Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-28T03:33:52.094Z Has data issue: false hasContentIssue false

Schistosoma mansoni: immunolocalization of two different fucose-containing carbohydrate epitopes

Published online by Cambridge University Press:  06 April 2009

B. Köster
Affiliation:
Department of Pharmacology and Molecular Sciences, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
M. Strand
Affiliation:
Department of Pharmacology and Molecular Sciences, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA

Summary

We have used two monoclonal antibodies, 128C3/3 and 504B1, to immunolocalize their carbohydrate epitopes in different developmental stages of Schistosoma mansoni. Both epitopes contain fucose: mAb 128C3/3, as we have shown previously, recognizes fucose in a novel, possibly internal linkage (Levery et al. 1992) while mAb 504B1, as we show here, bound to the Lex epitope, which contains fucose α1 → 3 linked to N-acetyl-glucosamine. The tissue expression of these epitopes was strikingly different and both elicit an immune response in infected hosts. The mAb 128C3/3-defined epitope was exposed on the surface of all larval stages but not on adult worms; however, it was found in the excretory system of adult worms of both sexes. In contrast, surface expression of the Lex epitope was initiated after the transformation of cercariae to schistosomula and was maintained throughout the adult life in both sexes.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1994

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

Bickle, Q. D. & Andrews, B. J. (1988). Characterization of Schistosoma mansoni monoclonal antibodies which block in vitro killing: failure to demonstrate blockage of immunity in vivo. Parasite Immunology 10, 151–68.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Andrews, B. J. & Taylor, M. G. (1986). Schistosoma mansoni: Characterization of two protective monoclonal antibodies. Parasite Immunology 8, 95107.CrossRefGoogle ScholarPubMed
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., Mugambi, M., Ouma, J. H., Arap Siongok, T. K. & Sturrock, R. F. (1987). Immunity in schistosomiasis mansoni: Prevention by blocking antibodies of the expression of immunity in young children. Parasitology 94, 281300.CrossRefGoogle ScholarPubMed
Caulfield, J. P., Cianci, C. M. L., McDiarmid, S. S., Suyemitsu, T. & Schmid, K. (1987). Ultrastructure, carbohydrate, and amino acid analysis of two preparations of the cercarial glycocalyx of Schistosoma mansoni. Journal of Parasitology 73, 514–22.CrossRefGoogle ScholarPubMed
Dalton, J. P., Lewis, S. A., Aronstein, W. S. & Strand, M. (1987). Schistosoma mansoni: Immunogenic glycoproteins of the cercarial glycocalyx. Experimental Parasitology 63, 215–26.CrossRefGoogle ScholarPubMed
Dalton, J. P., Strand, M., Mangold, B. L. & Dean, D. A. (1986). Identification of Schistosoma mansoni glycoproteins recognized by protective antibodies from mice immunized with irradiated cercariae. Journal of Immunology 136, 4689–94.CrossRefGoogle ScholarPubMed
Damjanov, I., Fox, N., Knowles, B. B., Solter, D., Lange, B. H. & Fraley, E. E. (1982). Immunohistochemical localization of murine stage specific embryonic antigens in human testicular germ cell tumors. American Journal of Pathology 108, 225–30.Google ScholarPubMed
Deelder, A. M., El-Dosoky, I., Van Marck, E. A. E. & Quian, Z. L. (1985). Immunofluorescent localization of Schistosoma mansoni circulating cathodic antigen in tissues of infected mice using monoclonal antibody. Zeitschrift für Parasitenkunde 71, 317–23.CrossRefGoogle ScholarPubMed
Deelder, A. M., Klappe, H. T. M., Van Den Aardweg, G. J. M. J. & Van Meerbeke, E. H. E. M. (1976). Schistosoma mansoni: Demonstration of two circulating antigens in infected hamsters. Experimental Parasitology 40, 189–97.CrossRefGoogle ScholarPubMed
De Water, R., Fransen, J. A. M. & Deelder, A. M. (1986). Ultrastructural localization of the circulating cathodic antigen in the digestive tract of various life-cycle stages of Schistosoma mansoni. Zeitschrift für Parasitenkunde 72, 635–46.CrossRefGoogle ScholarPubMed
Dissous, C., Grzych, J. M. & Capron, A. (1982). Schistosoma mansoni surface antigen defined by a rat monoclonal IgG2a. Journal of Immunology 129, 2233–5.Google ScholarPubMed
Dissous, C., Grzych, J. M. & Capron, A. (1986). Schistosoma mansoni shares a protective oligosaccharide epitope with freshwater and marine snails. Nature, London 323, 443–5.CrossRefGoogle ScholarPubMed
Dunne, D. W. & Bickle, Q. D. (1987). Identification and characterization of a polysaccharide-containing antigen from Schistosoma mansoni eggs which cross-reacts with the surface of schistosomula. Parasitology 94, 255–68.CrossRefGoogle ScholarPubMed
Fairless, B., Hornish, D. & Bartel, A. H. (1967). Preliminary chemical investigations of carbohydrate associated with key-hole limpet haemocyanin. Immunochemistry 4, 116–18.CrossRefGoogle Scholar
Feizi, T. & Childs, R. A. (1985). Carbohydrate structures of glycoproteins and glycolipids as differentiation antigens, tumour-associated antigens and components of receptor systems. Trends in Biochemical Sciences 10, 24–9.CrossRefGoogle Scholar
Gooi, H. C., Feizi, C., Kapadia, T., Knowles, B. B., Solter, D. & Evans, M. J. (1981). Stage-specific embryonic antigen involves αl-3 fucosylated type 2 blood group chains. Nature, London 292, 156–8.CrossRefGoogle ScholarPubMed
Gregoire, R. J., Shi, M., Rekosh, D. M. & Loverde, P. T. (1987). Protective monoclonal antibodies from mice vaccinated or chronically infected with Schistosoma mansoni that recognize the same antigens. Journal of Immunology 139, 3792–801.CrossRefGoogle ScholarPubMed
Grzych, J. M., Capron, M., Dissous, C. & Capron, A. (1984). Blocking activity of rat monoclonal antibodies in experimental schistosomiasis. Journal of Immunology 133, 9981004.CrossRefGoogle ScholarPubMed
Grzych, J. M., Dissous, C., Capron, M., Torres, S., Lambert, P. H. & Capron, A. (1987). Schistosoma mansoni shares a protective epitope with keyhole limpet haemocyanin. Journal of Experimental Medicine 165, 865–78.CrossRefGoogle Scholar
Hakomori, S. (1989). Aberrant glycosylation in tumors and tumor-associated carbohydrate antigens. Advances in Cancer Research 52, 257331.CrossRefGoogle ScholarPubMed
Harn, D. A., Cianci, C. M. & Caulfield, J. P. (1989). Schistosoma mansoni: immunization with cercarial glycocalyx preparation increases the adult worm burden. Experimental Parasitology 68, 108–10.CrossRefGoogle ScholarPubMed
Harn, D. A., Mitsuyama, M. & David, J. R. (1984). Schistosoma mansoni: Anti-egg monoclonal antibodies protect against cercarial challenge. Journal of Experimental Medicine 159, 1371–87.CrossRefGoogle ScholarPubMed
Harn, D. A. & Palanivel, V. (1993). Oligosaccharide (Lewis+) stimulated B220+ cells produce IL-10 and may contribute to downregulation of Th1CD4+ T cells in murine schistosomiasis. SRP International Conference on Schistosomiasis,Cairo, Egypt.Google Scholar
Harn, D. A., Quinn, J. J., Cianci, C. M. & Ko, A. I. (1987). Evidence that a protective membrane epitope is involved in early but not late phase immunity in Schistosoma mansoni. Journal of Immunology 138, 1571–80.CrossRefGoogle Scholar
Hassan, M. M., Badawi, M. A. & Strand, M. (1992). Circulating schistosomal antigen in diagnosis and assessment of cure in individuals infected with Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 46, 737–44.CrossRefGoogle ScholarPubMed
Hayunga, E. G. & Sumner, M. P. (1986). Expression of lectin-binding surface glycoproteins during the development of Schistosoma mansoni schistosomula. Journal of Parasitology 72, 913–20.CrossRefGoogle ScholarPubMed
Jwo, J. & Loverde, P. T. (1989). Fractionated sera from Schistosoma mansoni infected patients confers passive protection in mice. American Journal of Tropical Medicine and Hygiene 41, 553–62.CrossRefGoogle ScholarPubMed
Kannagi, R., Cochran, N. A., Ishigami, F., Hakomori, S., Andrews, P. W., Knowles, B. D. & Solter, D. (1983). Stage-specific embryonic antigen (SSEA-3 and -4) are epitopes of a unique globo-series ganglioside isolated from human teratocarcinoma cells. EMBO Journal 2, 2355–61.CrossRefGoogle ScholarPubMed
Karnovszky, M. J. (1965). A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. Journal of Cell Biology 27, 137a.Google Scholar
Kelly, C., Simpson, A. J. G., Fox, E., Phillips, S. M. & Smithers, S. R. (1986). The identification of Schistosoma mansoni surface antigens recognized by protective monoclonal antibodies. Parasite Immunology 8, 193–8.CrossRefGoogle ScholarPubMed
Khalife, J., Capron, M., Capron, A., Grzych, J. M., Butterworth, A. E., Dunne, D. W. & Ouma, J. H. (1986). Immunity in human schistosomiasis mansoni. Regulation of protective immune mechanisms by IgM blocking antibodies. Journal of Experimental Medicine 164, 1626–40.CrossRefGoogle ScholarPubMed
Ko, A. I., Dräger, U. C. & Harn, D. A. (1990). A Schistosoma mansoni epitope recognized by a protective monoclonal antibody is identical to the stage-specific embryonic antigen 1. Proceedings of the National Academy of Sciences, USA 87, 4159–63.CrossRefGoogle Scholar
Köster, B. (1987). Schistosoma mansoni: production of monoclonal antibodies and immunolocalization of their epitopes in different developmental stages. Ph.D. thesis. Rheinische Friedrich-Wilhelms Universität, Bonn School of Medicine, Germany.Google Scholar
Köster, B. & Strand, M. (1989). Developmentally regulated expression of Schistosoma mansoni glycoproteins. The 38th Annual Meeting of the American Society for Tropical Medicine and Hygiene,Honolulu, Hawaii.Google Scholar
Lasky, L. A. (1992). Selectins: interpreters of cell-specific carbohydrate information during inflammation. Science 258, 964–9.CrossRefGoogle ScholarPubMed
Levery, S. B., Weiss, J. B., Salyan, M. E. K., Roberts, C. E., Hakomori, S., Magnani, J. L. & Strand, M. (1992). Characterization of a series of novel fucose-containing glycosphingolipid immunogens from eggs of Schistosoma mansoni. Journal of Biological Chemistry 267, 5542–51.CrossRefGoogle ScholarPubMed
Linder, E. (1985). Schistosoma mansoni; Visualization with fluorescent lectins of secretions and surface carbohydrates of living cercariae. Experimental Parasitology 59, 307–12.CrossRefGoogle ScholarPubMed
Linder, E. & Huldt, G. (1982). Distribution of exposed and hidden carbohydrates of Schistosoma mansoni adult worms demonstrated by selective binding of fluorochrome-conjugated lectins. Parasitology 85, 503–9.CrossRefGoogle ScholarPubMed
Linder, E., Thors, C. & Lundin, L. (1991). Isolation of a SBA lectin-reactive glycoprotein (GP50) and its identification in Schistosoma mansoni larval and adult worm secretions. Journal of Parasitology 77, 391401.CrossRefGoogle ScholarPubMed
Macgregor, A. N., Stott, D. I. & Kusel, J. R. (1985). Lectin binding to glycoproteins in the surface membrane of Schistosoma mansoni. Molecular and Biochemical Parasitology 16, 163–72.CrossRefGoogle ScholarPubMed
Mansour, M. M., Omer-Ali, P., Farid, Z., Simpson, A. J. G. & Woody, J. W. (1989). Serological differentiation of acute and chronic schistosomiasis mansoni by antibody responses to keyhole limpet haemocyanin. American Journal of Tropical Medicine and Hygiene 41, 338–44.CrossRefGoogle Scholar
Nanduri, J., Dennis, J. E., Rosenberry, T. L., Mahmoud, A. A. F. & Tartakoff, A. M. (1991). Glycocalyx of bodies versus tails of Schistosoma mansoni cercariae. Journal of Biological Chemistry 266, 1341–7.CrossRefGoogle ScholarPubMed
Norden, A. P. & Strand, M. (1984). Schistosoma mansoni, S. haematobium, and S. japonicum: Identification of genus- and species-specific antigenic egg glycoproteins. Experimental Parasitology 58, 333–44.CrossRefGoogle ScholarPubMed
Norden, A. P. & Strand, M. (1985). Identification of antigenic Schistosoma mansoni glycoproteins during the course of infection in mice and humans. American Journal of Tropical Medicine and Hygiene 34, 495507.CrossRefGoogle ScholarPubMed
Nyame, K., Cummings, R. D. & Damian, R. T. (1988 a). Characterization of the N- and O-linked oligosaccharides in glycoproteins synthesized by Schistosoma mansoni schistosomula. Journal of Parasitology 74, 562–5.CrossRefGoogle Scholar
Nyame, K., Cummings, R. D. & Damian, R. T. (1988 b). Characterization of the high mannose asparagine-linked oligosaccharides synthesized by Schistosoma mansoni adult male worms. Molecular and Biochemical Parasitology 28, 265–74.CrossRefGoogle ScholarPubMed
Nayame, K., Smith, D. F., Damian, R. T. & Cummings, R. D. (1989). Complex-type asparagine-linked oligosaccharides in glycoproteins synthesized by Schistosoma mansoni adult males contain terminal-linked N-Acetylgalactosamine. Journal of Biological Chemistry 264, 3235–43.CrossRefGoogle Scholar
Omer-Ali, P., Hagan, P., Wilkins, H. A. & Simpson, A. J. G. (1989). Antibody to schistosomulum surface carbohydrate epitopes in subjects infected with Schistosoma haematobium. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 358–61.Google Scholar
Omer-Ali, P., Magee, A. I., Kelly, C. & Simpson, A. J. G. (1986). A major role for carbohydrate epitopes preferentially recognized by chronically infected mice in the determination of Schistosoma mansoni schistosomulum surface antigenicity. Journal of Immunology 137, 3601–7.CrossRefGoogle Scholar
Omer-Ali, P., Smithers, R. C., Bickle, Q., Phillips, S. M., Harn, D. & Simpson, A. J. G. (1988). Analysis of the anti-Schistosoma mansoni surface antibody response during murine infection and its potential contribution to protective immunity. Journal of Immunology 140, 3273–9.CrossRefGoogle ScholarPubMed
Paulson, J. C. & Colley, K. J. (1989). Glycosyltransferases. Journal of Biological Chemistry 264, 17615–18.CrossRefGoogle ScholarPubMed
Payares, G. & Simpson, A. J. G. (1985). Schistosoma mansoni surface glycoproteins. Analysis of their expression and antigenicity. European Journal of Biochemistry 153, 195201.CrossRefGoogle ScholarPubMed
Riengrojpitak, S., Vojvodic, M., Boot, C. & Wilson, R. A. (1989). Reactivity of anti-tegument monoclonal antibodies with target epitopes in different worm tissues and developmental stages of Schistosoma mansoni. Parasitology 98, 213–25.CrossRefGoogle ScholarPubMed
Rivera-Marrero, C A. & Cummings, R. D. (1990). Schistosoma mansoni contains a galactosyltransferase activity distinct from that typically found in mammalian cells. Journal of Parasitology 43, 5967.Google Scholar
Rumjanek, F. D., Broomfield, K. E. & Smithers, S. R. (1979). Schistosoma mansoni: Glycosyl transferase activity and the carbohydrate composition of the tegument. Experimental Parasitology 47, 2435.CrossRefGoogle ScholarPubMed
Samuelson, J. C. & Caulfield, J. P. (1982). Loss of covalently labelled glycoproteins and glycolipids from the surface of newly transformed schistosomula of Schistosoma mansoni. Journal of Cell Biology 94, 363–9.CrossRefGoogle ScholarPubMed
Samuelson, J. C. & Caulfield, J. P. (1985). The cercarial glycocalyx of Schistosoma mansoni. Journal of Cell Biology 100, 1423–34.CrossRefGoogle ScholarPubMed
Scheinberg, D. A. & Strand, M. (1982). Leukaemic cell targeting and therapy by monoclonal antibody in a mouse model system. Cancer Research 42, 44–9.Google Scholar
Simpson, A. J. G., Rumjanek, F. D., Payares, G. & Evans, W. H. (1981). Glycosyl transferase activities are associated with the surface membrane in adult Schistosoma mansoni. Molecular and Biochemical Parasitology 4, 107–15.CrossRefGoogle ScholarPubMed
Simpson, A. J. G. & Smithers, S. R. (1980). Characterization of the exposed carbohydrates on the surface membrane of adult Schistosoma mansoni by analysis of lectin binding. Parasitology 81, 115.CrossRefGoogle ScholarPubMed
Skubitz, K. M. & Snook, R. W. II (1987). Monoclonal antibodies that recognize lacto-N-fucopentaose III (CD15) react with the adhesion-promoting glycoprotein family (LFA-1/HMAC-l/GP 150, 95) and CR1 on human neutrophils. Journal of Immunology 139, 1631–9.CrossRefGoogle ScholarPubMed
Solter, D. & Knowles, B. B. (1978). Monoclonal antibodies defining a stage specific mouse embryonic antigen (SSEA-1). Proceedings of the National Academy of Sciences, USA 75, 5565–9.CrossRefGoogle ScholarPubMed
Spurr, A. R. (1969). A Low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructure Research 26, 3143.CrossRefGoogle ScholarPubMed
Srivatsan, J., Smith, D. F. & Cummings, R. D. (1992 a). The human blood fluke Schistosoma mansoni synthesizes glycoproteins containing the Lewis X antigen. Journal of Biological Chemistry 267, 20196–203.CrossRefGoogle ScholarPubMed
Srivatsan, J., Smith, D. F. & Cummings, R. D. (1992 b). Schistosoma mansoni synthesizes novel biantennary Asn-linked oligosaccharides containing terminal β-linked N-acetylgalactosamine. Glycobiology 2, 445–52.CrossRefGoogle ScholarPubMed
Strand, M., Aronstein, W. S., Norden, A. P., Lewis, S. A. & Weiss, J. B. (1984). Schistosoma Worm Proteins: Composition and Imtnunoreactivity. The Third John Jakob Abel Symposium on Molecular Parasitology (ed. August, J. T.), pp. 185201. New York: Academic Press.Google Scholar
Strand, M., McMillan, A. & Pan, X.-Q. (1982). Schistosoma mansoni: Reactivity with infected human sera and monoclonal antibody characterization of a glycoprotein in different developmental stages. Experimental Parasitology 54, 145–56.CrossRefGoogle ScholarPubMed
Uchikawa, R. & Loker, E. S. (1991). Lectin-binding properties of the surfaces of the in-vitro-transformed Schistosoma mansoni and Echinostoma paraensei sporocysts. Journal of Parasitology 77, 742–8.CrossRefGoogle ScholarPubMed
Van Lieshout, L., De Jonge, N., El Masry, N. A., Mansour, M. M., Krijger, F. W. & Deelder, A. M. (1992). Improved diagnostic performance of the circulating antigen assay in human schistosomiasis by parallel testing for circulating anodic and cathodic antigens in serum and urine. American Journal of Tropical Medicine and Hygiene 47, 463–9.CrossRefGoogle ScholarPubMed
Weiss, J. B., Magnani, J. L. & Strand, M. (1986). Identification of Schistosoma mansoni glycolipids that share immunogenic carbohydrate epitopes with glycoproteins. Journal of Immunology 136, 4275–81.CrossRefGoogle ScholarPubMed
Weiss, J. B. & Strand, M. (1985). Characterization of developmentally regulated epitopes of Schistosoma mansoni egg glycoprotein antigens. Journal of Immunology 135, 1421–9.CrossRefGoogle ScholarPubMed
Yi, X., Omer-Ali, P., Kelly, C., Simpson, A. J. G. & Smithers, R. S. (1986). IgM antibodies recognizing carbohydrate epitopes shared between schistosomula and miracidia of Schistosoma mansoni that block in vitro killing. Journal of Immunology 137, 3946–54.CrossRefGoogle ScholarPubMed