Skip to main content
NCBI home page
Immunology logoLink to Immunology
. 1993 Jun;79(2):189–195.

Schistosoma japonicum soluble egg antigens activate naive B cells to produce antibodies: definition of parasite mechanisms of immune deviation.

T Yamashita 1, T Watanabe 1, S Saito 1, Y Araki 1, F Sendo 1
PMCID: PMC1421876  PMID: 8344698

Abstract

This study analysed the effect of Schistosoma japonicum egg antigens (SEA) on the activation of lymphocytes from naive mice. T cells were found to be unaffected by SEA. B cells, however, were activated by SEA without participation of adherent cells such as macrophages. B-cell activating factor(s) in SEA were distributed into a fraction of M(r) 120,000 and a fraction of M(r) 650,000 by gel filtration. However, a fraction of M(r) 120,000 demonstrated the presence of a limited number of components by polyacrylamide gel electrophoresis (PAGE) under non-denaturing conditions. These activating factor(s) were destroyed by peroxidase oxidation, heat treatment, chymotrypsin and trypsin digestion. These results indicate that the B-cell activating factor(s) in SEA contain both carbohydrate and protein. IgM antibodies were detected in the culture supernatant of SEA-activated B cells after 48 hr in culture, but IgG antibodies were undetected in culture. These antibodies did not react with SEA but reacted with sheep, horse, mouse red blood cells, carbonic anhydrase and autoantigens in myelinated nerve fibres of cerebrum as well as luminal surface and parietal cells of the stomach of naive mice. Thus our data demonstrated that SEA directly stimulates naive B cells to produce antibodies against heterophile and autologous antigens.

Full text

PDF
189

Images in this article

192Figure 5
on p.192
192Figure 6
on p.192
193Figure 7
on p.193

Selected References

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

  1. Asahi H., Kawabata M., Sendo F., Naiki M., Hosaka Y., Kobayakawa T. The presence of anti-sheep red blood cell heterophile antibodies and their characteristics in murine schistosomiasis japonica. Microbiol Immunol. 1984;28(11):1241–1256. doi: 10.1111/j.1348-0421.1984.tb00781.x. [DOI] [PubMed] [Google Scholar]
  2. Asahi H., Moribayashi A., Sendo F., Kobayakawa T. Hemolytic factors in Schistosoma japonicum eggs. Infect Immun. 1984 Nov;46(2):514–518. doi: 10.1128/iai.46.2.514-518.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Corbel C., Melchers F. Requirement for macrophages or for macrophage- or T cell-derived factors in the mitogenic stimulation of murine B lymphocytes by lipopolysaccharides. Eur J Immunol. 1983 Jul;13(7):528–533. doi: 10.1002/eji.1830130703. [DOI] [PubMed] [Google Scholar]
  4. Cunningham A. J., Szenberg A. Further improvements in the plaque technique for detecting single antibody-forming cells. Immunology. 1968 Apr;14(4):599–600. [PMC free article] [PubMed] [Google Scholar]
  5. Fischer E., Camus D., Santoro F., Capron A. Schistosoma mansoni: autoantibodies and polyclonal B cell activation in infected mice. Clin Exp Immunol. 1981 Oct;46(1):89–97. [PMC free article] [PubMed] [Google Scholar]
  6. Garb K. S., Stavitsky A. B., Mahmoud A. A. Dynamics of antigen and mitogen-induced responses in murine schistosomiasis japonica: in vitro comparison between hepatic granulomas and splenic cells. J Immunol. 1981 Jul;127(1):115–120. [PubMed] [Google Scholar]
  7. 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]
  8. Greenwood B. M., Vick R. M. Evidence for a malaria mitogen in human malaria. Nature. 1975 Oct 16;257(5527):592–594. doi: 10.1038/257592a0. [DOI] [PubMed] [Google Scholar]
  9. Kawabata M., Hosaka Y., Kumada M., Matsui N., Kobayakawa T. Thymocytotoxic autoantibodies found in mice infected with Schistosoma japonicum. Infect Immun. 1981 May;32(2):438–442. doi: 10.1128/iai.32.2.438-442.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kishimoto T. Factors affecting B-cell growth and differentiation. Annu Rev Immunol. 1985;3:133–157. doi: 10.1146/annurev.iy.03.040185.001025. [DOI] [PubMed] [Google Scholar]
  11. Kobayakawa T., Louis J., Izui S., Lambert P. H. Autoimmune response to DNA, red blood cells, and thymocyte antigens in association with polyclonal antibody synthesis during experimental African trypanosomiasis. J Immunol. 1979 Jan;122(1):296–301. [PubMed] [Google Scholar]
  12. LEVIN J., BANG F. B. THE ROLE OF ENDOTOXIN IN THE EXTRACELLULAR COAGULATION OF LIMULUS BLOOD. Bull Johns Hopkins Hosp. 1964 Sep;115:265–274. [PubMed] [Google Scholar]
  13. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  14. Ly I. A., Mishell R. I. Separation of mouse spleen cells by passage through columns of sephadex G-10. J Immunol Methods. 1974 Aug;5(3):239–247. doi: 10.1016/0022-1759(74)90108-2. [DOI] [PubMed] [Google Scholar]
  15. Ohta N., Edahiro T., Tohgi N., Ishii A., Minai M., Hosaka Y. Generation and functional characterization of T cell lines and clones specific for Schistosoma japonicum egg antigen in humans. J Immunol. 1988 Oct 1;141(7):2445–2450. [PubMed] [Google Scholar]
  16. Olds G. R., Griffin A., Kresina T. F. Dynamics of collagen accumulation and polymorphism in murine Schistosoma japonicum. Gastroenterology. 1985 Sep;89(3):617–624. doi: 10.1016/0016-5085(85)90459-7. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Ortiz-Oritz L., Parks D. E., Lopez J. S., Weigle W. O. B-lymphocyte activation with an extract of Nocardia brasiliensis. Infect Immun. 1979 Aug;25(2):627–634. doi: 10.1128/iai.25.2.627-634.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Owhashi M., Horii Y., Ishii A. Schistosoma japonicum: identification and characterization of neutrophil chemotactic factors from egg antigen. Exp Parasitol. 1985 Oct;60(2):229–238. doi: 10.1016/0014-4894(85)90026-8. [DOI] [PubMed] [Google Scholar]
  20. Owhashi M., Ishii A. Purification and characterization of a high molecular weight eosinophil chemotactic factor from Schistosoma japonicum eggs. J Immunol. 1982 Nov;129(5):2226–2231. [PubMed] [Google Scholar]
  21. Pateraki E., Portocala R., Labrousse H., Guesdon J. L. Antiactin and antitubulin antibodies in canine visceral leishmaniasis. Infect Immun. 1983 Nov;42(2):496–500. doi: 10.1128/iai.42.2.496-500.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rosenberg S. A., Lipsky P. E. The role of monocytes in pokeweed mitogen-stimulated human B cell activation: separate requirements for intact monocytes and a soluble monocyte factor. J Immunol. 1981 Apr;126(4):1341–1345. [PubMed] [Google Scholar]
  23. Stavitsky A. B., Harold W. W. Deficiency of interleukin-2 activity upon addition of soluble egg antigen to cultures of spleen cells from mice infected with Schistosoma japonicum. Infect Immun. 1988 Jul;56(7):1778–1784. doi: 10.1128/iai.56.7.1778-1784.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Stunz L. L., Feldbush T. L. Polyclonal activation of rat B cells. I. A single mitogenic signal can stimulate proliferation, but three signals are required for differentiation. J Immunol. 1986 Jun 1;136(11):4006–4012. [PubMed] [Google Scholar]
  25. Tanaka Y., Shirakawa F., Ota T., Suzuki H., Eto S., Yamashita U. Mechanism of spontaneous activation of B cells in patients with systemic lupus erythematosus. Analysis with anti-class II antibody. J Immunol. 1988 Feb 1;140(3):761–767. [PubMed] [Google Scholar]
  26. Tanis R. J., Ferrell R. E., Tashian R. E. Amino acid sequence of sheep carbonic anhydrase C. Biochim Biophys Acta. 1974 Dec 18;371(2):534–548. doi: 10.1016/0005-2795(74)90050-6. [DOI] [PubMed] [Google Scholar]
  27. Ternynck T., Bleux C., Gregoire J., Avrameas S., Kanellopoulos-Langevin C. Comparison between autoantibodies arising during Trypanosoma cruzi infection in mice and natural autoantibodies. J Immunol. 1990 Feb 15;144(4):1504–1511. [PubMed] [Google Scholar]
  28. Warren K. S. The secret of the immunopathogenesis of schistosomiasis: in vivo models. Immunol Rev. 1982;61:189–213. doi: 10.1111/j.1600-065x.1982.tb00377.x. [DOI] [PubMed] [Google Scholar]
  29. Yamashita T., Watanabe T., Sendo F. Studies on the immunological disturbance in murine schistosomiasis japonica from the viewpoint of the interleukin cascade reaction. Immunology. 1987 Oct;62(2):215–221. [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES