Skip to main content
NCBI home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1988 Mar;81(3):775–781. doi: 10.1172/JCI113383

Schistosoma japonicum egg antigen-specific T cell lines in man. Induction of helper and suppressor T cell lines and clones in vitro in a patient with chronic schistosomiasis japonica.

N Ohta 1, T Itagaki 1, M Minai 1, K Hirayama 1, Y Hosaka 1
PMCID: PMC442525  PMID: 2449460

Abstract

T cell lines (TCLs) specific for Schistosoma japonicum egg antigen were established from a patient with chronic schistosomiasis japonica to investigate the regulatory mechanism of S.japonicum egg antigen-driven T cell responses in man. All five TCLs tested were CD2+, CD4+, CD8-, and were strongly proliferative only to S. japonicum egg antigen in the absence of exogenous IL-2. All but one TCL produced IL-2-like lymphokines in vitro, indicating their helper T cell functions. One TCL, SjE-3, failed to produce IL-2-like lymphokines. Moreover, this TCL suppressed the specific proliferation of autologous peripheral blood lymphocytes to S. japonicum egg antigen. This TCL produced a soluble suppressor factor(s). These functional diversities among established TCLs were also confirmed by cloned T cells. Our observations might suggest that the regulatory system through helper and suppressor T-T interactions somehow involved in T cell responses to the egg antigen in human chronic schistosomiasis japonica.

Full text

PDF
775

Selected References

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

  1. Abe T., Colley D. G. Modulation of Schistosoma mansoni egg-induced granuloma formation. III. Evidence for an anti-idiotypic, I-J-positive, I-J-restricted, soluble T suppressor factor. J Immunol. 1984 Apr;132(4):2084–2088. [PubMed] [Google Scholar]
  2. Arthur R. P., Mason D. T cells that help B cell responses to soluble antigen are distinguishable from those producing interleukin 2 on mitogenic or allogeneic stimulation. J Exp Med. 1986 Apr 1;163(4):774–786. doi: 10.1084/jem.163.4.774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boros D. L., Amsden A. F., Hood A. T. Modulation of granulomatous hypersensitivity. IV. Immunoglobulin and antibody production by vigorous and immunomodulated liver granulomas of Schistosoma mansoni-infected mice. J Immunol. 1982 Mar;128(3):1050–1053. [PubMed] [Google Scholar]
  4. Byram J. E., Doenhoff M. J., Musallam R., Brink L. H., von Lichtenberg F. Schistosoma mansoni infections in T-cell deprived mice, and the ameliorating effect of administering homologous chronic infection serum. II. Pathology. Am J Trop Med Hyg. 1979 Mar;28(2):274–285. doi: 10.4269/ajtmh.1979.28.274. [DOI] [PubMed] [Google Scholar]
  5. CHAFFEE E. F., BAUMAN P. M., SHAPILO J. J. Diagnosis of schistosomiasis by complement-fixation. Am J Trop Med Hyg. 1954 Sep;3(5):905–913. doi: 10.4269/ajtmh.1954.3.905. [DOI] [PubMed] [Google Scholar]
  6. Cheever A. W., Byram J. E., Hieny S., von Lichtenberg F., Lunde M. N., Sher A. Immunopathology of Schistosoma japonicum and S. mansoni infection in B cell depleted mice. Parasite Immunol. 1985 Jul;7(4):399–413. doi: 10.1111/j.1365-3024.1985.tb00086.x. [DOI] [PubMed] [Google Scholar]
  7. Cheever A. W., Byram J. E., von Lichtenberg F. Immunopathology of Schistosoma japonicum infection in athymic mice. Parasite Immunol. 1985 Jul;7(4):387–398. doi: 10.1111/j.1365-3024.1985.tb00085.x. [DOI] [PubMed] [Google Scholar]
  8. Chensue S. W., Boros D. L., David C. S. Regulation of granulomatous inflammation in murine schistosomiasis. II. T suppressor cell-derived, I-C subregion-encoded soluble suppressor factor mediates regulation of lymphokine production. J Exp Med. 1983 Jan 1;157(1):219–230. doi: 10.1084/jem.157.1.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chensue S. W., Boros D. L. Modulation of granulomatous hypersensitivity. I. Characterization of T lymphocytes involved in the adoptive suppression of granuloma formation in Schistosoma mansoni-infected mice. J Immunol. 1979 Sep;123(3):1409–1414. [PubMed] [Google Scholar]
  10. Chensue S. W., Wellhausen S. R., Boros D. L. Modulation of granulomatous hypersensitivity. II. Participation of Ly 1+ and Ly 2+ T lymphocytes in the suppression of granuloma formation and lymphokine production in Schistosoma mansoni-infected mice. J Immunol. 1981 Jul;127(1):363–367. [PubMed] [Google Scholar]
  11. Colley D. G., Hieny S. E., Bartholomew R. K., Cook J. A. Immune responses during human schistosomiasis mansoni. III. Regulatory effect of patient sera on human lymphocyte blastogenic responses to schistosome antigen preparations. Am J Trop Med Hyg. 1977 Sep;26(5 Pt 1):917–925. [PubMed] [Google Scholar]
  12. Colley D. G. Immune responses to a soluble schistosomal egg antigen preparation during chronic primary infection with Schistosoma mansoni. J Immunol. 1975 Jul;115(1):150–156. [PubMed] [Google Scholar]
  13. Colley D. G. T lymphocytes that contribute to the immunoregulation of granuloma formation in chronic murine schistosomiasis. J Immunol. 1981 Apr;126(4):1465–1468. [PubMed] [Google Scholar]
  14. Doughty B. L., Ottesen E. A., Nash T. E., Phillips S. M. Delayed hypersensitivity granuloma formation around Schistosoma mansoni eggs in vitro. III. Granuloma formation and modulation in human Schistosomiasis mansoni. J Immunol. 1984 Aug;133(2):993–997. [PubMed] [Google Scholar]
  15. Doughty B. L., Phillips S. M. Delayed hypersensitivity granuloma formation and modulation around Schistosoma mansoni eggs in vitro. II. Regulatory T cell subsets. J Immunol. 1982 Jan;128(1):37–42. [PubMed] [Google Scholar]
  16. Doughty B. L., Zodda D. M., el Kholy A., Phillips S. M. Delayed type hypersensitivity granuloma formation around Schistosoma mansoni eggs in vitro. IV. Granuloma formation in human schistosomiasis. Am J Trop Med Hyg. 1984 Nov;33(6):1173–1177. doi: 10.4269/ajtmh.1984.33.1173. [DOI] [PubMed] [Google Scholar]
  17. Ellner J. J., Olds G. R., Kamel R., Osman G. S., el-Kholy A., Mahmoud A. A. Suppression splenic T lymphocytes in human hepatosplenic Schistosomiasis mansoni. J Immunol. 1980 Jul;125(1):308–312. [PubMed] [Google Scholar]
  18. Feldmann M., Kontiainen S. Suppressor cell induction in vitro. II. Cellular requirements of suppressor cell induction. Eur J Immunol. 1976 Apr;6(4):302–305. doi: 10.1002/eji.1830060413. [DOI] [PubMed] [Google Scholar]
  19. Garb K. S., Stavitsky A. B., Olds G. R., Tracy J. W., Mahmoud A. A. Immune regulation in murine schistosomiasis japonica: inhibition of in vitro antigen- and mitogen-induced cellular responses by splenocyte culture supernatants and by purified fractions from serum of chronically infected mice. J Immunol. 1982 Dec;129(6):2752–2758. [PubMed] [Google Scholar]
  20. Gillis S., Ferm M. M., Ou W., Smith K. A. T cell growth factor: parameters of production and a quantitative microassay for activity. J Immunol. 1978 Jun;120(6):2027–2032. [PubMed] [Google Scholar]
  21. Green D. R., Flood P. M., Gershon R. K. Immunoregulatory T-cell pathways. Annu Rev Immunol. 1983;1:439–463. doi: 10.1146/annurev.iy.01.040183.002255. [DOI] [PubMed] [Google Scholar]
  22. Hirayama K., Matsushita S., Kikuchi I., Iuchi M., Ohta N., Sasazuki T. HLA-DQ is epistatic to HLA-DR in controlling the immune response to schistosomal antigen in humans. Nature. 1987 Jun 4;327(6121):426–430. doi: 10.1038/327426a0. [DOI] [PubMed] [Google Scholar]
  23. Ishizaka K., Adachi T. Generation of specific helper cells and suppressor cells in vitro for the IgE and IgG antibody responses. J Immunol. 1976 Jul;117(1):40–47. [PubMed] [Google Scholar]
  24. Lammie P. J., Linette G. P., Phillips S. M. Characterization of Schistosoma mansoni antigen-reactive T cell clones that form granulomas in vitro. J Immunol. 1985 Jun;134(6):4170–4175. [PubMed] [Google Scholar]
  25. Moldwin R. L., Lancki D. W., Herold K. C., Fitch F. W. An antigen receptor-driven, interleukin 2-independent pathway for proliferation of murine cytolytic T lymphocyte clones. J Exp Med. 1986 Jun 1;163(6):1566–1582. doi: 10.1084/jem.163.6.1566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Morimoto C., Reinherz E. L., Borel Y., Schlossman S. F. Direct demonstration of the human suppressor inducer subset by anti-T cell antibodies. J Immunol. 1983 Jan;130(1):157–161. [PubMed] [Google Scholar]
  27. Nutman T. B., Ottesen E. A., Fauci A. S., Volkman D. J. Parasite antigen-specific human T cell lines and clones. Major histocompatibility complex restriction and B cell helper function. J Clin Invest. 1984 Jun;73(6):1754–1762. doi: 10.1172/JCI111384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nutman T. B., Volkman D. J., Hussain R., Fauci A. S., Ottesen E. A. Filarial parasite-specific T cell lines: induction of IgE synthesis. J Immunol. 1985 Feb;134(2):1178–1184. [PubMed] [Google Scholar]
  29. Ohta N., Minai M., Sasazuki T. Antigen-specific suppressor T lymphocytes (Leu-2a+3a-) in human schistosomiasis japonica. J Immunol. 1983 Nov;131(5):2524–2528. [PubMed] [Google Scholar]
  30. Ohta N., Nishimura Y. K., Iuchi M., Sasazuki T. Immunogenetic analysis of patients with post-schistosomal liver cirrhosis in man. Clin Exp Immunol. 1982 Sep;49(3):493–499. [PMC free article] [PubMed] [Google Scholar]
  31. Ohta N., Reinsmoen N. L., Bach F. H. Cellular basis of anti-SB response. Hum Immunol. 1984 Nov;11(3):127–141. doi: 10.1016/0198-8859(84)90069-7. [DOI] [PubMed] [Google Scholar]
  32. Olds G. R., Kresina T. F. Network interactions in Schistosoma japonicum infection. Identification and characterization of a serologically distinct immunoregulatory auto-antiidiotypic antibody population. J Clin Invest. 1985 Dec;76(6):2338–2347. doi: 10.1172/JCI112245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Olds G. R., Mahmoud A. A. Kinetics and mechanisms of pulmonary granuloma formation around Schistosoma japonicum eggs injected into mice. Cell Immunol. 1981 May 15;60(2):251–260. doi: 10.1016/0008-8749(81)90267-7. [DOI] [PubMed] [Google Scholar]
  34. Olds G. R., Olveda R., Tracy J. W., Mahmoud A. A. Adoptive transfer of modulation of granuloma formation and hepatosplenic disease in murine schistosomiasis japonica by serum from chronically infected animals. J Immunol. 1982 Mar;128(3):1391–1393. [PubMed] [Google Scholar]
  35. Ottesen E. A., Hiatt R. A., Cheever A. W., Sotomayor Z. R., Neva F. A. The acquisition and loss of antigen-specific cellular immune responsiveness in acute and chronic schistosomiasis in man. Clin Exp Immunol. 1978 Jul;33(1):37–47. [PMC free article] [PubMed] [Google Scholar]
  36. Pelley R. P., Warren K. S. Immunoregulation in chronic infectious disease: schistosomiasis as a model. J Invest Dermatol. 1978 Jul;71(1):49–55. doi: 10.1111/1523-1747.ep12543940. [DOI] [PubMed] [Google Scholar]
  37. Pestel J., Dissous C., Dessaint J. P., Louis J., Engers H., Capron A. Specific Schistosoma mansoni rat T cell clones. I. Generation and functional analysis in vitro and in vivo. J Immunol. 1985 Jun;134(6):4132–4139. [PubMed] [Google Scholar]
  38. Rabin H., Hopkins R. F., 3rd, Ruscetti F. W., Neubauer R. H., Brown R. L., Kawakami T. G. Spontaneous release of a factor with properties of T cell growth factor from a continuous line of primate tumor T cells. J Immunol. 1981 Nov;127(5):1852–1856. [PubMed] [Google Scholar]
  39. Rocklin R. E., Brown A. P., Warren K. S., Pelley R. P., Houba V., Siongok T. K., Ouma J., Sturrock R. F., Butterworth A. E. Factors that modify the cellular-immune response in patients infected by Schistosoma mansoni. J Immunol. 1980 Nov;125(5):1916–1923. [PubMed] [Google Scholar]
  40. Rocklin R. E., Tracy J. W., El Kholy A. Activation of antigen-specific suppressor cells in human schistosomiasis mansoni by fractions of soluble egg antigens nonadherent to Con A sepharose. J Immunol. 1981 Dec;127(6):2314–2318. [PubMed] [Google Scholar]
  41. Sasazuki T., Ohta N., Kaneoka R., Kojima S. Association between an HLA haplotype and low responsiveness to schistosomal worm antigen in man. J Exp Med. 1980 Aug 1;152(2 Pt 2):314s–318s. [PubMed] [Google Scholar]
  42. Todd C. W., Goodgame R. W., Colley D. G. Immune responses during human schistosomiasis mansoni. V. Suppression of schistosome antigen-specific lymphocyte blastogenesis by adherent/phagocytic cells. J Immunol. 1979 Apr;122(4):1440–1446. [PubMed] [Google Scholar]
  43. Warren K. S. The immunopathogenesis of schistosomiasis: a multidisciplinary approach. Trans R Soc Trop Med Hyg. 1972;66(3):417–434. doi: 10.1016/0035-9203(72)90273-8. [DOI] [PubMed] [Google Scholar]
  44. Wee S. L., Bach F. H. Functionally distinct human T cell clones that produce lymphokines with IL-2-like activity. Hum Immunol. 1984 Mar;9(3):175–188. doi: 10.1016/0198-8859(84)90044-2. [DOI] [PubMed] [Google Scholar]
  45. Weinstock J. V., Boros D. L. Heterogeneity of the granulomatous response in the liver, colon, ileum, and ileal Peyer's patches to schistosome eggs in murine schistosomiasis mansoni. J Immunol. 1981 Nov;127(5):1906–1909. [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES