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Neutral glycolipids of Schistosoma mansoni as feasible antigens in the detection of schistosomiasis

Published online by Cambridge University Press:  06 April 2009

R. D. Dennis ,
S. Baumeister ,
G. Lauer ,
R. Richter  and
E. Geyer
R. D. Dennis*
Affiliation:
Biochemisches Institut am Klinikum der Universität Giessen, Friedrichstraβe 24, D-35385 Giessen, Germany
S. Baumeister
Affiliation:
Allgemeine und Medizinische Parasitologie, FB Biologie, Universität Marburg, D-35033 Marburg, Germany
G. Lauer
Affiliation:
Allgemeine und Medizinische Parasitologie, FB Biologie, Universität Marburg, D-35033 Marburg, Germany
R. Richter
Affiliation:
Allgemeine und Medizinische Parasitologie, FB Biologie, Universität Marburg, D-35033 Marburg, Germany
E. Geyer
Affiliation:
Allgemeine und Medizinische Parasitologie, FB Biologie, Universität Marburg, D-35033 Marburg, Germany
*
* Correspondence and reprint requests to Dr R. D. Dennis, Biochemisches Institut am Klinikum der Universität Giessen, Friedrichstraße 24, D-35385 Giessen, Germany.
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Summary

The neutral glycolipid fraction from mouse-propagated, Schistosoma mansoni adult worms has been investigated as to its chromatographic and antigenic properties, and whether it fulfills the serodiagnostic antigen requirements of sensitivity and specificity in the detection of schistosomiasis. Serological analyses were performed by thin-layer chromatography immunostaining and ELISA. In the acute-phase form of mouse schistosomiasis, the kinetics of development of neutral glycolipid-specific antibody levels was correlated with the intensity of the initial infection and the response was dominated by IgG, as represented by the subclass IgG1. With the experimental animal helminthiases screened, glycolipid antigenicity fulfilled the fundamental traits for a serodiagnostic reagent. In the chronic-phase form of human schistosomiasis mansoni, neutral glycolipid-specific antibody levels were not correlated with the intensity of infection, as estimated from the faecal content of parasite eggs, whilst the isotypic response was dominated by IgM and IgG, the latter represented primarily by IgG1 and secondarily by IgG3. With other human helminthiases, glycolipid antigenicity was incomplete, in that, the specificity was only partially fulfilled. The reason for this incomplete specificity has been clarified, in part, by the detection of cryptic schistosomiasis infections in the cohorts of African patient sera examined.

Keywords

trematodeSchistosoma mansoni adult glycolipidsHPTLC-immunostainingELISAdifferential sero-diagnosis.
Type
Research Article
Information
Parasitology , Volume 112 , Issue 3 , March 1996 , pp. 295 - 307
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Alving, C. R., Joseph, K. C., Lindsley, H. B. & Schoenbechler, M. S. (1974). Immune damage to liposomes containing lipids from Schistosoma mansoni worms (38125). Proceedings of the Society for Experimental Biology and Medicine 146, 458–61.CrossRefGoogle Scholar
Baumeister, S., Dennis, R. D., Klünder, R., Schares, G., Zahner, H. & Geyer, E. (1994). Litomosoides carinii: macrofilariae-derived glycolipids–chromatography, serology and potential in the evaluation of anthelminthic efficacy. Parasite Immunology 16, 629–41.CrossRefGoogle ScholarPubMed
Baumeister, S., Dennis, R. D., Kunz, J., Wiegandt, H. & Geyer, E. (1992). Comparative serological reactivity of Taenia crassiceps, Taenia solium and Taenia saginata metacestode neutral glycolipids to infection serum from Taenia crassiceps-infected mice. Molecular and Biochemical Parasitology 53, 53–62.CrossRefGoogle ScholarPubMed
Baumeister, S., Schuh, C., Dennis, R. D., Pfister, H., Walther, M. & Geyer, E. (1995). Bovine cysticercosis: Demonstration of serum IgG antibodies in experimentally infected calves reactive with neutral glycolipids of Taenia saginata and Taenia crassiceps metacestodes. Parasitology Research 81, 18–25.CrossRefGoogle Scholar
Bout, D., Rousseaux, R., Carlier, Y. & Capron, A. (1980). Kinetics of classes and subclasses of total immunoglobulins and specific antibodies to Schistosoma mansoni during murine infection. Parasitology 80, 247–56.CrossRefGoogle ScholarPubMed
Capron, M., Capron, A., Khalife, J., Butterworth, A. E. & Grzych, j. M. (1987). Blocking antibodies and vaccine strategy in schistosomiasis. Acta Tropica 44 (Suppl. 12), 55–62.Google Scholar
Caulfield, J. P., Ciani, 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
Demeure, C. E., Rihet, P., Abel, L., Ouattara, M., Bourgois, A. & Dessein, A. J. (1993). Resistance to Schistosoma mansoni in humans: Influence of the IgE/IgG4 balance and IgG2 in immunity to reinfection after chemotherapy. Journal of Infectious Diseases 168, 1000–8.CrossRefGoogle ScholarPubMed
Dennis, R. D., Baumeister, S., Geyer, R., Peter-Katalinic, J., Hartmann, R., Egge, H., Geyer, E. & Wiegandt, H. (1992). Glycosphingolipids in cestodes. Chemical structures of ceramide monosaccharide, disaccharide, trisaccharide and tetrasaccharide from metacestodes of the fox tapeworm, Taenia crassiceps (Cestoda: Cyclophyllidea). European Journal of Biochemistry 207, 1053–62.CrossRefGoogle ScholarPubMed
Dennis, R. D., Baumeister, S., Irmer, C., Gasser, R. B. & Geyer, E. (1993). Chromatographic and antigenic properties of Echinococcus granulosus hydatid cyst-derived glycolipids. Parasite Immunology 15, 669–81.CrossRefGoogle ScholarPubMed
Dennis, R. D., Baumeister, S., Smuda, C., Lochnit, G., Waider, T. & Geyer, E. (1995). Initiation of chemical studies on the immunoreactive glycolipids of adult Ascaris suum. Parasitology 110, 611–23.CrossRefGoogle ScholarPubMed
Dennis, R. D., Geyer, R., Egge, H., Menges, H., Stirm, S. & Wiegandt, H. (1985). Glycosphingolipids in insects. Chemical structures of ceramide monosaccharide, disaccharide and trisaccharide from pupae of Calliphora vicina (Insecta:Diptera). European Journal of Biochemistry 146, 51–8.CrossRefGoogle ScholarPubMed
Dunne, D. W. (1990). Schistosome carbohydrates. Parasitology Today 6, 45–8.CrossRefGoogle ScholarPubMed
Dunne, D. W., Butterworth, A. E., Fulford, A. J. C., Kariuki, H. C., Langley, J. G., Ouma, J. H., Capron, A., Pierce, R. J. & Sturrock, R. F. (1992). Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. European Journal of Immunology 22, 1483–94.CrossRefGoogle ScholarPubMed
Hagan, P., Blumenthal, U. J., Dunn, D., Simpson, A. J. G. & Wilkins, H. A. (1991). Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature, London 349, 243–5.CrossRefGoogle ScholarPubMed
Jassim, A., Hassan, K. & Catty, D. (1987). Antibody isotypes in human schistosomiasis mansoni. Parasite Immunology 9, 627–50.CrossRefGoogle ScholarPubMed
Jennemann, R., Gnewuch, C., Bosslet, S., Bauer, B. L. & Wiegandt, H. (1994). Specific immunization using keyhole limpet hemocyanin-ganglioside conjugates. Journal of Biochemistry 115, 1047–52.CrossRefGoogle ScholarPubMed
Kawakami, Y., Nakamura, K., Kojima, H., Suzuki, M., Inagaki, F., Suzuki, A., Sonoki, S., Uchida, A., Murata, Y. & Tamai, Y. (1993). A novel fucosylated glycosphingolipid with Galßl–4Glcßl–3Gal sequence in plerocercoids of the parasite, Spirometra erinacei. Journal of Biochemistry 114, 677–83.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. & Strand, M. (1994). Schistosoma mansoni: immunlocalization of two different fucose-containing carbohydrate epitopes. Parasitology 108, 433–46.CrossRefGoogle Scholar
Kunz, J., Baumeister, S., Dennis, R. D., Küytz, B., Wiegandt, H. & Geyer, E. (1991). Immunological recognition of larval Taenia crassiceps glycolipids by sera from parasite-infected mice. Parasitology Research 77, 443–7.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
Makaaru, C. K., Damian, R. T., Smith, D. F. & Cummings, R. D. (1992). The human blood fluke Schistosoma mansoni synthesizes a novel type of glycosphingolipid. Journal of Biological Chemistry 267, 2251–7.CrossRefGoogle ScholarPubMed
Maloney, M. D., Semprevivo, L. H. & Coles, G. C. (1990). A comparison of the glycolipid compositions of cercarial and adult Schistosoma mansoni and their associated hosts. International Journal for Parasitology 20, 1091–3.CrossRefGoogle ScholarPubMed
Meyer, F., Meyer, H. & Bueding, E. (1970). Lipid metabolism in the parasitic and free-living flatworms, Schistosoma mansoni and Dugesia dorotocephala. Biochimica et Biophysica Acta 210, 257–66.CrossRefGoogle ScholarPubMed
Murakami, H., Lams, Z., Furie, B. C., Reinhold, V. N., Asano, T. & Furie, B. (1991). Sulfated glycolipids are the platelet autoantigens for human platelet-binding monoclonal anti-DNA autoantibodies. Journal of Biological Chemistry 266, 15414–19.CrossRefGoogle ScholarPubMed
Naiki, M., Ramasamy, R., Ochanda, J. O. & Maina, G. (1985). Lipid composition of Schistosoma mansoni and surface labeling of glycolipid components. Japanese Journal of Veterinary Science 47, 777–86.Google ScholarPubMed
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. Lectin-binding, size, charge, and electron microscopic characterization. Journal of Biological Chemistry 266, 1341–7.CrossRefGoogle ScholarPubMed
Nishimura, K., Suzuki, A. & Kino, H. (1991). Sphingolipids of a cestode Metroliasthes coturnix. Biochimica et Biophysica Acta 1086, 141–50.CrossRefGoogle ScholarPubMed
Nores, G. A., Mizutamari, R. K. & Kremer, D. M. (1994). Chromatographic tank designed to obtain highly reproducible high-performance thin-layer chromatograms of gangliosides and neutral glycosphingolipids. Journal of Chromatography A 686, 155–7.CrossRefGoogle Scholar
Nyame, K., Cummings, R. D. & Damian, R. T. (1988 a). Characterization of the N- and O-linked oligosaccharides in glycoproteins synthesized by Schistosoma mansoni schistosomuia. Journal of Parasitology 74, 562–72.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
Nyame, K., Smith, D. F., Damian, R. T. & Cummings, R. D. (1989). Complex-type asparagine-linked oligosaccharides in glycoproteins synthesized by Schistosoma mansoni adult males containing terminal β-linked N-acetylgalactosamine. Journal of Biological Chemistry 264, 3235–43.CrossRefGoogle ScholarPubMed
Persat, F., Bouhours, J. F., Mojon, M. & Petavy, A. F. (1992). Glycosphingolipids with Galß1–6Gal sequences in metacestodes of the parasite Echinococcus multilocularis. Journal of Biological Chemistry 267, 8764–9.CrossRefGoogle ScholarPubMed
Persat, F., Vincent, C., Mojon, M. & Petavy, A. F. (1991). Detection of antibodies against glycolipids of Echinococcus multilocularis metacestodes in sera of patients with alveolar hydatid disease. Parasite Immunology 13, 379–89.CrossRefGoogle ScholarPubMed
Rauvala, H. & Finns, J. (1979). Structural similarity of the terminal carbohydrate sequences of glycoproteins and glycolipids. FEES Letters 97, 1–8.CrossRefGoogle ScholarPubMed
Richter, D., Incani, R. N. & Harn, D. A. (1993). Isotype responses to candidate vaccine antigens in protective sera obtained from mice vaccinated with irradiated cercariae of Schistosoma mansoni. Infection and Immunity 61, 3003–11.CrossRefGoogle ScholarPubMed
Rihet, P., Demeure, C. E., Dessein, A. J. & Bourgois, A. (1992). Strong serum inhibition of specific IgE correlated to competing IgG4, revealed by a new methodology in subjects from a S. mansoni endemic area. European Journal of Immunology 22, 2063–70.CrossRefGoogle ScholarPubMed
Rogers, M. V. & McLaren, D. J. (1987). Analysis of total and surface membrane lipids of Schistosoma mansoni. Molecular and Biochemical Parasitology 22, 273–88.CrossRefGoogle ScholarPubMed
Rousseaux-Prevost, R., Bout, D., Bazin, H. & Capron, A. (1980). Homocytotropic antibody responses during murine schistosomiasis. A follow-up study of both total immunoglobulins and Schistosoma mansoni specific antibodies. International Archives of Allergy and Applied Immunology 62, 86–93.CrossRefGoogle ScholarPubMed
Sher, A., McIntyre, S. & Von Lichtenberg, F. (1977). Schistosoma mansoni: kinetics and class specificity of hypergammaglobulinemia induced during murine infection. Experimental Parasitology 41, 415–22.CrossRefGoogle ScholarPubMed
Saito, T. & Hakomori, s. (1971). Quantitative isolation of total glycosphingolipids from animal cells. Journal of Lipid Research 12, 257–9.CrossRefGoogle ScholarPubMed
Simpson, A. J. G. & Smithers, S. R. (1985). Schistosomes: surface, egg and circulating antibodies. Current Topics in Microbiology and Immunology 120, 205–39.Google Scholar
Smithers, S. R., Simpson, A. J. G., Yi, X., Omar-Ali, P., Kelly, c. & McLaren, D. J. (1987). The mouse model of schistosome immunity. Acta Tropica 44 (Suppl. 12), 21–30.Google Scholar
Smyth, J. D. (1994). Introduction to Animal Parasitology, 3rd Edn.Cambridge: Cambridge University Press.Google Scholar
Srivatsan, J., Smith, D. F. & Cummings, R. D. (1992). The human blood fluke Schistosoma mansoni synthesizes glycoproteins containing the Lewis X antigen. Journal of Biological Chemistry 267, 20196–203.CrossRefGoogle ScholarPubMed
Taylor, M. G. (1994). Schistosomiasis vaccines: farewell to the god of plague? Journal of Tropical Medicine and Hygiene 97, 257–68.Google ScholarPubMed
Van Dam, G. J., Bergwerff, A. A., Thomas-OateS, J. E., Rotmans, J. P., Kamerling, J. P., Vliegenthart, J. F. G. & Deelder, A. M. (1994). The immunologically reactive O-linked polysaccharide chains derived from circulating cathodic antigen isolated from the human blood fluke Schistosoma mansoni have Lewis X as repeating unit. European Journal of Biochemistry 225, 467–82.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, 4275–82.CrossRefGoogle ScholarPubMed
Williams, M. A. & McCluer, R. H. (1980). The Use of Sep-Pak™ C18 cartridges during the isolation of gangliosides. Journal of Neurochemistry 35, 266–9.CrossRefGoogle ScholarPubMed
Woodward, M. P., Young, W. W. & Bloodgood, R. A. (1985). Detection of monoclonal antibodies specific for carbohydrate epitopes using periodate oxidation. Journal of Immunological Methods 78, 143–53.CrossRefGoogle ScholarPubMed