Skip to main content Accessibility help
×
Home
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 2
  • Print publication year: 2008
  • Online publication date: August 2009

14 - Theileria: life cycle stages associated with the ixodid tick vector

    • By R. Bishop, International Livestock Research Institute (ILRI) P.O. Box 30709 Nairobi 00100 Kenya, A. Musoke, Onderstepoort Veterinary Institute Private Bag X5 Onderstepoort 0110 South Africa, R. Skilton, International Livestock Research Institute (ILRI) P.O. Box 30709 Nairobi 00100 Kenya, S. Morzaria, Food and Agriculture Organization (FAO) 39 Phra Atit Road Bangkok 10200 Thailand, M. Gardner, Seattle Biomedical Research Institute 307 Westlake Ave. N. Suite 500 Seattle WA 98109 USA, V. Nene, The Institute for Genomic Research (TIGR) 9712 Medical Center Drive Rockville MD 20850 USA
  • Edited by Alan S. Bowman, University of Aberdeen, Patricia A. Nuttall
  • Publisher: Cambridge University Press
  • DOI: https://doi.org/10.1017/CBO9780511551802.015
  • pp 308-324

Summary

INTRODUCTION

The genus Theileria comprises tick-transmitted sporozoan protozoa that are the causative agents of a variety of disease syndromes in domestic and wild ruminants, and are collectively responsible for economic losses amounting to hundreds of millions of dollars annually in sub-Saharan Africa and Asia. Theileria are unique among protozoa, in that certain species are capable of immortalizing either mammalian lymphocytes, or cells of the monocyte/macrophage lineage that they infect. Theileria has been included within a subphylum designated the Apicomplexa, based on the common possession of an apical complex containing secretory organelles involved in invasion, or establishment, in the cells of their mammalian and invertebrate hosts. However the evolutionary and functional equivalence of the apical complex between different genera and hence the taxonomic validity of the Apicomplexa remains unclear. Analysis of 18S ribosomal RNA gene sequences demonstrates that the genus Theileria is phylogenetically most closely related to Babesia, a genus of tick-borne protozoan infective to the red cells of mammals including domestic livestock, and more distantly to the genus Plasmodium which causes malaria in humans and other species of vertebrates (Allsopp et al., 1994). There are similarities, but also significant differences, in features of the life cycle, genome organization and mammalian host immune responses to infection between Theileria and Plasmodium.

Economically important Theileria species that infect cattle and small ruminants are transmitted by ixodid ticks of the genera Rhipicephalus, Amblyomma, Hyalomma and Haemaphysalis. Theileria species infective to domestic ruminants are summarized in Table 14.1.

REFERENCES
Allsopp, B., Carrington, M., Bayliss, M. T., et al. (1989). Improved characterization of Theileria parva isolates using the polymerase chain reaction and oligonucleotide probes. Molecular and Biochemical Parasitology 35, 137–148.
Allsopp, B., Baylis, H. A., Allsopp, M. T. E. P., et al. (1993). Discrimination between six species of Theileria using oligonucleotide probes which detect small ribosomal RNA sequences. Parasitology 107, 157–165.
Allsopp, M. T. E. P., Cavalier-Smith, T., De, Waal D. T. & Allsopp, B. A. (1994). Phylogeny and evolution of the piroplasms. Parasitology 108, 147–152.
Andrews, N. W. & Webster, P. (1991). Phagolysomal escape by intracellular pathogens. Parasitology Today 7, 335–340.
Awadalla, P., Walliker, D., Babiker, H. & Mackinnon, M. (2001). The question of Plasmodium falciparum population structure. Trends in Parasitology 17, 351–353.
Babiker, H., Ranford-Cartwright, L., Currie, D., et al. (1994). Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology 109, 413–421.
Baldwin, C. L., Black, S. J., Brown, W. C., et al. (1988). Bovine T cells, B cells, and null cells are transformed by the protozoan parasite Theileria parva. Infection and Immunity 56, 462–467.
Baylis, H. A., Sohal, S. K., Carrington, M., Bishop, R. P. & Allsopp, B. A. (1991). An unusual repetitive gene family in Theileria parva which is stage-specifically transcribed. Molecular and Biochemical Parasitology 49, 133–142.
Bergman, D. K., Palmer, M. J., Caimano, M. J., Radolf, J. D. & Wikel, S. K. (2000). Isolation and molecular cloning of a secreted immunosuppressant protein from Dermacentor andersoni salivary glands. Journal of Parasitology 86, 516–525.
Bishop, R. P., Sohanpal, B. K., Allsopp, B. A., et al. (1993). Detection of polymorphisms among Theileria parva stocks using repetitive, telomeric and ribosomal DNA probes and anti-schizont monoclonal antibodies. Parasitology 107, 19–31.
Bishop, R. P., Sohanpal, B. K., Morzaria, S. P., et al. (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, 259–261.
Bishop, R., Musoke, A., Morzaria, S., Sohanpal, B. & Gobright, E. (1997). Concerted evolution at a multicopy locus in the protozoan parasite Theileria parva: extreme divergence of potential protein coding sequences. Molecular and Cellular Biology 17, 1666–1673.
Bishop, R., Geysen, D., Skilton, R., et al. (2002 a). Genomic polymorphism, sexual recombination and molecular epidemiology of Theileria parva. In World Class Parasites, vol. 3, Theileria, eds. Dobbelaere, D. A. E. & Mckeever, D. J., pp. 23–40. Amsterdam: Kluwer Academic.
Bishop, R., Lambson, B., Wells, C., et al. (2002 b). A cement protein of the tick Rhipicephalus appendiculatus, located in the secretory e cell granules of the type III salivary gland acini, induces strong antibody responses in cattle. International Journal for Parasitology 32, 833–842.
Bishop, R., Nene, V., Staeyert, J., et al. (2003). Immunity to East Coast fever induced by a polypeptide fragment of the major surface coat of Theileria parva sporozoites. Vaccine 21, 1205–1212.
Bishop, R., Shah, T., Pelle, R., et al. (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.
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, 1007–1014.
Borst, P., Bitter, W., McCulloch, R., Leuwen, F. & Rudenko, G. (1995). Antigenic variation in malaria. Cell 82, 1–4.
Boulter, N. & Hall, R. (1999). Immunity and vaccine development against bovine theilerioses. Advances in Parasitology 44, 41–97.
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, 93–100.
Carrington, M., Allsopp, B., Baylis, H., et al. (1995). Lymphoproliferation caused by Theileria parva and Theileria annulata. In Molecular Approaches to Parasitology, eds. Boothroyd, J. C. & Komuniecki, R., pp. 43–56. New York: Wiley–Liss.
Chae, J., Levy, M., Hunt, J., et al. (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, 3037–3040.
Conrad, P. A., Stagg, D. A., Grootenhuis, J. G., et al. (1987). Isolation of Theileria parasites from African buffalo (Syncercus caffer) and characterization with anti-schizont monoclonal antibodies. Parasitology 94, 413–423.
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, S35–S52.
Dimopoulos, G. (2003). Insect immunity and its implication in mosquito–malaria interactions. Cellular Microbiology 5, 3–14.
Dobbelaere, D. & Heussler, V. (1999). Transformation of leukocytes by Theileria parva and T. annulata. Annual Review of Microbiology 53, 1–42.
Dobbelaere, D. & Kaenzi, P. (2004). The strategies of the Theileria parasite: a new twist in host–parasite interactions. Current Opinion in Immunology 16, 524–530.
Dobbelaere, D. A. E., Spooner, P. R., Barry, W. C. & Irvin, A. D. (1984). Monoclonal antibodies neutralize the sporozoite stage of different Theileria parva stocks. Parasite Immunology 6, 361–370.
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, 3042–3048.
Fawcett, D. W., Doxsey, S. & Buscher, G. (1982). Salivary glands of the tick vector of East Coast fever. III. Ultrastructure of sporogony inTheileria parva. Tissue Cell 14, 183–206.
Gardner, M. J., Bishop, R., Shah, T., Villiers, E., Carlton, J. M., Hall, N., Ren, Q., Paulsen, I. T., Pain, A., Berriman, M., Wilson, R. J. M., Sato, Shigeharu., Ralph, S. A., Mann, D. J., Xiong, Zikai., Shallom, S. J., Weidman, J., Jiang, L., Lynn, J., Weaver, B., Shoaibi, A., Domingo, A. R., Wasawo, D., Crabtree, J., Wortman, J. R., Hass, B., Angiuoli, S. V., Creasy, T. H., Lu, C., Suh, B., Silva, J., Utterback, T. R., Feldblyum, T. V., Pertea, M., Allen, J., Nierman, W. C., Taracha, E., Salzberg, S. L., White, O. R., Fitzhugh, H. A., Morzaria, S., Venter, J. C., Fraser, C. M. & Nene, V. (2005). Genome sequences of Theileria parva, a bovine pathogen causing a lymphoproliferative disease. Science 309, 134–137.
Gauer, M., Mackenstedt, U., Mehlhorn, H., et al. (1995). DNA measurements and ploidy determination of developmental stages in the life cycles of Theileria annulata and T. parva. Parasitology Research 81, 565–574.
Heussler, V. T. (2002). Theileria survival strategies and host cell transformation. In World Class Parasites, vol. 3, Theileria, eds. Dobbelaere, D. A. E. & McKeever, D. J., pp. 69–84. Amsterdam: Kluwer Academic.
Iams, K. P., Young, J. R., Nene, V., et al. (1990). Characterization of the gene encoding a 104-kilodalton microneme-rhoptry protein of Theileria parva. Molecular and Biochemical Parasitology 39, 47–60.
Irvin, A. D. & Morrison, W. I. (1987). Immunopathology, immunology and immunoprophylaxis of Theileria Infections. In Immune Responses in Parasitic Infections, ed. Soulsby, E. J. L., pp. 223–274. Boca Raton, FL: CRC Press.
Irvin, A. D., Ocama, J. G. & Spooner, P. R. (1982). Cycle of bovine lymphoblastoid cells parasitized by Theileria parva. Research in Veterinary Science 33, 298–304.
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, 131–143.
Kaba, S. A., Nene, V., Musoke, A. J., Vlak, J. M. & van-Oers, M. M. (2002). Fusion of green fluorescent protein improves expression levels of Theileria parva sporozoite surface antigen p67 in insect cells. Parasitology 125, 497–505.
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, 1–10.
Knight, P. A., Musoke, A. J., Gachanja, J. N., et al. (1996). Conservation of neutralizing determinants between the sporozoite surface antigens of Theileria annulata and Theileria parva. Experimental Parasitology 82, 229–241.
Labuda, M., Trimnell, A. R., Lickova, M., et al. (2006). An antivector vaccine protects against a lethal vector-borne pathogen. PLoS Pathogens 2, 001–009.
Lambson, B., Nene, V., Obura, M., et al. (2005). Identification of candidate sialome components expressed in tick salivary glands using secretion signal complementation in mammalian cells. Insect Molecular Biology 14, 403–414.
McCutchan, T., Li, J., McConkey, G., Roegers, M. & Waters, A. (1995). The cytoplasmic RNAs of Plasmodium spp. Parasitology Today 11, 134–138.
Medley, G. F., Perry, B. D. & Young, A. S. (1993). Preliminary analysis of the transmission dynamics of Theileria parva in eastern Africa. Parasitology 106, 251–264.
Mehlhorn, H. & Schein, E. (1984). The piroplasms: life cycle and sexual stages. Advances in Parasitology 23, 37–103.
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. 67–73. Nairobi: International Laboratory for Research on Animal Diseases.
Mukhebi, A. W., Perry, B. D. & Kruska, R. (1992). Estimated economics of theileriosis control in Africa. Preventive Veterinary Medicine 12, 73–85.
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, 231–238.
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 of the USA 89, 514–518.
Musoke, A., Rowlands, J., Nene, V., et al. (2005). Subunit vaccines based on the p67 major surface protein of Theileria parva sporozoites reduce severity of infection derived from field tick challenge. Vaccine 23, 3084–3095.
Nene, V., Iams, K. P., Gobright, E. & Musoke, A. J. (1992). Characterization of the gene encoding a candidate vaccine antigen of Theileria parva sporozoites. Molecular and Biochemical Parasitology 51, 17–28.
Nene, V., Inumaru, S., McKeever, D. J., et al. (1995). Characterization of an insect cell-derived Theileria parva sporozoite vaccine antigen and immunogenicity in cattle. Infection and Immunity 63, 503–508.
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, 2056–2061.
Nene, V., Gobright, E., Bishop, R., Morzaria, S. & Musoke, A. (1999). Linear peptide specificity of antibody responses to p67 and sequence diversity of neutralizing epitopes: implications for a Theileria parva vaccine. Infection and Immunity 67, 1261–1266.
Nene, V., Lee, D., Quackenbush, J., et al. (2002). AvGI, an index of genes transcribed in the salivary glands of the ixodid tickAmblyomma variegatum. International Journal for Parasitology 32, 1447–1456.
Nene, V., Lee, D., K'anga, S., et al. (2004). Genes transcribed in the salivary glands of female Rhipicephalus appendiculatus ticks infected with Theileria parva. Insect Biochemistry and Molecular Biology 34, 1117–1118.
Ngumi, P. N., Lesan, A. C., Williamson, S. M., et al. (1994). Isolation and preliminary characterization of a previously unidentified Theileria parasite of cattle in Kenya. Research in Veterinary Science 57, 1–9.
Norval, R. A. I., Perry, B. D. & Young, A. S. (1992). The Epidemiology of Theileriosis in Africa. London: Academic Press.
Nuttall, P. A., Trimnell, A. R., Kazimirova, M. & Labuda, M. (2006). Exposed and concealed antigens as vaccine targets for controlling ticks and tick-borne diseases. Parasite Immunology 28, 155–163.
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, 243–253.
Ochanda, H., Young, A. S., Medley, G. F. & Perry, B. D. (1998). Vector competence of seven rhipicephalid tick stocks in transmitting two Theileria parva parasite stocks from Kenya and Zimbabwe. Parasitology 116, 539–545.
Odongo, D., Oura, C. A. L., Spooner, P., et al. (2006). Linkage disequilibrium and genetic diversity at mini- and micro-satellite loci of Theileria parva isolated from cattle in three regions of Kenya. International Journal for Parasitology 36, 937–946.
Oura, C. A. L., Odongo, D., Lubega, G., et al. (2003). A panel of microsatellite and minisatellite markers for the characterization of field isolates of Theileria parva. International Journal for Parasitology 33, 1641–1653.
Oura, C. A. L., Bishop, R., Lubega, G. W. & Tait, A. (2004). Application of a reverse line blot to the study of haemoparasites in cattle in Uganda. International Journal for Parasitology 34, 603–613.
Pain, A., Renauld, H., Berriman, M., Murphy, L., Yeats, C. A., Weir, W., Kerhornou, A., Aslett, M., Bishop, R., Bouchier, C., Cochet, M., Culson, R. M. R., Cronin, A., Villiers, E., 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., Neil, O' 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. E., Langsley, G., Rajandream, M. A., McKeever, D., Shiels, B., Tait, A., Barrell, B. & Hall, N. (2005). The genome of the host-cell transforming parasite Theileria annulata and a comparison withT. parva. Science 309, 131–133.
Paul, R. E. L. & Day, K. P. (1998). Mating patterns of Plasmodium falciparum. Parasitology Today 14, 197–202.
Paul, R., Packer, M., Walmsley, M., et al. (1995). Mating patterns in malaria parasite populations of Papua New Guinea. Science 269, 1709–1711.
Radley, D. E., Brown, C. G. D., Burridge, M. P., et al. (1975). East Coast fever. I. Chemoprophylactic immunization of cattle against Theileria parva (Muguga) and five theilerial strains. Veterinary Parasitology 1, 35–41.
Schnittger, L., Hong, Y., Jianxun, L., et al. (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, 271–275.
Shaw, M. K. (1997). The same but different: the biology of Theileria sporozoite entry into bovine cells. International Journal for Parasitology 27, 457–474.
Shaw, M. K. (2002). Theileria development and host cell invasion. In World Class Parasites, vol. 3, Theileria, eds. Dobbelaere, D. A. E. & McKeever, D. J., pp. 1–22. Amsterdam: Kluwer Academic.
Shaw, M. K. & Tilney, L. G. (1992). How individual cells develop from a syncytium: merogony in Theileria parva (Apicomplexa). Journal of Cell Science 101, 109–123.
Shaw, M. K. & Tilney, L. G. (1995). The entry of Theileria parva merozoites into bovine erythrocytes occurs by a process similar to sporozoite invasion of lymphocytes. Parasitology 111, 455–461.
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, 23–63.
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, 87–101.
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, 1486–1495.
Shiels, B., Langsley, G., Weir, W., et al. (2006). Alteration of host cell phenotype by Theileria annulata and Theileria parva: mining for manipulators in the parasite genomes. International Journal for Parasitology 36, 9–12.
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, 53–117.
Skilton, R. A., Bishop, R. P., Wells, C. W., et al. (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, 321–330.
Skilton, R. A., Musoke, A. J., Nene, V., et al. (2000). Molecular characterization of a Theileria lestoquardi gene encoding a candidate sporozoite vaccine antigen. Molecular and Biochemical Parasitology 107, 309–314.
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, 265–276.
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, 243–254.
Swan, D. G., Phillips, K., Tait, A. & Shiels, B. R. (1999). Evidence for localization of a Theileria parasite AT hook DNA-binding protein to the nucleus of immortalized bovine host cells. Molecular and Biochemical Parasitology 101, 117–129.
Tatchell, R. J. (1987). Tick control in the context of ECF immunization. Parasitology Today 3, 7–10.
Trimnell, A. R., Hails, R. S. & Nuttall, P. A. (2002). Dual action ectoparasite vaccine targeting ‘exposed’ and ‘concealed’ antigens. Vaccine 20, 3360–3568.
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, 87–90.
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, 89–94.
Willadsen, P. (2004). Anti-tick vaccines. Parasitology 129, S367–S387.
Wilson, R. J. M. & Williamson, D. H. (1997). Extrachromosomal DNA in the Apicomplexa. Microbiology and Molecular Biology Reviews 61, 1–16.
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, 199–211.
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, 9–16.
Young, A. S., Dolan, T. T., Mwakima, F. N., et al. (1995). Estimation of heritability of susceptibility to infection with Theileria parva in the tick Rhipicephalus appendiculatus. Parasitology 111, 31–38.
Young, A. S., Dolan, T. T., Morzaria, S. P., et al. (1996). Factors influencing infections in Rhipicephalus appendiculatus ticks fed on cattle infected with Theileria parva. Parasitology 113, 255–266.