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. 1991 Jul;73(3):327–333.

Patterns of cytokine production and proliferation by T lymphocytes differ in mice vaccinated or infected with Schistosoma mansoni.

R M Pemberton 1, L E Smythies 1, A P Mountford 1, R A Wilson 1
PMCID: PMC1384551  PMID: 1908821

Abstract

C57BL/6 mice vaccinated with irradiated cercariae of Schistosoma mansoni are highly resistant to challenge infection. To examine the role of T-helper (Th) activity in these vaccinated (V20) mice, cells from skin- and lung-draining lymph nodes (LN) and the spleen were cultured in vitro with soluble schistosomular antigen. Peak proliferation and release of T-cell growth factor (TCGF) by axillary LN cells on Day 5, and by mediastinal LN cells on Day 18, reflected the kinetics of parasite migration. High levels of interferon-gamma (IFN-gamma) were detected and production was prolonged, particularly in the mediastinal LN. The majority of the above activity was ablated with anti-CD4 antibody. IFN-gamma production by spleen cells increased, whilst proliferation and TCGF release remained low. Although levels of proliferation were similar, more IFN-gamma was released by LN cells from V20 mice than by those from mice infected with normal parasites (NI). This difference in IFN-gamma production was magnified by the greater number of cells in LN of V20 than NI mice. On Day 22 post-exposure, 24-fold more IFN-gamma was produced per pair of axillary LN in the former group. LN cells from V20 mice produced interleukin (IL)-2 and IL-4, whereas those from NI mice released IL-2 but negligible IL-4. Greater quantities of IL-3 were secreted by cells from V20 than from NI mice. These results support the conclusion that IFN-gamma-producing memory Th cells, generated in the LN of V20 mice, play an important role in protective immunity against S. mansoni.

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Selected References

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

  1. Aitken R., Coulson P. S., Wilson R. A. Pulmonary leukocytic responses are linked to the acquired immunity of mice vaccinated with irradiated cercariae of Schistosoma mansoni. J Immunol. 1988 May 15;140(10):3573–3579. [PubMed] [Google Scholar]
  2. Budd R. C., Cerottini J. C., MacDonald H. R. Selectively increased production of interferon-gamma by subsets of Lyt-2+ and L3T4+ T cells identified by expression of Pgp-1. J Immunol. 1987 Jun 1;138(11):3583–3586. [PubMed] [Google Scholar]
  3. Dean D. A. Schistosoma and related genera: acquired resistance in mice. Exp Parasitol. 1983 Feb;55(1):1–104. doi: 10.1016/0014-4894(83)90002-4. [DOI] [PubMed] [Google Scholar]
  4. Firestein G. S., Roeder W. D., Laxer J. A., Townsend K. S., Weaver C. T., Hom J. T., Linton J., Torbett B. E., Glasebrook A. L. A new murine CD4+ T cell subset with an unrestricted cytokine profile. J Immunol. 1989 Jul 15;143(2):518–525. [PubMed] [Google Scholar]
  5. Gillis S., Smith K. A. Long term culture of tumour-specific cytotoxic T cells. Nature. 1977 Jul 14;268(5616):154–156. doi: 10.1038/268154a0. [DOI] [PubMed] [Google Scholar]
  6. Hecht T. T., Longo D. L., Matis L. A. The relationship between immune interferon production and proliferation in antigen-specific, MHC-restricted T cell lines and clones. J Immunol. 1983 Sep;131(3):1049–1055. [PubMed] [Google Scholar]
  7. James S. L., Correa-Oliveira R., Leonard E. J. Defective vaccine-induced immunity to Schistosoma mansoni in P strain mice. II. Analysis of cellular responses. J Immunol. 1984 Sep;133(3):1587–1593. [PubMed] [Google Scholar]
  8. James S. L., Sher A. Cell-mediated immune response to schistosomiasis. Curr Top Microbiol Immunol. 1990;155:21–31. doi: 10.1007/978-3-642-74983-4_2. [DOI] [PubMed] [Google Scholar]
  9. Kelly E. A., Colley D. G. In vivo effects of monoclonal anti-L3T4 antibody on immune responsiveness of mice infected with Schistosoma mansoni. Reduction of irradiated cercariae-induced resistance. J Immunol. 1988 Apr 15;140(8):2737–2745. [PubMed] [Google Scholar]
  10. Kelso A., Glasebrook A. L., Kanagawa O., Brunner K. T. Production of macrophage-activating factor by T lymphocyte clones and correlation with other lymphokine activities. J Immunol. 1982 Aug;129(2):550–556. [PubMed] [Google Scholar]
  11. Kelso A., Gough N. M. Coexpression of granulocyte-macrophage colony-stimulating factor, gamma interferon, and interleukins 3 and 4 is random in murine alloreactive T-lymphocyte clones. Proc Natl Acad Sci U S A. 1988 Dec;85(23):9189–9193. doi: 10.1073/pnas.85.23.9189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lazdins J. K., Stein M. J., David J. R., Sher A. Schistosoma mansoni: rapid isolation and purification of schistosomula of different developmental stages by centrifugation on discontinuous density gradients of Percoll. Exp Parasitol. 1982 Feb;53(1):39–44. doi: 10.1016/0014-4894(82)90090-x. [DOI] [PubMed] [Google Scholar]
  13. Lewis F. A., Wilson E. M. Regional and splenic lymphocyte proliferative responses of mice exposed to normal or irradiated Schistosoma mansoni cercariae. Am J Trop Med Hyg. 1982 May;31(3 Pt 1):505–513. doi: 10.4269/ajtmh.1982.31.505. [DOI] [PubMed] [Google Scholar]
  14. Mangold B. L., Dean D. A. The migration and survival of gamma-irradiated Schistosoma mansoni larvae and the duration of host-parasite contact in relation to the induction of resistance in mice. Parasitology. 1984 Apr;88(Pt 2):249–265. [PubMed] [Google Scholar]
  15. Mastin A. J., Bickle Q. D., Wilson R. A. Schistosoma mansoni: migration and attrition of irradiated and challenge schistosomula in the mouse. Parasitology. 1983 Aug;87(Pt 1):87–102. doi: 10.1017/s0031182000052446. [DOI] [PubMed] [Google Scholar]
  16. Menson E. N., Wilson R. A. Lung-phase immunity to Schistosoma mansoni. Flow cytometric analysis of macrophage activation states in vaccinated mice. J Immunol. 1989 Oct 1;143(7):2342–2348. [PubMed] [Google Scholar]
  17. Mountford A. P., Wilson R. A. Schistosoma mansoni: the effect of regional lymphadenectomy on the level of protection induced in mice by radiation-attenuated cercariae. Exp Parasitol. 1990 Nov;71(4):463–469. doi: 10.1016/0014-4894(90)90072-k. [DOI] [PubMed] [Google Scholar]
  18. Ohara J., Paul W. E. Production of a monoclonal antibody to and molecular characterization of B-cell stimulatory factor-1. Nature. 1985 May 23;315(6017):333–336. doi: 10.1038/315333a0. [DOI] [PubMed] [Google Scholar]
  19. Pearce E. J., Caspar P., Grzych J. M., Lewis F. A., Sher A. Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med. 1991 Jan 1;173(1):159–166. doi: 10.1084/jem.173.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ramalho-Pinto F. J., Gazzinelli G., Howells R. E., Mota-Santos T. A., Figueiredo E. A., Pellegrino J. Schistosoma mansoni: defined system for stepwise transformation of cercaria to schistosomule in vitro. Exp Parasitol. 1974 Dec;36(3):360–372. doi: 10.1016/0014-4894(74)90076-9. [DOI] [PubMed] [Google Scholar]
  21. Sanders M. E., Makgoba M. W., Shaw S. Human naive and memory T cells: reinterpretation of helper-inducer and suppressor-inducer subsets. Immunol Today. 1988 Jul-Aug;9(7-8):195–199. doi: 10.1016/0167-5699(88)91212-1. [DOI] [PubMed] [Google Scholar]
  22. Scott P., Pearce E., Cheever A. W., Coffman R. L., Sher A. Role of cytokines and CD4+ T-cell subsets in the regulation of parasite immunity and disease. Immunol Rev. 1989 Dec;112:161–182. doi: 10.1111/j.1600-065x.1989.tb00557.x. [DOI] [PubMed] [Google Scholar]
  23. Sher A., Coffman R. L., Hieny S., Cheever A. W. Ablation of eosinophil and IgE responses with anti-IL-5 or anti-IL-4 antibodies fails to affect immunity against Schistosoma mansoni in the mouse. J Immunol. 1990 Dec 1;145(11):3911–3916. [PubMed] [Google Scholar]
  24. Spitalny G. L., Havell E. A. Monoclonal antibody to murine gamma interferon inhibits lymphokine-induced antiviral and macrophage tumoricidal activities. J Exp Med. 1984 May 1;159(5):1560–1565. doi: 10.1084/jem.159.5.1560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Vignali D. A., Crocker P., Bickle Q. D., Cobbold S., Waldmann H., Taylor M. G. A role for CD4+ but not CD8+ T cells in immunity to Schistosoma mansoni induced by 20 krad-irradiated and Ro 11-3128-terminated infections. Immunology. 1989 Aug;67(4):466–472. [PMC free article] [PubMed] [Google Scholar]
  26. Wilson R. A., Coulson P. S. Lung-phase immunity to Schistosomes: a new perspective on an old problem? Parasitol Today. 1989 Sep;5(9):274–278. doi: 10.1016/0169-4758(89)90017-3. [DOI] [PubMed] [Google Scholar]
  27. Wilson R. A. Leaky livers, portal shunting and immunity to schistosomes. Parasitol Today. 1990 Nov;6(11):354–358. doi: 10.1016/0169-4758(90)90414-y. [DOI] [PubMed] [Google Scholar]
  28. Zurawski S. M., Mosmann T. R., Benedik M., Zurawski G. Alterations in the amino-terminal third of mouse interleukin 2: effects on biological activity and immunoreactivity. J Immunol. 1986 Nov 15;137(10):3354–3360. [PubMed] [Google Scholar]

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