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The inhibition of Plasmodium falciparum growth in vitro by sera from mice infected with malaria or treated with TNF

Published online by Cambridge University Press:  06 April 2009

G. A. Butcher
Affiliation:
Department of Zoology, Australian National University, Canberra, ACT 2601, Australia
I. A. Clark
Affiliation:
Department of Zoology, Australian National University, Canberra, ACT 2601, Australia

Summary

Despite some years of enquiry, the mechanism that leads to intra-erythrocytic death of malarial parasites during the host's response to infection has not been elucidated. We report here that serum from mice undergoing a successful immune response to Plasmodium chabaudi does not inhibit Plasmodium falciparum unless the Pl. chabaudi is virulent enough to rise to at least 50% parasitaemia and to cause illness. This appears to be true of the 556 KA and DS strains of Pl chabaudi, and also other murine malaria parasites. In mice infected with Pl. chabaudi 556 KA inhibitory activity coincided with the presence of TNF in their serum. Exogenous TNF generated inhibitory activity in the serum of mice only if the animals were pretreated with Proprionobacterium acnes, implying a role for activated macrophages downstream from TNF in this process. The difference in inhibitory activity against Pl. falciparum in serum from mice infected with Pl. chabaudi of more or less virulence may be one of degree. Alternatively two distinct mechanisms may operate, the second coming into operation only in ill mice, with higher parasite burdens.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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References

REFERENCES

Buffinton, G. D., Hunt, N. H., Cowden, W. B., Butcher, G. A. & Clark, I. A. (1990). Lipid peroxidation processes in the immunopathology of malaria. In Membrane Lipid Oxidation (ed. Candenas, E. & Vigo-Pelfrey, C.). Boca Raton: CRC Press (In the Press).Google Scholar
Butcher, G. A., Clark, I. A. & Crane, G. (1987). Inhibition of intra-erythrocytic growth of Plasmodium falciparum human sera from Papua New Guinea. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 568–72.CrossRefGoogle ScholarPubMed
Butcher, G. A., Maxwell, L., Cowen, N., Clancy, R. L. & Stace, J. D. (1984). The development and ultrastructure of Plasmodium falciparum damaged in vitro by human ‘crisis’ sera and by chloroquine. Australian Journal of Experimental Biology and Medical Sciences 63, 918.CrossRefGoogle Scholar
Carlin, J. M., Jensen, J. B. & Geary, T. G. (1985). Comparison of inducers of crisis forms in Plasmodium falciparum in vitro. American Journal of Tropical Medicine and Hygiene 34, 668–74.CrossRefGoogle ScholarPubMed
Carswell, E. A., Old, L. J., Kassel, R. L., Green, S., Fiore, N. & Williamson, B. (1975). An endotoxin-induced serum factor that causes necrosis of tumors. Proceedings of the National Academy of Sciences, USA 72, 3666–70.CrossRefGoogle ScholarPubMed
Cavacini, L. A., Guidotti, M., Parke, L. A., Melanconkaplan, J. & Weidanz, W. P. (1989). Reassessment of the role of splenic leukocyte oxidative activity and macrophage activation in expression of immunity to malaria. Infection and Immunity 57, 3677–82.CrossRefGoogle ScholarPubMed
Clark, I. A. (1978). Does endotoxin cause both the disease and parasite death in acute malaria and babesiosis? Lancet 2, 75–7.CrossRefGoogle ScholarPubMed
Clark, I. A. (1987). Cell-mediated immunity in protection and pathology of malaria. Parasitology Today 3, 300–5.CrossRefGoogle ScholarPubMed
Clark, I. A., Butcher, G. A., Buffinton, G. D., Hunt, N. H. & Cowden, W. B. (1987 c). Toxicity of certain products of lipid peroxidation to the human malaria parasite Plasmodium falciparum. Biochemical Pharmacology 36, 543–6.CrossRefGoogle Scholar
Clark, I. A. & Chaudhri, G. (1988). Tumour necrosis factor may contribute to the anaemia of malaria by causing dyserythropoiesis and erythrophagocytosis. British Journal of Haematology 70, 90103.CrossRefGoogle Scholar
Clark, I. A., Cowden, W. B., Butcher, G. A. & Hunt, N. H. (1987 b). Possible roles of tumour necrosis factor in the pathology of malaria. American Journal of Pathology 129, 192–9.Google ScholarPubMed
Clark, I. A., Hunt, N. H., Butcher, G. A. & Cowden, W. B. (1987 a). Inhibition of murine malaria (Plasmodium chabaudi) in vivo by recombinant interferon-γ or tumor necrosis factor, and its enhancement by butylated hydroxyanisole. Journal of Immunology 139, 3493–7.CrossRefGoogle ScholarPubMed
Clark, I. A., Virelizier, J.-C., Carswell, E. A. & Wood, P. R. (1981). Possible importance of macrophage derived mediators in acute malaria. Infection and Immunity 32, 1058–66.CrossRefGoogle ScholarPubMed
Cohen, S., Butcher, G. A., Mitchell, G. H., Deans, J. A. & Langhorne, J. (1977). Acquired immunity and vaccination against malaria. American Journal of Tropical Medicine and Hygiene 26, 223–32.CrossRefGoogle Scholar
Cox, F. E. G. & Millott, S. (1984). The importance of parasite load in the killing of Plasmodium vinckei in mice treated with Corynebacterium parvum or alloxan monohydrate. Parasitology 89, 417–24.CrossRefGoogle ScholarPubMed
Jensen, J. B. (1989). Malaria crisis forms: intraerythrocytic development and derangement. In Malaria: Host Responses of Infection (ed. Stevenson, M. M.), pp. 109126. Boca Raton: CRC Press.Google Scholar
Jensen, J. B., Hoffman, S. L., Boland, T., Akood, M. A. S., Laughlin, L. W., Kurinawan, L. & Marwoto, H. A. (1984). Comparison of immunity to malaria in Sudan and Indonesia: crisis form versus merozoite invasion inhibition. Proceedings of the National Academy of Sciences, USA 81, 922–5.CrossRefGoogle ScholarPubMed
Jensen, J. B., van de Waa, J. A. & Karadsheh, A. J. (1987). Tumour necrosis factor does not induce Plasmodium falciparum crisis forms. Infection and Immunity 55, 1722–4.CrossRefGoogle Scholar
Lambros, C. & Vanderburg, J. P. (1979). Synchronisation of Plasmodium falciparum erythrocyte stages in culture. Journal of Parasitology 65, 418–20.CrossRefGoogle ScholarPubMed
Langhorne, J. (1989). The role of CD4 T-cells in the immune response to Plasmodium chabaudi. Parasitology Today 5, 362–4.CrossRefGoogle ScholarPubMed
Macpherson, G. G., Warrell, M. J., White, N. J., Looareesawan, S. & Warrell, D. A. (1985). Human cerebral malaria. A quantitative ultrastructure analysis of parasitised erythrocyte sequestration. American Journal of Pathology 119, 385401.Google Scholar
Nkuo, T. K. & Deas, J. E. (1988). Sera from Cameroon induce crisis forms during Plasmodium falciparum growth in vitro. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 380–3.CrossRefGoogle Scholar
Playfair, J. H. L., Jones, K. R. & Taverne, J. (1989). Cell-mediated immunity and its role in protection. In Malaria: Host Responses to Infection (ed. Stevenson, M. M.), pp. 6686. Boca Raton: CRC Press.Google Scholar
Rockett, K. A., Targett, G. A. T. & Playfair, J. H. L. (1988). Killing of blood stage Plasmodium falciparum by lipid peroxides from tumour necrosis serum. Infection and Immunity 56, 3180–3.CrossRefGoogle Scholar
Stevenson, M. M., Ghardirian, E., Phillips, N. C., Rae, D. A. & Podoba, J. E. (1989). Role of mononuclear phagocytes in elimination of Plasmodium chabaudi AS infection. Parasite Immunology 11, 529–44.CrossRefGoogle ScholarPubMed
Taverne, J., Tavernier, J., Fiers, W. & Playfair, J. H. L. (1987). Recombinant tumour necrosis factor inhibits malaria parasites in vivo but not in vitro. Clinical and Experimental Immunology 7, 14.Google Scholar
Taliaferro, W. H. & Taliaferro, L. G. (1934). Superinfection and protective experiments with Plasmodium brasilianum in monkeys. American Journal of Hygiene 20, 6072.Google Scholar
Tharavanij, S., Warrell, M. J., Tantivanich, S., Tapchaisiri, P., Choingsa-Nguan, M., Praesertsiriro, J. V. & Patarapotikul, J. (1984). Factors contributing to the development of cerebral malaria I. Humoral immune response. American Journal of Tropical Medicine and Hygiene 33, 111.CrossRefGoogle Scholar
Weiss, L. (1989). Mechanisms of splenic control of murine malaria: cellular reactions of the spleen in lethal (Strain 17XL) Plasmodium yoelii malaria in Balb/c mice, and the consequences of pre-infective splenectomy. American Journal of Tropical Medicine and Hygiene 41, 144–60.CrossRefGoogle ScholarPubMed
Wheatley, B. P. (1980). Malaria as a possible selective factor in the speciation of macaques. Journal of Mammalogy 61, 307–11.CrossRefGoogle ScholarPubMed