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The role of MHC- and non-MHC-associated genes in determining the human immune response to malaria antigens

Published online by Cambridge University Press:  06 April 2009

E. M. Riley
E. M. Riley
Affiliation:
Institute of Cell, Animal and Population Biology, Division of Biological Sciences, Ashworth Laboratories, University of Edinburgh, King's Buildings, Mayfield Road, Edinburgh EH9 3JT, UK
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Summary

Individual susceptibility to malaria infection, disease and death is influenced by host genotype, parasite virulence and a number of environmental factors including malaria-specific immunity. Immune responses are themselves determined by a combination of host genes and environmental effects. The extent to which host genotype limits the spectrum of possible immune responses may influence the outcome of infection and has consequences for vaccine design. Associations have been observed between human major histocompatibility complex (MHC) genotype and susceptibility to severe malaria, but no similar associations have been observed for mild malarial disease or for specific antibody responses to defined malaria antigens. Epidemiological studies have shown that, in practice, neither T helper cell nor antibody responses to malaria parasites are limited by host MHC genotype, but have revealed that genes lying outside the MHC may influence T cell proliferative responses. These genes have yet to be identified, but possible candidates include T cell receptor (TcR) genes, and genes involved in TcR gene rearrangements. More importantly, perhaps, longitudinal epidemiological studies have shown that the anti-malarial antibody repertoire is selective and becomes fixed in malaria-immune individuals, but is independent of host genotype. These findings suggest that the antibody repertoire may be determined, at least in part, by stochastic events. The first of these is the generation of the T and B cell repertoire, which results from random gene recombinations and somatic mutation and is thus partially independent of germline genes. Secondly, of the profusion of immunogenic peptides which are processed and presented by antigen presenting cells, a few will, by chance, interact with T and B cell surface antigen receptors of particularly high affinity. These T and B cell clones will be selected, will expand and may come to dominate the immune response, preventing the recognition of variant epitopes presented by subsequent infections - a process known as original antigenic sin or clonal imprinting. The immune response of an individual thus reflects the balance between genetic and stochastic effects. This may have important consequences for subunit vaccine development.

Keywords

Plasmodium falciparummalariaimmunogeneticsclonal imprinting.
Type
Research Article
Information
Parasitology , Volume 112 , Supplement S1: Symposia of the British Society for Parasitology Volume 33:Genetics of host and parasite: implications for immunity, epidemiology and evolution , March 1996 , pp. S39 - S51
Copyright
Copyright © Cambridge University Press 1996

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References

Al-Yaman, F., Genton, B., Anders, R. F., Falk, M., Triglia, T., Lewis, D., Hii, J., Beck, H.-P. & Alpers, M. P. (1994). Relationship between humoral response to Plasmodium falciparum merozoite surface antigen–2 and malaria morbidity in a highly endemic area of Papua New Guinea. American Journal of Tropical Medicine and Hygiene 51, 593–602.CrossRefGoogle Scholar
Allansmith, M., McClellan, B. & Butterworth, M. (1969). The influence of heredity and environment on human immunoglobulin levels. Journal of Immunology 102, 1504–10.CrossRefGoogle ScholarPubMed
Alper, C. A., Kruskall, M., Marcus-Bagley, D., Craven, D. E., Katz, A. J., Brink, S. J., Dienstag, J. L., Awdeh, Z. & Yunis, E. J. (1989). Genetic predisposition of nonresponse to hepatitis B vaccine. New England Journal of Medicine 321, 708–12.CrossRefGoogle Scholar
Anders, R. F., Coppel, R. L., Brown, G. V. & Kemp, D. J. (1988). Antigens with repeated amino acid sequences from the asexual blood stages of Plasmodium falciparum. Progress in Allergy 41, 148–72.Google ScholarPubMed
Banic, D. M., Delplace, P., Mazingue, C. & Camus, D. (1994). H–2b restriction of the immune response to the p26 Plasmodium falciparum antigen. Clinical and Experimental Immunology 95, 472–8.Google Scholar
Barbey, C., Watts, C. & Corradin, G. (1995). Antigen- processing organelles from DRB1*1101 and DRB1*1104 B cell lines display a differential degradation activity. European Journal of Immunology 25, 30–6.CrossRefGoogle Scholar
Bennett, S., Allen, S. J., Olerup, O., Jackson, D. J., Wheeler, J. G., Rowe, P. A., Riley, E. M. & Greenwood, B. M. (1993). Human leucocyte antigen (HLA) and malaria morbidity in a Gambian community. Transactions of the Royal Society of Tropical Medicine and Hygiene 87, 286–7.CrossRefGoogle Scholar
Bhatia, K. & Crane, G. (1985). HLA and tropical splenomegaly syndrome in the Upper Watut valley of Papua New Guinea. Human Immunology 13, 235–42.CrossRefGoogle ScholarPubMed
Björkman, A., Perlmann, H., Petersen, E., Högh, B., Lebbad, M., Warsame, M., Hanson, A. P. & Perlmann, p. (1990). Consecutive determinations of seroreactivities to Pf155/RESA antigen and to its different repetitive sequences in adult men from a holoendemic area of Liberia. Parasite Immunology 12, 115–23.CrossRefGoogle Scholar
Borre, M. B., Dziegiel, M., Petersen, E., Hogh, B., Rieneck, K., Riley, E., Meis, J., Aikawa, M., Nakamura, K., Harada, M., Wind, A., Jakobsen, P. H., Cowland, J., Jepsen, S., Axelsen, N. H. & Vuust, J. (1991). Primary structure and localisation of a partially conserved, immunogenic, glutamate rich protein (GLURP) expressed by all Plasmodium falciparum stages. Molecular and Biochemical Parasitology 49, 119–32.CrossRefGoogle Scholar
Bryceson, A. D. M., Fleming, A. F. & Edington, G. M. (1976). Splenomegaly in Northern Nigeria. Acta Tropica 33, 424–6.Google ScholarPubMed
Carter, R., Graves, P. M., Quakyi, I. A. & Good, M. F. (1989). Restricted or absent immune responses in human populations to Plasmodium falciparum gamete antigens that are targets of malaria transmission-blocking antibodies. Journal of Experimental Medicine 169, 135–47.CrossRefGoogle ScholarPubMed
Chougnet, C., Deloron, P., Lepers, J. P., Tallet, S., Rason, M. D., Astagneau, P., Savel, J. & Coulanges, P. (1990). Humoral and cell-mediated immune responses to the Plasmodium falciparum antigen Pf155/RESA and CS protein: seasonal variations in a population recently re-exposed to endemic malaria. American Journal of Tropical Medicine and Hygiene 43, 234–42.CrossRefGoogle Scholar
Chougnet, C., Tallet, S., Ringwald, P. & Deloron, P. (1992). Kinetics of lymphocyte subsets from peripheral blood during a Plasmodium falciparum malaria attack. Clinical and Experimental Immunology 90, 405–8.CrossRefGoogle ScholarPubMed
Colonna, M., Bresnahan, M., Bahram, S., Strominger, J. L. & Spies, T. (1992). Allelic variants of the human putative peptide transporter involved in antigen processing. Proceedings of the National Academcy of Sciences USA 89, 3932–6.CrossRefGoogle ScholarPubMed
De Groot, A. S., Johnson, A. H., Maloy, W. L., Quakyi, I. A., Riley, E. M., Menon, A., Banks, S. M., Berzofsky, J. A. & Good, M. F. (1989). Human T cell recognition of polymorphic epitopes from malaria circumsporozoite protein. Journal of Immunology 142, 4000–5.CrossRefGoogle Scholar
Del Giudice, G., Cooper, J. A., Merino, J., Verdini, A. S., Pessi, A., Togna, A. R., Engers, H. D., Corradin, G. P. & Lambert, P. H. (1986). The antibody response in mice to carrier-free synthetic polymers of Plasmodium falciparum circumsporozoite repetitive epitope is I-Ab restricted. Implications for malaria vaccines. Journal of Immunology 137, 2952–60.CrossRefGoogle ScholarPubMed
Dieye, A., Heidrich, H.-G., Rogier, C., Trape, J.-F., Launois, P., Holder, A. A. & Sarthou, J.-L. (1993). Lymphocyte response in vitro to Plasmodium falciparum merozoite antigens in donors from a holoendemic area. Parasitology Research 79, 629–33.CrossRefGoogle ScholarPubMed
Dunlap, N. E., Ballinger, S., Reed, T., Christian, J. C., Koopman, W. J. & Briles, D. E. (1993). The use Of monozygotic and dizygotic twins to estimate the effect of inheritance on the levels of immunoglobulin isotypes and antibodies to phosphocholine. Clinical Immunology and Immunopathology 66, 176–80.CrossRefGoogle ScholarPubMed
Egan, A. F., Chappel, J. A., Burghaus, P. A., Morris, J. S., Mcbride, J. S., Holder, A. A., Kaslow, D. C. & Riley, E. M. (1994). Serum antibodies from malaria-exposed people recognise conserved epitopes formed by the two epidermal growth factor motifs of MSP19, the carboxy-terminal fragment of the major merozoite surface protein of Plasmodium falciparum. Infection and Immunity 63, 456–66.CrossRefGoogle Scholar
Fazekas De St Groth, S. & Webster, R. G. (1966 a). Disquisitions on original antigenic sin. 1. Evidence in man. Journal of Experimental Medicine 124, 331–45.CrossRefGoogle ScholarPubMed
Fazekas De St Groth, S. & Webster, R. G. (1966 b). Disquisitions on original antigenic sin. 2. Proof in lower creatures. Journal of Experimental Medicine 124, 347–61.CrossRefGoogle Scholar
Francis, T. (1953). The newe acquayantance. Annals of Internal Medicine 39, 203.Google Scholar
Fuschiotti, P., Harindranath, N., Mage, R. G., McCormack, W. T., Dhanarajan, P. & Roux, K. H. (1993). Recombination activating genes-1 and -2 of the rabbit: cloning and expression of germline and expressed genes. Molecular Immunology 30, 1021–32.CrossRefGoogle ScholarPubMed
Gammon, G., Klotz, J., Ando, D. & Sercarz, E. (1990). The T cell repertoire to a multideterminant antigen: clonal heterogeneity of the T cell response, variation between syngeneic individuals and in vitro selection of T cell specificities. Journal of Immunology 144, 1571–7.CrossRefGoogle Scholar
Good, M. F., Berzofsky, J. A., Maloy, W. L., Hayashi, Y., Fujii, N., Hockmeyer, W. T. & Miller, L. H. (1986). Genetic control of the immune response in mice to a Plasmodium falciparum sporozoite vaccine: widespread non-responsiveness to single malaria T epitope in highly repetitive vaccine. Journal of Experimental Medicine 164, 655–60.CrossRefGoogle Scholar
Good, M. F., Miller, L. H., Kumar, S., Quakyi, I. A., Keister, D., Adams, J. H., Moss, B., Berzofsky, J. A. & Carter, R. (1988 a). Limited immunological recognition of critical malaria vaccine candidate antigens. Science 242, 574–7.CrossRefGoogle ScholarPubMed
Good, M. F., Pombo, D., Lunde, M. N., Maloy, W. L., Halenbeck, R., Koths, K., Miller, L. H. & Berzofsky, J. (1988 b). Recombinant human IL-2 overcomes genetic nonresponsiveness to malaria sporozoite peptides: correlation of effect with biologic activity of IL-2. Journal of Immunology 141, 972–7.CrossRefGoogle ScholarPubMed
Good, M. F., Pombo, D., Quakyi, I. A., Riley, E. M., Houghten, R. A., Menon, A., Alling, D. W., Berzofsky, J. A. & Miller, L. H. (1988 c). Human T cell recognition of the circumsporozoite protein of Plasmodium falciparum. Immunodominant T cell domains map to the polymorphic regions of the molecule. Proceedings of the National Academy of Sciences USA 85, 1199–203.CrossRefGoogle Scholar
Graves, P. M., Bhatia, K., Burkot, T. R., Prasad, M., Wirtz, R. A. & Beckers, P. (1989). Association between HLA type and antibody response to malaria sporozoite and gamete epitopes is not evident in immune Papua New Guineans. Clinical and Experimental Immunology 78, 418–23.Google Scholar
Gray, D. (1994). Regulation of immunological memory. Current Opinion in Immunology 6, 425–30.CrossRefGoogle ScholarPubMed
Greenwood, B. M., Groenendaal, F., Bradley, A. K., Greenwood, A. M., Shenton, F. & Tulloch, S. (1987). Ethnic differences in the prevalence of splenomegaly and malaria in The Gambia. Annals of Tropical Medicine and Parasitology 81, 345–54.CrossRefGoogle ScholarPubMed
Greenwood, B. M., Marsh, K. & Snow, R. W. (1991). Why do some African children develop severe malaria? Parasitology Today 7, 277–81.CrossRefGoogle ScholarPubMed
Gulwani-Akolkar, B., Shi, B., Akolkar, P. N., Iot, K., Bias, W. B. & Silver, J. (1995). Do HLA genes play a prominent role in determining T cell receptor Vα segment usage in humans? Journal of Immunology 154, 3843–51.CrossRefGoogle Scholar
Guttinger, M., Romagnoli, P., Vandel, L., Meloen, R., Takacs, B., Pink, R. J. L. & Sinigaglia, F. (1991). HLA polymorphism and T cell recognition of a conserved region of p190, a malaria vaccine candidate. International Immunology 3, 899–906.CrossRefGoogle Scholar
Hawes, G. E., Struvk, L. & Van Den Elsen, P. J. (1993). Differential usage of T cell receptor V gene segments in CD4+ and CD8+ subsets of T lymphocytes in monozygotic twins. Journal of Immunology 150, 2033–5.CrossRefGoogle ScholarPubMed
Hill, A. V. S., Allsopp, C. E. M., Kwiatkowski, D., Anstey, N. M., Twumasi, P., Rowe, P., Bennett, S., Brewster, D., McMichael, A. J. & Greenwood, B. M. (1991). Common West African HLA antigens are associated with protection from severe malaria. Nature 352, 595–600.CrossRefGoogle ScholarPubMed
Hill, A. V. S., Yates, S. N. R., Allsopp, C. E. M., Gupta, S., Gilbert, S. C., Lalvani, A., Aidoo, M., Davenport, M. & Plebanski, M. (1994). Human leucocyte antigens and natural selection by malaria. Philosophical Transactions of the Royal Society of London, Series B 346, 379–85.Google ScholarPubMed
Ho, P. C., Mutch, D. A., Winkel, K. D., Saul, A. J., Jones, G. L., Doran, T. J. & Rzepczyk, C. M. (1990). Identification of two promiscuous T cell epitopes from tetanus toxin. European Journal of Immunology 20, 477–83.CrossRefGoogle ScholarPubMed
Jepson, A. P., Banya, W. A. S., Sisay-Joof, F.., Hassan-King, M., Bennett, S & Whittle, H. C. (1995). Genetic regulation of fever in Plasmodium falciparum malaria in Gambian twin children. Journal of Infectious Diseases 172, 316–19.CrossRefGoogle ScholarPubMed
Kalff, M. w. & Hijmans, w. (1969). Serum immunoglobulin levels in twins. Clinical and Experimental Immunology 5, 469–77.Google ScholarPubMed
Kohler, P. F., Rivera, V. J., Eckert, E. D., Bouchard, T. J. & Heston, L. L. (1985). Genetic regulation of immunoglobulin and specific antibody levels in twins reared apart. Journal of Clinical Investigation 75, 883–8.CrossRefGoogle ScholarPubMed
Köhler, H., Müller, S. & Nara, P. L. (1994). Deceptive imprinting in the immune response to HIV–1. Immunology Today 15, 475–8.CrossRefGoogle ScholarPubMed
Konradsen, H. B., Henrichsen, J., Wachmann, H. & Holm, N. (1993). The influence of genetic factors on the immune response as judged by pneumococcal vaccination of mono- and dizygotic Caucasian twins. Clinical and Experimental Immunology 92, 532–6.CrossRefGoogle ScholarPubMed
Lew, A. M., Langford, C. J., Pye, D., Edwards, S., Corcoran, L. & Anders, R. F. (1989). Class II restriction in mice to the malaria candidate vaccine ring-infected erythrocyte surface antigen (RESA) as synthetic peptides or as expressed in recombinant vaccinia. Journal of Immunology 142, 4012–16.CrossRefGoogle ScholarPubMed
Marsh, K., Hayes, R. H., Carson, D. C., Otoo, L. N., Shenton, F., Byass, P., Zavala, F. & Greenwood, B. M. (1988). Anti-sporozoite antibodies and immunity to malaria in a rural Gambian population. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 532–7.CrossRefGoogle Scholar
McGuire, W., Hill, A. V. S., Allsopp, C. E. M., Greenwood, B. M. & Kwiatkowski, D. (1994). Variation in the TNFα promoter region associated with susceptibility to cerebral malaria. Nature 371, 508–11.CrossRefGoogle ScholarPubMed
Migot, F., Chougnet, C., Perichon, B., Danze, P.-M., Lepers, J.-P., Krishnamoorthy, R. & Deloron, P. (1995). Lack of correlation between HLA class II alleles and immune responses to Pf155/ring-infected erythrocyte surface antigen (RESA) from Plasmodium falciparum in Madagascar. American Journal of Tropical Medicine and Hygiene 52, 252–7.CrossRefGoogle ScholarPubMed
Murillo, L. A., Rocha, C. L., Mora, A. L., Kalil, J., Goldenberg, A. K. & Patarroyo, M. E. (1991). Molecular analysis of HLA DR4-β?1 gene in malaria vaccines. Typing and subtyping by PCR technique and oligonucleotides. Parasite Immunology 13, 201–10.CrossRefGoogle ScholarPubMed
Osoba, D., Dick, H. M., Voller, A., Goosen, T. J., Goosen, T., Draper, C. C. & De The, G. (1979). Role of the HLA complex in the antibody response to malaria under natural conditions. Immunogenetics 8, 323–38.CrossRefGoogle Scholar
Patarroyo, M. E., Vinasco, J., Amador, R., Espejo, F., Silva, Y., Moreno, A., Rojas, M., Mora, A. L., Salcedo, M., Valero, V., Goldberg, A. K. & Kalil, J. (1991). Genetic control of the immune response to a synthetic vaccine against Plasmodium falciparum. Parasite Immunology 13, 509–16.CrossRefGoogle ScholarPubMed
Piazza, A., Belvedere, M. C., Bernoco, D., Conighi, C., Contu, L., Curton, 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 Histocompatibility Testing 1972 (ed. Dausset, J. & Colombani, J.), pp. 73–84. Baltimore: Williams and Wilkins.Google Scholar
Powis, S. H., Mockridge, I., Kelly, A., Kerr, L. A., Glynne, R., Gileadi, U., Beck, S. & Trowsdale, J. (1992). Polymorphism in a second ABC transporter gene located within the class II region of the human major histocompatibility complex. Proceedings of the National Academy of Sciences USA 89, 1463–7.CrossRefGoogle Scholar
Quakyi, I. A., Otoo, L. N., Pombo, D., Sugars, L. Y., Menon, A., Degroot, A. S., Johnson, A., Alling, D., Miller, L. H. & Good, M. F. (1989). Differential non-responsiveness in humans of candidate Plasmodium falciparum vaccine antigens. American Journal of Tropical Medicine and Hygiene 41, 125–34.CrossRefGoogle ScholarPubMed
Rebai, N., Pantaleo, G., Demarest, J. F., Ciurli, C., Soudeyns, H., Adelsberger, J. W., Vaccarezza, M., Walker, R. E., Sekaly, R. P. & Fauci, A. S. (1994). Analysis of the T-cell receptor β-chain variable-region (Vβ) repertoire in monozygotic twins discordant for human immunodeficiency virus: evidence for perturbations of specific Vβ segments in CD4+ T cells of the virus-positive twins. Proceedings of the National Academy of Sciences USA 91, 1529–33.CrossRefGoogle Scholar
Restrepo, M., Rojas, W., Montoya, F., Montoya, A. E. & Dawson, D. (1988). HLA and malaria in four Colombian ethnic groups. Revista do Instituto de Medicina Tropical de São Paulo 30, 323–31.CrossRefGoogle ScholarPubMed
Riley, E. M., Allen, S. J., Bennett, S., Thomas, P. J., Andersson, G., O'Donnell, A., Lindsay, S. W., Good, M. F. & Greenwood, B. M. (1990 a). Recognition of dominant T cell stimulating epitopes from the circumsporozoite protein of Plasmodium falciparum and relationship to malaria morbidity in Gambian children. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 648–57.CrossRefGoogle ScholarPubMed
Riley, E. M., Allen, S. J., Troye-Blomberg, M., Bennett, S., Perlmann, H., Andersson, G., Smedman, L., Perlmann, P. & Greenwood, B. M. (1991). Immune recognition of the malaria vaccine candidate antigen Pf155/RESA is associated with resistance to clinical disease: a prospective study in a malaria endemic region of West Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 436–43.CrossRefGoogle Scholar
Riley, E. M., Olerup, O., Bennett, S., Rowe, P., Allen, S. J., Blackman, M. J., Troye-Blomberg, M., Holder, A. A. & Greenwood, B. M. (1992). MHC and malaria: the relationship between HLA class II alleles and immune responses to Plasmodium falciparum. International Immunology 4, 1055–63.CrossRefGoogle ScholarPubMed
Riley, E. M., Bennett, S., Jepson, A., Hassan-King, M., Whittle, H. C., Olerup, O. & Carter, R. (1994). Human antibody responses to Pfs230, a sexual stage-specific surface antigen of Plasmodium falciparum: non-responsiveness is a stable phenotype but does not appear to be genetically regulated. Parasite Immunology 16, 55–62.CrossRefGoogle Scholar
Riley, E. M., Ong, C. S. L., Olerup, O., Eida, S., Allen, S. J., Bennett, S., Andersson, G. & Targett, G. A. T. (1990 b). Cellular and humoral responses to Plasmodium falciparum gametocyte antigens in malaria immune individuals: limited response to the 48/45 KD surface antigen does not appear to be due to MHC restriction. Journal of Immunology 144, 4810–16.CrossRefGoogle Scholar
Roth, M. E., Holman, P. O. & Kranz, D. M. (1991). Nonrandom use of Jαgene segments: influence of Vα and Jα gene location. Journal of Immunology 147, 1075–81.CrossRefGoogle Scholar
Sayles, P. C. & Wassom, D. L. (1988). Immunoregulation in murine malaria: susceptibility of inbred mice to infection with Plasmodium yoelii depends on the dynamic interplay of host and parasite genes. Journal of Immunology 141, 241.CrossRefGoogle ScholarPubMed
Scherf, A., Behr, C., Sarthou, J.-L., Pla, M., Rogier, C., Trape, J.-F., Pereira Da Silva, L. & Dubois, P. (1993). Immune response in mouse and malaria-exposed humans to peptides derived from Pfll-1, a highly repetitive megadalton protein of Plasmodium falciparum. European Journal of Immunology 23, 1574–81.CrossRefGoogle ScholarPubMed
Sinigaglia, F., Guttinger, M., Kilgus, J., Doran, D. M., Matile, H., Etlinger, H., Trzeciak, A., Gillessen, D. & Pink, J. R. L. (1988). A malaria T-cell epitope recognised with most mouse and human MHC class II antigens. Nature 336, 778–80.CrossRefGoogle Scholar
Sjöberg, K., Lepers, J. P., Raharimalala, L., Larsson, Å., Olerup, O., Marbiah, N. T., Troye-Blomberg, M. & Perlmann, P. (1992). Genetic regulation of human anti-malarial antibodies in twins. Proceedings of the National Academy of Sciences USA 89, 2101–4.CrossRefGoogle ScholarPubMed
Stevenson, M. M., Huang, D. Y., Podoba, J. E. & Nowotarski, M. E. (1992). Macrophage activation during Plasmodium chabaudi AS infection in resistant C57B1/6 and susceptible A/J mice. Infection and Immunity 60, 1193–1201.CrossRefGoogle Scholar
Stevenson, M. M., Lyanga, J. J. & Skamene, E. (1982). Murine malaria: genetic control of resistance to Plasmodium chabaudi. Infection and Immunity 38, 80–8.CrossRefGoogle ScholarPubMed
Sturchler, D., Berger, R., Etlinger, H., Fernex, M., Matile, H., Pink, R., Schlumbom, V. & Just, M. (1989).Effects of interferons on immune response to a synthetic peptide malaria vaccine in non-immune adults. Vaccine 7, 457–61.CrossRefGoogle ScholarPubMed
Taylor, R. R., Egan, A., McGuinness, D., Jepson, A., Adair, R., Drakely, C. & Riley, E. (1996). Selective recognition of malaria antigens by human serum antibodies is not genetically determined but is reminiscent of clonal imprinting. International Immunology (in Press).CrossRefGoogle ScholarPubMed
Taylor, R. R., Smith, D. B., Robinson, V. J., McBride, J. S. & Riley, E. M. (1995). Human antibody response to Plasmodium falciparum merozoite surface protein 2 is serogroup specific and predominantly of the IgG3 subclass. Infection and Immunity 63, 4382–4388.CrossRefGoogle Scholar
Troye-Blomberg, M., Olerup, O., Larsson, Å., Sjöberg, K., Perlmann, H., Riley, E., Lepers, J.-P. & Perlmann, P. (1991). Failure to detect MHC class II associations of the human immune response induced by repeated malaria infections to the Plasmodium falciparum antigen Pf155/RESA. International Immunology 3, 1043–51.CrossRefGoogle Scholar
Walliker, D. (1994). The role of molecular genetics in field studies on malaria parasites. International Journal for Parasitology 24, 799–808.CrossRefGoogle ScholarPubMed
Wassom, D. L., Cruz, E. S., Avery, A. C., Sayles, P. C. & David, C. S. (1995). Expression of MLS-la (MTV-7) influences the outcome of murine malaria infections. Proceedings of the 9th International Congress of Immunology, 23–29 July 1995, San Francisco, USA, p. 807, Abstract number 4786.Google Scholar
Wassom, D. L. & Kelly, E. A. B. (1990). The role of the major histocompatibility complex in resistance to parasite infections. Critical Reviews in Immunology 10, 31–52.Google ScholarPubMed
Weiss, W. R., Good, M. F., Hollingdale, M. R., Miller, L. H. & Berzofsky, J. A. (1989). Genetic control of immunity to Plasmodium yoelii sporozoites. Journal of Immunology 143, 4263–6.CrossRefGoogle ScholarPubMed
Wilson, I. A. & cox, N. J. (1990). Structural basis of immune recognition of influenza virus hemagglutinin. Annual Review of Immunology 8, 737–71.CrossRefGoogle ScholarPubMed
Zhou, P., Cao, H., Smart, M. & David, C. (1993). Molecular basis of genetic polymorphism in major histocompatibility complex-linked proteasome gene (LMP2).Proceedings of the National Academy of Sciences USA 90, 2681–4.CrossRefGoogle ScholarPubMed