Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Mar 1;91(5):1959–1963. doi: 10.1073/pnas.91.5.1959

Adoptive transfer of immunity to Theileria parva in the CD8+ fraction of responding efferent lymph.

D J McKeever 1, E L Taracha 1, E L Innes 1, N D MacHugh 1, E Awino 1, B M Goddeeris 1, W I Morrison 1
PMCID: PMC43284  PMID: 8127915

Abstract

Evidence that class I major histocompatibility complex-restricted cytotoxic T lymphocytes (CTL) are involved in immunity to malaria has highlighted the potential importance of these cells in protection against intracellular parasites. Parasite-specific CTL are a prominent feature of the immune response of cattle to Theileria parva, a related apicomplexan parasite. The relationship between the appearance of these cells in the blood of immune cattle under challenge and the clearance of infection suggests that they are involved in the control of infection, but direct evidence is lacking that CTL can mediate protection. We have made a quantitative kinetic study of CTL responses in lymph originating from infected lymph nodes in a number of immune cattle under challenge with T. parva. Direct killing activity and the frequency of CTL precursors (CTLp) within responding cell populations were evaluated. A substantial increase in the proportion of CD8+ CTL was observed between days 8 and 11 after challenge. Frequencies of CTLp as high as 1:32 were observed and activity was essentially confined to the large blasting cell fraction. The analogous response in peripheral blood was of lower magnitude and delayed by 1-2 days. The high frequency of CTLp in efferent lymph permitted the adoptive transfer of this activity between immune and naive monozygotic twin calves. In separate experiments, naive calves lethally infected with T. parva were protected by inoculation of up to 10(10) responding CD8+ T cells derived from their immune twins. Elimination of CD8+ T cells within the inoculum abrogated this effect. These findings provide direct evidence that CD8+ T cells can control T. parva infections in immune cattle.

Full text

PDF
1959

Images in this article

1960Image
on p.1960
1961Image
on p.1961

Selected References

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

  1. 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. Bovine T cells, B cells, and null cells are transformed by the protozoan parasite Theileria parva. Infect Immun. 1988 Feb;56(2):462–467. doi: 10.1128/iai.56.2.462-467.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baldwin C. L., Teale A. J., Naessens J. G., Goddeeris B. M., MacHugh N. D., Morrison W. I. Characterization of a subset of bovine T lymphocytes that express BoT4 by monoclonal antibodies and function: similarity to lymphocytes defined by human T4 and murine L3T4. J Immunol. 1986 Jun 15;136(12):4385–4391. [PubMed] [Google Scholar]
  3. Bensaid A., Hadam M. Individual antigens of cattle. Bovine CD4 (BoCD4). Vet Immunol Immunopathol. 1991 Jan;27(1-3):51–54. doi: 10.1016/0165-2427(91)90078-q. [DOI] [PubMed] [Google Scholar]
  4. Brown C. G., Stagg D. A., Purnell R. E., Kanhai G. K., Payne R. C. Letter: Infection and transformation of bovine lymphoid cells in vitro by infective particles of Theileria parva. Nature. 1973 Sep 14;245(5420):101–103. doi: 10.1038/245101a0. [DOI] [PubMed] [Google Scholar]
  5. Clevers H., MacHugh N. D., Bensaid A., Dunlap S., Baldwin C. L., Kaushal A., Iams K., Howard C. J., Morrison W. I. Identification of a bovine surface antigen uniquely expressed on CD4-CD8- T cell receptor gamma/delta+ T lymphocytes. Eur J Immunol. 1990 Apr;20(4):809–817. doi: 10.1002/eji.1830200415. [DOI] [PubMed] [Google Scholar]
  6. Ellis J. A., Davis W. C., MacHugh N. D., Emery D. L., Kaushal A., Morrison W. I. Differentiation antigens on bovine mononuclear phagocytes identified by monoclonal antibodies. Vet Immunol Immunopathol. 1988 Oct;19(3-4):325–340. doi: 10.1016/0165-2427(88)90118-3. [DOI] [PubMed] [Google Scholar]
  7. Emery D. L., Eugui E. M., Nelson R. T., Tenywa T. Cell-mediated immune responses to Theileria parva (East Coast fever) during immunization and lethal infections in cattle. Immunology. 1981 Jun;43(2):323–336. [PMC free article] [PubMed] [Google Scholar]
  8. Emery D. L., MacHugh N. D., Ellis J. A. The properties and functional activity of non-lymphoid cells from bovine afferent (peripheral) lymph. Immunology. 1987 Oct;62(2):177–183. [PMC free article] [PubMed] [Google Scholar]
  9. Goddeeris B. M., Baldwin C. L., ole-MoiYoi O., Morrison W. I. Improved methods for purification and depletion of monocytes from bovine peripheral blood mononuclear cells. Functional evaluation of monocytes in responses to lectins. J Immunol Methods. 1986 May 22;89(2):165–173. doi: 10.1016/0022-1759(86)90354-6. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Hoffman S. L., Oster C. N., Plowe C. V., Woollett G. R., Beier J. C., Chulay J. D., Wirtz R. A., Hollingdale M. R., Mugambi M. Naturally acquired antibodies to sporozoites do not prevent malaria: vaccine development implications. Science. 1987 Aug 7;237(4815):639–642. doi: 10.1126/science.3299709. [DOI] [PubMed] [Google Scholar]
  12. Kumar S., Miller L. H., Quakyi I. A., Keister D. B., Houghten R. A., Maloy W. L., Moss B., Berzofsky J. A., Good M. F. Cytotoxic T cells specific for the circumsporozoite protein of Plasmodium falciparum. Nature. 1988 Jul 21;334(6179):258–260. doi: 10.1038/334258a0. [DOI] [PubMed] [Google Scholar]
  13. Lukacher A. E., Braciale V. L., Braciale T. J. In vivo effector function of influenza virus-specific cytotoxic T lymphocyte clones is highly specific. J Exp Med. 1984 Sep 1;160(3):814–826. doi: 10.1084/jem.160.3.814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. MacHugh N. D., Bensaid A., Davis W. C., Howard C. J., Parsons K. R., Jones B., Kaushal A. Characterization of a bovine thymic differentiation antigen analogous to CD1 in the human. Scand J Immunol. 1988 May;27(5):541–547. doi: 10.1111/j.1365-3083.1988.tb02381.x. [DOI] [PubMed] [Google Scholar]
  15. MacHugh N. D., Sopp P. Individual antigens of cattle. Bovine CD8 (BoCD8). Vet Immunol Immunopathol. 1991 Jan;27(1-3):65–69. doi: 10.1016/0165-2427(91)90081-m. [DOI] [PubMed] [Google Scholar]
  16. Malik A., Egan J. E., Houghten R. A., Sadoff J. C., Hoffman S. L. Human cytotoxic T lymphocytes against the Plasmodium falciparum circumsporozoite protein. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3300–3304. doi: 10.1073/pnas.88.8.3300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. McDermott M. R., Lukacher A. E., Braciale V. L., Braciale T. J., Bienenstock J. Characterization and in vivo distribution of influenza-virus-specific T-lymphocytes in the murine respiratory tract. Am Rev Respir Dis. 1987 Jan;135(1):245–249. doi: 10.1164/arrd.1987.135.1.245. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Muhammed S. I., Lauerman L. H., Jr, Johnson L. W. Effect of humoral antibodies on the course of Theileria parva infection (East Coast fever) of cattle. Am J Vet Res. 1975 Apr;36(4 PT1):399–402. [PubMed] [Google Scholar]
  20. Musoke A., Morzaria S., Nkonge C., Jones E., Nene V. A recombinant sporozoite surface antigen of Theileria parva induces protection in cattle. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):514–518. doi: 10.1073/pnas.89.2.514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Naessens J., Newson J., Williams D. J., Lutje V. Identification of isotypes and allotypes of bovine immunoglobulin M with monoclonal antibodies. Immunology. 1988 Apr;63(4):569–574. [PMC free article] [PubMed] [Google Scholar]
  22. Potocnjak P., Yoshida N., Nussenzweig R. S., Nussenzweig V. Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. J Exp Med. 1980 Jun 1;151(6):1504–1513. doi: 10.1084/jem.151.6.1504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Reimann J. Double-negative (CD4-CD8-), TCR alpha beta-expressing, peripheral T cells. Scand J Immunol. 1991 Dec;34(6):679–688. doi: 10.1111/j.1365-3083.1991.tb01592.x. [DOI] [PubMed] [Google Scholar]
  24. Romero P., Maryanski J. L., Corradin G., Nussenzweig R. S., Nussenzweig V., Zavala F. Cloned cytotoxic T cells recognize an epitope in the circumsporozoite protein and protect against malaria. Nature. 1989 Sep 28;341(6240):323–326. doi: 10.1038/341323a0. [DOI] [PubMed] [Google Scholar]
  25. Romero P., Maryanski J. L., Corradin G., Nussenzweig R. S., Nussenzweig V., Zavala F. Cloned cytotoxic T cells recognize an epitope in the circumsporozoite protein and protect against malaria. Nature. 1989 Sep 28;341(6240):323–326. doi: 10.1038/341323a0. [DOI] [PubMed] [Google Scholar]
  26. Taracha E. L., Goddeeris B. M., Scott J. R., Morrison W. I. Standardization of a technique for analysing the frequency of parasite-specific cytotoxic T lymphocyte precursors in cattle immunized with Theileria parva. Parasite Immunol. 1992 Mar;14(2):143–154. doi: 10.1111/j.1365-3024.1992.tb00457.x. [DOI] [PubMed] [Google Scholar]
  27. Taylor P. M., Askonas B. A. Influenza nucleoprotein-specific cytotoxic T-cell clones are protective in vivo. Immunology. 1986 Jul;58(3):417–420. [PMC free article] [PubMed] [Google Scholar]
  28. Teale A. J., Morrison W. I., Goddeeris B. M., Groocock C. M., Stagg D. A., Spooner R. L. Bovine alloreactive cytotoxic cells generated in vitro: target specificity in relation to BoLA phenotype. Immunology. 1985 Jun;55(2):355–362. [PMC free article] [PubMed] [Google Scholar]
  29. Weiss W. R., Berzofsky J. A., Houghten R. A., Sedegah M., Hollindale M., Hoffman S. L. A T cell clone directed at the circumsporozoite protein which protects mice against both Plasmodium yoelii and Plasmodium berghei. J Immunol. 1992 Sep 15;149(6):2103–2109. [PubMed] [Google Scholar]
  30. Williams D. J., Newson J., Naessens J. Quantitation of bovine immunoglobulin isotypes and allotypes using monoclonal antibodies. Vet Immunol Immunopathol. 1990 Mar;24(3):267–283. doi: 10.1016/0165-2427(90)90042-q. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES