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Theileria: intracellular protozoan parasites of wild and domestic ruminants transmitted by ixodid ticks

  • R. BISHOP (a1), A. MUSOKE (a1), S. MORZARIA (a1), M. GARDNER (a2) and V. NENE (a2)...
Abstract

Theileria are economically important, intra-cellular protozoa, transmitted by ixodid ticks, which infect wild and domestic ruminants. In the mammalian host, parasites infect leukocytes and erythrocytes. In the arthropod vector they develop in gut epithelial cells and salivary glands. All four intra-cellular stages of Theileria survive free in the cytoplasm. The schizont stages of certain Theileria species induce a unique, cancer-like, phenotype in infected host leukocytes. Theileria undergoes an obligate sexual cycle, involving fusion of gametes in the tick gut, to produce a transiently diploid zygote. The existence of sexual recombination in T. parva has been confirmed in the laboratory, and is presumed to contribute to the extensive polymorphism observed in field isolates. Key parameters in T. parva population dynamics are the relative importance of asymptomatic carrier cattle and animals undergoing severe disease, in transmission of the parasite to ticks, and the extent of transmission by nymphs as compared to adult ticks. Tick populations differ in vector competence for specific T. parva stocks. Recombinant forms of T. parva and T. annulata sporozoite surface antigens induce protection against parasite challenge in cattle. In future, vaccines might be improved by inclusion of tick peptides in multivalent vaccines.

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Corresponding author
Dr Richard Bishop, ILRI, P.O. Box 30709, Nairobi, Kenya. Tel: 254 2 630 743. Fax: 254 2 631 499. E-mail: R.Bishop@cgiar.org
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REFERENCES

ALLSOPP, B., BAYLIS, H. A., ALLSOPP, M. T. E. P., CAVALIER-SMITH, T., BISHOP, R. P., CARRINGTON, D. M., SOHANPAL, B. K. & SPOONER, P. R. ( 1993). Discrimination between six species of Theileria using oligonucleotide probes which detect small ribosomal RNA sequences. Parasitology 107, 157165.
ALLSOPP, B., CARRINGTON, M., BAYLISS, M. T., SOHAL, S., DOLAN, T. & IAMS, K. ( 1989). Improved characterisation of Theileria parva isolates using the polymerase chain reaction and oligonucleotide probes. Molecular and Biochemical Parasitology 35, 137148.
ALLSOPP, M. T. E. P., CAVALIER-SMITH, T., DE WAAL, D. T. & ALLSOPP, B. A. ( 1994). Phylogeny and evolution of the piroplasms. Parasitology 108, 147152.
ANDREWS, N. W. & WEBSTER, P. ( 1991). Phagolysomal escape by intracellular pathogens. Parasitology Today 7, 335340.
AWADALLA, P., WALLIKER, D., BABIKER, H. & MACKINNON, M. ( 2001). The question of Plasmodium falciparum population structure. Trends in Parasitology 17, 351353.
BABIKER, H., RANFORD-CARTWRIGHT, L., CURRIE, D., CHARLWOOD, J., BILLINGSLEY, P., TEUSCHER, T. & WALLIKER, D. ( 1994). Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology 109, 413421.
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. & NEWSON, J. ( 1988). Bovine T cells, B cells, and null cells are transformed by the protozoan parasite Theileria parva. Infection and Immunity 56, 462467.
BISHOP, R., GEYSEN, D., SKILTON, R., ODONGO, D., NENE, V., ALLSOPP, B., MBOGO, S., SPOONER, P. & MORZARIA, S. ( 2002). Genomic polymorphism, sexual recombination and molecular epidemiology of Theileria parva. In World Class Parasites: Volume 3, Theileria (ed. D. Mckeever & D. Dobbelaere), pp. 2340. Kluwer Academic Press, Boston, London.
BISHOP, R., NENE, V., STAEYERT, J., ROWLANDS, J., NYANJUI, J., OSASO, J., MORZARIA, S. & MUSOKE, A. ( 2003). Immunity to East Coast fever induced by a polypeptide fragment of the major surface coat of Theileria parva sporozoites. Vaccine 21, 12051212.
BISHOP, R. P., SOHANPAL, B. K., ALLSOPP, B. A., SPOONER, P. R., DOLAN, T. T. & MORZARIA, S. P. ( 1993). Detection of polymorphisms among Theileria parva stocks using repetitive, telomeric and ribosomal DNA probes and anti-schizont monoclonal antibodies. Parasitology 107, 1931.
BISHOP, R. P., SOHANPAL, B. K., MORZARIA, S. P., DOLAN, T. T., MWAKIMA, F. N. & YOUNG, A. S. ( 1994). Discrimination between Theileria parva and T. taurotragi in the salivary glands of Rhipicephalus appendiculatus ticks using oligonucleotides homologous to ribosomal RNA sequences. Parasitology Research 80, 259261.
BLOUIN, M. S., YOWELL, C. A., COURTENEY, C. H. & DAME, J. B. ( 1995). Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 10071014.
BOULTER, N. & HALL, R. ( 1999). Immunity and vaccine development against bovine theilerioses. Advances in Parasitology 44, 4197.
BUSCHER, G. & OTIM, B. ( 1986). Quantitative studies on Theileria parva in the salivary glands of Rhipicephalus appendiculatus adults: Quantitation and prediction of infection. International Journal for Parasitology 16, 93100.
CARRINGTON, M., ALLSOPP, B., BAYLIS, H., MALU, N. M., SHOCHAT, Y. & SOHAL, S. ( 1995). Lymphoproliferation caused by Theileria parva and Theileria annulata. In Molecular Approaches to Parasitology (ed. Boothroyd, J. C. and Komuniecki, R.), pp. 43526. New York, Wiley-Liss Inc.
CHAE, J. S., LEVY, M., HUNT, J. Jr., SCHLATER, J., SNIDER, G., WAGHELA, S. D., HOLMAN, P. J. & WAGNER, G. G. ( 1999). Theileria sp. infections associated with bovine fatalities in the United States confirmed by small-subunit rRNA gene analyses of blood and tick samples. Journal of Clinical Microbiology 37, 30373040.
CONRAD, P. A., STAGG, D. A., GROOTENHUIS, J. G., IRVIN, A. D., NEWSON, R. M., NJAMMUNGEH, R. E. G., ROSSITER, P. B. & YOUNG, A. S. ( 1987). Isolation of Theileria parasites from African buffalo (Syncercus caffer) and characterization with anti-schizont monoclonal antibodies. Parasitology 94, 413423.
DAY, K. P., KOELLA, J. C., NEE, S., GUPTA, S. & READ, A. F. ( 1992). Population genetics and dynamics of Plasmodium falciparum: an ecological view. Parasitology 104, S35S52.
DIMOPOULOS, G. ( 2003). Insect immunity and its implication in mosquito-malaria interactions. Cellular Microbiology 5, 314.
DOBBELAERE, D. A. E., SPOONER, P. R., BARRY, W. C. & IRVIN, A. D. ( 1984). Monoclonal antibodies neutralise the sporozoite stage of different Theileria parva stocks. Parasite Immunology 6, 361370.
EBEL, T., MIDDLETON, J. F. S., FRISCH, A. & LIPP, J. ( 1997). Characterization of a secretory type Theileria parva glutaredoxin homologue identified by novel screening procedures. Journal of Biological Chemistry 272, 30423048.
FAWCETT, D. W., DOXSEY, S. & BUSCHER, G. ( 1982). Salivary glands of the tick vector of East Coast fever: III. Ultrastructure of sporogony in Theileria parva. Tissue & Cell 14, 183206.
FELL, A. H., PRESTON, P. M. & ANSELL, J. D. ( 1990). Establishment of Theileria-infected bovine cell lines in SCID mice. Parasite Immunology 12, 335339.
HEUSSLER, V. T. ( 2002). Theileria survival strategies and host cell transformation. In World Class Parasites: Volume 3, Theileria ( ed. Dobbelaere, D. A. E. & McKeever, D. J.), pp 6984. Kluwer Academic Publishers, Boston.
HEUSSLER, V. T., ROTTENBERG, S., SCHWAB, R., KUENZI, P., FERNANDEZ, P. C., McKELLAR, S., SHIELS, B., CHEN, Z. J., ORTH, K., WALLACH, D. & DOBBELAERE, D. A. E. ( 2002). Highjacking of host cell IKK signalosomes by the transforming parasite Theileria. Science 288, 10331038.
GAUER, M., MACKENSTEDT, U., MEHLHORN, H., SCHEIN, E., ZAPF, F., NJENGA, E., YOUNG, A. & MORZARIA, S. ( 1995). DNA measurements and ploidy determination of developmental stages in the life cycles of Theileria annulata and T. parva. Parasitology Research 81, 565574.
GOUGH, J. M., JORGENSEN, W. K. & KEMP, D. H. ( 1998). Development of tick gut forms of Babesia bigemina in vitro. Journal of Eukaryotic Microbiology 45, 298306.
IAMS, K. P., YOUNG, J. R., NENE, V., DESAI, J., WEBSTER, P., OLE-MOIYOI, O. K. & MUSOKE, A. J. ( 1990). Characterisation of the gene encoding a 104-kilodalton microneme-rhoptry protein of Theileria parva. Molecular and Biological Parasitology 39, 4760.
IRVIN, A. D., BROWN, C. G., KANHAI, G. K. & STAGG, D. A. ( 1975). Comparative growth of bovine lymphosarcoma cells and lymphoid cells infected with Theileria parva in athymic (nude) mice. Nature 255, 713714.
IRVIN, A. D., OCAMA, J. G. & SPOONER, P. R. ( 1982). Cycle of bovine lymphoblastoid cells parasitised by Theileria parva. Research in Veterinary Science 33, 298304.
JANOO, R., MUSOKE, A., WELLS, C. & BISHOP, R. P. ( 1999). A Rab 1 homologue with a novel isoprenylation signal provides insight into the secretory pathway of Theileria parva. Molecular and Biochemical Parasitology 102, 131143.
KATZER, F., CARRINGTON, M. & KNIGHT, P. ( 1994). Polymorphism of SPAG-1, a candidate antigen for inclusion in a sub-unit vaccine against Theileria annulata. Molecular and Biochemical Parasitology 67, 110.
KNIGHT, P. A., 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., HUSSAIN, A. & TAIT, A. ( 1996). Conservation of neutralizing determinants between the sporozoite surface antigens of Theileria annulata and Theileria parva. Experimental Parasitology 82, 229241.
MEDLEY, G. F., PERRY, B. D. & YOUNG, A. S. ( 1993). Preliminary analysis of the transmission dynamics of Theileria parva in eastern Africa. Parasitology 106, 251264.
MEHLHORN, H. & SCHEIN, E. ( 1984). The piroplasms: Life cycle and sexual stages. Advances in Parasitology 23, 37103.
MORZARIA, S. P. & YOUNG, J. R. ( 1992). Restriction mapping of the genome of the protozoan parasite Theileria parva. Proceedings of the National Academy of Sciences, USA 89, 52415245.
MORZARIA, S. P., YOUNG, J. R., SPOONER, P. R., DOLAN, T. T. & BISHOP, R. P. ( 1993). Theileria parva: A restriction map and genetic recombination. In Genome Analysis of Protozoan Parasites (ed. Mozaria, S. P.), pp. 6773. Nairobi, ILRAD.
MUKHEBI, A. W., PERRY, B. D. & KRUSKA, R. ( 1992). Estimated economics of theileriosis control in Africa. Preventive Veterinary Medicine 12, 7385.
MUSOKE, A. J., MORZARIA, S., NKONGE, C., JONES, E. & NENE, V. ( 1992). A recombinant sporozoite surface antigen of Theileria parva induces protection in cattle. Proceedings of the National Academy of Sciences, USA 89, 514518.
MUSOKE, A. J., NANTULYA, V. M., RURANGIRA, F. R. & BUSCHER, G. ( 1984). Evidence for a common protective antigenic determinant on sporozoites of several Theileria parva strains. Immunology 52, 231238.
NENE, V., BISHOP, R. P., MORZARIA, S., GARDNER, M. J., SUGIMOTO, C., OLE-MOIYOI, O. K., FRASER, C. M. & IRVIN, A. ( 2000). Theileria parva genomics reveals an atypical apicomplexan genome. International Journal for Parasitology 30, 465474.
NENE, V., BISHOP, R., QUACKENBUSH, J., PERTEA, M., SALZBURG, S. L., TARACHA, E., MORZARIA, S., FRASER, C. M. & GARDNER, M. ( 2002). Genomics of Theileria parva. In World Class Parasites: Volume 3, Theileria (ed. Dobbelaere, D. A. E. & McKeever, D. J.), pp. 8592. Kluwer Academic Publishers, Boston, London.
NENE, V., GOBRIGHT, E., BISHOP, R., MORZARIA, S. & MUSOKE, A. ( 1999). Linear peptide specificity of antibody responses to p67 and sequence diversity of neutralising epitopes: implications for a Theileria parva vaccine. Infection and Immunity 67, 12611266.
NENE, V., IAMS, K. P., GOBRIGHT, E. & MUSOKE, A. J. ( 1992). Characterisation of the gene encoding a candidate vaccine antigen of Theileria parva sporozoites. Molecular and Biochemical Parasitology 51, 1728.
NENE, V., INUMARU, S., McKEEVER, D. J., MORZARIA, S. P. & SHAW, M. & MUSOKE, A. J. ( 1995). Characterization of an insect cell-derived Theileria parva sporozoite vaccine antigen and immunogenicity in cattle. Infection and Immunity 63, 503508.
NENE, V., MUSOKE, A., GOBRIGHT, E. & 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, 20562061.
NENE, V., MORZARIA, S. & BISHOP, R. P. ( 1998). Organisation and informational content of the Theileria parva genome. Molecular and Biochemical Parasitology 95, 18.
NGUMI, P. N., LESAN, A. C., WILLIAMSON, S. M., AWICH, J. R., MORZARIA, S. P., DOLAN, T. T., SHAW, M. K. & YOUNG, A. S. ( 1994). Isolation and preliminary characterisation of a previously unidentified Theileria parasite of cattle in Kenya. Research in Veterinary Science 57, 19.
NORVAL, R. A. I., PERRY, B. D. & YOUNG, A. S. ( 1992). The Epidemiology of Theileriosis in Africa. 1st edn. London, Academic Press.
OCHANDA, H., YOUNG, A. S., MEDLEY, G. F. & PERRY, B. D. ( 1998). Vector competence of 7 rhipicephalid tick stocks in transmitting 2 Theileria parva parasite stocks from Kenya and Zimbabwe. Parasitology 116, 539545.
OCHANDA, H., YOUNG, A. S., WELLS, C., MEDLEY, G. F. & PERRY, B. D. ( 1996). Comparison of the transmission of Theileria parva between different instars of Rhipicephalus appendiculatus. Parasitology 113, 243253.
OLE-MOIYOI, O. K. ( 1995). Casein kinase II in theileriosis. Science 267, 834.
OLE-MOIYOI, O. K., BROWN, W. C., IAMS, K. P., NAYAR, A., TSUKAMOTO, T. & MACKLIN, M. D. ( 1993). Evidence for the induction of casein kinase II in bovine lymphocytes transformed by the intracellular protozoan parasite Theileria parva. EMBO Journal 12, 16211631.
PAUL, R. E. L. & DAY, K. P. ( 1998). Mating patterns of Plasmodium falciparum. Parasitology Today 14, 197202.
PAUL, R., PACKER, M., WALMSLEY, M., LAGOG, M., RANFORD- CARTWRIGHT, L., PARU, R. & DAY, K. ( 1995). Mating patterns in Malaria parasite populations of Papua New Guinea. Science 269, 17091711.
RADLEY, D. E., BROWN, C. G. D., BURRIDGE, M. P., KIRIMI, I. M., PURNELL, R. E. & YOUNG, A. S. ( 1975). East Coast fever. 1. Chemoprophylatic immunization of cattle against Theileria parva (Muguga) and five theilerial strains. Veterinary Parasitology 1, 3541.
RUDZINSKA, M. A., LEWENGRUB, S., SPIELMAN, A. & PIESMA, J. ( 1983). Invasion of Babesia microti into epithelial cells of the tick gut. Journal of Protozoology 30, 338346.
SCHNITTGER, L., HONG, Y., JIANXUN, L., LUDWIG, W., SHAYAN, P., RAHBARI, S., VOSS-HOLTMANN, A. & AHMED, J. S. ( 2000). Phylogenetic analysis by rRNA comparison of the highly pathogenic sheep-infecting parasites Theileria lestoquardi and a Theileria species identified in China. Annals of New York Academy of Sciences 916, 271275.
SELDIN, D. C. & LEDER, P. ( 1995). Casein kinase α transgene-induced murine lymphoma: relation to Theileriosis in cattle. Science 267, 894897.
SHAW, M. K. ( 1997). The same but different: the biology of Theileria sporozoite entry into bovine cells. International Journal for Parasitology 27, 457474.
SHAW, M. K. ( 2002). Theileria development and host cell invasion. In World Class Parasites: Volume 3, Theileria ( ed. Dobbelaere, D. A. E. & McKeever, D. J.), pp. 122. Kluwer Academic Publishers, Boston, London.
SHAW, M. K. & TILNEY, L. G. ( 1992). How individual cells develop from a syncytium: merogony in Theileria parva (Apicomplexa). Journal of Cell Science 101, 109123.
SHAW, M. K., TILNEY, L. G. & McKEEVER, D. J. ( 1993). Tick salivary gland extract and Interlukeukin-2 stimulation enhance susceptibility of lymphocytes to infection by Theileria parva sporozoites. Infection and Immunity 61, 14861495.
SHAW, M. K., TILNEY, L. G. & MUSOKE, A. J. ( 1991). The entry of Theileria parva sporozoites into bovine lymphocytes: evidence for MHC Class I involvement. Journal of Cell Biology 113, 87101.
SHAW, M. K. & YOUNG, A. S. ( 1994). The biology of Theileria species in ixodid ticks in relation to parasite transmission. Advances in Disease Vector Research 10, 2363.
SINDEN, R. E., BUTCHER, G. A., BILLKER, O. & FLECK, S. L. ( 1996). Regulation of infectivity of Plasmodium to the mosquito vector. Advances in Parasitology 38, 53117.
SKILTON, R. A., BISHOP, R. P., KATENDE, J. M., MWAURA, S. & 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, 265276.
SKILTON, R. A., BISHOP, R. P., WELLS, C. W., SPOONER, P. R., GOBRIGHT, E., NKONGE, C. N., MUSOKE, A. J., MACKLIN, M. & IAMS, K. P. ( 1998). Cloning and characterisation of a 150 kDa microsphere antigen of Theileria parva that is immunologically cross-reactive with the polymorphic immunodominant molecule (PIM). Parasitology 117, 321330.
SKILTON, R. A., MUSOKE, A. J., NENE, V., WASAWO, D. P. S., WELLS, C. W., SPOONER, P. R., BISHOP, R. P., OSASO, J., NKONGE, C., LATIF, A. & MORZARIA, S. P. ( 2000). Molecular characterisation of a Theileria lestoquardi gene encoding a candidate sporozoite vaccine antigen. Molecular and Biochemical Parasitology 107, 309314.
STAGG, D. A., YOUNG, A. S., LEITCH, B. L., GROOTENHUIS, J. G. & DOLAN, T. T. ( 1983). Infection of mammalian cells with Theileria species. Parasitology 86, 243254.
TATCHELL, R. J. ( 1987). Tick control in the context of ECF immunization. Parasitology Today 3, 710.
WALKER, A. R., LATIF, A. A., MORZARIA, S. P. & JONGEHAN, F. ( 1983). Natural infection rate of Hyalomma anatolicum with Theileria in Sudan. Research in Veterinary Science 35, 8790.
WATT, D. M., WALKER, A. R., LAMZA, K. A. & AMBROSE, N. C. ( 2001). Tick–Theileria interactions in response to immune activation of the vector. Experimental Parasitology 97, 8994.
WILSON, R. J. M. & WILLIAMSON, D. H. ( 1997). Extrachromosomal DNA in the Apicomplexa. Microbiology and Molecular Biology Reviews 61, 116.
YOUNG, A. S., DOLAN, T. T., MORZARIA, S. P., MWAKIMA, F. N., NORVAL, R. A. I., SCOTT, J. S., SHERRIFF, A. & GETTINBY, G. ( 1996). Factors influencing infections in Rhipicephalus appendiculatus ticks fed on cattle infected with Theileria parva. Parasitology 113, 255266.
YOUNG, A. S., DOLAN, T. T., MWAKIMA, F. N., OCHANDA, H., MWAURA, S. N., NJIHIA, G. M., MUTHONI, M. W. & DOLAN, R. B. ( 1995). Estimation of heritability of susceptibility to infection with Theileria parva in the tick Rhipicephalus appendiculatus. Parasitology 111, 3138.
YOUNG, A. S., LEITCH, B. L., NEWSON, R. L. & CUNNINGHAM, P. M. ( 1986). Maintenance of Theileria parva parva infections in an endemic area of Kenya. Parasitology 93, 916.
YOUNG, A. S. & LEITCH, B. L. ( 1982). Epidemiology of East Coast fever: some effects of temperature on the development of Theileria parva in the tick vector, Rhipicephalus appendiculatus. Parasitology 83, 199211.
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