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. 1984 May 1;159(5):1371–1387. doi: 10.1084/jem.159.5.1371

Schistosoma mansoni. Anti-egg monoclonal antibodies protect against cercarial challenge in vivo

PMCID: PMC2187298  PMID: 6538899

Abstract

Monoclonal antibodies that bind to surface membranes of developing schistosomula and/or cercarial tails were generated from mice immunized with living schistosome eggs or soluble egg antigen. These monoclonal antibodies detected at least three different surface epitopes. One surface antigen detected by anti-egg monoclonal antibody EG1C4B1 (E.1) persisted on the surface of developing schistosomula for 96 h posttransformation . The same or a cross-reactive antigen was also detected on the surfaces of S. japonicum and S. haematobium schistosomula and cercarial tails. Monoclonal antibody E.1 killed schistosomula in vitro as well or better than infected mouse sera and transferred immunity to naive mice when administered in vivo. The monoclonal antibody reduced the number of lung worms recoverable on day 4 postchallenge by up to 85% and reduced the adult worm burden up to 41% as compared with controls. The data also show that the molecular weights of the egg antigens detected by monoclonal antibody E.1 were different from those detected on schistosomula.

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Selected References

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  1. Aronstein W. S., Norden A. P., Strand M. Tegumental expression in larval and adult stages of a major schistosome structural glycoprotein. Am J Trop Med Hyg. 1983 Mar;32(2):334–342. doi: 10.4269/ajtmh.1983.32.334. [DOI] [PubMed] [Google Scholar]
  2. Bickle Q. D., Ford M. J., Andrews B. J. Studies on the development of anti-schistosomular surface antibodies by mice exposed to irradiated cercariae, adults and/or eggs of S. mansoni. Parasite Immunol. 1983 Sep;5(5):499–511. doi: 10.1111/j.1365-3024.1983.tb00764.x. [DOI] [PubMed] [Google Scholar]
  3. Boros D. L., Pelley R. P., Warren K. S. Spontaneous modulation of granulomatous hypersensitivity in schistosomiasis mansoni. J Immunol. 1975 May;114(5):1437–1441. [PubMed] [Google Scholar]
  4. Boros D. L., Warren K. S. Delayed hypersensitivity-type granuloma formation and dermal reaction induced and elicited by a soluble factor isolated from Schistosoma mansoni eggs. J Exp Med. 1970 Sep 1;132(3):488–507. doi: 10.1084/jem.132.3.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  6. COKER C. M., LICHTENBERG F. A revised method for isolation of Schistosoma mansoni eggs for biological experimentation. Proc Soc Exp Biol Med. 1956 Aug-Sep;92(4):780–782. doi: 10.3181/00379727-92-22612. [DOI] [PubMed] [Google Scholar]
  7. Carter C. E., Colley D. G. Partial purification and characterization of Schistosoma mansoni soluble egg antigen with Con A-Sepharose chromatography. J Immunol. 1979 Jun;122(6):2204–2209. [PubMed] [Google Scholar]
  8. Colley D. G. Eosinophils and immune mechanisms. Eosinophil stimulation promoter (ESP): a lymphokine induced by specific antigen or phytohemagglutinin. J Immunol. 1973 May;110(5):1419–1423. [PubMed] [Google Scholar]
  9. Colley D. G. Immune responses to a soluble schistosomal egg antigen preparation during chronic primary infection with Schistosoma mansoni. J Immunol. 1975 Jul;115(1):150–156. [PubMed] [Google Scholar]
  10. Colley D. G. Intradermal immune responses to a schistosomal egg antigen during experimental murine Schistosoma mansoni infection. Proc Soc Exp Biol Med. 1972 Jul;140(3):772–775. doi: 10.3181/00379727-140-36550. [DOI] [PubMed] [Google Scholar]
  11. Colley D. G. Schistosome Antigen Laboratory Workshop: summary of a meeting sponsored by the Edna McConnell Clark Foundation. J Parasitol. 1983 Feb;69(1):45–48. [PubMed] [Google Scholar]
  12. Dean D. A., Bukowski M. A., Cheever A. W. Relationship between acquired resistance, portal hypertension, and lung granulomas in ten strains of mice infected with Schistosoma mansoni. Am J Trop Med Hyg. 1981 Jul;30(4):806–814. doi: 10.4269/ajtmh.1981.30.806. [DOI] [PubMed] [Google Scholar]
  13. Dean D. A., Minard P., Murrell K. D., Vannier W. E. Resistance of mice to secondary infection with Schistosoma mansoni. II. Evidence for a correlation between egg deposition and work elimination. Am J Trop Med Hyg. 1978 Sep;27(5):957–965. doi: 10.4269/ajtmh.1978.27.957. [DOI] [PubMed] [Google Scholar]
  14. Dean D. A., Minard P., Stirewalt M. A., Vannier W. E., Murrell K. D. Resistance of mice to secondary infection with Schistosoma mansoni. I. Comparison of bisexual and unisexual initial infections. Am J Trop Med Hyg. 1978 Sep;27(5):951–956. doi: 10.4269/ajtmh.1978.27.951. [DOI] [PubMed] [Google Scholar]
  15. Dessein A., Samuelson J. C., Butterworth A. E., Hogan M., Sherry B. A., Vadas M. A., David J. R. Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules. Parasitology. 1981 Jun;82(Pt 3):357–374. doi: 10.1017/s0031182000066890. [DOI] [PubMed] [Google Scholar]
  16. Dissous C., Grzych J. M., Capron A. Schistosoma mansoni surface antigen defined by a rat monoclonal IgG2a. J Immunol. 1982 Nov;129(5):2232–2234. [PubMed] [Google Scholar]
  17. Dunne D. W., Lucas S., Bickle Q., Pearson S., Madgwick L., Bain J., Doenhoff M. J. Identification and partial purification of an antigen (omega 1) from Schistosoma mansoni eggs which is putatively hepatotoxic in T-cell deprived mice. Trans R Soc Trop Med Hyg. 1981;75(1):54–71. doi: 10.1016/0035-9203(81)90013-4. [DOI] [PubMed] [Google Scholar]
  18. El Naggar A., Colley D. G. Modulation of schistosoma mansoni egg-induced granuloma formation. II. Soluble suppressor activity from lymphoid cels during chronic infection. Cell Immunol. 1982 Sep 1;72(1):151–156. doi: 10.1016/0008-8749(82)90292-1. [DOI] [PubMed] [Google Scholar]
  19. Eveland L. K., Morse S. I. Schistosoma mansoni: infectivity and immunizing effects of in vitro derived schistosomula attenuated by X irradiation. Exp Parasitol. 1978 Jun;45(1):19–25. doi: 10.1016/0014-4894(78)90040-1. [DOI] [PubMed] [Google Scholar]
  20. Ey P. L., Prowse S. J., Jenkin C. R. Isolation of pure IgG1, IgG2a and IgG2b immunoglobulins from mouse serum using protein A-sepharose. Immunochemistry. 1978 Jul;15(7):429–436. doi: 10.1016/0161-5890(78)90070-6. [DOI] [PubMed] [Google Scholar]
  21. Grzych J. M., Capron M., Bazin H., Capron A. In vitro and in vivo effector function of rat IgG2a monoclonal anti-S. mansoni antibodies. J Immunol. 1982 Dec;129(6):2739–2743. [PubMed] [Google Scholar]
  22. Hamburger J., Lustigman S., Siongok T. K., Ouma J. H., Mahmoud A. A. Characterization of a purified glycoprotein from Schistosoma mansoni eggs: specificity, stability, and the involvement of carbohydrate and peptide moieties in its serologic activity. J Immunol. 1982 Apr;128(4):1864–1869. [PubMed] [Google Scholar]
  23. Harrison D. J., Carter C. E., Colley D. G. Immunoaffinity purification of Schistosoma mansoni soluble egg antigens. J Immunol. 1979 Jun;122(6):2210–2217. [PubMed] [Google Scholar]
  24. Harrison R. A., Bickle Q., Doenhoff M. J. Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. Evidence that the mechanisms which mediate resistance during early patent infections may lack immunological specificity. Parasitology. 1982 Feb;84(1):93–110. doi: 10.1017/s0031182000051696. [DOI] [PubMed] [Google Scholar]
  25. Kennett R. H., Denis K. A., Tung A. S., Klinman N. R. Hybrid plasmacytoma production: fusions with adult spleen cells, monoclonal spleen fragments, neonatal spleen cells and human spleen cells. Curr Top Microbiol Immunol. 1978;81:77–91. doi: 10.1007/978-3-642-67448-8_13. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Minard P., Dean D. A., Jacobson R. H., Vannier W. E., Murrell K. D. Immunization of mice with cobalt-60 irradiated Schistosoma mansoni cercariae. Am J Trop Med Hyg. 1978 Jan;27(1 Pt 1):76–86. doi: 10.4269/ajtmh.1978.27.76. [DOI] [PubMed] [Google Scholar]
  29. Mota-Santos T. A., Toledo M. I., Correa M. C., Correa-Oliveira R., Gazzinelli G. Schistosomiasis from S. mansoni in mice: the relationship between acquired immunity and serum levels of lethal antibody. Parasite Immunol. 1981 Winter;3(4):319–327. doi: 10.1111/j.1365-3024.1981.tb00410.x. [DOI] [PubMed] [Google Scholar]
  30. Norden A. P., Aronstein W. S., Strand M. Schistosoma mansoni: identification, characterization, and purification of the spine glycoprotein by monoclonal antibody. Exp Parasitol. 1982 Dec;54(3):432–442. doi: 10.1016/0014-4894(82)90053-4. [DOI] [PubMed] [Google Scholar]
  31. Pelley R. P., Pelley R. J., Hamburger J., Peters P. A., Warren K. S. Schistosoma mansoni soluble egg antigens. I. Identification and purification of three major antigens, and the employment of radioimmunoassay for their further characterization. J Immunol. 1976 Nov;117(5 Pt 1):1553–1560. [PubMed] [Google Scholar]
  32. RITCHIE L. S., GARSON S., ERICKSON D. G. Attempts to induce resistance against Schistosoma mansoni by injecting cercarial, adult worm, and egg homogenates in sequence. J Parasitol. 1962 Apr;48:233–236. [PubMed] [Google Scholar]
  33. Ramalho-Pinto F. J., Gazzinelli G., Howells R. E., Mota-Santos T. A., Figueiredo E. A., Pellegrino J. Schistosoma mansoni: defined system for stepwise transformation of cercaria to schistosomule in vitro. Exp Parasitol. 1974 Dec;36(3):360–372. doi: 10.1016/0014-4894(74)90076-9. [DOI] [PubMed] [Google Scholar]
  34. STIREWALT M. A., KUNTZ R. E., EVANS A. S. The relative susceptibilities of the commonly-used laboratory mammal to infection by Schistosoma mansoni. Am J Trop Med Hyg. 1951 Jan;31(1):57–82. doi: 10.4269/ajtmh.1951.s1-31.57. [DOI] [PubMed] [Google Scholar]
  35. STIREWALT M. A. The influence of previous infection of mice with Schistosoma mansoni on a challenging infection with the homologous parasite. Am J Trop Med Hyg. 1953 Sep;2(5):867–882. doi: 10.4269/ajtmh.1953.2.867. [DOI] [PubMed] [Google Scholar]
  36. Samuelson J. C., Sher A., Caulfield J. P. Newly transformed schistosomula spontaneously lose surface antigens and C3 acceptor sites during culture. J Immunol. 1980 Apr;124(4):2055–2057. [PubMed] [Google Scholar]
  37. 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]
  38. Sher A., Mackenzie P., Smithers S. R. Decreased recovery of invading parasites from the lungs as a parameter of acquired immunity to schistosomiasis in the mouse. J Infect Dis. 1974 Dec;130(6):626–633. doi: 10.1093/infdis/130.6.626. [DOI] [PubMed] [Google Scholar]
  39. Smith M. A., Clegg J. A., Snary D., Trejdosiewicz A. J. Passive immunization of mice against Schistosoma mansoni with an IgM monoclonal antibody. Parasitology. 1982 Feb;84(1):83–91. doi: 10.1017/s0031182000051684. [DOI] [PubMed] [Google Scholar]
  40. Taylor D. W., Butterworth A. E. Monoclonal antibodies against surface antigens of schistosomula of Schistosoma mansoni. Parasitology. 1982 Feb;84(1):65–82. doi: 10.1017/s0031182000051672. [DOI] [PubMed] [Google Scholar]
  41. 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]
  42. VONLICHTENBERG F., SADUN E. H., BRUCE J. I. HOST RESPONSE TO EGGS OF SCHISTOSOMA MANSONI. III. THE ROLE OF EGGS IN RESISTANCE. J Infect Dis. 1963 Sep-Oct;113:113–122. doi: 10.1093/infdis/113.2.113. [DOI] [PubMed] [Google Scholar]
  43. Warren K. S., Domingo E. O. Schistosoma mansoni: stage specificity of granuloma formation around eggs after exposure to irradiated cercariae, unisexual infections, or dead worms. Exp Parasitol. 1970 Feb;27(1):60–66. doi: 10.1016/s0014-4894(70)80010-8. [DOI] [PubMed] [Google Scholar]
  44. Watten K. S., Peters P. A. Comparison of penetration and maturation of Schistosoma mansoni in the hamster, mouse, guinea pig, rabbit, and rat. Am J Trop Med Hyg. 1967 Nov;16(6):718–722. [PubMed] [Google Scholar]
  45. Zodda D. M., Phillips S. M. Monoclonal antibody-mediated protection against Schistosoma mansoni infection in mice. J Immunol. 1982 Dec;129(6):2326–2328. [PubMed] [Google Scholar]

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