Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T12:08:44.939Z Has data issue: false hasContentIssue false

Genetic and antigenic diversity of Theileria parva in cattle in Eastern and Southern zones of Tanzania. A study to support control of East Coast fever

Published online by Cambridge University Press:  24 November 2014

MWEGA ELISA*
Affiliation:
Biosciences eastern and central Africa – International Livestock Research Institute Hub (BecA-ILRI Hub), P.O. Box 30709-00100, Nairobi, Kenya Faculty of Veterinary Medicine, Genome Science Center, Sokoine University of Agriculture (SUA), P.O. Box 3019, Morogoro, Tanzania
SALIH DIA HASAN
Affiliation:
Biosciences eastern and central Africa – International Livestock Research Institute Hub (BecA-ILRI Hub), P.O. Box 30709-00100, Nairobi, Kenya Veterinary Research Institute (VRI), P.O. Box 8067, Khartoum, Sudan
NJAHIRA MOSES
Affiliation:
Biosciences eastern and central Africa – International Livestock Research Institute Hub (BecA-ILRI Hub), P.O. Box 30709-00100, Nairobi, Kenya
RUKAMBILE ELPIDIUS
Affiliation:
Tanzania Veterinary Laboratory Agency (TVLA), P.O. Box 9254, Dar es Salaam, Tanzania
ROBERT SKILTON
Affiliation:
Biosciences eastern and central Africa – International Livestock Research Institute Hub (BecA-ILRI Hub), P.O. Box 30709-00100, Nairobi, Kenya
PAUL GWAKISA
Affiliation:
Faculty of Veterinary Medicine, Genome Science Center, Sokoine University of Agriculture (SUA), P.O. Box 3019, Morogoro, Tanzania
*
* Corresponding author: Mwega Elisa Biosciences eastern and central Africa – International Livestock Research Institute Hub (BecA-ILRI Hub), P.O. Box 30709-00100, Nairobi, Kenya. E-mail: elisa_mwega@yahoo.co.uk

Summary

This study investigated the genetic and antigenic diversity of Theileria parva in cattle from the Eastern and Southern zones of Tanzania. Thirty-nine (62%) positive samples were genotyped using 14 mini- and microsatellite markers with coverage of all four T. parva chromosomes. Wright's F index (F ST = 0 × 094) indicated a high level of panmixis. Linkage equilibrium was observed in the two zones studied, suggesting existence of a panmyctic population. In addition, sequence analysis of CD8+ T-cell target antigen genes Tp1 revealed a single protein sequence in all samples analysed, which is also present in the T. parva Muguga strain, which is a component of the FAO1 vaccine. All Tp2 epitope sequences were identical to those in the T. parva Muguga strain, except for one variant of a Tp2 epitope, which is found in T. parva Kiambu 5 strain, also a component the FAO1 vaccine. Neighbour joining tree of the nucleotide sequences of Tp2 showed clustering according to geographical origin. Our results show low genetic and antigenic diversity of T. parva within the populations analysed. This has very important implications for the development of sustainable control measures for T. parva in Eastern and Southern zones of Tanzania, where East Coast fever is endemic.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bishop, R., Geysen, D., Spooner, P., Skilton, R., Nene, V., Dolan, T. and Morzaria, S. (2001). Molecular and immunological characterisation of Theileria parva stocks which are components of the ‘Muguga cocktail’ used for vaccination against East Coast fever in cattle. Veterinary Parasitology 94, 227237.CrossRefGoogle ScholarPubMed
Bishop, R. P., Spooner, P. R., Kanhai, G. K., Kiarie, J., Latif, A. A, Hove, T. and Masaka, S., Dolan, T. T. (1994). Molecular characterization of Theileria parasites: application to the epidemiology of theileriosis in Zimbabwe. Parasitology 109 (Pt 5), 573581.CrossRefGoogle Scholar
De Deken, R., Martin, V., Saido, A., Madder, M., Brandt, J. and Geysen, D. (2007). An outbreak of East Coast Fever on the Comoros: a consequence of the import of immunised cattle from Tanzania? Veterinary Parasitology 143, 245253.Google Scholar
Di Giulio, G., Lynen, G., Morzaria, S., Oura, C. and Bishop, R. (2009). Live immunization against East Coast fever – current status. Trends in Parasitology 25, 8592.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, A21A27.Google Scholar
George, J. E., Pound, J. M. and Davey, R. B. (2004). Chemical control of ticks on cattle and resistance of these parasites to acaricides. Parasitology 129, S353S356.CrossRefGoogle ScholarPubMed
Graham, S. P., Pellé, 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. et al. (2006). Theileria parva candidate vaccine antigens recognized by immune bovine cytotoxic T lymphocytes. Proceedingsof the National Academy of Sciences of the United States of America 103, 32863291.CrossRefGoogle ScholarPubMed
Graham, S. P., Pellé, R., Yamage, M., Mwangi, D. M., Honda, Y., Mwakubambanya, R. S., de Villiers, E. P., 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. N. (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, 685694.CrossRefGoogle ScholarPubMed
Hayashida, K., Abe, T., Weir, W., Nakao, R., Ito, K., Kajino, K., Suzuki, Y., Jongejan, F., Geysen, D. and Sugimoto, C. (2013). Whole-genome sequencing of Theileria parva strains provides insight into parasite migration and diversification in the African continent. DNA Research 20, 209220.CrossRefGoogle ScholarPubMed
Haubold, B. and Hudson, R. R. (2000). LIAN 3.0, detecting linkage disequilibrium in multilocus data. Linkage analysis. Bioinformatics, 16, 847848.Google Scholar
Katzer, F., Ngugi, D., Oura, C., Bishop, R. P., Taracha, E. L. N., Walker, A. R. and McKeever, D. J. (2006). Extensive genotypic diversity in a recombining population of the apicomplexan parasite Theileria parva . Infection and Immunity 74, 54565464.Google Scholar
Katzer, F., Lizundia, R., Ngugi, D., Blake, D. and McKeever, D. (2011). Construction of a genetic map for Theileria parva: identification of hotspots of recombination. International Journal of Parasitology 41, 669675.CrossRefGoogle ScholarPubMed
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.CrossRefGoogle ScholarPubMed
Liu, K. and Muse, S. V. (2005). PowerMarker: integrated analysis environment for genetic marker data. Bioinformatics 21, 21282129.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 39, 24592469.CrossRefGoogle ScholarPubMed
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, 563578.CrossRefGoogle ScholarPubMed
Muleya, W., Namangala, B., Simuunza, M., Nakao, R., Inoue, N., Kimura, T., Ito, K., Sugimoto, C. and Sawa, H. (2012). Population genetic analysis and sub-structuring of Theileria parva in the northern and eastern parts of Zambia. Parasites and Vectors 5, 255.CrossRefGoogle ScholarPubMed
Nene, V., Iams, E., Gobright, E. and Musoke, A. (1992). Characterization of a gene encoding a candidate vaccine antigen of Theileria parva sporozoites. Mol. Biol. Parasitol. 51, 1728.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, 937946.CrossRefGoogle ScholarPubMed
Odongo, D. O., Sunter, J. D., Kiara, H. K., Skilton, R. A. and Bishop, R. P. (2010). A nested PCR assay exhibits enhanced sensitivity for detection of Theileria parva infections in bovine blood samples from carrier animals., 2010. Parasitology Research. 106, 357365.Google Scholar
Oura, C. A., Odongo, D., Lubega, G., Spooner, P., Tait, A. and Bishop, R. (2003). A panel of microsatellite and minisatellite markers for the characterisation of field isolates of Theileria parva . International Journal of Parasitology 33, 16411653.CrossRefGoogle ScholarPubMed
Oura, C. A. L., Bishop, R. P., Wampande, E. M., Lubega, G. W. and Tait, A. (2004). Application of a reverse line blot assay to the study of haemoparasites in cattle in Uganda. International Journal of Parasitology 34, 603613.CrossRefGoogle 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, 229239.Google Scholar
Oura, C. A. L., 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, 12051213.Google Scholar
Oura, C. A L., Tait, A., Asiimwe, B., Lubega, G. W. and Weir, W. (2011). Haemoparasite prevalence and Theileria parva strain diversity in Cape buffalo (Syncerus caffer) in Uganda. Veterinary Parasitology 175, 212219.CrossRefGoogle ScholarPubMed
Peakall, R. and Smouse, P. E. (2006). GENALEX 6: genetic analysis in excel. Population geneticsoftware for teaching and research. Molecular Ecology Notes 6, 288295.CrossRefGoogle Scholar
Pelle, R., Graham, S. P., Njahira, M. N., Osaso, J., Saya, R. M., Odongo, D. O., Toye, P. G., Spooner, P. R., Musoke, A. J., Mwangi, D. M., Taracha, E. L. N., Morrison, W. I., Weir, W., Silva, J. C. and Bishop, R. P. (2011). Two Theileria parva CD8 T cell antigen genes are more variable in buffalo than cattle parasites, but differ in pattern of sequence diversity. PLoS One 6, e19015.CrossRefGoogle ScholarPubMed
Taracha, E. L., Goddeeris, B. M., Morzaria, S. P. and Morrison, W. I. (1995). Parasite strain specificity of precursor cytotoxic T cells in individual animals correlates with cross-protection in cattle challenged with Theileria parva. Parasite strain specificity of precursor cytotoxic T Cells in individual animals correlates with. Infection and Immunity 63, 1258.Google Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4480.Google Scholar
Waladde, S. M., Young, A. S., Ochieng, S. A., Mwaura, S. N. and Mwakima, F. N. (1993). Transmission of Theileria parva to cattle by Rhipicephalus appendiculatus adults fed as nymphae in vitro on infected blood through an artificial membrane. Parasitology 107 (Pt 3), 249256.CrossRefGoogle ScholarPubMed
Wambura, P. N., Gwakisa, P. S., Silayo, R. S. and Rugaimukamu, E. A. (1998). Breed-associated resistance to tick infestation in Bos indicus and their crosses with Bos taurus. Veterinary Parasitology 77, 6370.Google Scholar
Weir, W., Karagenç, T., Gharbi, M., Simuunza, M., Aypak, S., Aysul, N., Darghouth, M. A., Shiels, B. and Tait, A. (2011). Population diversity and multiplicity of infection in Theileria annulata . International Journal of Parasitology 41, 193203.CrossRefGoogle ScholarPubMed