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Progress towards understanding the immunobiology of Theileria parasites

Published online by Cambridge University Press:  20 August 2009

W. IVAN MORRISON
W. IVAN MORRISON*
Affiliation:
The Roslin Institute, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK
*
*Corresponding author: Tel: (0)131 650 6216. E-mail: [email protected]
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Summary

The pathogenic Theileria species Theileria parva and T. annulata infect bovine leukocytes and erythrocytes causing acute, often fatal lymphoproliferative diseases in cattle. The parasites are of interest not only because of their economic importance as pathogens, but also because of their unique ability to transform the leukocytes they infect. The latter property allows parasitized leukocytes to be cultured as continuously growing cell lines in vitro, thus providing an amenable in vitro system to study the parasite/host cell relationship and parasite-specific cellular immune responses. This paper summarizes important advances in knowledge of the immunobiology of these parasites over the last 40 years, focusing particularly on areas of relevance to vaccination.

Keywords

Theileriacell biologyCD8 T cellantigenic diversityimmunodominancevaccination
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 12: Special Centenary Issue – Parasitology 1908–2008 , October 2009 , pp. 1415 - 1426
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

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., Malu, M. N., Kinuthia, S. W., Conrad, P. A. and Grootenhuis, J. G. (1986). Comparative analysis of infection and transformation of lymphocytes from African buffalo and Boran cattle with Theileria parva subsp. parva and T. parva subsp. lawrencei. Infection and Immunity 53, 186–191.CrossRefGoogle Scholar
Bishop, R., Shah, T., Pelle, R., Hoyle, D., Pearson, T., Haines, L., Brass, A., Hulme, H., Graham, S. P., Taracha, E. L., Kanga, S., Lu, C., Hass, B., Wortman, J., White, O., Gardner, M. J., Nene, V. and de Villiers, E. P. (2005). Analysis of the transcriptome of the protozoan Theileria parva using MPSS reveals that the majority of genes are transcriptionally active in the schizont stage. Nucleic Acids Research 33, 5503–5511.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, London 245, 101–103.Google Scholar
Connelley, T., MacHugh, N. D., Burrells, A. and Morrison, W. I. (2008). Dissection of the clonal composition of bovine alpha beta T cell responses using T cell receptor Vbeta subfamily-specific PCR and heteroduplex analysis. Journal of Immunological Methods, 335, 28–40.Google Scholar
Cranefield, P. F. (1991). Science and Empire: East Coast Fever in Rhodesia and the Transvaal. Cambridge University Press, Cambridge, UK.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.Google 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.Google Scholar
De Plaen, E., Lurquin, C., Lethe, B., van der, B. P., Brichard, V., Renauld, J. C., Coulie, P., Van, P. A. and Boon, T. (1997). Identification of genes coding for tumor antigens recognized by cytolytic T lymphocytes. Methods 12, 125–142.Google Scholar
Dessauge, F., Lizundia, R., Baumgartner, M., Chaussepied, M. and Langsley, G. (2005). Taking the Myc is bad for Theileria. Trends in Parasitology 21, 377–385.CrossRefGoogle ScholarPubMed
Dobbelaere, D. A. and Küenzi, P. (2004). The strategies of the Theileria parasite: a new twist in host-pathogen interactions. Current Opinions in Immunology 16, 525–530.Google 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 ScholarPubMed
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.Google Scholar
Dschunkowsky, E. and Luhs, J. (1904). Die Piroplasmen der Rinder. Zentralblatt für Bacteriologie, Parasitenkunde und Infektionskrankheiten 35, 486–492.Google 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., MacHugh, N. D. and Morrison, W. I. (1988). Theileria parva (Muguga) infects bovine T-lymphocytes in vivo and induces co-expression of BoT4 and BoT8. Parasite Immunology 10, 379–391.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, London 290, 251–254.CrossRefGoogle ScholarPubMed
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.Google Scholar
Glass, E. J., Preston, P. M., Springbett, A., Craigmile, S., Kirvar, E., Wilkie, G. and Brown, C. G. D. (2005). Bos taurus and Bos indicus (Sahiwal) calves respond differently to infection with Theileria annulata and produce markedly different levels of acute phase proteins. International Journal for Parasitology 35, 337–347.CrossRefGoogle ScholarPubMed
Goddeeris, B. M., Morrison, W. I., Teale, A. J., Bensaid, A. and Baldwin, C. L. (1986). 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
Graham, S. P., Honda, Y., Pellé, R., Mwangi, D. M., Glew, E. J., de Villiers, E. P., Shah, T., Bishop, R., van der Bruggen, P., Nene, V. and Taracha, E. L. (2007). A novel strategy for the identification of antigens that are recognised by bovine MHC class I restricted cytotoxic T cells in a protozoan infection using reverse vaccinology. Immunome Research 3, 2.Google 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 Bruggen, 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.Google Scholar
Graham, S. P., Pellé, R., Yamage, M., Mwangi, D. M., Honda, Y., Mwakubambanya, R., de Villiers, E., Abuya, E., Awino, E., Gachanja, J., Mbwika, F., Muthiani, A. M., Muriuki, C., Nyanjui, J. K., Onono, F. O., Osaso, J., Riitho, V., Saya, R. M., Ellis, S. A., McKeever, D. J., MacHugh, N. D., Gilbert, S. C., Audonnet, J. C., Morrison, W. I., van der Bruggen, P. and Taracha, E. L. (2008). Characterization of the fine specificity of bovine CD8 T cell responses to defined antigens from the protozoan parasite Theileria parva. Infection and Immunity 76, 685–694.Google Scholar
Guergnon, J., Chaussepied, M., Sopp, P., Lizundia, R., Moreau, M. F., Blumen, B., Werling, D., Howard, C. J. and Langsley, G. (2003). A tumour necrosis factor alpha autocrine loop contributes to proliferation and nuclear factor-kappa B activation of Theileria parva-transformed B cells. Cell Microbiology 5, 709–716.Google 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.Google 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 ScholarPubMed
Heussler, V. T., Rottenberg, S., Schwab, R., Küenzi, P., Fernandez, P. C., McKellar, S., Shiels, B., Chen, Z. J., Orth, K., Wallach, D. and Dobbelaere, D. A. (2002). Hijacking of host cell IKK signalosomes by the transforming parasite Theileria. Science 298, 1033–1036.Google Scholar
Heussler, V., Sturm, A. and Langsley, G. (2006). Regulation of host cell survival by intracellular Plasmodium and Theileria parasites. Parasitology 132, S49–S60.Google Scholar
Houston, E. F., Taracha, E. L., Brackenbury, L., MacHugh, N. D., McKeever, D. J., Charleston, B. and Morrison, W. I. (2008). Infection of cattle with Theileria parva induces an early CD8 T cell response lacking appropriate effector function. International Journal for Parasitology 38, 1693–1704.CrossRefGoogle ScholarPubMed
Hulliger, L. (1965). Cultivation of three species of Theileria in lymphoid cells in vitro. Journal of Protozoology 12, 649–655.Google 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, London 203, 728–730.Google Scholar
Kaba, S. A., Musoke, A. J., Schaap, D., Schletters, 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.Google Scholar
Katzer, F., Ngugi, D., Oura, C., Bishop, R. P., Taracha, E. L. N., Walker, A. R. and McKeever, D. J. (2006). Extensive genetic diversity in a recombining population of the apicomplexan parasite Theileria parva. Infection and Immunity 74, 5456–5464.Google Scholar
Lizundia, R., Chaussepied, M., Huerre, M., Werling, D., Di Santo, J. P. and Langsley, G. (2006). c-Jun NH2-terminal kinase/c-Jun signaling promotes survival and metastasis of B lymphocytes transformed by Theileria. Cancer Research 66, 6105–6110.Google Scholar
MacHugh, N. D., Connelley, T., Graham, S. P., Pelle, R., Formisano, P., Taracha, E. L., Ellis, S. A, McKeever, D. J., Burrells, A. and Morrison, W. I. (2009). CD8 T cell responses to Theileria parva are preferentially directed to a single dominant antigen: Implications for parasite strain-specific immunity. European Journal of Immunology (in the Press).CrossRefGoogle ScholarPubMed
McKeever, D. J., Nyanjui, J. K. 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.Google 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 ScholarPubMed
Melhorn, H. and Schein, E. (1984). The piroplasms: Life cycle and sexual stages. Advances in Parasitology 23, 37–103.Google Scholar
Morrison, W. I. (2007). The biological and practical significance of antigenic variability in protective immune responses against Theileria parva. Veterinary Parasitology 148, 21–30.Google 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 ScholarPubMed
Morrison, W. I., MacHugh, N. D. and Lalor, P. A. (1996). Pathogenicity of Theileria parva is influenced by the host cell type infected by the parasite. Infection and Immunity 64, 557–562.Google Scholar
Morrison, W. I. and McKeever, D. J. (2006). Current status of vaccine development against Theileria parasites. Parasitology 133, S169–S187.Google Scholar
Morzaria, S. P., Dolan, T. T., Norval, R. A., Bishop, R. P. and Spooner, P. R. (1995). Generation and characterization of cloned Theileria parva parasites. Parasitology 111, 39–49.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.Google 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., 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.Google Scholar
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.Google ScholarPubMed
Neitz, W. O., Canham, A. S. and Kluge, E. B. (1955). Corridor disease: A fatal form of bovine theileriosis encountered in Zululand. Journal of the South African Veterinary Medical Association 26, 79–87.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.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., Craigmile, S. C., Spooner, R. L. and Campbell, J. D. M. (1998). Diminished IL-2 and alteration of CD2 expression on CD8+ T cells are associated with a lack of cytotoxic T cell responses during Theileria annulata infection. Clinical and Experimental Immunology 116, 316–321.Google Scholar
Odongo, D. O., Oura, C. A. L., Spooner, P. R., Kiara, H., Mburu, D., Hanotte, O. H. and Bishop, R. P. (2006). Linkage disequilibrium between alleles at highly polymorphic mini- and micro-satellite loci of Theileria parva isolated from cattle in three regions of Kenya. International Journal for Parasitology 36, 937–946.Google Scholar
Oura, C. A. L., Asiimwe, B. B., Weir, W., Lubega, G. W. and Tait, A. (2005). Population genetic analysis and sub-structuring of Theileria parva in Uganda. Molecular and Biochemical Parasitology 140, 229–239.CrossRefGoogle ScholarPubMed
Oura, C. A., Bishop, R., Asiimwe, B. B., Spooner, P., Lubega, G. W. and Tait, A. (2007). Theileria parva live vaccination: parasite transmission, persistence and heterologous challenge in the field. Parasitology 134, 1205–1213.CrossRefGoogle ScholarPubMed
Oura, C. A., Odongo, D. O., Lubega, G. W., Spooner, P. R., Tait, A. and Bishop, R. P. (2003). A panel of microsatellite and minisatellite markers for the characterisation of field isolates of Theileria parva. International Journal for Parasitology 33, 1641–1653.Google Scholar
Pain, A., Renauld, H., Berriman, M., Murphy, L., Yeats, C. A., Weir, W., Kerhornou, A., Aslett, M., Bishop, R., Bouchier, C., Cochet, M., Coulson, R. M., Cronin, A., de Villiers, E. P., Fraser, A., Fosker, N., Gardner, M., Goble, A., Griffiths-Jones, S., Harris, D. E., Katzer, F., Larke, N., Lord, A., Maser, P., McKellar, S., Mooney, P., Morton, F., Nene, V., O'Neil, S., Price, C., Quail, M. A., Rabbinowitsch, E., Rawlings, N. D., Rutter, S., Saunders, D., Seeger, K., Shah, T., Squares, R., Squares, S., Tivey, A., Walker, A. R., Woodward, J., Dobbelaere, D. A., Langsley, G., Rajandream, M. A., McKeever, D., Shiels, B., Tait, A., Barrell, B. and Hall, N. (2005). Genome of the host-cell transforming parasite Theileria annulata compared to T. parva. Science 309, 131–133.Google Scholar
Palmer, G. H., Machado, J. Jr., Fernandez, P., Heussler, V., Perinat, T. and Dobbelaere, D. A. (1997). Parasite-mediated nuclear factor kappaB regulation in lymphoproliferation caused by Theileria parva infection. Proceedings of the National Academy of Sciences, USA 94, 12527–12532.Google Scholar
Pearson, T. W., Lundin, L. B., Dolan, T. T. and Stagg, D. A. (1979). Cell-mediated immunity to Theileria-transformed cell lines. Nature, London 281, 678–680.Google Scholar
Pipano, E. (1974). Immunological aspects of Theileria annulata infection. Bulletin Office Internationale Epizootique 81, 139–159.Google Scholar
Pipano, E. (1989). Vaccination against Theileria annulata theileriosis. In Veterinary Protozoan and Hemoparasite Vaccines (ed. Wright, I. G.), pp. 203–234. CRC Press, Boca Raton, FL, USA.Google Scholar
Pipano, E. and Tsur, I. (1966). Experimental immunisation against Theileria annulata with a tissue culture vaccine. I. Laboratory trials. Refuah Veterinarian 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.Google 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
Sager, H., Bertoni, G. and Jungi, T. W. (1998 a). Differences between B cell and macrophage transformation by the bovine parasite, Theileria annulata: A clonal approach. Journal of Immunology 161, 335–341.Google Scholar
Sager, H., Brunschwiler, C. and Jungi, T. W. (1998 b). Interferon production by Theileria annulata-transformed cell lines is restricted to the beta family. Parasite Immunology 20, 175–182.CrossRefGoogle Scholar
Sager, H., Davis, W. C., Dobbelaere, D. A. and Jungi, T. W. (1997). Macrophage-parasite relationship in theileriosis. Reversible phenotypic and functional dedifferentiation of macrophages infected with Theileria annulata. Journal of Leukocyte Biology 61, 459–468.Google Scholar
Schmuckli-Maurer, J., Casanova, C., Schmied, S., Affentranger, S., Parvanova, I., Kang'a, S., Nene, V., Katzer, F., McKeever, D., Müller, J., Bishop, R., Pain, A. and Dobbelaere, D. A. (2009). Expression analysis of the Theileria parva subtelomere-encoded variable secreted protein gene family. PLos ONE 4, e4839.Google Scholar
Schreuder, B. E. C., Uilenberg, G. and Tondeur, W. (1977). Studies on Theileriidae (Sporozoa) in Tanzania. VIII. Experiments with African buffalo (Syncerus caffer). Tropenmedizin und Parasitologie 28, 367–371.Google ScholarPubMed
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.Google 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
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.Google Scholar
Swan, D. G., Stadler, L., Okan, E., Hoffs, M., Katzer, F., Kinnaird, J., McKellar, S. and Shiels, B. R. (2003). TashHN, a Theileria annulata encoded protein transported to the host nucleus displays an association with attenuation of parasite differentiation. Cellular Microbiology 5, 947–956.Google Scholar
Swan, D. G., Phillips, K., Mckellar, S., Hamilton, C. and Shiels, B. R. (2001 a). Temporal co-ordination of macroschizont and merozoite gene expression during stage differentiation of Theileria annulata. Molecular and Biochemical Parasitology 113, 233–239.Google Scholar
Swan, D. G., Stern, R., McKellar, S., Phillips, K., Oura, C. A., Karagenc, T. I., Stadler, L. and Shiels, B. R. (2001 b). 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 Science 114, 2747–2754.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.Google 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.CrossRefGoogle ScholarPubMed
Theiler, A. (1903). The Rhodesian tick fever. Transvaal Agricultural Journal 1, 93–110.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). Tropenmedizin und Parasitologie 27, 329–336.Google 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
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 ScholarPubMed
Yewdell, J. W. (2006). Confronting complexity: Real-world immunodominance in antiviral CD8+ T cell responses. Immunity 25, 533–543.Google Scholar
Young, A. S., Radley, D. E., Cunningham, M. P., Musisi, F. L., Payne, R. C. and Purnell, R. E. (1977). Exposure of immunised cattle to prolonged natural challenge of Theileria lawrencei derived from African buffalo (Syncerus caffer). Veterinary Parasitology 3, 283–290.Google Scholar