Skip to main content
NCBI home page
Immunology logoLink to Immunology
. 1996 Apr;87(4):642–646. doi: 10.1046/j.1365-2567.1996.505586.x

Acceleration of IgE responses by treatment with recombinant interleukin-3 prior to infection with Trichinella spiralis in mice.

M Korenaga 1, N Watanabe 1, T Abe 1, Y Hashiguchi 1
PMCID: PMC1384145  PMID: 8675221

Abstract

Treatment of mice with recombinant interleukin-3 (rIL-3) accelerated an IL-4-dependent IgE production following infection with Trichinella spiralis. When mice were treated with a total of 1.5 x 10(4) units rIL-3 for 5 days before infection with 400 muscle larvae, the serum IgE level increased prominently on day 5. Acceleration of IgE responses was dependent on the dose of rIL-3 injected. Treatment of mice with a total of 10(3) units rIL-3 could accelerate IgE responses. IgE responses were detected by a sandwich enzyme-linked immunosorbent assay at least from day 3 in mice treated with rIL-3. Acceleration of IgE responses was inhibited by anti-IL-4 monoclonal antibody. In contrast to this, IgG1 and IgG2a responses were not suppressed by the anti-IL-4 treatment. IL-3 treatment could up-regulate IgE and IgG1 responses but not the IgG2a response. IL-3 treatment could also accelerate IgE responses in W/Wv mice infected with the parasites. These results suggest that IL-3 is involved in regulation of IgE responses in mice and that mast cells do not play an essential role in acceleration of IgE responses induced by rIL-3 treatment in this system.

Full text

PDF
642

Images in this article

645Figure 5
on p.645

Selected References

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

  1. Abe T., Nawa Y. Worm expulsion and mucosal mast cell response induced by repetitive IL-3 administration in Strongyloides ratti-infected nude mice. Immunology. 1988 Feb;63(2):181–185. [PMC free article] [PubMed] [Google Scholar]
  2. Alizadeh H., Urban J. F., Jr, Katona I. M., Finkelman F. D. Cells containing IgE in the intestinal mucosa of mice infected with the nematode parasite Trichinella spiralis are predominantly of a mast cell lineage. J Immunol. 1986 Oct 15;137(8):2555–2560. [PubMed] [Google Scholar]
  3. Brunner T., Heusser C. H., Dahinden C. A. Human peripheral blood basophils primed by interleukin 3 (IL-3) produce IL-4 in response to immunoglobulin E receptor stimulation. J Exp Med. 1993 Mar 1;177(3):605–611. doi: 10.1084/jem.177.3.605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Finkelman F. D., Katona I. M., Urban J. F., Jr, Holmes J., Ohara J., Tung A. S., Sample J. V., Paul W. E. IL-4 is required to generate and sustain in vivo IgE responses. J Immunol. 1988 Oct 1;141(7):2335–2341. [PubMed] [Google Scholar]
  5. Finkelman F. D., Urban J. F., Jr, Beckmann M. P., Schooley K. A., Holmes J. M., Katona I. M. Regulation of murine in vivo IgG and IgE responses by a monoclonal anti-IL-4 receptor antibody. Int Immunol. 1991 Jun;3(6):599–607. doi: 10.1093/intimm/3.6.599. [DOI] [PubMed] [Google Scholar]
  6. Gauchat J. F., Henchoz S., Mazzei G., Aubry J. P., Brunner T., Blasey H., Life P., Talabot D., Flores-Romo L., Thompson J. Induction of human IgE synthesis in B cells by mast cells and basophils. Nature. 1993 Sep 23;365(6444):340–343. doi: 10.1038/365340a0. [DOI] [PubMed] [Google Scholar]
  7. Ha T. Y., Reed N. D., Crowle P. K. Delayed expulsion of adult Trichinella spiralis by mast cell-deficient W/Wv mice. Infect Immun. 1983 Jul;41(1):445–447. doi: 10.1128/iai.41.1.445-447.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ihle J. N., Rebar L., Keller J., Lee J. C., Hapel A. J. Interleukin 3: possible roles in the regulation of lymphocyte differentiation and growth. Immunol Rev. 1982;63:5–32. doi: 10.1111/j.1600-065x.1982.tb00409.x. [DOI] [PubMed] [Google Scholar]
  9. Katona I. M., Urban J. F., Jr, Kang S. S., Paul W. E., Finkelman F. D. IL-4 requirements for the generation of secondary in vivo IgE responses. J Immunol. 1991 Jun 15;146(12):4215–4221. [PubMed] [Google Scholar]
  10. Kay A. B., Ying S., Varney V., Gaga M., Durham S. R., Moqbel R., Wardlaw A. J., Hamid Q. Messenger RNA expression of the cytokine gene cluster, interleukin 3 (IL-3), IL-4, IL-5, and granulocyte/macrophage colony-stimulating factor, in allergen-induced late-phase cutaneous reactions in atopic subjects. J Exp Med. 1991 Mar 1;173(3):775–778. doi: 10.1084/jem.173.3.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kimoto M., Kindler V., Higaki M., Ody C., Izui S., Vassalli P. Recombinant murine IL-3 fails to stimulate T or B lymphopoiesis in vivo, but enhances immune responses to T cell-dependent antigens. J Immunol. 1988 Mar 15;140(6):1889–1894. [PubMed] [Google Scholar]
  12. Kindler V., Thorens B., de Kossodo S., Allet B., Eliason J. F., Thatcher D., Farber N., Vassalli P. Stimulation of hematopoiesis in vivo by recombinant bacterial murine interleukin 3. Proc Natl Acad Sci U S A. 1986 Feb;83(4):1001–1005. doi: 10.1073/pnas.83.4.1001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kopf M., Le Gros G., Bachmann M., Lamers M. C., Bluethmann H., Köhler G. Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature. 1993 Mar 18;362(6417):245–248. doi: 10.1038/362245a0. [DOI] [PubMed] [Google Scholar]
  14. Korenaga M., Abe T., Hashiguchi Y. Injection of recombinant interleukin 3 hastens worm expulsion in mice infected with Trichinella spiralis. Parasitol Res. 1996;82(2):108–113. doi: 10.1007/s004360050079. [DOI] [PubMed] [Google Scholar]
  15. Korenaga M., Watanabe N., Tada I. Effects of anti-IgE monoclonal antibody on a primary infection of Strongyloides ratti in mice. Parasitol Res. 1991;77(4):362–363. doi: 10.1007/BF00930917. [DOI] [PubMed] [Google Scholar]
  16. Madden K. B., Urban J. F., Jr, Ziltener H. J., Schrader J. W., Finkelman F. D., Katona I. M. Antibodies to IL-3 and IL-4 suppress helminth-induced intestinal mastocytosis. J Immunol. 1991 Aug 15;147(4):1387–1391. [PubMed] [Google Scholar]
  17. Matsumoto T., Clark S., Rocklin R. E. Induction of IgE synthesis in anti-IgM-activated nonatopic human B cells by recombinant interleukin-3. Int Arch Allergy Appl Immunol. 1989;89(1):24–30. doi: 10.1159/000234918. [DOI] [PubMed] [Google Scholar]
  18. Metcalf D., Begley C. G., Johnson G. R., Nicola N. A., Lopez A. F., Williamson D. J. Effects of purified bacterially synthesized murine multi-CSF (IL-3) on hematopoiesis in normal adult mice. Blood. 1986 Jul;68(1):46–57. [PubMed] [Google Scholar]
  19. Nabel G., Galli S. J., Dvorak A. M., Dvorak H. F., Cantor H. Inducer T lymphocytes synthesize a factor that stimulates proliferation of cloned mast cells. Nature. 1981 May 28;291(5813):332–334. doi: 10.1038/291332a0. [DOI] [PubMed] [Google Scholar]
  20. Nagao K., Yokoro K., Aaronson S. A. Continuous lines of basophil/mast cells derived from normal mouse bone marrow. Science. 1981 Apr 17;212(4492):333–335. doi: 10.1126/science.7209531. [DOI] [PubMed] [Google Scholar]
  21. Palacios R., Henson G., Steinmetz M., McKearn J. P. Interleukin-3 supports growth of mouse pre-B-cell clones in vitro. Nature. 1984 May 10;309(5964):126–131. doi: 10.1038/309126a0. [DOI] [PubMed] [Google Scholar]
  22. Palacios R., Steinmetz M. Il-3-dependent mouse clones that express B-220 surface antigen, contain Ig genes in germ-line configuration, and generate B lymphocytes in vivo. Cell. 1985 Jul;41(3):727–734. doi: 10.1016/s0092-8674(85)80053-2. [DOI] [PubMed] [Google Scholar]
  23. Plaut M., Pierce J. H., Watson C. J., Hanley-Hyde J., Nordan R. P., Paul W. E. Mast cell lines produce lymphokines in response to cross-linkage of Fc epsilon RI or to calcium ionophores. Nature. 1989 May 4;339(6219):64–67. doi: 10.1038/339064a0. [DOI] [PubMed] [Google Scholar]
  24. Rivera-Ortiz C. I., Nussenzweig R. Trichinella spiralis: anaphylactic antibody formation and susceptibility in strains of inbred mice. Exp Parasitol. 1976 Feb;39(1):7–17. doi: 10.1016/0014-4894(76)90004-7. [DOI] [PubMed] [Google Scholar]
  25. Ruitenberg E. J., Elgersma A. Absence of intestinal mast cell response in congenitally athymic mice during Trichinella spiralis infection. Nature. 1976 Nov 18;264(5583):258–260. doi: 10.1038/264258a0. [DOI] [PubMed] [Google Scholar]
  26. Sadun E. H., Mota I., Gore R. W. Demonstration of homocytotropic reaginlike antibodies in mice and rabbits infected with Trichinella spiralis. J Parasitol. 1968 Aug;54(4):814–821. [PubMed] [Google Scholar]
  27. Schrader J. W., Lewis S. J., Clark-Lewis I., Culvenor J. G. The persisting (P) cell: histamine content, regulation by a T cell-derived factor, origin from a bone marrow precursor, and relationship to mast cells. Proc Natl Acad Sci U S A. 1981 Jan;78(1):323–327. doi: 10.1073/pnas.78.1.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sideras P., Palacios R. Bone marrow pro-T and pro-B lymphocyte clones express functional receptors for interleukin (IL) 3 and IL 4/BSF-1 and nonfunctional receptors for IL 2. Eur J Immunol. 1987 Feb;17(2):217–221. doi: 10.1002/eji.1830170211. [DOI] [PubMed] [Google Scholar]
  29. Snapper C. M., Moorman M. A., Rosas F. R., Kehry M. R., Maliszewski C. R., Mond J. J. IL-3 and granulocyte-macrophage colony-stimulating factor strongly induce Ig secretion by sort-purified murine B cell activated through the membrane Ig, but not the CD40, signaling pathway. J Immunol. 1995 Jun 1;154(11):5842–5850. [PubMed] [Google Scholar]
  30. Watanabe N., Katakura K., Kobayashi A., Okumura K., Ovary Z. Protective immunity and eosinophilia in IgE-deficient SJA/9 mice infected with Nippostrongylus brasiliensis and Trichinella spiralis. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4460–4462. doi: 10.1073/pnas.85.12.4460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wodnar-Filipowicz A., Heusser C. H., Moroni C. Production of the haemopoietic growth factors GM-CSF and interleukin-3 by mast cells in response to IgE receptor-mediated activation. Nature. 1989 May 11;339(6220):150–152. doi: 10.1038/339150a0. [DOI] [PubMed] [Google Scholar]
  32. Yung Y. P., Eger R., Tertian G., Moore M. A. Long-term in vitro culture of murine mast cells. II. Purification of a mast cell growth factor and its dissociation from TCGF. J Immunol. 1981 Aug;127(2):794–799. [PubMed] [Google Scholar]
  33. Zakroff S. G., Beck L., Platzer E. G., Spiegelberg H. L. The IgE and IgG subclass responses of mice to four helminth parasites. Cell Immunol. 1989 Mar;119(1):193–201. doi: 10.1016/0008-8749(89)90235-9. [DOI] [PubMed] [Google Scholar]

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

RESOURCES