Skip to main content
NCBI home page
Immunology logoLink to Immunology
. 1984 Jun;52(2):211–219.

Immunoregulation in experimental filariasis. III. Demonstration and characterization of antigen-specific suppressor cells in the spleen of Brugia pahangi-infected jirds.

P J Lammie, S P Katz
PMCID: PMC1454610  PMID: 6203831

Abstract

Antigen specific immunoregulatory phenomena in both human and experimental filariasis are correlated with the presence of circulating microfilariae. Previous studies of inbred jirds infected with Brugia pahangi have demonstrated that the onset of microfilaremia (8-10 weeks post-infection) is associated with a loss of responsiveness to parasite antigens in the spleen, but not the lymph nodes of infected animals. The present experiments defined immunoregulatory phenomena responsible for altered antigen-specific in vitro lymphocyte blastogenesis in the spleen of B. pahangi-infected jirds. Diminished splenic responsiveness to B. pahangi antigens was associated with the presence of a cell capable of suppressing the responsiveness of lymph node cells from infected jirds to parasite antigens. antigen-induced in vitro blastogenic responsiveness of spleen cells from microfilaremic , but not normal animals was restored by depletion of cells adherent to nylon wool or bearing receptors for histamine, peanut agglutinin, soybean agglutinin or jird Fc. The responsiveness of spleen cells from chronically infected (greater than or equal to 20 weeks) animals to mitogens, but not parasite antigens, was enhanced by removal of plastic-adherent cells. The results suggest the involvement of antigen-specific suppressor T cells, in the spleen of B. phangi -infected jirds which are distinct from non-specific suppressor cells previously described in this system.

Full text

PDF
211

Selected References

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

  1. Askenase P. W., Schwartz A., Siegel J. N., Gershon R. K. Role of histamine in the regulation of cell-mediated immunity. Int Arch Allergy Appl Immunol. 1981;66 (Suppl 1):225–233. doi: 10.1159/000232907. [DOI] [PubMed] [Google Scholar]
  2. Beer D. J., Osband M. E., McCaffrey R. P., Soter N. A., Rocklin R. E. Abnormal histamine-induced suppressor-cell function in atopic subjects. N Engl J Med. 1982 Feb 25;306(8):454–458. doi: 10.1056/NEJM198202253060804. [DOI] [PubMed] [Google Scholar]
  3. Beer D. J., Rosenwasser L. J., Dinarello C. A., Rocklin R. E. Cellular interactions in the generation and expression of histamine-induced suppressor activity. Cell Immunol. 1982 May 1;69(1):101–112. doi: 10.1016/0008-8749(82)90054-5. [DOI] [PubMed] [Google Scholar]
  4. Berrih S., London J., Bonavida B. Murine spleen lymphocytes bearing receptors for peanut agglutinin. VII Separation and functional characterization. Cell Immunol. 1981 Sep 15;63(2):249–258. doi: 10.1016/0008-8749(81)90004-6. [DOI] [PubMed] [Google Scholar]
  5. Ellner J. J. Suppressor adherent cells in human tuberculosis. J Immunol. 1978 Dec;121(6):2573–2579. [PubMed] [Google Scholar]
  6. Gupta S., Good R. A. Subpopulations of human T lymphocytes: laboratory and clinical studies. Immunol Rev. 1981;56:89–114. doi: 10.1111/j.1600-065x.1981.tb01048.x. [DOI] [PubMed] [Google Scholar]
  7. Holroyde M. C., Eyre P. Modulation of antigen-induced histamine release from bovine granulocytes by several anti-allergic agents. Int Arch Allergy Appl Immunol. 1977;53(6):515–519. doi: 10.1159/000231793. [DOI] [PubMed] [Google Scholar]
  8. Julius M. H., Simpson E., Herzenberg L. A. A rapid method for the isolation of functional thymus-derived murine lymphocytes. Eur J Immunol. 1973 Oct;3(10):645–649. doi: 10.1002/eji.1830031011. [DOI] [PubMed] [Google Scholar]
  9. Katz S. P., Lammie P. J. Effect of cyclophosphamide on the immune responsiveness of jirds infected with Brugia pahangi. Infect Immun. 1984 Feb;43(2):753–755. doi: 10.1128/iai.43.2.753-755.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Klei T. R., Enright F. M., Blanchard D. P., Uhl S. A. Specific hypo-responsive granulomatous tissue reactions in Brugia pahangi-infected jirds. Acta Trop. 1981 Sep;38(3):267–276. [PubMed] [Google Scholar]
  11. Kwa B. H., Mak J. W. Specific depression of cell-mediated immunity in Malayan filariasis. Trans R Soc Trop Med Hyg. 1980;74(4):522–527. doi: 10.1016/0035-9203(80)90070-x. [DOI] [PubMed] [Google Scholar]
  12. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  13. Lammie P. J., Katz S. P. Immunoregulation in experimental filariasis. I. In vitro suppression of mitogen-induced blastogenesis by adherent cells from Jirds chronically infected with Brugia pahangi. J Immunol. 1983 Mar;130(3):1381–1385. [PubMed] [Google Scholar]
  14. Lammie P. J., Katz S. P. Immunoregulation in experimental filariasis. IV. Induction of non-specific suppression following in vitro exposure of spleen cells from infected jirds to Brugia pahangi antigen. Immunology. 1984 Jun;52(2):221–229. [PMC free article] [PubMed] [Google Scholar]
  15. McCall J. W., Malone J. B., Hyong-Sun A., Thompson P. E. Mongolian jirds (Meriones unguiculatus) infected with Brugia pahangi by the intraperitoneal route: a rich source of developing larvae, adult filariae, and microfilariae. J Parasitol. 1973 Jun;59(3):436–436. [PubMed] [Google Scholar]
  16. Mitchell G. F., Anders R. F., Brown G. V., Handman E., Roberts-Thomson I. C., Chapman C. B., Forsyth K. P., Kahl L. P., Cruise K. M. Analysis of infection characteristics and antiparasite immune responses in resistant compared with susceptible hosts. Immunol Rev. 1982;61:137–188. doi: 10.1111/j.1600-065x.1982.tb00376.x. [DOI] [PubMed] [Google Scholar]
  17. Moretta L., Webb S. R., Grossi C. E., Lydyard P. M., Cooper M. D. Functional analysis of two human T-cell subpopulations: help and suppression of B-cell responses by T cells bearing receptors for IgM or IgG. J Exp Med. 1977 Jul 1;146(1):184–200. doi: 10.1084/jem.146.1.184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nakano T., Imai Y., Naiki M., Osawa T. Characterization of mouse helper and suppressor T cell subsets separated by lectins. J Immunol. 1980 Nov;125(5):1928–1932. [PubMed] [Google Scholar]
  19. Ogden B. E., Hill H. R. Histamine regulates lymphocyte mitogenic responses through activation of specific H1 and H2 histamine receptors. Immunology. 1980 Sep;41(1):107–114. [PMC free article] [PubMed] [Google Scholar]
  20. Ottesen E. A., Kumaraswami V., Paranjape R., Poindexter R. W., Tripathy S. P. Naturally occurring blocking antibodies modulate immediate hypersensitivity responses in human filariasis. J Immunol. 1981 Nov;127(5):2014–2020. [PubMed] [Google Scholar]
  21. Ottesen E. A. Modulation of the host response in human schistosomiasis. I. Adherent suppressor cells that inhibit lymphocyte proliferative responses to parasite antigens. J Immunol. 1979 Oct;123(4):1639–1644. [PubMed] [Google Scholar]
  22. Ottesen E. A., Neva F. A., Paranjape R. S., Tripathy S. P., Thiruvengadam K. V., Beaven M. A. Specific allergic sensitsation to filarial antigens in tropical eosinophilia syndrome. Lancet. 1979 Jun 2;1(8127):1158–1161. doi: 10.1016/s0140-6736(79)91842-7. [DOI] [PubMed] [Google Scholar]
  23. Ottesen E. A., Weller P. F., Heck L. Specific cellular immune unresponsiveness in human filariasis. Immunology. 1977 Sep;33(3):413–421. [PMC free article] [PubMed] [Google Scholar]
  24. Petersen E. A., Neva F. A., Oster C. N., Bogaert Diaz H. Specific inhibition of lymphocyte-proliferation responses by adherent suppressor cells in diffuse cutaneous leishmaniasis. N Engl J Med. 1982 Feb 18;306(7):387–392. doi: 10.1056/NEJM198202183060702. [DOI] [PubMed] [Google Scholar]
  25. Piessens W. F., McGreevy P. B., Piessens P. W., McGreevy M., Koiman I., Saroso J. S., Dennis D. T. Immune responses in human infections with Brugia malayi: specific cellular unresponsiveness to filarial antigens. J Clin Invest. 1980 Jan;65(1):172–179. doi: 10.1172/JCI109648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Piessens W. F., Partono F., Hoffman S. L., Ratiwayanto S., Piessens P. W., Palmieri J. R., Koiman I., Dennis D. T., Carney W. P. Antigen-specific suppressor T lymphocytes in human lymphatic filariasis. N Engl J Med. 1982 Jul 15;307(3):144–148. doi: 10.1056/NEJM198207153070302. [DOI] [PubMed] [Google Scholar]
  27. Piessens W. F., Ratiwayanto S., Piessens P. W., Tuti S., McGreevy P. B., Darwis F., Palmieri J. R., Koiman I., Dennis D. T. Effect of treatment with diethylcarbamazine on immune responses to filarial antigens in patients infected with Brugia malayi. Acta Trop. 1981 Sep;38(3):227–234. [PubMed] [Google Scholar]
  28. Piessens W. F., Ratiwayanto S., Tuti S., Palmieri J. H., Piessens P. W., Koiman I., Dennis D. T. Antigen-specific suppressor cells and suppressor factors in human filariasis with Brugia malayi. N Engl J Med. 1980 Apr 10;302(15):833–837. doi: 10.1056/NEJM198004103021503. [DOI] [PubMed] [Google Scholar]
  29. Plaut M. Histamine, H1 and H2 antihistamines, and immediate hypersensitivity reactions. J Allergy Clin Immunol. 1979 Jun;63(6):371–375. doi: 10.1016/0091-6749(79)90208-2. [DOI] [PubMed] [Google Scholar]
  30. Reisner Y., Pahwa S., Chiao J. W., Sharon N., Evans R. L., Good R. A. Separation of antibody helper and antibody suppressor human T cells by using soybean agglutinin. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6778–6782. doi: 10.1073/pnas.77.11.6778. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Reisner Y., Ravid A., Sharon N. Use of soybean agglutinin for the separation of mouse B and T lymphocytes. Biochem Biophys Res Commun. 1976 Oct 18;72(4):1585–1591. doi: 10.1016/s0006-291x(76)80195-7. [DOI] [PubMed] [Google Scholar]
  32. Rocklin R. E., Breard J., Gupta S., Good R. A., Melmon K. L. Characterization of the human blood lymphocytes that produce a histamine-induced suppressor factor (HSF). Cell Immunol. 1980 May;51(2):226–237. doi: 10.1016/0008-8749(80)90255-5. [DOI] [PubMed] [Google Scholar]
  33. Segal S., Melmon K. L., Weinstein Y. Isolation of suppressor T lymphocytes adherent to histamine conjugated albumin and their role in suppression of IgG response to SRBC. Cell Immunol. 1981 Mar 15;59(1):171–180. doi: 10.1016/0008-8749(81)90444-5. [DOI] [PubMed] [Google Scholar]
  34. Suzuki S., Huchet R. Mechanism of histamine-induced inhibition of lymphocyte response to mitogens in mice. Cell Immunol. 1981 Aug;62(2):396–405. doi: 10.1016/0008-8749(81)90340-3. [DOI] [PubMed] [Google Scholar]
  35. Suzuki S., Huchet R. Properties of histamine-induced suppressor factor in the regulation of lymphocyte response to PHA in mice. Cell Immunol. 1982 Apr;68(2):349–358. doi: 10.1016/0008-8749(82)90119-8. [DOI] [PubMed] [Google Scholar]
  36. Szewczuk M. R., Campbell R. J., Smith J. W. Evidence for histamine-induced auto-anti-idiotypic antibody immunoregulation in vivo. Cell Immunol. 1981 Nov 15;65(1):152–165. doi: 10.1016/0008-8749(81)90060-5. [DOI] [PubMed] [Google Scholar]
  37. Thomas Y., Huchet R., Granjon D. Histamine-induced suppressor cells of lymphocyte mitogenic response. Cell Immunol. 1981 Apr;59(2):268–275. doi: 10.1016/0008-8749(81)90408-1. [DOI] [PubMed] [Google Scholar]
  38. Weinstein Y., Melmon K. L., Bourne H. R., Sela M. Specific leukocyte receptors for small endogenous hormones. Detection by cell binding to insolubilized hormone preparations. J Clin Invest. 1973 Jun;52(6):1349–1361. doi: 10.1172/JCI107307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Weiss N. Dipetalonema viteae: in vitro blastogenesis of hamster spleen and lymph node cells to phytohemagglutinin and filarial antigens. Exp Parasitol. 1978 Dec;46(2):283–299. doi: 10.1016/0014-4894(78)90142-x. [DOI] [PubMed] [Google Scholar]
  40. Wong M. M., Guest M. F. Filarial antibodies and eosinophilia in human subjects in an endemic area. Trans R Soc Trop Med Hyg. 1969;63(6):796–800. doi: 10.1016/0035-9203(69)90123-0. [DOI] [PubMed] [Google Scholar]

Articles from Immunology are provided here courtesy of British Society for Immunology

RESOURCES