Hostname: page-component-84b7d79bbc-7nlkj Total loading time: 0 Render date: 2024-07-28T13:39:58.588Z Has data issue: false hasContentIssue false
  • English
  • Français

Reactivity of anti-tegument monoclonal antibodies with target epitopes in different worm tissues and developmental stages of Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

Suda Riengrojpitak ,
Maria Vojvodic ,
C. Boot  and
R. A. Wilson
Suda Riengrojpitak
Affiliation:
Department of Biology, University of York, York YO1 5DD
Maria Vojvodic
Affiliation:
Department of Biology, University of York, York YO1 5DD
C. Boot
Affiliation:
Department of Biology, University of York, York YO1 5DD
R. A. Wilson
Affiliation:
Department of Biology, University of York, York YO1 5DD
Get access Rights & Permissions [Opens in a new window]

Summary

Sixteen monoclonal antibodies (MABs) were selected for their reactivity with adult schistosome tegument. The distribution of target epitopes in different tissues of the adult and in various developmental stages was investigated by indirect immunofluorescence. The distinct patterns of reactivity of the MABs permitted their classification into 9 groups. The distribution of epitopes in larvae, particularly 3 h schistosomula, generally mirrored that in adults. A change in distribution of epitopes coincided with transformation from cercaria to schistosomulum providing a marker for this process. Two MABs reacted with surface membranes of intact cercariae, and 5 with the surfaces of intact 3 h schistosomula. The target epitopes of these 5 MABs were present in the tegument of adults, but not accessible externally. These observations suggest masking of antigens, not shedding, in the course of development. Indeed, no MAB reacted with intact lung or liver worms unless they were damaged. Three MABs reacted with membranes of the tegument and most other tissues, implying properties in common. Evidence for shared functions between epithelia was provided by the reactivity of 2 MABs with the tegument and protonephridia. Eight MABs bound both to the tegument and its cell bodies. Since the latter contains the machinery for protein synthesis, it is difficult to explain why 5 MABs bound to the tegument alone. Little cross-reactivity was found with the tissues of the tapeworm Hymenolepis, rather more with the closely related Schistosoma japonicum. It was concluded that tegument antigens are to a degree tissue specific but definitely not stage specific.

Keywords

Schistosoma mansoniepitopesanti-tegument antibodiesantigen maskingtegument antigens
Type
Research Article
Information
Parasitology , Volume 98 , Issue 2 , April 1989 , pp. 213 - 225
Copyright
Copyright © Cambridge University Press 1989

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aronstein, W. S., Dalton, J. P., Weiss, J. B. & Strand, M.(1985). Identification and characterisation of a major Schistosoma mansoni glycoprotein antigen cross-reactive with Fasciola hepatica. American Journal of Tropical Medicine and Hygiene 34, 879–88.CrossRefGoogle Scholar
Aronstein, W. S., Lewis, S. A., Norden, A. P., Dalton, J. P. & Strand, M. (1986). Molecular identity of a major antigen of Schistosoma mansoni which cross-reacts with Trichinella spiralis and Fasciola hepatica. Parasitology 92, 133–51.CrossRefGoogle Scholar
Aronstein, W. S., Norden, A. P. & Strand, M. (1983). Tegumental expression in larval and adult stages of a major schistosome structural glycoprotein. American Journal of Tropical Medicine and Hygiene 32, 334–42.CrossRefGoogle Scholar
Aronstein, W. S. & Strand, M. (1983). Identification of species-specific and gender-specific proteins and glycoproteins of three human schistosomes. Journal of Parasitology 69, 1006–17.CrossRefGoogle ScholarPubMed
Aronstein, W. S. & Strand, M. (1985). A glycoprotein antigen of Schistosoma mansoni expressed in the gynecophoral canal of mature male worms. American Journal of Tropical Medicine and Hygiene 34, 508–12.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Andrews, B. J., Doenhoff, M. J., Ford, M. J. & Taylor, M. G. (1985). Resistance against Schistosoma mansoni induced by highly irradiated infections: studies of species specificity of immunization and attempts to transfer resistance. Parasitology 90, 301–12.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Andrews, B. J. & Taylor, M. G. (1986). Schistosoma mansoni: characterisation of two protective monoclonal antibodies. Parasite Immunology 8, 95–107.CrossRefGoogle ScholarPubMed
Butterworth, A. E. (1984). Cell-mediated damage to helminths. Advances in Parasitology 23, 143–235.CrossRefGoogle ScholarPubMed
Capron, M. & Capron, A. (1986). Rats, mice and men-models for immune effector mechanisms against schistosomiasis. Parasitology Today 2, 69–75.CrossRefGoogle ScholarPubMed
Capron, A., Dessaint, J. P., Capron, M., Ouma, J. H. & Butterworth, A. E. (1987). Immunity to Schistosomes: progress toward vaccine. Science 238, 1065–72.CrossRefGoogle ScholarPubMed
Carneiro, C. R. W. & Lopes, J. D. (1986). Surface antigen detected by a Schistosoma mansoni monoclonal antibody in worm extracts and kidney deposits of infected mice and hamsters. Infection and Immunity 52, 230–5.CrossRefGoogle Scholar
Cheever, A. W., Hieny, S., Duvall, R. H. & Sher, A. (1983). Lack of resistance to Schistosoma japonicum in mice immunized with irradiated S. mansoni cercariae. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 812–14.CrossRefGoogle ScholarPubMed
Clegg, J. A. (1965). In vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133–47.CrossRefGoogle ScholarPubMed
Clegg, J. A. & Smithers, S. R. (1972). The effects of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. International Journal for Parasitology 2, 79–98.CrossRefGoogle ScholarPubMed
Cousin, C. E., Stirewalt, M. A. & Dorsey, C. H. (1981). Schistosoma mansoni: ultrastructure of early transformation of skin – and shear – pressure-derived schistosomules. Experimental Parasitology 51, 341–65.CrossRefGoogle ScholarPubMed
Dissous, C., Gryzch, J. M. & Capron, A. (1982). Schistosoma mansoni surface antigen defined by a rat monoclonal IgG2a. Journal of Immunology 129, 2232–4.CrossRefGoogle ScholarPubMed
Dissous, C. & Capron, A. (1983). Schistosoma mansoni: antigenic community between schistosomula and adult worm incubation products as a support for concomitant immunity. FEBS Letters 169, 355–9.CrossRefGoogle Scholar
Harn, D. A., Mitsuyama, M. & David, J. R. (1984). Schistosoma mansoni: anti-egg monoclonal antibodies protect against cercarial challenge in vivo. Journal of Experimental Medicine 159, 1371–87.CrossRefGoogle ScholarPubMed
Hillyer, G. V. (1984). Immunity to schistosomes using heterologous trematode antigens – a review. Veterinary Parasitology 14, 263–83.CrossRefGoogle ScholarPubMed
Hockley, D. J. & McLaren, D. J. (1973). Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. International Journal for Parasitology 3, 13–25.CrossRefGoogle ScholarPubMed
Johnson, G. D., Davidson, R. S., McNamee, K. C., Russell, G., Goodwin, D. & Holborow, E. J. (1982). Fading of immunofluorescence during microscopy: a study of the phenomenon and its remedy. Journal of Immunological Methods 55, 231–42.CrossRefGoogle ScholarPubMed
Knight, M., Simpson, A. J. G., Payares, G., Chaudri, M. & Smithers, S. R. (1984). Cell-free synthesis of Schistosoma mansoni surface antigens: stage specificity of their expression. EMBO Journal 3, 213–19.CrossRefGoogle ScholarPubMed
Mitchell, G. F. & Cruise, K. M. (1986). Schistosomiasis: antigens and host-parasite interactions. In Parasite Antigens: Toward New Strategies for Vaccines (ed. Pearson, T. W.), pp. 275–316. New York: Marcel Dekker.Google Scholar
McDiarmid, S. S., Dean, L. L. & Podesta, R. B. (1983). Sequential removal of outer bilayer and apical plasma membrane from surface epithelial syncytium of Schistosoma mansoni. Molecular and Biochemical Parasitology 7, 141–57.CrossRefGoogle ScholarPubMed
Macgregor, A. N., Kusel, J. R. & Wilson, R. A. (1988). Isolation and characterization of discoid granules from the tegument of adult Schistosoma mansoni. Parasitology Research 74, 250–4.CrossRefGoogle ScholarPubMed
Norden, A. P., Aronstein, W. S. & Strand, M. (1982). Schistosoma mansoni: Identification, characterization and purification of the spine glycoprotein by monoclonal antibody. Experimental Parasitology 54, 432–42.CrossRefGoogle ScholarPubMed
Payares, G., Smithers, S. R. & Evans, W. H. (1984). Purification and topographical location of tegumental alkaline phosphatase from adult Schistosoma mansoni. Molecular and Biochemical Parasitology 13, 343–60.CrossRefGoogle ScholarPubMed
Payares, G., McLaren, D. J., Evans, W. H. & Smithers, S. R. (1985). Antigenicity and immunogenicity of the tegumental outer membrane of adult Schistosoma mansoni. Parasite Immunology 7, 45–61.CrossRefGoogle ScholarPubMed
Pearce, E. J., Basch, P. F. & Sher, A. (1986). Evidence that the reduced surface antigenicity of developing Schistosoma mansoni schistosomula is due to antigen shedding rather than host molecule acquisition. Parasite Immunology 8, 79–94.CrossRefGoogle ScholarPubMed
Riengrojpitak, S. (1987). Schistosoma mansoni: localization of schistosome antigens using monospecific antibodies raised against adult worm tegument membranes. D.Phil, thesis, University of York.Google Scholar
Roberts, S. M., Macgregor, A. N., Vojvodic, M., Wells, E., Crabtree, J. E. & Wilson, R. A. (1983). Tegument surface membranes of adult Schistosoma mansoni: development of a method for their isolation. Molecular and Biochemical Parasitology 9, 105–27.CrossRefGoogle ScholarPubMed
Roberts, S. M., Wilson, R. A., Ouma, J. H., Kariuki, H. C., Koech, D., Arap Siongok, T. K., Sturrock, R. F. & Butterworth, A. E. (1987). Immunity after treatment of human schistosomiasis mansoni: quantitative and qualitative antibody responses to tegumental membrane antigens prepared from adult worms. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 786–93.CrossRefGoogle ScholarPubMed
Samuelson, J. C. & Caulfield, J. P. (1985). The cercarial glycocalyx of Schistosoma mansoni. Journal of Cell Biology 100, 1423–34.CrossRefGoogle ScholarPubMed
Simpson, A. J. G., Payares, G., Walker, T., Knight, M. & Smithers, S. R. (1984). The modulation of expression of polypeptide surface antigens on developing schistosomula of Schistosoma mansoni. Journal of Immunology 133, 2725–30.CrossRefGoogle ScholarPubMed
Simpson, A. J. G. & Smithers, S. R. (1985). Schistosomes: surface, egg and circulating antigens. Current Topics in Microbiology and Immunology 120, 205–39.Google ScholarPubMed
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695–700.CrossRefGoogle ScholarPubMed
Taylor, D. W. & Butterworth, A. E. (1982). Monoclonal antibodies against surface antigens of schistosomula of Schistosoma mansoni. Parasitology 84, 65–82.CrossRefGoogle ScholarPubMed
De Water, R., Fransen, J. A. M., Schut, D. W. O. A. & Deelder, A. M. (1987). Three monoclonal antibodies with specific binding activity to the excretory system of Schistosoma mansoni: an immunoelectron microscope study using the gold labeling technique. American Journal of Tropical Medicine and Hygiene 37, 345–52.CrossRefGoogle Scholar
Wheater, P. R. & Wilson, R. A. (1976). The tegument of Schistosoma mansoni: a histochemical investigation. Parasitology 72, 99–109.CrossRefGoogle ScholarPubMed
Wilson, R. A. (1987). Cercariae to liver worms: development and migration in the mammalian host. In The Biology of Schistosomes (ed. Rollinson, D. and Simpson, A. J. G.), pp. 115–46. London: Academic Press.Google Scholar
Zodda, D. M. & Phillips, S. M. (1982). Monoclonal antibody-mediated protection against Schistosoma mansoni infection in mice. Journal of Immunology 129, 2326–8.CrossRefGoogle ScholarPubMed