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. 1991 Apr;72(4):502–507.

The role of interleukin-5 in protective immunity to Strongyloides venezuelensis infection in mice.

M Korenaga 1, Y Hitoshi 1, N Yamaguchi 1, Y Sato 1, K Takatsu 1, I Tada 1
PMCID: PMC1384368  PMID: 2037312

Abstract

We depleted or neutralized interleukin-5 (IL-5) and IL-5 receptor of C57BL/6 mice, using rat anti-murine IL-5 monoclonal antibody (NC17) and anti-murine IL-5 receptor monoclonal antibody (H7). Mice treated with these monoclonal antibodies were infected with Strongyloides venezuelensis larvae. The time-course of faecal egg output and peripheral eosinophilia were monitored. In a primary infection, anti-IL-5 treatment did not affect faecal egg output, although the eosinophil count in peripheral blood was markedly reduced. There was no difference in intestinal worm burden or faecal egg output between anti-IL-5 treated and non-treated mice. In a secondary infection, worms were expelled from the small intestine of anti-IL-5-treated mice as well as from non-treated mice. Worm recovery from the lungs of mice treated with either anti-IL-5 or anti-IL-5 receptor monoclonal antibody was the same as that of normal controls. However, a marked reduction in worm recovery was observed in re-infected mice that had not been treated with monoclonal antibodies. Treatment with anti-IL-5 or anti-IL-5 receptor monoclonal antibody suppressed blood and tissue eosinophilia. Thus the results suggested that the host's protective immunity against tissue-migrating larvae was IL-5-dependent but intestinal immunity was not.

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Selected References

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

  1. Abe T., Kiyota M., Nawa Y. Strongyloides ratti: increase in susceptibility to infection following blockade of the mononuclear phagocyte system in female mice. Aust J Exp Biol Med Sci. 1985 Dec;63(Pt 6):651–653. doi: 10.1038/icb.1985.68. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Bell R. G., Adams L. S., Gerb J. Strongyloides ratti: dissociation of the rat's protective immunity into systemic and intestinal components. Exp Parasitol. 1981 Dec;52(3):386–395. doi: 10.1016/0014-4894(81)90097-7. [DOI] [PubMed] [Google Scholar]
  4. Butterworth A. E., Sturrock R. F., Houba V., Mahmoud A. A., Sher A., Rees P. H. Eosinophils as mediators of antibody-dependent damage to schistosomula. Nature. 1975 Aug 28;256(5520):727–729. doi: 10.1038/256727a0. [DOI] [PubMed] [Google Scholar]
  5. Clutterbuck E. J., Sanderson C. J. Human eosinophil hematopoiesis studied in vitro by means of murine eosinophil differentiation factor (IL5): production of functionally active eosinophils from normal human bone marrow. Blood. 1988 Mar;71(3):646–651. [PubMed] [Google Scholar]
  6. Coffman R. L., Seymour B. W., Hudak S., Jackson J., Rennick D. Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science. 1989 Jul 21;245(4915):308–310. doi: 10.1126/science.2787531. [DOI] [PubMed] [Google Scholar]
  7. Grove D. I., Mahmoud A. A., Warren K. S. Eosinophils and resistance to Trichinella spiralis. J Exp Med. 1977 Mar 1;145(3):755–759. doi: 10.1084/jem.145.3.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Grove D. I., Northern C. Dissociation of the protective immune response in the mouse to Strongyloides ratti. J Helminthol. 1989 Dec;63(4):307–314. doi: 10.1017/s0022149x00009202. [DOI] [PubMed] [Google Scholar]
  9. Harada N., Kikuchi Y., Tominaga A., Takaki S., Takatsu K. BCGFII activity on activated B cells of a purified murine T cell-replacing factor (TRF) from a T cell hybridoma (B151K12). J Immunol. 1985 Jun;134(6):3944–3951. [PubMed] [Google Scholar]
  10. Harada N., Takahashi T., Matsumoto M., Kinashi T., Ohara J., Kikuchi Y., Koyama N., Severinson E., Yaoita Y., Honjo T. Production of a monoclonal antibody useful in the molecular characterization of murine T-cell-replacing factor/B-cell growth factor II. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4581–4585. doi: 10.1073/pnas.84.13.4581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Korenaga M., Nawa Y., Mimori T., Tada I. Effects of preintestinal larval antigenic stimuli on the generation of intestinal immunity in Strongyloides ratti infection in rats. J Parasitol. 1983 Feb;69(1):78–82. [PubMed] [Google Scholar]
  12. Korenaga M., Nawa Y., Mimori T., Tada I. Strongyloides ratti: the role of enteral antigenic stimuli by adult worms in the generation of protective immunity in rats. Exp Parasitol. 1983 Jun;55(3):358–363. doi: 10.1016/0014-4894(83)90032-2. [DOI] [PubMed] [Google Scholar]
  13. Lee T. D., Befus D. Effects of rat and human intestinal lamina propria cells on viability and muscle establishment of Trichinella spiralis newborn larvae. J Parasitol. 1989 Feb;75(1):124–128. [PubMed] [Google Scholar]
  14. Limaye A. P., Abrams J. S., Silver J. E., Ottesen E. A., Nutman T. B. Regulation of parasite-induced eosinophilia: selectively increased interleukin 5 production in helminth-infected patients. J Exp Med. 1990 Jul 1;172(1):399–402. doi: 10.1084/jem.172.1.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lopez A. F., Begley C. G., Williamson D. J., Warren D. J., Vadas M. A., Sanderson C. J. Murine eosinophil differentiation factor. An eosinophil-specific colony-stimulating factor with activity for human cells. J Exp Med. 1986 May 1;163(5):1085–1099. doi: 10.1084/jem.163.5.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nawa Y., Kiyota M., Korenaga M., Kotani M. Defective protective capacity of W/Wv mice against Strongyloides ratti infection and its reconstitution with bone marrow cells. Parasite Immunol. 1985 Jul;7(4):429–438. doi: 10.1111/j.1365-3024.1985.tb00088.x. [DOI] [PubMed] [Google Scholar]
  17. Sato Y., Toma H. Effects of spleen cells and serum on transfer of immunity to Strongyloides venezuelensis infection in hypothymic (nude) mice. Int J Parasitol. 1990 Feb;20(1):63–67. doi: 10.1016/0020-7519(90)90174-l. [DOI] [PubMed] [Google Scholar]
  18. Sher A., Coffman R. L., Hieny S., Scott P., Cheever A. W. Interleukin 5 is required for the blood and tissue eosinophilia but not granuloma formation induced by infection with Schistosoma mansoni. Proc Natl Acad Sci U S A. 1990 Jan;87(1):61–65. doi: 10.1073/pnas.87.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Swain S. L., McKenzie D. T., Weinberg A. D., Hancock W. Characterization of T helper 1 and 2 cell subsets in normal mice. Helper T cells responsible for IL-4 and IL-5 production are present as precursors that require priming before they develop into lymphokine-secreting cells. J Immunol. 1988 Nov 15;141(10):3445–3455. [PubMed] [Google Scholar]
  20. Takatsu K., Kikuchi Y., Takahashi T., Honjo T., Matsumoto M., Harada N., Yamaguchi N., Tominaga A. Interleukin 5, a T-cell-derived B-cell differentiation factor also induces cytotoxic T lymphocytes. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4234–4238. doi: 10.1073/pnas.84.12.4234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Takatsu K., Tominaga A., Hamaoka T. Antigen-induced T cell-replacing factor (TRF). I. Functional characterization of a TRF-producing helper T cell subset and genetic studies on TRF production. J Immunol. 1980 May;124(5):2414–2422. [PubMed] [Google Scholar]
  22. Tam N. D., Papadimitriou J., Keast D. The location of antigenic sites on the surface of the nematode parasite Strongyloides ratti reactive to antibody-directed cellular cytotoxicity from both macrophages and eosinophils from the natural host. Aust J Exp Biol Med Sci. 1983 Dec;61(Pt 6):629–636. doi: 10.1038/icb.1983.59. [DOI] [PubMed] [Google Scholar]
  23. Yamaguchi N., Hitoshi Y., Mita S., Hosoya Y., Murata Y., Kikuchi Y., Tominaga A., Takatsu K. Characterization of the murine interleukin 5 receptor by using a monoclonal antibody. Int Immunol. 1990;2(2):181–187. doi: 10.1093/intimm/2.2.181. [DOI] [PubMed] [Google Scholar]
  24. Yamaguchi Y., Hayashi Y., Sugama Y., Miura Y., Kasahara T., Kitamura S., Torisu M., Mita S., Tominaga A., Takatsu K. Highly purified murine interleukin 5 (IL-5) stimulates eosinophil function and prolongs in vitro survival. IL-5 as an eosinophil chemotactic factor. J Exp Med. 1988 May 1;167(5):1737–1742. doi: 10.1084/jem.167.5.1737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yamaguchi Y., Matsui T., Kasahara T., Etoh S., Tominaga A., Takatsu K., Miura Y., Suda T. In vivo changes of hemopoietic progenitors and the expression of the interleukin 5 gene in eosinophilic mice infected with Toxocara canis. Exp Hematol. 1990 Dec;18(11):1152–1157. [PubMed] [Google Scholar]
  26. Yamaguchi Y., Suda T., Suda J., Eguchi M., Miura Y., Harada N., Tominaga A., Takatsu K. Purified interleukin 5 supports the terminal differentiation and proliferation of murine eosinophilic precursors. J Exp Med. 1988 Jan 1;167(1):43–56. doi: 10.1084/jem.167.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yokota T., Coffman R. L., Hagiwara H., Rennick D. M., Takebe Y., Yokota K., Gemmell L., Shrader B., Yang G., Meyerson P. Isolation and characterization of lymphokine cDNA clones encoding mouse and human IgA-enhancing factor and eosinophil colony-stimulating factor activities: relationship to interleukin 5. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7388–7392. doi: 10.1073/pnas.84.21.7388. [DOI] [PMC free article] [PubMed] [Google Scholar]

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