Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1990 Nov;58(11):3574–3581. doi: 10.1128/iai.58.11.3574-3581.1990

Immunization with Theileria parva parasites from buffaloes results in generation of cytotoxic T cells which recognize antigens common among cells infected with stocks of T. parva parva, T. parva bovis, and T. parva lawrencei.

T M Kariuki 1, J G Grootenhuis 1, T T Dolan 1, R P Bishop 1, C L Baldwin 1
PMCID: PMC313700  PMID: 1699896

Abstract

Immunity to infection by the protozoan parasite Theileria parva in cattle is partially attributable to cytotoxic T cells, which kill lymphocytes infected with the schizont stage of the parasite. Here we evaluated five stocks of buffalo-derived T. parva lawrencei parasites and two stocks of cattle-derived T. parva parva parasites for their ability to induce in vivo cytotoxic T cells which can kill lymphocytes infected with a wide variety of strains of T. parva parasites. A group of seven full-sibling cattle, produced by embryo transfer and matched for at least one major histocompatibility complex class I haplotype, were immunized by infection and treatment with the parasite stocks. Target cells used in in vitro cytotoxicity assays were infected with five buffalo-derived parasite stocks and five cattle-derived parasite stocks, including T. parva parva and T. parva bovis. Immunization with any of the seven parasite stocks resulted in the generation of cytotoxic T cells which recognized parasite antigens on most if not all of the target cell lines tested, although the T. parva bovis stock was the least effective at doing so. Further in-depth analyses performed with peripheral blood mononuclear cells from one of the cattle immunized with T. parva lawrencei parasites showed that the pattern of killing of the panel of target cells was altered when either cells infected with different parasite stocks or clones of infected cells were used as stimulator cells in vitro, suggesting the presence of more than one population of parasite-specific cytotoxic effector cells in the peripheral blood mononuclear cells. However, clones of these cytotoxic effector cells recognized common or cross-reactive antigen epitopes expressed by the entire panel of infected target cells. These T-cell clones will be useful for identifying common T-cell antigen epitopes of T. parva and the parasite genes encoding them.

Full text

PDF
3574

Images in this article

3576Image
on p.3576

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allsopp B. A., Allsopp M. T. Theileria parva: genomic DNA studies reveal intra-specific sequence diversity. Mol Biochem Parasitol. 1988 Feb;28(1):77–83. doi: 10.1016/0166-6851(88)90183-1. [DOI] [PubMed] [Google Scholar]
  2. Baldwin C. L., Goddeeris B. M., Morrison W. I. Bovine helper T-cell clones specific for lymphocytes infected with Theileria parva (Muguga). Parasite Immunol. 1987 Jul;9(4):499–513. doi: 10.1111/j.1365-3024.1987.tb00526.x. [DOI] [PubMed] [Google Scholar]
  3. Baldwin C. L., Malu M. N., Grootenhuis J. G. Evaluation of cytotoxic lymphocytes and their parasite strain specificity from African buffalo infected with Theileria parva. Parasite Immunol. 1988 Jul;10(4):393–403. doi: 10.1111/j.1365-3024.1988.tb00229.x. [DOI] [PubMed] [Google Scholar]
  4. Conrad P. A., Iams K., Brown W. C., Sohanpal B., ole-MoiYoi O. K. DNA probes detect genomic diversity in Theileria parva stocks. Mol Biochem Parasitol. 1987 Oct;25(3):213–226. doi: 10.1016/0166-6851(87)90085-5. [DOI] [PubMed] [Google Scholar]
  5. Conrad P. A., ole-MoiYoi O. K., Baldwin C. L., Dolan T. T., O'Callaghan C. J., Njamunggeh R. E., Grootenhuis J. G., Stagg D. A., Leitch B. L., Young A. S. Characterization of buffalo-derived theilerial parasites with monoclonal antibodies and DNA probes. Parasitology. 1989 Apr;98(Pt 2):179–188. doi: 10.1017/s0031182000062089. [DOI] [PubMed] [Google Scholar]
  6. Cunningham M. P., Brown C. G., Burridge M. J., Irvin A. D., Kirimi I. M., Purnell R. E., Radley D. E., Wagner G. G. Theileriosis: the exposure of immunized cattle in a Theileria lawrencei enzootic area. Trop Anim Health Prod. 1974 Feb;6(1):39–43. doi: 10.1007/BF02380747. [DOI] [PubMed] [Google Scholar]
  7. Cunningham M. P., Brown C. G., Burridge M. J., Purnell R. E. Cryopreservation of infective particles of Theileria parva. Int J Parasitol. 1973 Sep;3(5):583–587. doi: 10.1016/0020-7519(73)90082-9. [DOI] [PubMed] [Google Scholar]
  8. Dolan T. T., Linyonyi A., Mbogo S. K., Young A. S. Comparison of long acting oxytetracycline and parvaquone in immunisation against East Coast fever by infection and treatment. Res Vet Sci. 1984 Sep;37(2):175–178. [PubMed] [Google Scholar]
  9. Eugui E. M., Emery D. L. Genetically restricted cell-mediated cytotoxicity in cattle immune to Theileria parva. Nature. 1981 Mar 19;290(5803):251–254. doi: 10.1038/290251a0. [DOI] [PubMed] [Google Scholar]
  10. Goddeeris B. M., Katende J. M., Irvin A. D., Chumo R. S. Indirect fluorescent antibody test for experimental and epizootiological studies on East coast fever (Theileria parva infection in cattle). Evaluation of a cell culture schizont antigen fixed and stored in suspension. Res Vet Sci. 1982 Nov;33(3):360–365. [PubMed] [Google Scholar]
  11. Goddeeris B. M., Morrison W. I., Teale A. J., Bensaid A., Baldwin C. L. Bovine cytotoxic T-cell clones specific for cells infected with the protozoan parasite Theileria parva: parasite strain specificity and class I major histocompatibility complex restriction. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5238–5242. doi: 10.1073/pnas.83.14.5238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goddeeris B. M., Morrison W. I., Teale A. J. Generation of bovine cytotoxic cell lines, specific for cells infected with the protozoan parasite Theileria parva and restricted by products of the major histocompatibility complex. Eur J Immunol. 1986 Oct;16(10):1243–1249. doi: 10.1002/eji.1830161010. [DOI] [PubMed] [Google Scholar]
  13. Goddeeris B. M., Morrison W. I. The bovine autologous Theileria mixed leucocyte reaction: influence of monocytes and phenotype of the parasitized stimulator cell on proliferation and parasite specificity. Immunology. 1987 Jan;60(1):63–69. [PMC free article] [PubMed] [Google Scholar]
  14. Goddeeris B. M., Morrison W. I., Toye P. G., Bishop R. Strain specificity of bovine Theileria parva-specific cytotoxic T cells is determined by the phenotype of the restricting class I MHC. Immunology. 1990 Jan;69(1):38–44. [PMC free article] [PubMed] [Google Scholar]
  15. Irvin A. D., Dobbelaere D. A., Mwamachi D. M., Minami T., Spooner P. R., Ocama J. G. Immunisation against East Coast fever: correlation between monoclonal antibody profiles of Theileria parva stocks and cross immunity in vivo. Res Vet Sci. 1983 Nov;35(3):341–346. [PubMed] [Google Scholar]
  16. Irvin A. D., Morzaria S. P., Munatswa F. C., Norval R. A. Immunization of cattle with a Theileria parva bovis stock from Zimbabwe protects against challenge with virulent T.p. parva and T.p. lawrencei stocks from Kenya. Vet Parasitol. 1989 Aug 1;32(4):271–278. doi: 10.1016/0304-4017(89)90037-x. [DOI] [PubMed] [Google Scholar]
  17. Jordt T., Mahon G. D., Touray B. N., Ngulo W. K., Morrison W. I., Rawle J., Murray M. Successful transfer of N'Dama embryos into Boran recipients. Vet Rec. 1986 Sep 6;119(10):246–247. doi: 10.1136/vr.119.10.246. [DOI] [PubMed] [Google Scholar]
  18. Kurtti T. J., Munderloh U. G., Irvin A. D., Büscher G. Theileria parva: early events in the development of bovine lymphoblastoid cell lines persistently infected with macroschizonts. Exp Parasitol. 1981 Oct;52(2):280–290. doi: 10.1016/0014-4894(81)90083-7. [DOI] [PubMed] [Google Scholar]
  19. Lalor P. A., Morrison W. I., Goddeeris B. M., Jack R. M., Black S. J. Monoclonal antibodies identify phenotypically and functionally distinct cell types in the bovine lymphoid system. Vet Immunol Immunopathol. 1986 Sep;13(1-2):121–140. doi: 10.1016/0165-2427(86)90054-1. [DOI] [PubMed] [Google Scholar]
  20. Minami T., Spooner P. R., Irvin A. D., Ocama J. G., Dobbelaere D. A., Fujinaga T. Characterisation of stocks of Theileria parva by monoclonal antibody profiles. Res Vet Sci. 1983 Nov;35(3):334–340. [PubMed] [Google Scholar]
  21. Morrison W. I., Goddeeris B. M., Teale A. J. Bovine cytotoxic T cell clones which recognize lymphoblasts infected with two antigenically different stocks of the protozoan parasite Theileria parva. Eur J Immunol. 1987 Dec;17(12):1703–1709. doi: 10.1002/eji.1830171205. [DOI] [PubMed] [Google Scholar]
  22. Morrison W. I., Goddeeris B. M., Teale A. J., Groocock C. M., Kemp S. J., Stagg D. A. Cytotoxic T-cells elicited in cattle challenged with Theileria parva (Muguga): evidence for restriction by class I MHC determinants and parasite strain specificity. Parasite Immunol. 1987 Sep;9(5):563–578. doi: 10.1111/j.1365-3024.1987.tb00530.x. [DOI] [PubMed] [Google Scholar]
  23. Newson J., Naessens J., Stagg D. A., Black S. J. A cell surface antigen associated with Theileria parva lawrencei-infected bovine lymphoid cells. Parasite Immunol. 1986 Mar;8(2):149–158. doi: 10.1111/j.1365-3024.1986.tb00841.x. [DOI] [PubMed] [Google Scholar]
  24. Pearson T. W., Hewett R. S., Roelants G. E., Stagg D. A., Dolan T. T. Studies on the induction and specificity of cytotoxicity to Theileria-transformed cell lines. J Immunol. 1982 Jun;128(6):2509–2513. [PubMed] [Google Scholar]
  25. Teale A. J., Kemp S. J., Young F., Spooner R. L. Selection, by major histocompatibility type (BoLA), of lymphoid cells derived from a bovine chimaera and transformed by Theileria parasites. Parasite Immunol. 1983 May;5(3):329–335. doi: 10.1111/j.1365-3024.1983.tb00748.x. [DOI] [PubMed] [Google Scholar]
  26. Young A. S., Brown C. G., Burridge M. J., Cunningham M. P., Kirimi I. M., Irvin A. D. Observations on the cross-immunity between Theileria lawrencei (Serengeti) and Theileria parva (Muguga) in cattle. Int J Parasitol. 1973 Nov;3(6):723–728. doi: 10.1016/0020-7519(73)90063-5. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES