molecular and Cellular Parasitology Research Group, Department of Biology, Imperial College, London SW7 2BB
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 effects of purified monoclonal immunoglobulins from control, or transmission-blocking anti-Pbs21 antibodies, upon the infection of Anopheles stephensi by ookinetes of Plasmodium berghei are compared. Anti-Phs21 antibody reduced mean intensity and prevalence of infection by 94·7 and 58·7% respectively if added to the infectious bloodfeed at a concentration of 100 μg/ml. Fab fragments were of similar efficacy. No transmission enhancement was detected with declining antibody concentrations. Addition to subsequent (second) feeds reduced mean oocyst intensity but not prevalence. The reduction in blockade declined from 41% at day 2, to 4% at day 8. Second bloodfeeds, containing control globulin taken 4 or 6 days (but not 2 days) after infection, increased sporozoite burden in the salivary glands. At all times anti-Pbs21 reduced sporozoite number in the thorax compared to time-matched controls, but again highest gland intensities were obtained when the second bloodfeed was given on day 4. We conclude that second bloodfeeds containing transmission-blocking antibody simultaneously serve two opposing roles, (1) inhibition of parasite development and (2) the supply of nutrients which permit more sporozoites to be produced by each oocyst.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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

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.Google Scholar
Boulanger, N., Matile, H. & Betschart, B. (1988). Formation of the circumsporozoite protein of Plasmodium falciparum in Anopheles stephensi. Acta Tropica 45, 5566.Google 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 Scholar
Feldmann, A. M. & Ponnudurai, T. (1989). Selection of Anopheles stephensi for refractoriness and susceptibility to Plasmodium falciparum. Medical and Veterinary Entomology 3, 4152.Google Scholar
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 Scholar
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 Scholar
Huff, C. G. & Marchbank, D. F. (1955). Changes in the infectiousness of malarial gametocytes. I. Patterns of oocyst production in seven host-parasite combinations. Experimental Parasitology 4, 256–70.Google Scholar
Huff, C. G., Marchbank, D. F. & Shiroishi, T. (1958). Changes in infectiousness of malarial gametes. II. Analysis of possible causative factors. Experimental Parasitology 7, 399417.Google Scholar
Kaslow, D. C. (1990). Immunogenicity of Plasmodium falciparum sexual stage antigens-implications for the design of a transmission blocking vaccine. Immunology Letters 25, 83–6.Google Scholar
Kaslow, D. C., Bathurst, I. C. & Barr, P. J. (1992). Malaria transmission-blocking vaccines. Trends in Biotechnology 10, 388–91.CrossRefGoogle ScholarPubMed
Kaslow, D. C., Quakyi, I. A. & Keister, D. B. (1989). Minimal variation in a candidate from the sexual stage of Plasmodium falciparum. Molecular and Biochemical Parasitology 32, 101–4.CrossRefGoogle Scholar
Kaslow, D. C., Quakyi, I. A., Syin, C., Raum, M. G., Keister, D. B., Coligan, J. E., McCutchan, T. F. & Miller, L. H. (1988). A vaccine candidate from the sexual stage of human malaria that contains EGF-like domains. Nature, London 333, 74–6.Google Scholar
Kaslow, D. C., Syin, C., McCutchan, T. F. & Miller, L. H.(1989). Comparison of the primary structure of the 25 kDa ookinete surface antigens of Plasmodium falciparum and Plasmodium gallinaceum reveals six conserved regions. Molecular and Biochemical Parasitology 33, 283–8.CrossRefGoogle ScholarPubMed
Kumar, N. & Carter, R. (1984). Biosynthesis of the target antigens of antibodies blocking transmission of Plasmodium falciparum. Molecular and Biochemical Parasitology 13, 333–42.Google Scholar
Lal, A. A., Goldman, I. F. & Campbell, G. H. (1990). Primary structure of the 25-kilodalton ookinete antigen from Plasmodium reichenowi. Molecular and Biochemical Parasitology 43, 143–6.Google Scholar
Lensen, A. H. W., Van Gemert, G. J. A., Bolmer, M. G., Meis, J. F. G. M., Kaslow, D., Meuwissen, J. H. E. T. & Ponnudurai, T. (1992). Transmission blocking antibody of Plasmodium falciparum zygote/ookinete surface protein Pfs25 also influences sporozoite development. Parasite Immunology 14, 471–9.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.Google Scholar
Ozaki, L. S., Gwadz, R. W. & Godson, G. N. (1984). Simple centrifugation method for rapid separation of sporozoites from mosquitoes. Parasitology 70, 831–3.CrossRefGoogle ScholarPubMed
Parham, P. (1986). Preparation and purification of active fragments from mouse monoclonal antibodies. In Immunocytochemistry, Vol. 1 (ed. Weir, D. M.), pp. 14.114.17. Oxford: Blackwell Scientific Publications.Google Scholar
Ponnudurai, T., Van Gemert, G. J. A., 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.Google Scholar
Ponnudurai, T., Lensen, A. H. W., Van Gemert, G. J. A., Bolmer, M. G. & Meuwissen, J. H. E. T. (1991). Feeding behaviour and sporozoite ejection by infected Anopheles stephensi. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 175–80.Google Scholar
Rosenberg, R., Wirtz, R. A., Schneider, I. & Burge, 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.Google Scholar
Simonetti, A. B., Billingsley, P. F., Winger, L., Ranawaka, G. & Sinden, R. E. (1993). Kinetics of antigen expression of Plasmodium berghei in the mosquito vector Anopheles stephensi. Journal of Protozoology (in the Press).Google Scholar
Sinden, R. E. (1991). Asexual blood stages of malaria modulate gametocyte infectivity to the mosquito vector possible implications for control strategies. Parasitology 103, 191–6.CrossRefGoogle Scholar
Sinden, R. E., Hartley, R. H. & Winger, L. (1985). The development of Plasmodium ookinetes in vitro: an ultrastructural study including a description of meiotic division. Parasitology 91, 227–44.Google Scholar
Sinden, R. E., Winger, L. A., Hartley, R. H., Carter, H. E., Tirawanchai, N., Davies, C. S. & Sluiters, J. G. (1987). Ookinete antigens of Plasmodium berghei: a light and electron microscopic immunogold study of the 21 kD determinant recognised by transmission blocking antibodies. Proceedings of the Royal Society, B 230, 443–58.Google 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.Google Scholar
Winger, L., Suhrbier, A., O'dowd, C. A., Hodivala, K. J. & Sinden, R. E. (1990). A liver-stage specific antigen of P. berghei identified by a monoclonal antibody. Bulletin of the World Health Organization 68, 172–7.Google 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 of an M r 21 K surface determinant identified by transmission blocking monoclonal antibodies. Parasite Immunology 10, 193207.CrossRefGoogle Scholar
Wirtz, R. A., Burkot, J. R., Graves, P. M. & Andrea, R. C. (1987). Field evaluation of enzyme-linked immunosorbent assays (ELISAs) for Plasmodium falciparum and Plasmodium vivax sporozoites in mosquitoes (Diptera: Culicidae) from Papua New Guinea. Journal of Medical Entomology 24, 433–7.CrossRefGoogle ScholarPubMed