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Current status of vaccine development against Theileria parasites

Published online by Cambridge University Press:  02 February 2007

W. I. MORRISON  and
D. J. McKEEVER
W. I. MORRISON
Affiliation:
Division of Veterinary Clinical Sciences, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
D. J. McKEEVER
Affiliation:
Division of Veterinary Clinical Sciences, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
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Abstract

The tick-borne protozoan parasites Theileria parva and Theileria annulata cause economically important diseases of cattle in tropical and sub-tropical regions. Because of shortcomings in disease control measures based on therapy and tick control, there is a demand for effective vaccines against these diseases. Vaccines using live parasites have been available for over two decades, but despite their undoubted efficacy they have not been used on a large scale. Lack of infrastructure for vaccine production and distribution, as well as concerns about the introduction of vaccine parasite strains into local tick populations have curtailed the use of these vaccines. More recently, research has focused on the development of subunit vaccines. Studies of immune responses to different stages of the parasites have yielded immunological probes that have been used to identify candidate vaccine antigens. Immunisation of cattle with antigens expressed in the sporozoite, schizont or merozoite stages has resulted in varying degrees of protection against challenge. Although the levels of protection achieved have not been sufficient to allow exploitation for vaccination, there are clearly further lines of investigation, relating to both the choice of antigens and the antigen delivery systems employed, that need to be pursued to fully explore the potential of the candidate vaccines. Improved knowledge of the molecular biology and immunology of the parasites gained during the course of these studies has also opened up opportunities to refine and improve the quality of live vaccines.

Keywords

Theileriavaccinationlivesubunit vaccinesimmune responsesT cellsantigens
Type
Research Article
Information
Parasitology , Volume 133 , Supplement S2: Parasite Vaccines , October 2006 , pp. S169 - S187
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Ackerman, A. L. and Cresswell, P. ( 2004). Cellular mechanisms governing cross-presentation of exogenous antigens. Nature Immunology 5, 678–684.CrossRefGoogle Scholar
Ahmed, J. S. and Mehlhorn, H. ( 1999). Review: the cellular basis of the immunity to and immunopathogenesis of tropical theileriosis. Parasitology Research 85, 539–549.CrossRefGoogle Scholar
Ahmed, J. S., Wiegers, P., Ritz, H., Hartwig, H., Schein, E. and Schnittger, L. ( 2000). Generation of cytotoxic T lymphocytes and cytostatic acting cells in T. annulata-immune cattle. Annals of the New York Academy of Sciences 916, 595–599.Google Scholar
Badovinac, V. P. and Harty, J. T. ( 2000). Adaptive immunity and enhanced CD8+ T cell response to Listeria monocytogenes in the absence of perforin and IFN-gamma. Journal of Immunology 164, 6444–6452.CrossRefGoogle Scholar
Baldwin, C. L., Black, S. J., Brown, W. C., Conrad, P. A., Goddeeris, B. M., Kinuthia, S. W., Lalor, P. A., MacHugh, N. D., Morrison, W. I., Morzaria, S. P., Naessens, J. and Newson, J. ( 1988). Bovine T cells, B cells, and null cells are transformed by the protozoan parasite Theileria parva. Infection and Immunity 56, 462–467.Google Scholar
Baldwin, C. L., Goddeeris, B. M. and Morrison, W. I. ( 1987). Bovine helper T-cell clones specific for lymphocytes infected with Theileria parva (Muguga). Parasite Immunology 9, 499–513.CrossRefGoogle Scholar
Ballingall, K. T., Luyai, A., Rowlands, G. J., Sales, J., Musoke, A. J., Morzaria, S. P. and McKeever, D. J. ( 2004). Bovine leukocyte antigen major histocompatibility complex class II DRB3*2703 and DRB3*1501 alleles are associated with variation in levels of protection against Theileria parva challenge following immunization with the sporozoite p67 antigen. Infection and Immunity 72, 2738–2741.CrossRefGoogle Scholar
Ballingall, K. T., Mwangi, D. M., MacHugh, N. D., Taracha, E. L., Totte, P. and McKeever, D. J. ( 2000). A highly sensitive non-radioactive assay for T cell activation in cattle: applications in screening for antigens recognised by CD4+ and CD8+ T cells. Journal of Immunological Methods 239, 85–93.CrossRefGoogle Scholar
Bishop, R., Nene, V., Staeyert, J., Rowlands, J., Nyanjui, J., Osaso, J., Morzaria, S. and Musoke, A. ( 2003). Immunity to East Coast fever in cattle induced by a polypeptide fragment of the major surface coat protein of Theileria parva sporozoites. Vaccine 21, 1205–1212.CrossRefGoogle Scholar
Boehm, U., Klamp, T., Groot, M. and Howard, J. C. ( 1997). Cellular responses to interferon-gamma. Annual Reviews of Immunology 15, 749–795.CrossRefGoogle Scholar
Boulter, N., Brown, D., Wilkie, G., Williamson, S., Kirvar, E., Knight, P., Glass, E., Campbell, J., Morzaria, S., Nene, V., Musoke, A., d'Oliveira, C., Gubbels, M. J., Jongejan, F. and Hall, R. ( 1999). Evaluation of recombinant sporozoite antigen SPAG-1 as a vaccine candidate against Theileria annulata by the use of different delivery systems. Tropical Medicine and International Health 4, A71–A77.CrossRefGoogle Scholar
Boulter, N., Knight, P. A., Hunt, P. D., Hennessey, E. S., Katzer, F., Tait, A., Williamson, S., Brown, D., Baylis, H. A. and Hall, R. ( 1994). Theileria annulata sporozoite surface-antigen (spag-1) contains neutralizing determinants in the c-terminus. Parasite Immunology 16, 97–104.CrossRefGoogle Scholar
Boulter, N. R., Glass, E. J., Knight, P. A., Bell-Sakyi, L., Brown, C. G. D. and Hall, R. ( 1995). Theileria annulata sporozoite antigen fused to hepatitis-b core antigen used in a vaccination trial. Vaccine 13, 1152–1160.CrossRefGoogle Scholar
Brocklesby, D. W. and Bailey, K. P. ( 1965). The immunisation of cattle against East Coast fever (Theileria parva infection) using tetracyclines: A review of the literature and a reappraisal of the method. Bulletin of Epizootic Diseases of Africa 13, 161–168.Google Scholar
Brown, C. G. D., Stagg, D. A., Purnell, R. E., Kanhai, G. K. and Payne, R. C. ( 1973). Infection and transformation of bovine lymphoid cell in vitro by infective particles of Theileria parva. Nature 245, 101–103.CrossRefGoogle Scholar
Brown, D. J., Campbell, J. D., Russell, G. C., Hopkins, J. and Glass, E. J. ( 1995). T cell activation by Theileria annulata-infected macrophages correlates with cytokine production. Clinical and Experimental Immunology 102, 507–514.CrossRefGoogle Scholar
Brown, W. C., Sugimoto, C. and Grab, D. J. ( 1989). Theileria parva: bovine helper T cell clones specific for both infected lymphocytes and schizont membrane antigens. Experimental Parasitology 69, 234–248.CrossRefGoogle Scholar
Burridge, M. J., Morzaria, S. P., Kimber, C. D., Cunningham, M. P. and Brown, C. G. D. ( 1972). Duration of immunity to East Coast fever (Theileria parva infection) of cattle. Parasitology 64, 511–515.CrossRefGoogle Scholar
Buscher, G., Morrison, W. I. and Nelson, R. T. ( 1984). Titration in cattle of infectivity and immunogenicity of autologous cell lines infected with Theileria parva. Veterinary Parasitology 15, 29–38.CrossRefGoogle Scholar
Butz, E. A. and Bevan, M. J. ( 1998). Massive expansion of antigen-specific CD8+ T cells during an acute virus infection. Immunity 8, 167–175.CrossRefGoogle Scholar
Conze, G., Campbell, J. D., Nichani, A. K., Glass, E. J., Spooner, R. L. and Ahmed, J. S. ( 1998). Evidence for strain specificity in cytotoxic T-lymphocyte-mediated, major histocompatibility complex class I-dependent killing of Theileria annulata-infected cells. Parasitology Research 84, 593–595.CrossRefGoogle Scholar
Crotzer, V. L., Christian, R. E., Brooks, J. M., Shabanowitz, J., Settlage, R. E., Marto, J. A., White, F. M., Rickinson, A. B., Hunt, D. F. and Engelhard, V. H. ( 2000). Immunodominance among EBV-derived epitopes restricted by HLA-B27 does not correlate with epitope abundance in EBV-transformed B-lymphoblastoid cell lines. Journal of Immunology 164, 6120–6129.CrossRefGoogle Scholar
Cunningham, M. P., Brown, C. G. D., Burridge, M. J., Musoke, A. J., Purnell, R. E., Radley, D. E. and Sempebwa, C. ( 1974). East Coast fever: titration in cattle of suspensions of Theileria parva derived from ticks. British Veterinary Journal 130, 179–187.CrossRefGoogle Scholar
Cunningham, M. P., Brown, C. G., Burridge, M. J. and Purnell, R. E. ( 1973). Cryopreservation of infective particles of Theileria parva. International Journal for Parasitology 3, 583–587.CrossRefGoogle Scholar
Dargouth, M. A., Ben Miled, L., Bouattour, A., Melrose, T. R., Brown, C. G. D. and Kilani, M. ( 1996). A preliminary study on the attenuation of Tunisian schizont-infected cell lines of Theileria annulata. Parasitology Research 82, 647–655.CrossRefGoogle Scholar
DeMartini, J. C. and Baldwin, C. L. ( 1991). Effects of gamma interferon, tumor necrosis factor alpha, and interleukin-2 on infection and proliferation of Theileria parva-infected bovine lymphoblasts and production of interferon by parasitized cells. Infection and Immunity 59, 4540–4546.Google Scholar
De Plaen, E., Lurquin, C., Lethe, B., van der, B. P., Brichard, V., Renauld, J. C., Coulie, P., Van Pel, A. and Boon, T. ( 1997). Identification of genes coding for tumor antigens recognized by cytolytic T lymphocytes. Methods in Immunology 12, 125–142.CrossRefGoogle Scholar
Dickson, J. and Shiels, B. R. ( 1993). Antigenic diversity of a major merozoite surface molecule in Theileria annulata. Molecular and Biochemical Parasitology 57, 55–64.CrossRefGoogle Scholar
Dobbelaere, D. A., Fernandez, P. C. and Heussler, V. T. ( 2000). Theileria parva: taking control of host cell proliferation and survival mechanisms. Cellular Microbiology 2, 91–99.CrossRefGoogle Scholar
Dobbelaere, D. A., Spooner, P. R., Barry, W. C. and Irvin, A. D. ( 1984). Monoclonal antibody neutralizes the sporozoite stage of different Theileria parva stocks. Parasite Immunology 6, 361–370.CrossRefGoogle Scholar
Dobbelaere, D. A. E. and Rottenberg, S. ( 2003). Theileria-induced leukocyte transformation. Current Opinion in Microbiology 6, 377–382.CrossRefGoogle Scholar
Dobbelaere, D. A. E., Shapiro, S. Z. and Webster, P. ( 1985). Identification of a surface antigen on Theileria parva sporozoites by monoclonal antibody. Proceedings of the National Academy of Sciences, USA 82, 1771–1775.CrossRefGoogle Scholar
Dolan, T. T., Linyonyi, A., McHardy, N., Bond, A. L. and Clampitt, R. B. ( 1988). Chemotherapy of East Coast fever: parvaquone treatment of Theileria parva parva at intervals after infection. Research in Veterinary Science 44, 15–20.Google Scholar
Dolan, T. T., Young, A. S., Losos, G. J., McMilian, I., Minder, C. E. and Soulsby, K. ( 1984). Dose dependent responses of cattle to Theileria parva stabilate. International Journal for Parasitology 14, 89–95.CrossRefGoogle Scholar
d'Oliveira, C., Feenstra, A., Vos, H., Osterhaus, A. D., Shiels, B. R., Cornelissen, A. W. and Jongejan, F. ( 1997). Induction of protective immunity to Theileria annulata using two major merozoite surface antigens presented by different delivery systems. Vaccine 15, 1796–1804.CrossRefGoogle Scholar
Emery, D. L. ( 1981). Adoptive transfer of immunity to infection with Theileria parva (East Coast fever) between cattle twins. Research in Veterinary Science 30, 364–367.Google Scholar
Emery, D. L., Eugui, E. M., Nelson, E. R. T. and Tenywa, T. ( 1981). Cell-mediated immune responses to Theileria parva (East Coast fever) during immunization and lethal infection in cattle. Immunology 43, 323–336.Google Scholar
Emery, D. L., Morrison, W. I., Buscher, G. and Nelson, R. T. ( 1982). Generation of cell-mediated cytotoxicity to Theileria parva (East Coast fever) after inoculation of cattle with parasitized lymphoblasts. Journal of Immunology 128, 195–200.Google Scholar
Eugui, E. M. and Emery, D. L. ( 1981). Genetically restricted cell-mediated cytotoxicity in cattle immune to Theileria parva. Nature 290, 251–254.CrossRefGoogle Scholar
Fawcett, D., Musoke, A. J. and Voight, W. ( 1984). Interaction of sporozoites of Theileria parva with bovine lymphocytes in vitro. 1. Early events after invasion. Tissue and Cell 16, 873–884.Google Scholar
Fawcett, D. W., Doxsey, S., Stagg, D. A. and Young, A. S. ( 1982). The entry of sporozoites of Theileria parva into bovine lymphocytes in vitro. Electron microscopic observations. European Journal of Cell Biology 27, 10–21.Google Scholar
Gardner, M. J., Bishop, R., Shah, T., de Villiers, E. P., Carlton, J. M., Hall, N., Ren, Q., Paulsen, I. T., Pain, A., Berriman, M., Wilson, R. J., Sato, S., Ralph, S. A., Mann, D. J., Xiong, Z., Shallom, S. J., Weidman, J., Jiang, L., Lynn, J., Weaver, B., Shoaibi, A., Domingo, A. R., Wasawo, D., Crabtree, J., Wortman, J. R., Haas, B., Angiuoli, S. V., Creasy, T. H., Lu, C., Suh, B., Silva, J. C., Utterback, T. R., Feldblyum, T. V., Pertea, M., Allen, J., Nierman, W. C., Taracha, E. L., Salzberg, S. L., White, O. R., Fitzhugh, H. A., Morzaria, S., Venter, J. C., Fraser, C. M. and Nene, V. ( 2005). Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309, 134–137.CrossRefGoogle Scholar
Gazzinelli, R. T., Ropert, C. and Campos, M. A. ( 2004). Role of the Toll/interleukin-1 receptor signaling pathway in host resistance and pathogenesis during infection with protozoan parasites. Immunological Reviews 201, 9–25.CrossRefGoogle Scholar
Gentschev, I., Glaser, I., Goebel, W. I., McKeever, D. J., Musoke, A. J. and Heussler, V. T. ( 1998). Delivery of the p67 sporozoite antigen of Theileria parva using recombinant Salmonella: secretion of the antigen enhances specific antibody responses in cattle. Infection and Immunity 66, 2660–2664.Google Scholar
Geysen, D., Bishop, R., Skilton, R., Dolan, T. T. and Morzaria, S. ( 1999). Molecular epidemiology of Theileria parva in the field. Tropical Medicine and International Health 4, A21–A27.CrossRefGoogle Scholar
Goddeeris, B. M., Morrison, W. I. and Teale, A. J. ( 1986 a). Generation of bovine cytotoxic cell lines specific for cells infected with the protozoan parasite Theileria parva and restriction by products of the major histocompatibility complex. European Journal of Immunology 16, 1243–1249.Google Scholar
Goddeeris, B. M., Morrison, W. I., Teale, A. J., Bensaid, A. and Baldwin, C. L. ( 1986 b). Bovine cytotoxic T-cell clones specific for cells infected with the protozoan parasite Theileria parva: Parasite strain specificity and class I major histocompatibility restriction. Proceedings of the National Academy of Sciences, USA 83, 5238–5242.Google Scholar
Goddeeris, B. M., Morrison, W. I., Toye, P. G. and Bishop, R. ( 1990). Strain specificity of bovine Theileria parva-specific cytotoxic T cells is determined by the phenotype of the restricting class I MHC. Immunology 69, 38–44.Google Scholar
Goulder, P. J., Sewell, A. K., Lalloo, D. G., Price, D. A., Whelan, J. A., Evans, J., Taylor, G. P., Luzzi, G., Giangrande, P., Phillips, R. E. and McMichael, A. J. ( 1997). Patterns of immunodominance in HIV-1-specific cytotoxic T lymphocyte responses in two human histocompatibility leukocyte antigens (HLA)-identical siblings with HLA-A*0201 are influenced by epitope mutation. Journal of Experimental Medicine 185, 1423–1433.CrossRefGoogle Scholar
Graham, S. P., Brown, D. J., Vatansever, Z., Waddington, D., Taylor, L. H., Nichani, A. K., Campbell, J. D., Adamson, R. E., Glass, E. J. and Spooner, R. L. ( 2001). Proinflammatory cytokine expression by Theileria annulata infected cell lines correlates with the pathology they cause in vivo. Vaccine 19, 2932–2944.CrossRefGoogle Scholar
Graham, S. P., Pelle, R., Honda, Y., Mwangi, D. M., Tonukari, N. J., Yamage, M., Glew, E. J., de Villiers, E. P., Shah, T., Bishop, R., Abuya, E., Awino, E., Gachanja, J., Luyai, A. E., Mbwika, F., Muthiani, A. M., Ndegwa, D. M., Njahira, M., Nyanjui, J. K., Onono, F. O., Osaso, J., Saya, R. M., Wildmann, C., Fraser, C. M., Maudlin, I., Gardner, M. J., Morzaria, S. P., Loosmore, S., Gilbert, S. C., Audonnet, J. C., van der, B. P., Nene, V. and Taracha, E. L. ( 2006). Theileria parva candidate vaccine antigens recognized by immune bovine cytotoxic T lymphocytes. Proceedings of the National Academy of Sciences, USA 103, 3286–3291.CrossRefGoogle Scholar
Hall, R., Boulter, N. R., Brown, C. G., Wilkie, G., Kirvar, E., Nene, V., Musoke, A. J., Glass, E. J. and Morzaria, S. P. ( 2000). Reciprocal cross-protection induced by sporozoite antigens SPAG-1 from Theileria annulata and p67 from Theileria parva. Parasite Immunology 22, 223–230.CrossRefGoogle Scholar
Hall, R., Hunt, P. D., Carrington, M., Simmons, D., Williamson, S., Mecham, R. P. and Tait, A. ( 1992). Mimicry of elastin repetitive motifs by Theileria annulata sporozoite surface antigen. Molecular and Biochemical Parasitology 53, 105–112.CrossRefGoogle Scholar
Heussler, V. T., Taracha, E. L., Musoke, A., Duchateau, L. and McKeever, D. J. ( 1998). Immunisation with live attenuated Salmonella dublin expressing a sporozoite protein confers partial protection against Theileria parva. Vaccine 16, 834–841.CrossRefGoogle Scholar
Honda, Y., Waithaka, M., Taracha, E. L. N., Duchateau, L., Musoke, A. J. and McKeever, D. J. ( 1998). Delivery of the Theileria parva p67 antigen to cattle using recombinant vaccinia virus: IL2 enhances protection. Vaccine 16, 1276–1282.CrossRefGoogle Scholar
Huang, S., Hendriks, W., Althage, A., Hemmi, S., Bluethmann, H., Kamijo, R., Vilcek, J., Zinkernagel, R. M. and Aguet, M. ( 1993). Immune response in mice that lack the interferon-gamma receptor. Science 259, 1742–1745.CrossRefGoogle Scholar
Hulliger, L., Wilde, J. H. K., Brown, C. G. D. and Turner, L. ( 1964). Mode of multiplication of Theileria in cultures of bovine lymphocytic cells. Nature 203, 728–730.CrossRefGoogle Scholar
Innes, E. A., Millar, P., Brown, C. G. and Spooner, R. L. ( 1989). The development and specificity of cytotoxic cells in cattle immunized with autologous or allogeneic Theileria annulata-infected lymphoblastoid cell lines. Parasite Immunology 11, 57–68.CrossRefGoogle Scholar
Irvin, A. D. and Morrison, W. I. ( 1987). Immunopathology, immunology and immunoprophylaxis of Theileria infections. In Immune Responses in Parasitic Infections: Immunology Immunopathology and Immunoprophylaxis ( ed. Soulsby, E. J. L.), CRC Press, Boca Raton, Florida, pp. 223–274.
Jefferies, C. A. and Fitzgerald, K. A. ( 2005). Interferon gene regulation: not all roads lead to Tolls. Trends in Molecular Medicine 11, 403–411.CrossRefGoogle Scholar
Kaba, S. A., Musoke, A. J., Schaap, D., Schetters, T., Rowlands, J., Vermeulen, A. N., Nene, V., Vlak, J. M. and van Oers, M. M. ( 2005). Novel baculovirus-derived p67 subunit vaccines efficacious against East Coast fever in cattle. Vaccine 23, 2791–2800.CrossRefGoogle Scholar
Kaba, S. A., Schaap, D., Roode, E. C., Nene, V., Musoke, A. J., Vlak, J. M. and van Oers, M. M. ( 2004). Improved immunogenicity of novel baculovirus-derived Theileria parva p67 subunit antigens. Veterinary Parasitology 121, 53–64.CrossRefGoogle Scholar
Kagi, D., Ledermann, B., Burki, K., Hengartner, H. and Zinkernagel, R. M. ( 1994). CD8+ T cell-mediated protection against an intracellular bacterium by perforin-dependent cytotoxicity. European Journal of Immunology 24, 3068–3072.CrossRefGoogle Scholar
Katzer, F., Carrington, M., Knight, P., Williamson, S., Tait, A., Morrison, W. I. and Hall, R. ( 1994). Polymorphism of spag-1, a candidate antigen for inclusion in a subunit vaccine against Theileria annulata. Molecular and Biochemical Parasitology 67, 1–10.Google Scholar
Knight, P. ( 1993). The characterisation of Theileria annulata sporozoite surface proteins. Ph.D. thesis, University of Glasgow.
Knight, P., Musoke, A. J., Gachanja, J. N., Nene, V., Katzer, F., Boulter, N., Hall, R., Brown, C. G. D., Williamson, S., Kirvar, E., Bell-Sakyi, L. and Hussain, K. ( 1996). Conservation of neutralizing determinants between the sporozoite surface antigens of Theileria annulata and Theileria parva. Experimental Parasitology 82, 229–241.CrossRefGoogle Scholar
McHardy, N., Wekesa, L. S., Hudson, A. T. and Randall, A. W. ( 1985). Anti-theilerial activity of BW720C (buparvaquone): a comparison with parvaquone. Research in Veterinary Science 39, 29–33.Google Scholar
McKeever, D. J. and Morrison, W. I. ( 2002). Epidemiological significance of strain-specific immunity to Theileria parva. In World Class Parasites: Volume 3. Theileria ( ed. Dirk Dobbelaere and Declan McKeever), Kluwer Academic Publishers, Boston. pp. 41–42.
McKeever, D. J. and Morrison, W. I. ( 1998). Novel vaccines against Theileria parva; prospects for sustainability. International Journal for Parasitology 28, 693–706.CrossRefGoogle Scholar
McKeever, D. J., Nyanjui, J. and Ballingall, K. T. ( 1997). In vitro infection with Theileria parva is associated with IL10 expression in all bovine lymphocyte lineages. Parasite Immunology 19, 319–324.CrossRefGoogle Scholar
McKeever, D. J., Taracha, E. L. N., Innes, E. A., MacHugh, N. D., Awino, E., Goddeeris, B. M. and Morrison, W. I. ( 1994). Adoptive transfer of immunity to Theileria parva in the CD8+ fraction of responding efferent lymph. Proceedings of the National Academy of Sciences, USA 91, 1959–1963.CrossRefGoogle Scholar
Medley, G. F., Perry, B. D. and Young, A. S. ( 1993). Preliminary analysis of the transmission dynamics of Theileria parva in eastern Africa. Parasitology 106, 251–264.CrossRefGoogle Scholar
Morrison, W. I. ( 1996). Influence of host and parasite genotypes on immunological control of Theileria parasites. Parasitology 112, S53–S66.Google Scholar
Morrison, W. I., Buscher, G., Murray, M., Emery, D. L., Masake, R. A., Cook, R. H. and Wells, P. W. ( 1981). Theileria parva: Kinetics of infection in the lymphoid system of cattle. Experimental Parasitology 52, 248–260.CrossRefGoogle Scholar
Morrison, W. I., Goddeeris, B. M., Teale, A. J., Groocock, C. M., Kemp, S. J. and Stagg, D. A. ( 1987). Cytotoxic T cells elicited in cattle challenged with Theileria parva (Muguga): evidence for restriction by class I MHC determinants and parasite strain specificity. Parasite Immunology 9, 563–578.CrossRefGoogle Scholar
Morrison, W. I. and McKeever, D. J. ( 1998). Immunology of infections with Theileria parva in cattle. In Immunology of Intracellular Parasitism ( ed. F. W. Liew and F. E. G. Cox), Chemical Immunology Vol. 70, pp. 163–185.
Morzaria, S. P., Irvin, A. D., Taracha, E., Spooner, P. R., Voigt, W. P., Fujinaga, T. and Katende, J. ( 1987 a). Immunization against East Coast fever: the use of selected stocks of Theileria parva for immunization of cattle exposed to field challenge. Veterinary Parasitology 23, 23–41.Google Scholar
Morzaria, S. P., Irvin, A. D., Voigt, W. P. and Taracha, E. L. ( 1987 b). Effect of timing and intensity of challenge following immunization against East Coast fever. Veterinary Parasitology 26, 29–41.Google Scholar
Muhammed, S. I., Lauerman, L. H. and Johnson, L. W. ( 1975). Effect of humoral antibodies on the course of Theileria parva infection (East Coast fever) of cattle. American Journal of Veterinary Research 36, 399–402.Google Scholar
Musoke, A., Morzaria, S., Nkonge, C., Jones, E. and Nene, V. ( 1992). A recombinant sporozoite surface antigen of Theileria parva induces protection in cattle. Proceedings of the National Academy of Sciences, USA. 89, 514–518.CrossRefGoogle Scholar
Musoke, A., Rowlands, J., Nene, V., Nyanjui, J., Katende, J., Spooner, P., Mwaura, S., Odongo, D., Nkonge, C., Mbogo, S., Bishop, R. and Morzaria, S. ( 2005). Subunit vaccine based on the p67 major surface protein of Theileria parva sporozoites reduces severity of infection derived from field tick challenge. Vaccine 23, 3084–3095.CrossRefGoogle Scholar
Musoke, A. J., Nantulya, V. M., Buscher, G., Masake, R. A. and Otim, B. ( 1982). Bovine immune response to Theileria parva: neutralizing antibodies to sporozoites. Immunology 45, 663–668.Google Scholar
Musoke, A. J., Nantulya, V. M., Rurangirwa, F. R. and Buscher, G. ( 1984). Evidence for a common protective antigenic determinant on sporozoites of several Theileria parva strains. Immunology 52, 231–238.Google Scholar
Musoke, A. J., Nene, V. and McKeever, D. J. ( 1995). Epitope specificity of bovine immune responses to the major surface antigen of Theileria parva sporozoites. In Molecular Approaches to the Control of Infectious Diseases ( ed. R. M. Chanock, F. Brown, H. S. Ginsberg and E. Norrby), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp. 57–61.
Ndungu, S. G., Brown, C. G. and Dolan, T. T. ( 2005). In vivo comparison of susceptibility between Bos indicus and Bos taurus cattle types to Theileria parva infection. Ondersteepoort Journal of Veterinary Research 72, 13–22.CrossRefGoogle Scholar
Nene, V., Gobright, E., Bishop, R., Morzaria, S. and Musoke, A. ( 1999). Linear peptide specificity of bovine antibody responses to p67 of Theileria parva and sequence diversity of sporozoite-neutralizing epitopes: implications for a vaccine. Infection and Immunity 67, 1261–1266.Google Scholar
Nene, V., Iams, K. P., Gobright, E. and Musoke, A. J. ( 1992). Characterisation of the gene encoding a candidate vaccine antigen of Theileria parva sporozoites. Molecular and Biochemical Parasitology 51, 17–28.CrossRefGoogle Scholar
Nene, V., Inumaru, S., McKeever, D. J., Morzaria, S., Shaw, M. and Musoke, A. J. ( 1995). Characterisation of an insect cell-derived Theileria parva sporozoite vaccine antigen and immunogenicity in cattle. Infection and Immunity 63, 503–508.Google Scholar
Nene, V., Musoke, A., Gobright, E. and Morzaria, S. ( 1996). Conservation of the sporozoite p67 vaccine antigen in cattle-derived Theileria parva stocks with different cross-immunity profiles. Infection and Immunity 64, 2056–2061.Google Scholar
Nichani, A. K., Campbell, J. D., Glass, E. J., Graham, S. P., Craigmile, S. C., Brown, C. G. and Spooner, R. L. ( 2003). Characterization of efferent lymph cells and their function following immunization of cattle with an allogenic Theileria annulata infected cell line. Veterinary Immunology and Immunopathology 93, 39–49.CrossRefGoogle Scholar
Nichani, A. K., Thorp, B. H., Brown, C. G., Campbell, J. D., Brown, D. J., Ritchie, M. and Spooner, R. L. ( 1999). In vivo development of Theileria annulata: major changes in efferent lymph following infection with sporozoites or allogeneic schizont-infected mononuclear cells. Parasitology 118, 327–333.CrossRefGoogle Scholar
Nickell, S. P. and Sharma, D. ( 2000). Trypanosoma cruzi: roles for perforin-dependent and perforin-independent immune mechanisms in acute resistance. Experimental Parasitology 94, 207–216.CrossRefGoogle Scholar
Pearson, T. W., Lundin, L. B., Dolan, T. T. and Stagg, D. A. ( 1979). Cell-mediated immunity to Theileria-transformed cell lines. Nature 281, 678–680.CrossRefGoogle Scholar
Pipano, E. ( 1974). Immunological aspects of Theileria annulata infection. Bulletin de l' Office International des Epizooties 81, 139–159.Google Scholar
Pipano, E. ( 1981). Schizonts and tick stages in immunisation against Theileria annulata infection. In Advances in the Control of Theileriosis. Current Topics in Veterinary Medicine and Animal Science ( ed. A. D. Irvin, M. P. Cunningham and A. S. Young), Martinus Nijhoff, The Netherlands, Vol. 14, 242–252.
Pipano, E. ( 1989). Vaccination against Theileria annulata theileriosis. In Veterinary Protozoan and Hemoparasite Vaccines ( ed. I. G. Wright), CRC Press, Boca Raton, pp. 203–234.
Pipano, E. and Tsur, I. ( 1966). Experimental Immunisation against Theileria annulata with a tissue culture vaccine. I. Laboratory trials. Refuah Veterinarith 23, 186–194.Google Scholar
Pirie, H. M., Jarrett, W. F. H. and Crighton, G. W. ( 1970). Studies on vaccination against East Coast fever using macroschizonts. Experimental Parasitology 27, 55–66.CrossRefGoogle Scholar
Preston, P. M. and Brown, C. G. ( 1988). Macrophage-mediated cytostasis and lymphocyte cytotoxicity in cattle immunized with Theileria annulata sporozoites or macroschizont-infected cell lines. Parasite Immunology 10, 631–647.CrossRefGoogle Scholar
Preston, P. M., Brown, C. G., Entrican, G., Richardson, W. and Boid, R. ( 1993). Synthesis of tumour necrosis factor-alpha and interferons by mononuclear cells from Theileria annulata-infected cattle. Parasite Immunology 15, 525–534.CrossRefGoogle Scholar
Preston, P. M., Brown, C. G. and Richardson, W. ( 1992). Cytokines inhibit the development of trophozoite-infected cells of Theileria annulata and Theileria parva but enhance the proliferation of macroschizont-infected cell lines. Parasite Immunology 14, 125–141.CrossRefGoogle Scholar
Preston, P. M., Hall, F. R., Glass, E. J., Campbell, J. D., Darghouth, M. A., Ahmed, J. S., Shiels, B. R., Spooner, R. L., Jongejan, F. and Brown, C. G. ( 1999). Innate and adaptive immune responses co-operate to protect cattle against Theileria annulata. Parasitology Today 15, 268–274.CrossRefGoogle Scholar
Radley, D. E., Brown, C. G. D., Burridge, M. J., Cunningham, M. P., Kirimi, I. M., Purnell, R. E. and Young, A. S. ( 1975 a). East Coast Fever. 1. Chemoprophylactic immunisation of cattle against Theileria parva (Muguga) and five Theileria strains. Veterinary Parasitology 1, 35–41.Google Scholar
Radley, D. E., Brown, C. G. D., Cunningham, M. P., Kimber, C. D., Musisi, F. L., Payne, R. C., Purnell, R. E., Stagg, D. A. and Young, A. S. ( 1975 b). East Coast fever: 3. Chemoprophylactic immunization of cattle using oxytetracycline and a combination of Theilerial strains. Veterinary Parasitology 1, 51–60.Google Scholar
Rose, M. E., Wakelin, D. and Hesketh, P. ( 1991). Interferon-gamma mediated effects upon immunity to coccidial infections in the mouse. Parasite Immunology 13, 63–74.CrossRefGoogle Scholar
Sager, H., Brunschwiler, C. and Jungi, T. W. ( 1998). Interferon production by Theileria annulata-transformed cell lines is restricted to the beta family. Parasite Immunology 20, 175–182.CrossRefGoogle Scholar
Schofield, L., Villaquiran, J., Ferreira, A., Schellekens, H., Nussenzweig, R. and Nussenzweig, V. ( 1987). Gamma interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites. Nature 330, 664–666.CrossRefGoogle Scholar
Sher, A. and Coffman, R. L. ( 1992). Regulation of immunity to parasites by T cells and T cell-derived cytokines. Annual Reviews of Immunology 10, 749–795.CrossRefGoogle Scholar
Shiels, B. R. ( 1999). Should I stay or should I go now? A stochastic model of stage differentiation in Theileria annulata. Parasitology Today 15, 241–245.CrossRefGoogle Scholar
Shiels, B. R., d'Oliveira, C., McKellar, S., Ben-Miled, L., Kawazu, S. and Hide, G. ( 1995). Selection of diversity at putative glycosylation sites in the immunodominant merozoite/piroplasm surface antigen of Theileria parasites. Molecular and Biochemical Parasitology 72, 149–162.CrossRefGoogle Scholar
Shiels, B. R., McKellar, S., Katzer, F., Lyons, K., Kinnaird, J., Ward, C., Wastling, J. M. and Swan, D. ( 2004). A Theileria annulata DNA binding protein localized to the host cell nucleus alters the phenotype of a bovine macrophage cell line. Eukaryotic Cell 3, 495–505.CrossRefGoogle Scholar
Skilton, R. A., Bishop, R. P., Katende, J. M., Mwaura, S. and Morzaria, S. P. ( 2002). The persistence of Theileria parva infection in cattle immunized using two stocks which differ in their ability to induce a carrier state: analysis using a novel blood spot PCR assay. Parasitology 124, 265–276.CrossRefGoogle Scholar
Spooner, R. L., Innes, E. A., Glass, E. J. and Brown, C. G. ( 1989). Theileria annulata and T. parva infect and transform different bovine mononuclear cells. Immunology 66, 284–288.Google Scholar
Spreull, J. ( 1914). East Coast fever inoculations in the Transkeian Territories, South Africa. Journal of Comparative Pathology and Therapeutics 27, 299–304.CrossRefGoogle Scholar
Stark, G. R., Kerr, I. M., Williams, B. R., Silverman, R. H. and Schreiber, R. D. ( 1998). How cells respond to interferons. Annual Reviews of Biochemistry 67, 227–264.CrossRefGoogle Scholar
Stephens, S. A. and Howard, C. J. ( 2002). Infection and transformation of dendritic cells from bovine afferent lymph by Theileria annulata. Parasitology 124, 485–493.CrossRefGoogle Scholar
Suzuki, Y., Orellana, M. A., Schreiber, R. D. and Remington, J. S. ( 1988). Interferon-gamma: the major mediator of resistance against Toxoplasma gondii. Science 240, 516–518.CrossRefGoogle Scholar
Swan, D. G., Phillips, K., Tait, A. and Shiels, B. R. ( 1999). Evidence for localisation of a Theileria parasite AT hook DNA-binding protein to the nucleus of immortalised bovine host cells. Molecular and Biochemical Parasitology 101, 117–129.CrossRefGoogle Scholar
Swan, D. G., Stern, R., McKellar, S., Phillips, K., Oura, C. A., Karagenc, T. I., Stadler, L. and Shiels, B. R. ( 2001). Characterisation of a cluster of genes encoding Theileria annulata AT hook DNA-binding proteins and evidence for localisation to the host cell nucleus. Journal of Cell Sciences 114, 2747–2754.Google Scholar
Takeda, K. and Akira, S. ( 2005). Toll-like receptors in innate immunity. International Immunology 17, 1–14.Google Scholar
Taracha, E. L., Awino, E. and McKeever, D. J. ( 1997). Distinct CD4+ T cell helper requirements in Theileria parva-immune and – naive bovine CTL precursors. Journal of Immunology 159, 4539–4545.Google Scholar
Taracha, E. L. N., Goddeeris, B. M., Morzaria, S. P. and Morrison, W. I. ( 1995 a). Parasite strain specificity of precursor cytotoxic T cells in individual animals correlates with cross-protection in cattle challenged with Theileria parva. Infection and Immunity 63, 1258–1262.Google Scholar
Taracha, E. L. N., Goddeeris, B. M., Scott, J. R. and Morrison, W. I. ( 1992). Standardization of a technique for analysing the frequency of parasite-specific cytotoxic T lymphocyte precursors in cattle immunized with Theileria parva. Parasite Immunology 14, 143–154.CrossRefGoogle Scholar
Taracha, E. L. N., Goddeeris, B. M., Teale, A. J., Kemp, S. J. and Morrison, W. I. ( 1995 b). Parasite strain specificity of bovine cytotoxic T cell responses to Theileria parva is determined primarily by immunodominance. Journal of Immunology 155, 4854–4860.Google Scholar
Theiler, A. ( 1911). The artificial transmission of East Coast fever. In Report of the Government Bacteriologist, Union of South Africa, 1909–1010. pp. 7–55.
Toye, P. G., Goddeeris, B. M., Iams, K., Musoke, A. J. and Morrison, W. I. ( 1991). Characterization of a polymorphic immunodominant molecule in sporozoites and schizonts of Theileria parva. Parasite Immunology 13, 49–62.CrossRefGoogle Scholar
Tsur, I. and Adler, S. ( 1965). The cultivation of lymphoid cells and Theileria annulata schizonts from infected bovine blood. Refuah Veterinarith 62, 225.Google Scholar
Uilenberg, G., Schreuder, B. E. C., Silayo, R. S. and Mpangala, C. ( 1976). Studies on theileriidae (Sporozoa) in Tanzania. IV. A field trial on immunisation against East Coast fever (Theileria parva infection in cattle). Tropenmedicin und Parasitologie 27, 329–336.Google Scholar
Visser, A. E., Abraham, A., Sakyi, L. J., Brown, C. G., Preston, P. M. ( 1995). Nitric oxide inhibits establishment of macroschizont-infected cell lines and is produced by macrophages of calves undergoing bovine tropical theileriosis or East Coast fever. Parasite Immunology 17, 91–102.CrossRefGoogle Scholar
Walker, A. R. and Fletcher, J. D. ( 1986). Histological study of the attachment site of adult Rhipicephalus appendiculatus on cattle. International Journal for Parasitology 16, 399–413.CrossRefGoogle Scholar
Walsh, C. M., Matloubian, M., Liu, C. C., Ueda, R., Kurahara, C. G., Christensen, J. L., Huang, M. T., Young, J. D., Ahmed, R. and Clark, W. R. ( 1994). Immune function in mice lacking the perforin gene. Proceedings of the National Academy of Sciences, USA 91, 10854–10858.CrossRefGoogle Scholar
Webster, P., Dobbelaere, D. A. E. and Fawcett, D. W. ( 1985). The entry of sporozoites of Theileria parva into bovine lymphocytes in vitro. Immunoelectron microscopic observations. European Journal of Cell Biology 36, 157–162.Google Scholar
Werling, D. and Jungi, T. W. ( 2003). TOLL-like receptors linking innate and adaptive immune response. Veterinary Immunology and Immunopathology 91, 1–12.CrossRefGoogle Scholar
White, D. W. and Harty, J. T. ( 1998). Perforin-deficient CD8+ T cells provide immunity to Listeria monocytogenes by a mechanism that is independent of CD95 and IFN-gamma but requires TNF-alpha. Journal of Immunology 160, 898–905.Google Scholar
Williamson, S., Tait, A., Brown, D., Walker, A., Beck, P., Shiels, B., Fletcher, J. and Hall, R. ( 1989). Theileria annulata sporozoite surface antigen expressed in Escherichia coli elicits neutralizing antibody. Proceedings of the National Academy of Sciences, USA 86, 4639–4643.CrossRefGoogle Scholar
Yarovinsky, F. and Sher, A. ( 2006). Toll-like receptor recognition of Toxoplasma gondii. International Journal for Parasitology 36, 255–259.CrossRefGoogle Scholar