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Mechanisms of immunity to malaria and the possibilities of a blood-stage vaccine: a critical appraisal

Published online by Cambridge University Press:  06 April 2009

G. A. Butcher
Affiliation:
Department of Zoology, Australian National University, Canberra, A.C.T., Australia

Summary

Resistance developed by the immune system in response to blood-stage malaria is complex in nature, involving humoral and non-antibody effector mechnisms. Different species of malarial parasites may vary in their ability to elicit, or their susceptibility to, those immune effectors. This complexity is enhanced by the different results obtained in vaccinated as opposed to drug-controlled infections. It is therefore important that some attempt be made to unravel these interactions. This is particularly so when we have to decide on methods for assessing the potentiality of antigens to induce protective immunity. In this review the limitations of some in vitro assays of immunity, as well as those of various host–parasite models, are discussed. The relative importance of cell-mediated and humoral immunity in laboratory models and natural infections is also considered in the context of vaccine development.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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References

REFERENCES

Allison, A. C. & Byars, N. E. (1986). An adjuvant formulation that selectivity elicits the formation of antibodies of protective isotopes of a cell-mediated immunity. Journal of Immunological Methods 95, 157–68.CrossRefGoogle Scholar
Allison, A. C. & Eugui, E. (1981). The role of cell-mediated immune responses in resistance to malaria, with special reference to oxidant stress. Annual Review of Immunology 1, 361–92.CrossRefGoogle Scholar
Anders, R. F. (1986). Multiple cross-reactivities amongst antigens of Plasmodium falciparum impair the development of protective immunity against malaria. Parasite Immunology 8, 529–39.CrossRefGoogle ScholarPubMed
Ballou, W. P., Hoffman, J. L., Sherwood, J. A., Hollingdale, M. R., Neva, F. A., Hockmeyer, W. T., Gordon, D. M., Schneider, I., Wirtz, R. A., Young, J. F., Wasserman, G. F., Reeve, P., Diggs, C. L. & Chulay, J. D. (1987). Safety and efficacy of a recombinant DNA Plasmodium falciparum sporozoite vaccine. Lancet 1, 1277–81.CrossRefGoogle ScholarPubMed
Bannister, L. H., Mitchell, G. H., Butcher, G. A., Dennis, E. D. & Cohen, S. (1986). Structure and development of the surface coat of erythrocytic merozoites of Plasmodium knowlesi. Cell and Tissue Research 245, 281–90.CrossRefGoogle ScholarPubMed
Bate, C. A. W., Taverne, J. & Playfair, J. H. L. (1988). Malarial parasites induce tumour necrosis factor production by macrophages. Immunology 64, 224–31.Google ScholarPubMed
Brown, J. & Greenwood, B. M. (1985). Cellular and humoral inhibition of Plasmodium falciparum growth in vitro and recovery from acute malaria. Parasite Immunology 7, 265–75.CrossRefGoogle ScholarPubMed
Brown, J. & Smalley, M. E. (1981). Inhibition of the in vitro growth of Plasmodium falciparum by human polymorphonuclear neutrophil leucocytes. Clinical and Experimental Immunology 46, 106–9.Google ScholarPubMed
Brown, J., Greenwood, B. M. & Terry, R. J. (1986). Cellular mechanisms involved in recovery from acute malaria in Gambian children. Parasite Immunology 8, 551–64.CrossRefGoogle ScholarPubMed
Bruce-Chwatt, L. J. (1963). A longitudinal survey of natural malaria infection in a group of West African adults. West African Medical Journal 12, 141–73.Google Scholar
Butcher, G. A. (1970). Experimental studies on immunity to P. knowlesi. Ph.D. thesis, London University.Google Scholar
Butcher, G. A. (1974). Immunological aspects of malaria. Guy's Hospital Reports, 23, 247–70.Google Scholar
Butcher, G. A. (1977). Antigenic change in Plasmodium knowlesi. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 554.CrossRefGoogle ScholarPubMed
Butcher, G. A. (1982). The behaviour of different strains of Plasmodium falciparum in suspension and static culture. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 407–9.CrossRefGoogle ScholarPubMed
Butcher, G. A., Bannister, L. H. & Mitchell, G. H. (1976). Immune damage to intracellular parasites. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 1112.Google Scholar
Butcher, G. A. & Clancy, R. L. (1984). Non-Specific immunity to Plasmodium falciparum: in vitro studies. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 806–11.CrossRefGoogle ScholarPubMed
Butcher, G. A., Clark, I. A. & Crane, G. (1987). Inhibition of intra-erythrocytic growth of Plasmodium falciparum by human sera from Papua New Guinea. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 568–72.CrossRefGoogle ScholarPubMed
Butcher, G. A. & Cohen, S. (1970). Schizogony of Plasmodium knowlesi in the presence of normal and immune sera. Transactions of the Royal Society of Tropical Medicine and Hygiene 64, 470.CrossRefGoogle ScholarPubMed
Butcher, G. A. & Cohen, S. (1971). Short-term culture of Plasmodium knowlesi. Parasitology 62, 309–20.CrossRefGoogle ScholarPubMed
Butcher, G. A. & Cohen, S. (1972). Antigenic variation and protective immunity in Plasmodium knowlesi malaria. Immunology 23, 503–21.Google ScholarPubMed
Butcher, G. A., Cohen, S. & Garnham, P. C. C. (1970). Passive immunity in P. knowlesi malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 64, 850–6.CrossRefGoogle Scholar
Butcher, G. A., Maxwell, L., Cowen, N., Clancy, R. L. & Stace, J. D. (1985). The development and ultrastructure of Plasmodium falciparum damaged in vitro by human ‘crisis’ sera and by chloroquine. Australian Journal of Experimental Biology and Medical Science 63, 918.CrossRefGoogle ScholarPubMed
Butcher, G. A., Mitchell, G. H. & Cohen, S. (1978). Antibody mediated mechanisms of immunity to malaria induced by vaccination with Plasmodium knowlesi merozoites. Immunology 34, 7786.Google ScholarPubMed
Butcher, G. A., Parish, C. R. & Cowden, W. B. (1988). Inhibition of in vitro growth of P. falciparum by complex polysaccharides. Transactions of the Royal Society of Tropical Medicine and Hygiene (in the Press).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
Cheung, A., Leban, J., Shaw, A. R., Merkli, B., Stocker, J., Chizzolini, C., Sander, C. & Perrin, L. H. (1986). Immunisation with synthetic peptides of a Plasmodium falciparum surface antigen induces anti-merozoite antibodies. Proceedings of the National Academy of Sciences 83, 8328–32.CrossRefGoogle Scholar
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. & Hunt, N. H. (1983). Evidence for reactive oxygen intermediates causing hemolysis and parasite death in malaria. Infection and Immunity 39, 16.CrossRefGoogle ScholarPubMed
Clark, I. A., Butcher, G. A., Buffington, G. D., Hunt, N. H. & Cowden, W. B (1987 a). Certain products of lipid peroxidation are toxic to the human malaria parasite Plasmodium falciparum. Biochemical Pharmacology 36, 543–6.CrossRefGoogle Scholar
Clark, I. A., Cowden, W. B. & Hunt, N. H. (1986). Oxygen-derived free radicals in the pathogenesis of parasite disease. Advances in Parasitology 25, 144.CrossRefGoogle Scholar
Clark, I. A., Hunt, N. H., Butcher, G. A. & Cowden, W. B. (1987). Inhibition of murine malaria (Plasmodium chabaudi) in vitro by recombinant interferon-γ or tumour necrosis factor, and its enhancement by butylated hydroxyanisole. Journal of Immunology 139, 3493–6.CrossRefGoogle ScholarPubMed
Coggeshall, L. T. (1943). Immunity in malaria. Medicine 22, 87102.CrossRefGoogle Scholar
Cohen, J. (1973). Heterologous immunity in human malaria. Quarterly Reviews in Biology 48, 467–87.CrossRefGoogle ScholarPubMed
Cohen, S. & Butcher, G. A. (1970). Properties of protective malarial antibody. Nature, London 225, 732–4.CrossRefGoogle ScholarPubMed
Cohen, S., Butcher, G. A. & Crandall, R. B. (1969). Action of malarial antibody in vitro. Nature, London 223, 368–71.CrossRefGoogle ScholarPubMed
Cohen, S., Butcher, G. A. & Mitchell, G. H. (1977). Immunity to blood parasites of animals and man. Advances in Experimental Medicine and Biology 73, 89112.CrossRefGoogle Scholar
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
Cohen, S. & McGregor, I. A. (1963). Gamma globulin and acquired immunity to malaria. In Immunity to Protozoa (ed. Garnham, P. C. C., Pierce, A. E. and Riott, I.), p. 123. Oxford: Blackwell.Google Scholar
Collins, W. E., Anders, R. F., Pappaionou, M., Campbell, G. H., Brown, G. V., Kemp, D. J., Coppel, R. L., Skinner, J. C., Andrysiak, P. M., Favaloro, J. M., Corcoran, L. M., Broderson, J. R., Mitchell, G. F. & Campbell, C. C. (1986). Immunisation of Aotus monkeys with recombinant proteins of an erythrocyte surface antigen of Plasmodium falciparum. Nature, London 323, 259–62.CrossRefGoogle ScholarPubMed
Cox, F. E. G. (1970). Protective immunity between malaria parasites and piroplasms in mice. Bulletin of the World Health Organization 43, 325–36.Google ScholarPubMed
Cox, F. E. G. & Millot, S. M. (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
David, P. H., Hudson, D. E., Hadley, T. J., Klotz, F. W. & Miller, L. H. (1985). Immunisation of monkeys with a 140 kilodalton merozoite surface protein of Plasmodium knowlesi malaria: appearance of alternate forms of this protein. Journal of Immunology 134, 4146–52.CrossRefGoogle ScholarPubMed
De Souza, J. R. & Playfair, J. H. L. (1988). Immunisation of mice against blood-stage Plasmodium yoelii malaria with isoelectrically focused antigens and correlation of immunity with T-cell priming in vivo. Infection and Immunity 56, 8891.CrossRefGoogle ScholarPubMed
Dennis, E. D., Mitchell, G. H., Butcher, G. A. & Cohen, S. (1975). In vitro isolation of Plasmodium knowlesi merozoites using polycarbonate sieves Parasitology 71, 475–81.CrossRefGoogle ScholarPubMed
Dockrell, H. M. & Playfair, J. H. L. (1983). Killing of Plasmodium yoelii by enzyme-induced products of the oxidative host. Infection and Immunity 43, 456–9.CrossRefGoogle Scholar
Fandeur, T., Dubois, P., Gysin, J., Dedet, J. P. & De Silva, L. (1984). In vitro and in vivo studies on protective and inhibitory antibodies against Plasmodium falciparum in the Saimiri monkey. Journal of Immunology 132, 432–7.CrossRefGoogle ScholarPubMed
Freeman, R. R. & Holder, A. A. (1983 a). Surface antigens of malaria merozoites. Journal of Experimental Medicine 158, 1647–53.CrossRefGoogle ScholarPubMed
Freeman, R. R. & Holder, A. A. (1983 b). Characteristics of the protective response of BALB/c mice immunised with a purified Plasmodium yoelii schizont antigen. Clinical and Experimental Immunology 54, 609–16.Google ScholarPubMed
Garnham, P. C. C. (1966). Malarial Parasites and Other Haemosporidea. Oxford: Blackwell.Google Scholar
Geczy, C. L. & Meyer, P. A. (1982). Leukocyte procoagulant activity in man: an in vitro correlate of delayed-type hypersensitivity. Journal of Immunology 128, 331–6.CrossRefGoogle Scholar
Grau, G. E., Giudice, G. D. & Lambert, P.-H. (1987). Host immune responses and pathological expression in malaria: possible implications for malaria vaccines. Parasitology 94, S122–S137.CrossRefGoogle ScholarPubMed
Green, T. J., Morhardt, M., Brackett, R. G. & Jacobs, R. L. (1981). Serum inhibition of merozoite dispersal from Plasmodium falciparum schizonts: indicators of immune status. Infection and Immunity 31, 1203–8.CrossRefGoogle ScholarPubMed
Grun, J. L. & Weidanz, W. P. (1981). Immunity to Plasmodium chabaudi adami in the B cell deficient mouse. Nature, London 290, 143–5.CrossRefGoogle ScholarPubMed
Haidaris, C. G., Haynes, J. D., Meltzer, M. S. & Allison, A. C. (1983). Serum containing tumour necrosis factor is cytotoxic for the human malaria parasite Plasmodium falciparum. Infection and Immunity 42, 385–93.CrossRefGoogle ScholarPubMed
Hall, R., Hyde, J. E., Goman, M., Simmons, D. L., Hopel, I. A., Mackay, M. & Scaife, J. (1984). Major surface antigen gene of a human malaria parasite cloned and expressed in bacteria. Nature, London 311, 379–82.CrossRefGoogle ScholarPubMed
Handunnetti, S. M., Mendis, K. N. & David, P. H. (1987). Antigenic variation of cloned Plasmodium fragile in its natural host Macaca sinica. Journal of Experimental Medicine 165, 1269–83.CrossRefGoogle ScholarPubMed
Harrison, G. (1978). Mosquitoes, Malaria, and Man: A History of Hostilities Since 1880, London: John Murray.Google Scholar
Hermentin, P. (1987). Malaria invasion of human erythrocytes. Parasitology Today 3, 52–5.CrossRefGoogle ScholarPubMed
Herrington, D. A., Clyde, D. F., Losonsky, G., Cortesia, M., Murphy, J. R., Davis, J., Bagar, S., Felix, A. M., Heimer, E. P., Gillessen, D., Nardin, E., Nussenzweig, R. S., Nussenzweig, V., Hollingdale, M. R. & Levine, M. M. (1987). Safety and immunogenicity in man of a synthetic peptide malaria vaccine against Plasmodium falciparum sporozoites. Nature, London 328, 257–9.CrossRefGoogle ScholarPubMed
Hill, R. B., Cambournac, F. J. C. & Simoes, M. P. (1943). Observations on the course of malaria in children in endemic regions. American Journal of Tropical Medicine and Hygiene 23, 147–62.CrossRefGoogle Scholar
Hoffman, E. J., Weidanz, W. P. & Long, C. A. (1984). Susceptibility of CXB recombinant inbred mice to murine Plasmodia. Infection and Immunity 43, 981–5.CrossRefGoogle Scholar
Holder, A. A. & Freeman, R. R. (1984). Protective antigens of rodent and human blood stage malaria. Philosophical Transactions of the Royal Society, B 307 171–7.Google Scholar
Hommel, M., David, P. H. & Oligino, L. (1983). Surface alterations of erythrocytes in Plasmodium falciparum malaria. Journal of Experimental Medicine 157, 1137–48.CrossRefGoogle ScholarPubMed
Hommel, M., David, P. H., Oligino, L. D. & David, J. R. (1982). Expression of strain-specific surface antigens on Plasmodium falciparum infected erythrocytes. Parasite Immunology 4, 409–19.CrossRefGoogle ScholarPubMed
Hyman, A. S. (1945). Clinical masquerades of malaria. US Naval Medical Bulletin 45, 287303.Google Scholar
James, M. A., Kakoma, I., Ristic, M. & Cagnard, M. (1985). Induction of protective immunity to Plasmodium falciparum in Saimiri sciureus monkeys with partially purified exoantigens. Infection and Immunity 49, 476–80.CrossRefGoogle ScholarPubMed
Jarra, W., Hills, L. A., March, J. C. & Brown, K. N. (1986). Protective immunity to malaria. Studies with cloned lines of Plasmodium chabaudi chabaudi and P. berghei in CBA/Ca mice. II. The effectiveness and inter or intra-species specificity of the passive transfer of immunity with serum. Parasite Immunology 8, 239–54.CrossRefGoogle ScholarPubMed
Jensen, J. B., Boland, M. T. & Akood, M. (1982). Induction of crisis forms in cultured Plasmodium falciparum with human immune serum from Sudan. Science 216, 1230–3.CrossRefGoogle ScholarPubMed
Jensen, J. B., Boland, M. T., Allan, J. S., Carlin, J. M., Van De Waa, J. A., Divo, A. A. & Akood, M. A. S. (1983). Association between human serum-induced crisis forms in cultured Plasmodium falciparum and clinical immunity to malaria in Sudan. Infection and Immunity 41, 1302–11.CrossRefGoogle ScholarPubMed
Jensen, J. B., Hoffman, S. L., Boland, M. T., Akood, M. A. S., Laughlin, L. W., Kurniawan, 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
Kaye, P. M. (1987). Antigen presentation and the response to parasitic infection. Parasitology Today 3, 293–7.CrossRefGoogle ScholarPubMed
Kemp, D., Coppel, R. & Anders, R. (1987). Repetitive proteins and genes of malaria. Annual Review of Microbiology 41, 181208.CrossRefGoogle ScholarPubMed
Kharazami, A. & Jepsen, S. (1984). Enhanced inhibition of in vitro multiplication of Plasmodium falciparum by stimulated human polymorphonuclear leucocytes. Clinical and Experimental Immunology 57, 287–92.Google Scholar
Langhorne, J., Butcher, G. A., Mitchell, G. H. & Cohen, S. (1979). Preliminary investigations on the role of the spleen in immunity to Plasmodium knowlesi malaria. In Role of the Spleen in the Immunology of Parasitic Diseases. Tropical Disease Research Series 1: UNDP/World Bank/WHO, pp. 205–25. Basel: Schwabe.Google Scholar
Lelchuk, R. & Playfair, J. H. L. (1980). Two distinct types of non-specific immunosuppression in murine malaria. Clinical and Experimental Immunology 42, 428–35.Google ScholarPubMed
Lewis-hughes, P. H. (1984). Malaria infections in mice. Ph.D. thesis, Australian National University, Canberra, Australia.Google Scholar
Marsh, K., Otoo, L. & Greenwood, B. M. (1987). Absence of crisis form factor in subjects immune to Plasmodium falciparum in the Gambia, West Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 514–15.CrossRefGoogle ScholarPubMed
Miller, L. H. (1988). Effective vaccine for humans. Nature, London 332, 109–10.CrossRefGoogle ScholarPubMed
Miller, L. H., Aikawa, M. & Dvorak, J. A. (1975). Malaria (Plasmodium knowlesi) merozoites: immunity and the surface coat. Journal of Immunology 114, 1237–74.CrossRefGoogle ScholarPubMed
Mitchell, G. H., Richards, W. G., Butcher, G. A. & Cohen, S. (1977). Merozoite vaccination of Douroucouli monkeys against falciparum malaria. Lancet 1, 1335–8.CrossRefGoogle ScholarPubMed
Mitchell, G. H., Butcher, G. A. & Cohen, S. (1975). Merozoite vaccination against Plasmodium knowlesi malaria. Immunology 29, 397407.Google ScholarPubMed
Mitchell, G. H., Cohen, S., Black, C. D. V., Voller, A., Dietrich, F. M. & Dukor, P. (1980). Viral adjuvants in malaria vaccination. In The Host Invader Interplay, (ed. Van den Bossche, H.), pp. 629–32. Amsterdam: Elsevier.Google Scholar
Mitchell, G. H., Hadley, T. J., Mcginniss, M. A., Klotz, F. W. & Miller, L. H. (1986). Invasion of erythrocytes by Plasmodium falciparum malaria parasites: evidence for receptor heterogeneity and two receptors. Blood 67, 1519–21.CrossRefGoogle ScholarPubMed
McLean, S. A., Phillips, R. S., Pearson, C. D. & Walliker, D. (1987). The effect of mosquito transmission of antigenic variants of Plasmodium chabaudi. Parasitology 94, 443–9.CrossRefGoogle ScholarPubMed
Ockenhouse, C. F., Schulman, S. & Shear, H. L. (1984). Induction of crisis forms in the human malaria parasite Plasmodium falciparum by γ-interferon activated monocyte derived macrophages. Journal of Immunology 133, 1601–8.CrossRefGoogle ScholarPubMed
Ojo-Amaize, E. A., Salimonu, L. S., Williams, A. I. O., Akinwolere, O. A. A., Sheba, R., Alm, G. & Wigzell, H. (1981). Positive correlation between degree of parasitaemia, interferon titres, and natural killer cell activity in Plasmodium falciparum-infected children. Journal of Immunology 127, 2296–300.CrossRefGoogle ScholarPubMed
Patarroyo, M. E., Amador, R., Clavijo, P., Moreno, A., Guzman, F., Romero, P., Tascon, R., Franco, A., Murillo, L. A., Ponton, G. & Trujillo, G. (1988). A synthetic vaccine protects humans against challenge with asexual blood stages of Plasmodium falciparum malaria. Nature, London 332, 158–61.CrossRefGoogle ScholarPubMed
Patarroyo, M. E., Romero, P., Torres, M. L., Clavijo, P., Moreno, A., Martinez, A., Rodriguez, R., Guzman, F. & Cabezas, E. (1987). Induction of protective immunity against experimental infection with malaria using synthetic peptides. Nature, London 328, 629–32.CrossRefGoogle ScholarPubMed
Perrin, L. H., Loche, M., Dedeb, J.-P., Roussilhon, C. & Fandeur, T. (1984). Immunisation against Plasmodium falciparum asexual blood stages using soluble antigens. Clinical and Experimental Immunology 56, 6772.Google ScholarPubMed
Perrin, L. H., Merkli, B., Loche, M., Chizzolini, C., Smart, J. & Richle, R. (1984). Antimalarial immunity in Saimiri monkeys. Journal of Experimental Medicine 160, 441–51.CrossRefGoogle ScholarPubMed
Perrin, L. H., Merkli, B., Gabra, M. S., Stocker, J. W., Chizzolini, C. & Richle, R. (1985). Immunization with a Plasmodium falciparum merozoite surface antigen induces a partial immunity in monkeys. Journal of Clinical Investigations 75, 1718–21.CrossRefGoogle ScholarPubMed
Perrin, L. H., Ramirez, E., Lambert, P. H. & Miescher, P. A. (1981). Inhibition of P. falciparum growth in human erythrocytes by monoclonal antibodies. Nature, London 289, 301–2.CrossRefGoogle ScholarPubMed
Phillips, R. S., Wolstencroft, R. A., Brown, I. N., Brown, K. N. & Dumonde, D. C. (1970). Immunity to malaria. III. Possible occurrence of a cell-mediated immunity to Plasmodium knowlesi in chronically infected and Freund's Complete Adjuvant-sensitised monkeys. Experimental Parasitology 28, 339–55.CrossRefGoogle Scholar
Piazza, A., Belvedere, M. C., Bernoco, D., Conighi, C., Contu, L., Curtoni, E. S., Mattiuz, P. L., Mayr, W., Richiardi, P., Scudeller, G. & Ceppellini, R. (1973). HLA variation in four Sardinian villages under differential selective pressure by malaria. In Histocompability Testing 1972 (ed. Dausset, J. and Colombani, J.) pp. 7384.Copenhagen: Munksgaard.Google Scholar
Playfair, J. H. L. (1982). Immunity to malaria. British Medical Bulletin 38, 153–9.CrossRefGoogle ScholarPubMed
Reibnegger, G., Fuchs, D., Hausen, A., Schmutzhard, E., Werner, E. R. & Wachter, H. (1987). The dependence of cell-mediated immune activation in malaria on age and endemicity. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 729–33.CrossRefGoogle ScholarPubMed
Rhodes-Feuillette, A., Jauraguiberry, G., Ballet, J. J., Andrieu, B., Druilhe, P., Le Bras, J., Galibert, F. & Peries, J. (1985). The interferon compartment of the immune response in human malaria. I. Interferon inducers in Plasmodium falciparum cultures. Journal of Interferon Research 5, 159168.CrossRefGoogle ScholarPubMed
Sadoff, J. C., Ballou, W. R., Baron, L. S., Majarian, W. R., Brey, R. N., Hockmeyer, W. T., Young, J. F., Cryz, S. J., Ou, J., Lowell, G. H. & Chulay, J. D. (1988). Oral Salmonella typhimurium vaccine expressing circumsporozoite protein protects against malaria. Science 240, 336–8.CrossRefGoogle ScholarPubMed
Saul, A. (1986). Kinetic constraints on the development of a malaria vaccine. Parasite Immunology 9, 19.CrossRefGoogle Scholar
Schofield, L., Ferreira, A., Altszuler, R., Nussenzweig, V. & Nussenzweig, R. S. (1987). Interferon-γ inhibits the intrahepatic development of malaria parasites in vitro. Journal of Immunology 139, 2020–5.CrossRefGoogle Scholar
Siddiqui, W. A. (1977). An effective immunisation of experimental monkeys against a human malaria parasite Plasmodium falciparum. Science 197, 388–9.CrossRefGoogle ScholarPubMed
Siddiqui, W. A., Tam, L. Q., Kramer, K. J., Hui, G. S., Case, S. E., Yamaga, K. M., Chang, S. P., Chan, E. B. T. & Kan, S.-C. (1987). Merozoite surface coat precursor protein completely protects Aotus monkeys against Plasmodium falciparum malaria. Proceedings of the National Academy of Sciences, USA 84, 3014–18.CrossRefGoogle ScholarPubMed
Skamene, E., Stevenson, M. M. & Lemieux, S. (1983). Murine malaria: dissociation of natural killer (NK) cell activity and resistance to Plasmodium chabaudi. Parasite Immunology 5, 557–65.CrossRefGoogle ScholarPubMed
Spitalney, G. S. & Nussenzweig, R. S. (1973). Plasmodium berghei: relationship between protective immunity and anti-sporozoite (CSP) antibody in mice. Experimental Parasitology 33, 168–78.CrossRefGoogle Scholar
Stevenson, M. M. & Skamene, E. (1985). Murine malaria: resistance of AXB/BXA recombinant inbred mice to Plasmodium chabaudi. Infection and Immunity 47, 452–6.CrossRefGoogle ScholarPubMed
Taliaferro, W. H. (1949). Immunity to the malaria infections. In Malariology, vol. 2 (ed. Boyd, M. F.) pp. 935–65. Philadelphia: W. B. Saunders.Google Scholar
Taverne, J., Rahman, D., Dockrell, H. M., Alvai, A., Leveton, C. & Playfair, J. H. L. (1987 a). Activation of liver macrophages in murine malaria is enhanced by vaccination. Clinical and Experimental Immunology 70, 508–14.Google ScholarPubMed
Taverne, J., Tavernier, J., Fiers, W. & Playfair, J. H. L. (1987 b). Recombinant tumour necrosis factor inhibits malaria parasites in vivo but not in vitro. Clinical and Experimental Immunology 67, 14.Google Scholar
Tharavanij, S., Warrell, M. J., Tantiranich, S., Tapchaisri, P., Chongsunguan, N., Praesertsiriros, V. & Patarapotikul, J. (1984). Factors contributing to the development of cerebral malaria. I. Humoral immune responses. American Journal of Tropical Medicine and Hygiene 33, 111.CrossRefGoogle Scholar
Theander, T. G., Bygbjerg, I. C., Hepsen, S., Svenson, M., Kharazami, A., Larsen, P. B. & Bendtzen, K. (1986). Proliferation induced by Plasmodium falciparum antigen and interleukin-2 production by lymphocytes isolated from malaria-immune individuals. Infection and Immunity 53, 221–5.CrossRefGoogle ScholarPubMed
Troye-Blomberg, M., Anderson, G., Stockowsa, M., Shabo, R., Romero, P., Patarroyo, M. E., Wigzell, H. & Perlmann, P. (1985). Production of IL2 and IFN by T cells from malaria patients in response to Plasmodium falciparum or erythrocyte antigens in vitro. Journal of Immunology 135, 3498–504.CrossRefGoogle ScholarPubMed
Udomsangpetch, R., Lundgren, K., Berzins, K., Wahlin, B., Perlmann, H., Troye-Blomberg, M., Carlsson, J., Wahlgren, M., Perlmann, P. & Bjorkmann, A. (1986). Human monoclonal antibodies to Pf155, a major antigen of malaria parasite Plasmodium falciparum. Science 231, 57–9.CrossRefGoogle Scholar
Van De Waa, J. A., Jensen, J. B., Akood, M. A. S. & Bayoumi, R. (1984). Longitudinal study on the in vitro immune response to Plasmodium falciparum in Sudan. Infection and Immunity 45, 505–10.CrossRefGoogle Scholar
Voller, A. & Rossan, R. N. (1969 a). Immunological studies on simian malaria. IV. Heterologous superinfection of monkeys with chronic Plasmodium knowlesi infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 837–45.CrossRefGoogle ScholarPubMed
Voller, A. & Rossan, R. N. (1969 b). Immunological studies on simian malaria. III. Immunity to challenge and antigenic variation in P. knowlesi. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 507–23.CrossRefGoogle Scholar
Walliker, D., Quaki, I. A., Wellems, T. E., McCutchan, T. F., Szarfman, A., London, W. T., Corcoran, L. M., Burkot, T. R. & Carter, R. (1987). Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236, 1661–6.CrossRefGoogle ScholarPubMed
Wandiworanum, C., Barnwell, J. W. & Shear, H. L. (1987). Protective antigen in the membranes of mouse erythrocytes infected with Plasmodium chabaudi. Molecular and Biochemical Parasitology 25, 195201.CrossRefGoogle Scholar
Waters, L. S., Taverne, J., Tai, P.-C., Spry, C. J. F., Targett, G. A. T. & Playfair, J. H. L. (1987). Killing of Plasmodium falciparum by eosinophil secretory products. Infection and Immunity 55, 877–81.CrossRefGoogle ScholarPubMed
Wilson, R. J. M. & Phillips, R. S. (1976). Method to test inhibitory antibodies in human sera to wild populations of Plasmodium falciparum. Nature, London 263, 132–4.CrossRefGoogle ScholarPubMed
Wood, P. R. & Clark, I. A. (1982). Apparent irrelevance of NK cells to resolution of infections with Babesia microti and Plasmodium vinckei peterri in mice. Parasite Immunology 4, 319–27.CrossRefGoogle Scholar
World Health Organization (1986). Sporozoite vaccine development, and research towards development of asexual blood stage vaccines. Report of Ninth Meeting of the Scientific Working Group on the Immunology of Malaira. TDR/IMMAL/SWG(9)/86.3.Google Scholar
Wyler, D. J. (1983). Splenic functions in malaria. Lymphology 16, 121–7.Google ScholarPubMed
Wyler, D. J., Herrod, H. G. & Weinbaum, F. I. (1979). Response of sensitised and unsensitised human lymphocyte subpopulations to Plasmodium falciparum antigens. Infection and Immunity 24, 105–10.CrossRefGoogle Scholar