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. 1996 May;64(5):1826–1831. doi: 10.1128/iai.64.5.1826-1831.1996

Lacto-N-fucopentaose III (Lewis x), a target of the antibody response in mice vaccinated with irradiated cercariae of Schistosoma mansoni.

D Richter 1, R N Incani 1, D A Harn 1
PMCID: PMC173998  PMID: 8613397

Abstract

Carbohydrates on soluble egg antigens are major epitopes for the antibody responses of patients and mice infected with Schistosoma mansoni. Recently, protective sera of mice vaccinated with irradiated cercariae were shown to recognize carbohydrate epitopes on schistosomal glutathione S-transferase. The present study demonstrates that carbohydrate epitopes are major targets of sera from C57BL/6J and CBA/J mice vaccinated with 15- or 50-kilorad-irradiated cercariae of S. mansoni. Antibody titers to carbohydrate epitopes increased with the number of vaccinations and were considerably higher in C57BL/6J mice than in CBA/J mice. The specificity of this anticarbohydrate response was determined by measuring antibody binding to defined oligosaccharide residues known to be present on the parasite. A predominant target of the humoral anticarbohydrate response of vaccinated mice was lacto-N-fucopentaose III, a molecule relevant for cell trafficking. We observed no binding to its nonfucosylated homolog, lacto-N-neotetraose, or to oligosaccharides present on keyhole limpet hemocyanin. The strongest antibody response to lacto-N-fucopentaose III was observed for C57BL/6J and CBA/J mice repeatedly vaccinated with 15-kilorad-irradiated cercariae, which also achieve the highest levels of protection. Immunoglobulin M was the predominant antibody class binding to lacto-N-fucopentaose III. We conclude that in the irradiated-cercariae vaccine model, C57BL/6J and CBA/J mice produce anticarbohydrate antibodies against various stages of S. mansoni and that the oligosaccharide lacto-N-fucopentaose III is one target of this response. Lacto-N-fucopentaose III and its specific antibodies may profoundly affect host resistance and parasite homing.

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Selected References

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  1. Grzych J. M., Dissous C., Capron M., Torres S., Lambert P. H., Capron A. Schistosoma mansoni shares a protective carbohydrate epitope with keyhole limpet hemocyanin. J Exp Med. 1987 Mar 1;165(3):865–878. doi: 10.1084/jem.165.3.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Harn D. A., Mitsuyama M., David J. R. Schistosoma mansoni. Anti-egg monoclonal antibodies protect against cercarial challenge in vivo. J Exp Med. 1984 May 1;159(5):1371–1387. doi: 10.1084/jem.159.5.1371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Hsü S. Y., Hsü H. F., Burmeister L. F. Schistosoma mansoni: vaccination of mice with highly x-irradiated cercariae. Exp Parasitol. 1981 Aug;52(1):91–104. doi: 10.1016/0014-4894(81)90065-5. [DOI] [PubMed] [Google Scholar]
  4. Jwo J., LoVerde P. T. The ability of fractionated sera from animals vaccinated with irradiated cercariae of Schistosoma mansoni to transfer immunity to mice. J Parasitol. 1989 Apr;75(2):252–260. [PubMed] [Google Scholar]
  5. Ko A. I., Dräger U. C., Harn D. A. A Schistosoma mansoni epitope recognized by a protective monoclonal antibody is identical to the stage-specific embryonic antigen 1. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4159–4163. doi: 10.1073/pnas.87.11.4159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ko A. I., Harn D. A. Characterization of protective and non-protective surface membrane carbohydrate epitopes of Schistosoma mansoni. Mem Inst Oswaldo Cruz. 1987;82 (Suppl 4):115–119. doi: 10.1590/s0074-02761987000800019. [DOI] [PubMed] [Google Scholar]
  7. Köster B., Strand M. Schistosoma mansoni: immunolocalization of two different fucose-containing carbohydrate epitopes. Parasitology. 1994 May;108(Pt 4):433–446. doi: 10.1017/s0031182000075995. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Larsen E., Palabrica T., Sajer S., Gilbert G. E., Wagner D. D., Furie B. C., Furie B. PADGEM-dependent adhesion of platelets to monocytes and neutrophils is mediated by a lineage-specific carbohydrate, LNF III (CD15). Cell. 1990 Nov 2;63(3):467–474. doi: 10.1016/0092-8674(90)90443-i. [DOI] [PubMed] [Google Scholar]
  10. Lasky L. A. Selectins: interpreters of cell-specific carbohydrate information during inflammation. Science. 1992 Nov 6;258(5084):964–969. doi: 10.1126/science.1439808. [DOI] [PubMed] [Google Scholar]
  11. Lazdins J. K., Stein M. J., David J. R., Sher A. Schistosoma mansoni: rapid isolation and purification of schistosomula of different developmental stages by centrifugation on discontinuous density gradients of Percoll. Exp Parasitol. 1982 Feb;53(1):39–44. doi: 10.1016/0014-4894(82)90090-x. [DOI] [PubMed] [Google Scholar]
  12. Mangold B. L., Dean D. A. Passive transfer with serum and IgG antibodies of irradiated cercaria-induced resistance against Schistosoma mansoni in mice. J Immunol. 1986 Apr 1;136(7):2644–2648. [PubMed] [Google Scholar]
  13. Mulligan M. S., Lowe J. B., Larsen R. D., Paulson J., Zheng Z. L., DeFrees S., Maemura K., Fukuda M., Ward P. A. Protective effects of sialylated oligosaccharides in immune complex-induced acute lung injury. J Exp Med. 1993 Aug 1;178(2):623–631. doi: 10.1084/jem.178.2.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Mulligan M. S., Paulson J. C., De Frees S., Zheng Z. L., Lowe J. B., Ward P. A. Protective effects of oligosaccharides in P-selectin-dependent lung injury. Nature. 1993 Jul 8;364(6433):149–151. doi: 10.1038/364149a0. [DOI] [PubMed] [Google Scholar]
  15. Omer Ali P., Smithers S. R., Bickle Q., Phillips S. M., Harn D., Simpson A. J. Analysis of the anti-Schistosoma mansoni surface antibody response during murine infection and its potential contribution to protective immunity. J Immunol. 1988 May 1;140(9):3273–3279. [PubMed] [Google Scholar]
  16. Omer-Ali P., Magee A. I., Kelly C., Simpson A. J. A major role for carbohydrate epitopes preferentially recognized by chronically infected mice in the determination of Schistosoma mansoni schistosomulum surface antigenicity. J Immunol. 1986 Dec 1;137(11):3601–3607. [PubMed] [Google Scholar]
  17. Reynolds S. R., Harn D. A. Comparison of irradiated-cercaria schistosome vaccine models that use 15- and 50-kilorad doses: the 15-kilorad dose gives greater protection, smaller liver sizes, and higher gamma interferon levels after challenge. Infect Immun. 1992 Jan;60(1):90–94. doi: 10.1128/iai.60.1.90-94.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Richter D., Incani R. N., Harn D. A. Isotype responses to candidate vaccine antigens in protective sera obtained from mice vaccinated with irradiated cercariae of Schistosoma mansoni. Infect Immun. 1993 Jul;61(7):3003–3011. doi: 10.1128/iai.61.7.3003-3011.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sher A., Hieny S., James S. L., Asofsky R. Mechanisms of protective immunity against Schistosoma mansoni infection in mice vaccinated with irradiated cercariae. II. Analysis of immunity in hosts deficient in T lymphocytes, B lymphocytes, or complement. J Immunol. 1982 Apr;128(4):1880–1884. [PubMed] [Google Scholar]
  20. 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]
  21. Springer T. A. Adhesion receptors of the immune system. Nature. 1990 Aug 2;346(6283):425–434. doi: 10.1038/346425a0. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. Umeda M., Diego I., Marcus D. M. The occurrence of anti-3-fucosyllactosamine antibodies and their cross-reactive idiotopes in preimmune and immune mouse sera. J Immunol. 1986 Nov 15;137(10):3264–3269. [PubMed] [Google Scholar]
  24. Velupillai P., Harn D. A. Oligosaccharide-specific induction of interleukin 10 production by B220+ cells from schistosome-infected mice: a mechanism for regulation of CD4+ T-cell subsets. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):18–22. doi: 10.1073/pnas.91.1.18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Weiss J. B., Strand M. Characterization of developmentally regulated epitopes of Schistosoma mansoni egg glycoprotein antigens. J Immunol. 1985 Aug;135(2):1421–1429. [PubMed] [Google Scholar]
  26. Woodward M. P., Young W. W., Jr, Bloodgood R. A. Detection of monoclonal antibodies specific for carbohydrate epitopes using periodate oxidation. J Immunol Methods. 1985 Apr 8;78(1):143–153. doi: 10.1016/0022-1759(85)90337-0. [DOI] [PubMed] [Google Scholar]

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