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Ultrastructural localization of Sm28 GST protective antigen in Schistosoma mansoni adult worms

Published online by Cambridge University Press:  06 April 2009

J. L. Liu
Affiliation:
Centre d’ Immunologie et de Biologie Parasitaire, Unité INSERM U-J67, Institut Pasteur de Lille, 1 rue du Pr Calmette1, B.P. 245, 59019 Lille Cédex, France
J. Fontaine
Affiliation:
Centre d’ Immunologie et de Biologie Parasitaire, Unité INSERM U-J67, Institut Pasteur de Lille, 1 rue du Pr Calmette1, B.P. 245, 59019 Lille Cédex, France
A. Capron
Affiliation:
Centre d’ Immunologie et de Biologie Parasitaire, Unité INSERM U-J67, Institut Pasteur de Lille, 1 rue du Pr Calmette1, B.P. 245, 59019 Lille Cédex, France
J. M. Grzych*
Affiliation:
Centre d’ Immunologie et de Biologie Parasitaire, Unité INSERM U-J67, Institut Pasteur de Lille, 1 rue du Pr Calmette1, B.P. 245, 59019 Lille Cédex, France
*
*Corresponding author: Tel: +33 20 87 78 09. Fax: +33 20 87 78 88.

Summary

The localization of the 28 kDa Schistosoma mansoni glutathione S-transferase (Sm28 GST) has been investigated using immunohistochemistry and electron microscopy and the results compared with previously published data. This study confirms the wide distribution of this antigen in the parasite. In male and female worms, Sm28 GST is localized in the tegument, the parenchyma, the oesophageal epithelium and in genital organs. Sm28 GST was clearly detected in germinal and sustentacular cells. The decrease of staining intensity during the differentiation of germinal cells suggests a down-regulated expression of the molecule. At the ultrastructural level, this antigen was abundant in nuclei and less present in the cytoplasm. The marked heterogeneity observed in the staining of individual worms indicates that Sm28 GST seems to be closely associated with the parasite’s metabolism. The results are discussed in relation to the biological and protective functions of the protein.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Balloul, J. M., Pierce, R. J., Grzych, J. M. & Capron, A. (1985). In vitro synthesis of a 28-Kilodalton antigen present on the surface of the schistosomulum of Schistosoma mansoni. Molecular and Biochemical Parasitology 17, 105114.CrossRefGoogle ScholarPubMed
Balloul, J. M., Sondermeyer, P., Dreyer, D., Capron, M., Grzych, J. M., Pierce, R. J., Carvallo, D., Lecocq, J. P. & Capron, A. (1987 a). Molecular-cloning of a protective antigen of schistosomes. Nature, London 326, 149153.CrossRefGoogle ScholarPubMed
Balloul, J. M., Grzych, J. M., Pierce, R. J. & Capron, A. (1987 b). A purified 28,000 dalton protein from Schistosoma mansoni adult worms protects rats and mice against experimental schistosomiasis. Journal of Immunology 138, 34483453.CrossRefGoogle ScholarPubMed
Boulanger, D., Reid, G. D. F., Sturrock, R. F., Wolowczuk, I., Balloul, J. M., Grezel, D., Pierce, R. J., Otieno, M. F., Guerret, S., Grimaud, J. A., Butterworth, A. E. & Capron, A. (1991). Immunization of mice and baboons with the recombinant Sm28 GST affects both worm viability and fecundity after experimental infection with Schistosoma mansoni. Parasite Immunology 13, 473490.CrossRefGoogle Scholar
Boulanger, D., Trottein, F., Mauny, F., Brémond, P., Couret, D., Pierce, R. J., Kadri, S., Godin, C., Sellin, E., Lecocq, J. P. & Capron, A. (1994). Vaccination of goats against the trematode Schistosoma bovis with a recombinant homologous schistosome-derived glutathione S-transferase. Parasite Immunology 16, 399406.CrossRefGoogle ScholarPubMed
Boulanger, D., Warter, A., Trottein, F., Mauny, F., Brémond, P., Audibert, F., Couret, D., Kadri, S., Godin, C., Sellin, E., Pierce, R. J., Lecocq, J. P., Sellin, B. & Capron, A. (1995). Vaccination of patas monkeys experimentally infected with Schistosoma haematobium using a recombinant glutathione S-transferase cloned from S. mansoni. Parasite Immunology 17, 361369.CrossRefGoogle ScholarPubMed
Brophy, P. M. & Barrett, J. (1989). Glutathione transferase in helminths. Parasitology 100, 345349.CrossRefGoogle Scholar
Brophy, P. M. & Pritchard, D. I. (1994). Parasitic helminth glutathione S-transferases: an update on their potential as targets for immuno- and chemotherapy. Experimental Parasitology 79, 8996.CrossRefGoogle ScholarPubMed
Campbell, J. A. H., Corrigall, A. V., Guy, A. & Kirsch, R. E. (1991). Immunohistologic localization of Apha, Mu and Pi class glutathione S-transferases in human tissues. Cancer 67, 16081613.3.0.CO;2-S>CrossRefGoogle Scholar
Capron, A., Balloul, J. M., Grezel, D., Grzych, J. M., Wolowczuk, I., Auriault, C., Boulanger, D., Capron, M. & Pierce, R. J. (1990). Progress towards vaccine against schistosomiasis. In Molecular Aspects of Immune Response and Infectious Disease (ed. Kiyono, H., Jirillo, E. & DeSimone, C.) pp. 183191. Raven Press, Ltd, New York.Google Scholar
Creaney, J., Wijffels, G. L., Sexton, J. L., Sandeman, R. M., Spithill, T. W. & Parsons, J. C. (1995). Fasciola hepatica: localization of glutathione S-transferase isoenzymes in adult and juvenile liver fluke. Experimental Parasitology 81, 106116.CrossRefGoogle ScholarPubMed
Grezel, D., Capron, M., Grzych, J. M., Fontaine, J., Lecocq, J. P. & Capron, A. (1993). Protective immunity induced in rat schistosomiasis by a single dose of the Sm28 GST recombinant antigen: effector mechanisms involving IgE and IgA antibodies. European Journal of Immunology 23, 454460.CrossRefGoogle Scholar
Hiley, C., Fryer, A., Bell, J., Hume, R. & Strange, R. C. (1988). The human glutathione S-transferases, Immunohistochemical studies of the developmental expression of Alpha- and Pi-class isoenzymes in liver. The Biochemical Journal 254, 255259.CrossRefGoogle ScholarPubMed
Holy, J. M., O’Leary, K. A., Oaks, J. A. & Tracy, J. W. (1989). Immunocytochemical localization of the major glutathione S-transferase in adult Schistosoma mansoni. Journal of Parasitology 75, 181190.CrossRefGoogle ScholarPubMed
Ketterer, B., Tan, H., Mayer, D. J. & Coles, B. (1987). Glutathione S-transferases: a possible role in the detoxification of DNA and lipid hydroperoxides. In Glutathione S-transferases and Carcinogenesis (ed.Mantle, T. J., Pickett, C. B. & Hayes, J. D.) pp. 149163. Taylor & Francis, London.Google Scholar
Mannervik, B. (1985). Isoenzymes of glutathione transferase. Advances in Enzymology and Related Areas of Molecular Biology 57, 357417.Google ScholarPubMed
McLean, I. W. & Nakane, P. K. (1977). Periodate-lysine- paraformaldehyde fixative. A new fixative for immunoelectron microscopy. Journal of Histochemistry and Cytochemistry 22, 10771083.CrossRefGoogle Scholar
Mitchell, G. F. (1989). Glutathione S-transferase: potential components of anti-schistosome vaccine? Parasitology Today 5, 3437.CrossRefGoogle Scholar
Moeremans, M., Daneels, G., Van Dijck, A., Langanger, G. & De Mey, J. (1988). Sensitive visualization of antigen-antibody reaction in dot and blot immune overlay assays with immunogold and immunogold/silver staining. Journal of Immunological Methods 74, 353360.CrossRefGoogle Scholar
O’Leary, K. A. & Tracy, J. W. (1988). Purification of three cytosolic glutathione S-transferases from adult Schistosoma mansoni. Archives of Biochemistry and Biophysics 264, 112.CrossRefGoogle ScholarPubMed
Ostlund, Farrants A.-K., Meyer, D. J., Coles, B., Southan, C., Aitken, A., Johnson, P. J. & Ketterer, B. (1987). The separation of glutathione transferase subunits by using reverse-phase high-pressure liquid chromatography. The Biochemical Journal 245, 423428.CrossRefGoogle Scholar
Pierce, R. J., Khalife, J., Williams, D. L., Kanno, R., Trottein, F., Lepresle, T., Sabatier, J., Achstetter, T. & Capron, A. (1994). Schistosoma mansoni: Characterization of sequence variants of the 28-kDa glutathione S-transferase. Experimental Parasitology 79, 8184.CrossRefGoogle ScholarPubMed
Porchet, E., McNair, A., Caron, A., Kusnierz, J. P., Zemzoumi, K. & Capron, A. (1994). Tissue expression of the Schistosoma mansoni 28 kDa glutathione S-transferase. Parasitology 109, 565572.CrossRefGoogle ScholarPubMed
Precious, W. Y. & Barrett, J. (1989). The possible absence of cytochrome P-450 linked xenobiotic metabolism in helminths. Biochimica et Biophysica Acta 992, 215222.CrossRefGoogle ScholarPubMed
Reissig, M. (1970). Characterization of cell types in the parenchyma of Schistosoma mansoni. Parasitology 60, 273279.CrossRefGoogle ScholarPubMed
Salvatore, L., Wijffels, G., Sexton, J. L., Panaccio, M., Mailer, S., McCauley, I. & Spithill, T. W. (1995). Biochemical analysis of recombinant glutathione S-transferase of Fasciola hepatica. Molecular and Biochemical Parasitology 69, 281288.CrossRefGoogle ScholarPubMed
Sexton, J. L., Milner, A. R., Panaccio, M., Waddington, J., Wijffels, G., Chandler, D., Thompson, C., Wilson, L., Spithill, T. W., Mitchell, G. F. & Campbell, N. J. (1990). Glutathione S-transferase: novel vaccine against Fasciola hepatica infection in sheep. Journal of Immunology 145, 39053910.CrossRefGoogle ScholarPubMed
Taylor, J. B., Vidal, A., Torpier, G., Meyer, D. J., Roitsch, C., Balloul, J. M., Southan, C., Sondermeyer, P., Pemble, S., Lecocq, J. P., Capron, A. & Ketterer, B. (1988). The glutathione transferase activity and tissue distribution of a cloned Mr28K protective antigen of Schistosoma mansoni. EMBO Journal 7, 465472.CrossRefGoogle ScholarPubMed
Terrier, P., Townsend, A. J., Coindre, J. M., Triche, T. J. & Cowan, K. H. (1990). An immunohistochemical study of Pi class glutathione S-transferase expression in normal human tissue. American Journal of Pathology 137, 845853.Google ScholarPubMed
Vande, Waa E. A., Campbell, C. K., O’Leary, K. A. & Tracy, J. W. (1993). Induction of Schistosoma mansoni glutathione S-transferase by xenobiotics. Archives of Biochemistry and Biophysics 303, 1521.CrossRefGoogle Scholar
Walker, J., Crowley, P., Moreman, A. D. & Barrett, J. (1993). Biochemical properties of cloned glutathione S-transferases from Schistosoma mansoni and Schistosoma japonicum. Molecular and Biochemical Parasitology 61, 255264.CrossRefGoogle ScholarPubMed
Wijffels, G. L., Sexton, J. L., Salvatore, L., Pettit, J. M., Humphris, D. C., Panaccio, M. & Spithill, T. W. (1992). Primary sequence heterogeneity and tissue expression of glutathione S-transferases of Fasciola hepatica. Experimental Parasitology 74, 8799.CrossRefGoogle ScholarPubMed
Xu, C. B., Verwaerde, C., Grzych, J. M., Fontaine, J. & Capron, A. (1991). A monoclonal antibody blocking the Schistosoma mansoni 28-kDa glutathione S-transferase activity reduces female worm fecundity and egg viability. European Journal of Immunology 21, 18011807.CrossRefGoogle ScholarPubMed
Xu, C. B., Verwaerde, C., Gras-Masse, H., Fontaine, J., Bossus, M., Trottein, F., Wolowczuk, I., Tartar, A. & Capron, A. (1993). Schistosoma mansoni 28-kDa glutathione S-transferase and immunity against parasite fecundity and egg viability. Role of the amino- and carboxyl-terminal domains. Journal of Immunology 150, 940949.CrossRefGoogle ScholarPubMed