Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1996 Oct;64(10):4042–4046. doi: 10.1128/iai.64.10.4042-4046.1996

Human immunoglobulin E responses to a recombinant 22.6-kilodalton antigen from Schistosoma mansoni adult worms are associated with low intensities of reinfection after treatment.

M Webster 1, A J Fulford 1, G Braun 1, J H Ouma 1, H C Kariuki 1, J C Havercroft 1, K Gachuhi 1, R F Sturrock 1, A E Butterworth 1, D W Dunne 1
PMCID: PMC174334  PMID: 8926066

Abstract

Schistosoma mansoni-infected individuals who have low intensities of reinfection following treatment produce immunoglobulin E (IgE) antibodies against a range of S. mansoni adult-worm antigens. One of the targets of the IgE response is an adult-worm sodium dodecyl sulfate-polyacrylamide gel electrophoresis band of 22 kDa (Sm22), which contains an antigen(s) located within the tegument and gut lining of adult worms and relatively late schistosomula life cycle stages only. A significant negative correlation between the level of anti-Sm22 IgE and the intensity of reinfection following treatment suggests that IgE responses against this antigen(s) are characteristic of individuals who are resistant to reinfection. To identify the antigen(s) in the Sm22 band that are associated with these IgE responses, we have cloned and characterized a recombinant 22-kDa protein (rSm22) that cross-reacts immunologically with Sm22. There was a high correlation between native and recombinant Sm22 isotype responses, indicating that the correct antigen had been cloned and that responses against rSm22 made up the majority of the responses against Sm22. By analyzing human isotype responses to rSm22 with human sera from a longitudinal treatment and reinfection study and correlating the anti-rSm22 isotype responses, retrospectively, with the intensity of reinfection following treatment for each individual, we observed a negative correlation between the IgE response to rSm22 and the intensity of reinfection. This relationship remained significant after allowing for age and other isotype responses to rSm22, in particular IgG4.

Full Text

The Full Text of this article is available as a PDF (188.0 KB).

Selected References

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

  1. Abu-Ghazaleh R. I., Fujisawa T., Mestecky J., Kyle R. A., Gleich G. J. IgA-induced eosinophil degranulation. J Immunol. 1989 Apr 1;142(7):2393–2400. [PubMed] [Google Scholar]
  2. Auriault C., Damonneville M., Verwaerde C., Pierce R., Joseph M., Capron M., Capron A. Rat IgE directed against schistosomula-released products is cytotoxic for Schistosoma mansoni schistosomula in vitro. Eur J Immunol. 1984 Feb;14(2):132–138. doi: 10.1002/eji.1830140206. [DOI] [PubMed] [Google Scholar]
  3. Auriault C., Gras-Masse H., Pierce R. J., Butterworth A. E., Wolowczuk I., Capron M., Ouma J. H., Balloul J. M., Khalife J., Neyrinck J. L. Antibody response of Schistosoma mansoni-infected human subjects to the recombinant P28 glutathione-S-transferase and to synthetic peptides. J Clin Microbiol. 1990 Sep;28(9):1918–1924. doi: 10.1128/jcm.28.9.1918-1924.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Butterworth A. E., Bensted-Smith R., Capron A., Capron M., Dalton P. R., Dunne D. W., Grzych J. M., Kariuki H. C., Khalife J., Koech D. Immunity in human schistosomiasis mansoni: prevention by blocking antibodies of the expression of immunity in young children. Parasitology. 1987 Apr;94(Pt 2):281–300. doi: 10.1017/s0031182000053956. [DOI] [PubMed] [Google Scholar]
  5. Butterworth A., Dunne D., Fulford A., Capron M., Khalife J., Capron A., Koech D., Ouma J., Sturrock R. Immunity in human schistosomiasis mansoni: cross-reactive IgM and IgG2 anti-carbohydrate antibodies block the expression of immunity. Biochimie. 1988 Aug;70(8):1053–1063. doi: 10.1016/0300-9084(88)90268-4. [DOI] [PubMed] [Google Scholar]
  6. Capron M., Tomassini M., Van der Vorst E., Kusnierz J. P., Papin J. P., Capron A. Existence et fonctions d'un récepteur pour l'immunoglobuline A sur les éosinophiles humains. C R Acad Sci III. 1988;307(7):397–402. [PubMed] [Google Scholar]
  7. Dalton P. R., Pole D. Water-contact patterns in relation to Schistosoma haematobium infection. Bull World Health Organ. 1978;56(3):417–426. [PMC free article] [PubMed] [Google Scholar]
  8. Demeure C. E., Rihet P., Abel L., Ouattara M., Bourgois A., Dessein A. J. Resistance to Schistosoma mansoni in humans: influence of the IgE/IgG4 balance and IgG2 in immunity to reinfection after chemotherapy. J Infect Dis. 1993 Oct;168(4):1000–1008. doi: 10.1093/infdis/168.4.1000. [DOI] [PubMed] [Google Scholar]
  9. Dunne D. W., Butterworth A. E., Fulford A. J., Kariuki H. C., Langley J. G., Ouma J. H., Capron A., Pierce R. J., Sturrock R. F. Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. Eur J Immunol. 1992 Jun;22(6):1483–1494. doi: 10.1002/eji.1830220622. [DOI] [PubMed] [Google Scholar]
  10. Dunne D. W., Grabowska A. M., Fulford A. J., Butterworth A. E., Sturrock R. F., Koech D., Ouma J. H. Human antibody responses to Schistosoma mansoni: the influence of epitopes shared between different life-cycle stages on the response to the schistosomulum. Eur J Immunol. 1988 Jan;18(1):123–131. doi: 10.1002/eji.1830180119. [DOI] [PubMed] [Google Scholar]
  11. Dunne D. W., Richardson B. A., Jones F. M., Clark M., Thorne K. J., Butterworth A. E. The use of mouse/human chimaeric antibodies to investigate the roles of different antibody isotypes, including IgA2, in the killing of Schistosoma mansoni schistosomula by eosinophils. Parasite Immunol. 1993 Mar;15(3):181–185. doi: 10.1111/j.1365-3024.1993.tb00598.x. [DOI] [PubMed] [Google Scholar]
  12. Francis P., Bickle Q. Cloning of a 21.7-kDa vaccine-dominant antigen gene of Schistosoma mansoni reveals an EF hand-like motif. Mol Biochem Parasitol. 1992 Feb;50(2):215–224. doi: 10.1016/0166-6851(92)90218-9. [DOI] [PubMed] [Google Scholar]
  13. Grant J. W., Zhong R. Q., McEwen P. M., Church S. L. Human nonsarcomeric 20,000 Da myosin regulatory light chain cDNA. Nucleic Acids Res. 1990 Oct 11;18(19):5892–5892. doi: 10.1093/nar/18.19.5892. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grzych J. M., Grezel D., Xu C. B., Neyrinck J. L., Capron M., Ouma J. H., Butterworth A. E., Capron A. IgA antibodies to a protective antigen in human Schistosomiasis mansoni. J Immunol. 1993 Jan 15;150(2):527–535. [PubMed] [Google Scholar]
  15. Hagan P., Blumenthal U. J., Dunn D., Simpson A. J., Wilkins H. A. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature. 1991 Jan 17;349(6306):243–245. doi: 10.1038/349243a0. [DOI] [PubMed] [Google Scholar]
  16. Havercroft J. C., Huggins M. C., Nene V., Dunne D. W., Richardson B. A., Taylor D. W., Butterworth A. E. Cloning of the gene encoding a 50 kilodalton potential surface antigen of Schistosoma mansoni. Mol Biochem Parasitol. 1988 Jul;30(1):83–88. doi: 10.1016/0166-6851(88)90135-1. [DOI] [PubMed] [Google Scholar]
  17. Inoue A., Yanagisawa M., Takano-Ohmuro H., Masaki T. Two isoforms of smooth muscle myosin regulatory light chain in chicken gizzard. Eur J Biochem. 1989 Aug 15;183(3):645–651. doi: 10.1111/j.1432-1033.1989.tb21094.x. [DOI] [PubMed] [Google Scholar]
  18. Jeffs S. A., Hagan P., Allen R., Correa-Oliveira R., Smithers S. R., Simpson A. J. Molecular cloning and characterisation of the 22-kilodalton adult Schistosoma mansoni antigen recognised by antibodies from mice protectively vaccinated with isolated tegumental surface membranes. Mol Biochem Parasitol. 1991 May;46(1):159–167. doi: 10.1016/0166-6851(91)90209-o. [DOI] [PubMed] [Google Scholar]
  19. Khalife J., Dunne D. W., Richardson B. A., Mazza G., Thorne K. J., Capron A., Butterworth A. E. Functional role of human IgG subclasses in eosinophil-mediated killing of schistosomula of Schistosoma mansoni. J Immunol. 1989 Jun 15;142(12):4422–4427. [PubMed] [Google Scholar]
  20. Kloetzel K., da Silva J. R. Schistosomiasis mansoni acquired in adulthood: behavior of egg counts and the intradermal test. Am J Trop Med Hyg. 1967 Mar;16(2):167–169. doi: 10.4269/ajtmh.1967.16.167. [DOI] [PubMed] [Google Scholar]
  21. Knight M., Simpson A. J., Payares G., Chaudri M., Smithers S. R. Cell-free synthesis of Schistosoma mansoni surface antigens: stage specificity of their expression. EMBO J. 1984 Jan;3(1):213–219. doi: 10.1002/j.1460-2075.1984.tb01786.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Langley J. G., Kariuki H. C., Hammersley A. P., Ouma J. H., Butterworth A. E., Dunne D. W. Human IgG subclass responses and subclass restriction to Schistosoma mansoni egg antigens. Immunology. 1994 Dec;83(4):651–658. [PMC free article] [PubMed] [Google Scholar]
  24. Lodes M. J., Yoshino T. P. Characterization of excretory-secretory proteins synthesized in vitro by Schistosoma mansoni primary sporocysts. J Parasitol. 1989 Dec;75(6):853–862. [PubMed] [Google Scholar]
  25. Maeda K., Müller-Gerhardt E., Wittinghofer A. Sequence of two isoforms of myosin light chain 2 isolated from a rabbit fast skeletal muscle lambda library. Nucleic Acids Res. 1990 Nov 25;18(22):6687–6687. doi: 10.1093/nar/18.22.6687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nudel U., Calvo J. M., Shani M., Levy Z. The nucleotide sequence of a rat myosin light chain 2 gene. Nucleic Acids Res. 1984 Sep 25;12(18):7175–7186. doi: 10.1093/nar/12.18.7175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Oligino L. D., Percy A. J., Harn D. A. Purification and immunochemical characterization of a 22 kilodalton surface antigen from Schistosoma mansoni. Mol Biochem Parasitol. 1988 Mar;28(2):95–103. doi: 10.1016/0166-6851(88)90056-4. [DOI] [PubMed] [Google Scholar]
  28. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rihet P., Demeure C. E., Bourgois A., Prata A., Dessein A. J. Evidence for an association between human resistance to Schistosoma mansoni and high anti-larval IgE levels. Eur J Immunol. 1991 Nov;21(11):2679–2686. doi: 10.1002/eji.1830211106. [DOI] [PubMed] [Google Scholar]
  30. Rihet P., Demeure C. E., Dessein A. J., Bourgois A. Strong serum inhibition of specific IgE correlated to competing IgG4, revealed by a new methodology in subjects from a S. mansoni endemic area. Eur J Immunol. 1992 Aug;22(8):2063–2070. doi: 10.1002/eji.1830220816. [DOI] [PubMed] [Google Scholar]
  31. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sauma S. Y., Strand M. Identification and characterization of glycosylphosphatidylinositol-linked Schistosoma mansoni adult worm immunogens. Mol Biochem Parasitol. 1990 Jan 15;38(2):199–209. doi: 10.1016/0166-6851(90)90023-f. [DOI] [PubMed] [Google Scholar]
  33. Simpson A. J., James S. L., Sher A. Identification of surface antigens of schistosomula of Schistosoma mansoni recognized by antibodies from mice immunized by chronic infection and by exposure to highly irradiated cercariae. Infect Immun. 1983 Aug;41(2):591–597. doi: 10.1128/iai.41.2.591-597.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
  35. Smithers S. R., Terry R. J. The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology. 1965 Nov;55(4):695–700. doi: 10.1017/s0031182000086248. [DOI] [PubMed] [Google Scholar]
  36. Stein L. D., David J. R. Cloning of a developmentally regulated tegument antigen of Schistosoma mansoni. Mol Biochem Parasitol. 1986 Sep;20(3):253–264. doi: 10.1016/0166-6851(86)90106-4. [DOI] [PubMed] [Google Scholar]
  37. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Warren K. S. Regulation of the prevalence and intensity of schistosomiasis in man: immunology or ecology? J Infect Dis. 1973 May;127(5):595–609. doi: 10.1093/infdis/127.5.595. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES