Skip to main content
NCBI home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1980 Jun 1;151(6):1398–1412. doi: 10.1084/jem.151.6.1398

Regulation of granulomatous inflammation in murine schistosomiasis. In vitro characterization of T lymphocyte subsets involved in the production and suppression of migration inhibition factor

PMCID: PMC2185871  PMID: 6155422

Abstract

Host granulomatous inflammation in murine schistosomiasis mansoni is a T cell-mediated immune response, which, at the chronic stage of the disease, undergoes T suppressor lymphocyte-dependent modulation. In the present study this phenomenon was further analyzed in vitro. Spleen cells of mice undergoing modulation (20 wk of infection) when mixed with spleen cells of animals exhibiting vigorous granulomatous responses (8 wk of infection) abrogated in vitro migration inhibition factor (MIF) production by the latter. Characterization of the delayed- type hypersensitivity T lymphocytes involved in lymphokine production showed that they belonged to the Lyt-1+ subset and did not express I region-encoded antigens. In contrast, T lymphocytes involved in the suppression of MIF activity belonged to the Lyt-2+ subpopulation of cells, which expressed I-J- and I-C-subregion determinants. These results suggest that the modulation of the granulomatous hypersensitivity response in mice is the result of T-T cell interaction with subsequent regulation of inflammatory lymphokine production.

Full Text

The Full Text of this article is available as a PDF (794.3 KB).

Selected References

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

  1. ANDRADE Z. A. WARREN KS: MILD PROLONGED SCHISTOSOMIASIS IN MICE: ALTERATIONS IN HOST RESPONSE WITH TIME AND THE DEVELOPMENT OF PORTAL FIBROSIS. Trans R Soc Trop Med Hyg. 1964 Jan;58:53–57. doi: 10.1016/0035-9203(64)90068-9. [DOI] [PubMed] [Google Scholar]
  2. Artz R. P., Bullock W. E. Immunoregulatory responses in experimental disseminated histoplasmosis: depression of T-cell-dependent and T-effectory responses by activation of splenic suppressor cells. Infect Immun. 1979 Mar;23(3):893–902. doi: 10.1128/iai.23.3.893-902.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bloom B. R., Shevach E. Requirement for T cells in the production of migration inhibitory factor. J Exp Med. 1975 Nov 1;142(5):1306–1311. doi: 10.1084/jem.142.5.1306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boros D. L., Pelley R. P., Warren K. S. Spontaneous modulation of granulomatous hypersensitivity in schistosomiasis mansoni. J Immunol. 1975 May;114(5):1437–1441. [PubMed] [Google Scholar]
  5. Boros D. L., Warren K. S. Delayed hypersensitivity-type granuloma formation and dermal reaction induced and elicited by a soluble factor isolated from Schistosoma mansoni eggs. J Exp Med. 1970 Sep 1;132(3):488–507. doi: 10.1084/jem.132.3.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boros D. L., Warren K. S., Pelley R. P. The secretion of migration inhibitory factor by intact schistosome egg granulomas maintained in vitro. Nature. 1973 Nov 23;246(5430):224–226. doi: 10.1038/246224a0. [DOI] [PubMed] [Google Scholar]
  7. Bullock W. E., Carlson E. M., Gershon R. K. The evolution of immunosuppressive cell populations in experimental mycobacterial infection. J Immunol. 1978 May;120(5):1709–1716. [PubMed] [Google Scholar]
  8. Cantor H., Boyse E. A. Regulation of cellular and humoral immune responses by T-cell subclasses. Cold Spring Harb Symp Quant Biol. 1977;41(Pt 1):23–32. doi: 10.1101/sqb.1977.041.01.006. [DOI] [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., Boros D. L. Population dynamics of T and B lymphocytes in the lymphoid organs, circulation, and granulomas of mice infected with Schistosoma mansoni. Am J Trop Med Hyg. 1979 Mar;28(2):291–299. doi: 10.4269/ajtmh.1979.28.291. [DOI] [PubMed] [Google Scholar]
  11. Colley D. G. Adoptive suppression of granuloma formation. J Exp Med. 1976 Mar 1;143(3):696–700. doi: 10.1084/jem.143.3.696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Colley D. G., Lewis F. A., Todd C. W. Adoptive suppression of granuloma formation by T lymphocytes and by lymphoid cells sensitive to cyclophosphamide. Cell Immunol. 1979 Aug;46(1):192–200. doi: 10.1016/0008-8749(79)90258-2. [DOI] [PubMed] [Google Scholar]
  15. DAVID J. R., LAWRENCE H. S., THOMAL L. DELAYED HYPERSENSITIVITY IN VITRO. II. EFFECT OF SENSITIVE CELLS ON NORMAL CELLS IN THE PRESENCE OF ANTIGEN. J Immunol. 1964 Aug;93:274–278. [PubMed] [Google Scholar]
  16. David J. R. Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc Natl Acad Sci U S A. 1966 Jul;56(1):72–77. doi: 10.1073/pnas.56.1.72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Domingo E. O., Warren K. S. Endogenous desensitization: changing host granulomatou response to schistosome eggs at different stages of infection with schistosoma mansoni. Am J Pathol. 1968 Feb;52(2):369–379. [PMC free article] [PubMed] [Google Scholar]
  18. Eardley D. D., Hugenberger J., McVay-Boudreau L., Shen F. W., Gershon R. K., Cantor H. Immunoregulatory circuits among T-cell sets. I. T-helper cells induce other T-cell sets to exert feedback inhibition. J Exp Med. 1978 Apr 1;147(4):1106–1115. doi: 10.1084/jem.147.4.1106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fox R. A., Rajaraman K. Macrophage migration stimulation factor, migration inhibition factor and the role of suppressor cells in their production. Cell Immunol. 1979 Sep 15;47(1):69–78. doi: 10.1016/0008-8749(79)90315-0. [DOI] [PubMed] [Google Scholar]
  20. Greene M. I., Pierres A., Dorf M. E., Benacerraf B. The I-J subregion codes for determinats on suppressor factor(s) which limit the contact sensitivity response to picryl chloride. J Exp Med. 1977 Jul 1;146(1):293–296. doi: 10.1084/jem.146.1.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. James S. L., Colley D. G. Eosinophils and immune mechanisms: production of the lymphokine eosinophil stimulation promoter (ESP) in vitro by isolated intact granulomas. J Reticuloendothel Soc. 1975 Nov;18(5):283–293. [PubMed] [Google Scholar]
  22. Mage M. G., McHugh L. L., Rothstein T. L. Mouse lymphocytes with and without surface immunoglobulin: preparative scale separation in polystyrene tissue culture dishes coated with specifically purified anti-immunoglobulin. J Immunol Methods. 1977;15(1):47–56. doi: 10.1016/0022-1759(77)90016-3. [DOI] [PubMed] [Google Scholar]
  23. Newman W., Gordon S., Hämmerling U., Senik A., Bloom B. R. Production of migration inhibition factor (MIF) and an inducer of plasminogen activator (IPA) by subsets of T cells in MLC. J Immunol. 1978 Mar;120(3):927–931. [PubMed] [Google Scholar]
  24. Okumura K., Herzenberg L. A., Murphy D. B., McDevitt H. O., Herzenberg L. A. Selective expression of H-2 (i-region) loci controlling determinants on helper and suppressor T lymphocytes. J Exp Med. 1976 Sep 1;144(3):685–698. doi: 10.1084/jem.144.3.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. 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]
  27. Rich S. S., David C. S., Rich R. R. Regulatory mechanisms in cell-mediated immune responses. VII. Presence of I-C subregion determinants on mixed leukocyte reaction suppressor factor. J Exp Med. 1979 Jan 1;149(1):114–126. doi: 10.1084/jem.149.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sogandares-Bernal F., Brandt S. Antibodies sequestered in the liver granulomata of 8-week infections of CF1 mice by Schistosoma mansoni Sambon, 1907. Z Parasitenkd. 1976 Oct 12;50(3):331–334. doi: 10.1007/BF02462977. [DOI] [PubMed] [Google Scholar]
  29. Sy M. S., Miller S. D., Moorhead J. W., Claman H. N. Active suppression of 1-fluoro-2,4-dinitrobenzene-immune T cells. Requirement of an auxiliary T cell induced by antigen. J Exp Med. 1979 May 1;149(5):1197–1207. doi: 10.1084/jem.149.5.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tada T., Taniguchi M., David C. S. Properties of the antigen-specific suppressive T-cell factor in the regulation of antibody response of the mouse. IV. Special subregion assignment of the gene(s) that codes for the suppressive T-cell factor in the H-2 histocompatibility complex. J Exp Med. 1976 Sep 1;144(3):713–725. doi: 10.1084/jem.144.3.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Talwar G. P., Krishnan A. D., Mehra V. L., Blum E. A., Pearson J. M. Evaluation of cell mediated immune responses in untreated cases of leprosy. Clin Exp Immunol. 1972 Oct;12(2):195–203. [PMC free article] [PubMed] [Google Scholar]
  32. Vadas M. A., Miller J. F., McKenzie I. F., Chism S. E., Shen F. W., Boyse E. A., Gamble J. R., Whitelaw A. M. Ly and Ia antigen phenotypes of T cells involved in delayed-type hypersensitivity and in suppression. J Exp Med. 1976 Jul 1;144(1):10–19. doi: 10.1084/jem.144.1.10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Warren K. S., Domingo E. O., Cowan R. B. Granuloma formation around schistosome eggs as a manifestation of delayed hypersensitivity. Am J Pathol. 1967 Nov;51(5):735–756. [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES