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Schistosoma: analysis of monoclonal antibodies reactive with the circulating antigens CAA and CCA

Published online by Cambridge University Press:  06 April 2009

A. M. Deelder
Affiliation:
University of Leiden, Department of Parasitology, Wassenaarseweg 62, P.O. Box 9605, 2300 RC Leiden, The Netherlands
G. J. Van Dam
Affiliation:
University of Leiden, Department of Parasitology, Wassenaarseweg 62, P.O. Box 9605, 2300 RC Leiden, The Netherlands
D. Kornelis
Affiliation:
University of Leiden, Department of Parasitology, Wassenaarseweg 62, P.O. Box 9605, 2300 RC Leiden, The Netherlands
Y. E. Fillié
Affiliation:
University of Leiden, Department of Parasitology, Wassenaarseweg 62, P.O. Box 9605, 2300 RC Leiden, The Netherlands
R. J. M. Van Zeyl
Affiliation:
University of Leiden, Department of Parasitology, Wassenaarseweg 62, P.O. Box 9605, 2300 RC Leiden, The Netherlands

Summary

Using spleen cells of mice infected or immunized respectively with cercariae or antigen preparations of Schistosoma mansoni, S. haematobium or S. japonicum monoclonal antibodies (mAbs) were produced against the schistosome gut-associated antigens CAA (circulating anodic antigen) and CCA (circulating cathodic antigen). Fusions nearly exclusively produced either anti-CAA (n = 25) or anti-CCA mAbs (n = 55) with a strong isotype restriction (IgM, IgG1 and IgG3) against both antigens, the majority of anti-CAA mAbs being IgG1 and the majority of anti-CCA mAbs being IgM. The mAbs, which on the basis of their selection were reactive with multiple carbohydrate epitopes of CAA or CCA, were applied in different immunological techniques including immunofluorescence, a dot immunobinding assay and immuno-electrophoresis to study the epitope repertoire. Anti-CAA mAbs were found to be reactive with 5 different epitopes, none of which occurred as multiple epitopes on eggs. Anti-CCA mAbs, on the other hand, recognized at least 10 different epitopes, while 44% of anti-CCA mAbs recognized epitopes common to the adult worm and the egg. Both CAA-and CCA-epitopes were found to be developmentally expressed at the level of the tegument in cercariae, schistosomula and 5-day-old lung worms, but in the adult worm were primarily found in the gut. Thus, the production of panels of mAbs has not only resulted in the selection of reagents optimally performing in diagnostic immunoassays, but also allowed a more detailed study of the epitope repertoire of these important schistosome antigens.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Aalberse, R. C., Van Der Gaag, R. & Van Leeuwen, J. (1983). Serological aspects of IgG4 antibodies. I. Prolonged immunization results in an IgG4-restricted response. Journal of Immunology 32, 722–6.CrossRefGoogle Scholar
Abraham, K. M. & Teale, J. M. (1987). Isotype restriction during infection of mice with the cestode Mesocestoides corti: role of immune suppression. Journal of Immunology 138, 1699–704.CrossRefGoogle ScholarPubMed
Appriou, M., Tribouley-Duret, J. & Tribouley, J. (1986). Étude par la réaction d'immunofluorescence des anticorps dirigés centre les antigènes de l'épithélium intestinal de Schistosoma mansoni. III. Étude de la réactivité d'un anticorps monoclonal. Annales de Parasitologie Humaine et Comparée 61, 435–46.CrossRefGoogle Scholar
Barsoum, I. S., Colley, D. G. & Kamal, K. A. (1990). Schistosoma mansoni: detection of circulating antigens in murine schistosomiasis by antigen-capture sandwich ELISA using a monoclonal antibody. Experimental Parasitology 71, 107–13.CrossRefGoogle ScholarPubMed
Barsoum, I. S., Kamal, K. A., Bassily, S., Deelder, A. M. & Colley, D. G. (1991). Diagnosis of human schistosomiasis by detection of circulating cathodic antigen with a monoclonal antibody. Journal of Infectious Diseases 164, 1010–13.CrossRefGoogle ScholarPubMed
Berggren, W. L. & Weller, T. H. (1967). Immunoelectrophoretic demonstration of specific circulating antigen in animals infected with Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 16, 606–12.CrossRefGoogle ScholarPubMed
Bergwerff, A. A., Van Dam, G. J., Rotmans, J. P., Deelder, A. M., Kamerling, J. P. & Vliegenthart, J. F. G. (1994). The immunologically reactive part of immunopurified circulating anodic antigen from Schistosoma mansoni is a threonine-linked polysaccharide consisting of →6]-[β-d-GlcpA-(1→3)]-β-d-GalpNAc-(1→ repeating units. Journal of Biological Chemistry 269, 31510–17.CrossRefGoogle Scholar
Bogers, J. J. P. M., Nibbeling, H. A. M., Van Marck, E. A. E. & Deelder, A. M. (1994). Immunofluorescent visualization of the excretory and gut system of Schistosoma mansoni by confocal laser scanning microscopy. American Journal of Tropical Medicine and Hygiene 50, 612–19.CrossRefGoogle ScholarPubMed
Briles, D. E., Claflin, J. L., Schroer, K. & Forman, C. (1981). Mouse IgG3 antibodies are highly protective against infection with Streptococcus pneumoniae. Nature, London 294, 88–9.CrossRefGoogle ScholarPubMed
Capron, A., Biguet, J., Rose, F. & Vernes, J.. (1965). Les antigènes de Schistosoma mansoni. II. Étude immunoélectrophorétique comparée de divers stades larvaires et des adultes des deux sexes. Aspects immunologiques des relations hôte–parasite de la cercaire et de l'adulte de S. mansoni. Annales de I'lnstitut Pasteur 109, 798810.Google Scholar
Carlier, Y., Bout, D., Bina, J. C., Camus, D., Figueiredo, J. F. M. & Capron, A. (1975). Immunological studies in human schistosomiasis. I. Parasitic antigen in urine. American Journal of Tropical Medicine and Hygiene 24, 949–54.CrossRefGoogle ScholarPubMed
Carlier, Y., Bout, D. & Capron, A. (1978). Further studies on the circulating M antigen in human and experimental Schistosoma mansoni infections. Annales de I'Immunologie (Institut Pasteur) 129C, 811–18.Google ScholarPubMed
Carlier, Y., Bout, D. & Capron, A. (1980). Detection of Schistosoma mansoni M antigen in circulating immune-complexes and in kidneys of infected hamsters. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 534–8.CrossRefGoogle ScholarPubMed
Carlier, Y., Bout, D., Strecker, G., Debray, H. & Capron, A. (1980). Purification, immunochemical, and biological characterization of the Schistosoma circulating M antigen. Journal of Immunology 124, 2442–50.CrossRefGoogle ScholarPubMed
De Jonge, N., De Caluwé, P., Hilberath, G. W., Krijger, F. W., Polderman, A. M. & Deelder, A. M. (1989 a). Circulating anodic antigen levels in serum before and after chemotherapy with praziquantel in schistosomiasis mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 368–72.CrossRefGoogle ScholarPubMed
De Jonge, N., Fillié, Y. E., Hilberath, G. W., Krijger, F. W., Lengeler, C., De Savigny, D. H., Van Vliet, N. G. & Deelder, A. M. (1989 b). Presence of the schistosome circulating anodic antigen (CAA) in urine of patients with Schistosoma mansoni or S. haematobium infections. American Journal of Tropical Medicine and Hygiene 41, 563–9.CrossRefGoogle ScholarPubMed
De Jonge, N., Gryseels, B., Hilberath, G. W., Polderman, A. M. & Deelder, A. M. (1988). Detection of circulating anodic antigen by ELISA for seroepidemiology of schistosomiasis mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 591–4.CrossRefGoogle ScholarPubMed
De Jonge, N., Kremsner, P. G., Krijger, F. W., Schommer, G., Fillié, Y. E., Kornelis, D., Van Zeyl, R. J. M., Van Dam, G. J., Feldmeier, H. & Deelder, A. M. (1990). Detection of the schistosome circulating cathodic antigen by enzyme immunoassay using biotinylated monoclonal antibodies. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 815–18.CrossRefGoogle ScholarPubMed
De Water, R., Van Marck, E. A. E., Fransen, J. A. M. & Deelder, A. M. (1987). Ultrastructural localization of the circulating anodic antigen and the circulating cathodic antigen in the liver of mice infected with Schistosoma mansoni: a sequential study. Experimental Parasitology 64, 499509.CrossRefGoogle ScholarPubMed
De Water, R., Van Marck, E. A. E., Fransen, J. A. M. & Deelder, A. M. (1988). Schistosoma mansoni: ultrastructural localization of the circulating anodic antigen and the circulating cathodic antigen in the mouse kidney glomerulus. American Journal of Tropical Medicine and Hygiene 38, 118–24.CrossRefGoogle ScholarPubMed
Deelder, A. M., De Jonge, N., Boerman, O. C., Fillié, Y. E., Hilberath, G. W., Rotmans, J. P., Gerritse, M. J. & Schut, D. W. O. A. (1989). Sensitive determination of circulating anodic antigen in Schistosoma mansoni infected individuals by an enzyme-linked immunosorbent assay using monoclonal antibodies. American Journal of Tropical Medicine and Hygiene 40, 268–72.CrossRefGoogle ScholarPubMed
Deelder, A. M., Fillié, Y. E., Engels, M. J. A. J., Helaha, D. & Kornelis, D. (1983 a). Application of monoclonal antibodies for the determination of circulating anodic antigen (CAA) of Schistosoma mansoni. Tropical and Geographical Medicine 35, 207.Google Scholar
Deelder, A. M., Fillié, Y. E., Helaha, D. & Kornelis, D. (1983 b). Application of monoclonal antibodies for the determination of circulating cathodic antigen (CCA) of Schistosoma mansoni. Tropical and Geographical Medicine 35, 208.Google Scholar
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
Deelder, A. M., Kornelis, D., Makbin, M., Noordpool, H. N., Codfried, R. M., Rotmans, J. P. & Oostbrug, B. F. (1980 a). Applicability of different antigen preparations in the enzyme-linked immunosorbent assay for schistosomiasis mansoni. American Journal of Tropical Medicine and Hygiene 29, 401–10.CrossRefGoogle ScholarPubMed
Deelder, A. M., Kornelis, D., Van Marck, E. A. E., Eveleigh, P. C. & Van Egmond, J. G. (1980 b). Schistosoma mansoni: characterization of two circulating polysaccharide antigens and the immunological response to these antigens in mouse, hamster, and human infections. Experimental Parasitology 50, 1632.CrossRefGoogle ScholarPubMed
Deelder, A. M., Van Zeyl, R. J. M., Fillié, Y. E., Rotmans, J. P. & Duchenne, W. (1989). Recognition of gut-associated antigens by immunoglobulin M in the indirect fluorescent antibody test for schistosomiasis mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 364–7.CrossRefGoogle ScholarPubMed
Dunne, D. W., Bickle, Q. D., Butterworth, A. E. & Richardson, B. A. (1987). The blocking of human antibody-dependent, eosinophil-mediated killing of Schistosoma mansoni schistosomula by monoclonal antibodies which cross-react with a polysaccharide-containing egg antigen. Parasitology 94, 269–80.CrossRefGoogle ScholarPubMed
Falconer, A. E., Friedmann, P. S., Bird, P. & Calvert, J. E. (1992). Abnormal immunoglobulin G subclass production in response to keyhole limpet haemocyanin in atopic patients. Clinical and Experimental Immunology 89, 495–9.CrossRefGoogle ScholarPubMed
Feldmeier, H., Nogueira-Queiroz, J. A., Peixoto-Queiroz, M. A., Doehring, E., Dessaint, J. P., De Alencar, J. E., Dafalla, A. A. & Capron, A. (1986). Detection and quantification of circulating antigen in schistosomiasis by monoclonal antibody. II. The quantification of circulating antigens in human schistosomiasis mansoni and haematobium: relationship to intensity of infection and disease status. Clinical and Experimental Immunology 65, 232–43.Google ScholarPubMed
Gold, R., Rosen, F. S. & Weller, T. H. (1969). A Specific circulating antigen in hamsters infected with Schistosoma mansoni. Detection of antigen in serum and urine, and correlation between antigenic concentration and worm burden. American Journal of Tropical Medicine and Hygiene 18, 545–52.CrossRefGoogle ScholarPubMed
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
Kestens, L., Mangelschots, K., Van Marck, E. A. E., Gigase, P. L. J. & Deelder, A. M. (1988). Schistosoma mansoni: impaired clearance of model immune complexes consisting of circulating anodic antigen and monoclonal IgGl in infected mice. Parasitology Research 74, 356–62.CrossRefGoogle Scholar
Khalife, J., Dunne, D. W., Richardson, B. A., Mazza, G., Thorne, K. J. I., Capron, A. & Butterworth, A. E. (1989). Functional role of human IgG subclasses in eosinophil-mediated killing of schistosomula of Schistosoma mansoni. Journal of Immunology 142, 4422–7.CrossRefGoogle ScholarPubMed
Köster, B. & Strand, M. (1994). Schistosoma mansoni: immunolocalization of two different fucose-containing carbohydrate epitopes. Parasitology 108, 433–46.CrossRefGoogle ScholarPubMed
Kremsner, P. G., De Jonge, N., Simarro, P. G., Mühlschlegel, F., Mir, M., Sima, P. O., Feldmeier, H., Bienzle, U. & Deelder, A. M. (1993). Quantitative determination of circulating anodic and cathodic antigens in serum and urine of individuals infected with Schistosoma intercalatum. Transactions of the Royal Society of Tropical Medicine and Hygiene 87, 167–9.CrossRefGoogle ScholarPubMed
Kremsner, P. G., Enyong, P., Krijger, F. W., De Jonge, N., Zotter, G. M., Thalhammer, F., Mühlschlegel, F., Bienzle, U., Feldmeier, H. & Deelder, A. M. (1994). Circulating anodic and cathodic antigen in serum and urine of Schistosoma haematobium-infected Cameroonian children receiving praziquantel: a longitudinal study. Clinical Infectious Diseases 18, 408–13.CrossRefGoogle ScholarPubMed
Krijger, F. W., Van Lieshout, L. & Deelder, A. M. (1994). A simple technique to pretreat urine and serum samples for quantitation of schistosome circulating anodic and cathodic antigen. Acta Tropica 56, 5563.CrossRefGoogle ScholarPubMed
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227, 680–5.CrossRefGoogle ScholarPubMed
Lal, R. B., Dhawan, R. R., Tarrand, J. J., Ayoub, E. M. & Ottesen, E. A. (1991). Lack of IgG4 antibody response to carbohydrate antigens in patients with lymphatic filariasis. Immunology 74, 333–7.Google ScholarPubMed
Lou, W. X., Qian, Z. L., Xue, C. L., Yu, A. Z., Xu, C. B., Zheng, H. Y., Yang, S. J., Su, X. S. & Sheng, L. (1991). Preparation and diagnostic application of monoclonal antibodies against Schistosoma japonicum. Chung Kuo Chi Sheng Chung Hsueh Yu Chi Sheng Chung Ping Tsa Chih 9, 254–7.Google ScholarPubMed
Massa, G., Dunne, D. W. & Butterworth, A. E. (1990). Antibody isotype responses to the Schistosoma mansoni schistosomulum in the CBA/N mouse induced by different stages of the parasite life cycle. Parasite Immunology 12, 529–43.Google Scholar
Moreno, C. & Esdaine, J. (1983). Immunoglobulin isotype in the murine response to polysaccharide antigens. European Journal of Immunology 13, 262–4.CrossRefGoogle ScholarPubMed
Mushens, R. E. & Scott, M. L. (1990). A fast and efficient method for quantification of monoclonal antibodies in an ELISA using a novel incubation system. Journal of Immunological Methods 131, 83–9.CrossRefGoogle Scholar
Nash, T. E. (1978). Antibody response to a polysaccharide antigen present in the schistosome gut. I. Sensitivity and specificity. American Journal of Tropical Medicine and Hygiene 27, 939–43.CrossRefGoogle Scholar
Nash, T. E., Nasir, U. D. & Jeanloz, R. W. (1977). Further purification and characterization of a circulating antigen in schistosomiasis. Journal of Immunology 119, 1627–33.CrossRefGoogle ScholarPubMed
Nash, T. E., Prescott, B. & Neva, F. A. (1974). The characteristics of a circulating antigen in schistosomiasis. Journal of Immunology 112, 1500–7.CrossRefGoogle ScholarPubMed
Nogueira-Queiroz, J. A., Lutsch, C., Capron, M., Dessaint, J. P. & Capron, A. (1986). Detection and quantification of circulating antigen in schistosomiasis by a monoclonal antibody. I. Specificity analysis of a monoclonal antibody with immunodiagnostic capacity. Clinical and Experimental Immunology 65, 223–31.Google ScholarPubMed
Nour El Din, M. S. A., Kornelis, D., Van Zeyl, R. J. M. & Deelder, A. M. (1994 a). Immunologic characterization of two monoclonal antibodies reactive with repetitive carbohydrate epitopes of circulating Schistosoma mansoni egg antigen. American Journal of Tropical Medicine and Hygiene 50, 487–98.CrossRefGoogle Scholar
Nour El Din, M. S. A., Nibbeling, R., Rotmans, J. P., Polderman, A. M., Krijger, F. W. & Deelder, A. M. (1994 b). Quantitative determination of circulating soluble egg antigen in urine and serum of Schistosoma mansoni-infected individuals using a combined two-site enzyme-linked immunosorbent assay. American Journal of Tropical Medicine and Hygiene 50, 585–94.CrossRefGoogle Scholar
Perlmutter, R. M., Hansburg, D., Briles, D. E., Nicolotti, R. A. & Davie, J. M. (1978). Subclass restriction of murine anti-carbohydrate antibodies. Journal of Immunology 121, 566–72.CrossRefGoogle ScholarPubMed
Qian, Z. L. & Deelder, A. M. (1993). Dot immunoassay with biotinylated antigen for determination of antibodies against the circulating cathodic antigen (CCA) in schistosomiasis japonica. American Journal of Tropical Medicine and Hygiene 49, 777–82.CrossRefGoogle ScholarPubMed
Qian, Z. L., Van Dam, G. J. & Deelder, A. M. (1993). Diagnostic evaluation of dot-binding assays for circulating cathodic antigen (CCA) and anti-CCA determinations in schistosomiasis japonica using defined biotinylated conjugates. Chinese Medical Journal 106, 584–92.Google ScholarPubMed
Sobh, M. A., Moustafa, F. E., El Housseini, F., Basta, M. T., Deelder, A. M. & Ghoniem, M. A. (1987). Schistosomal specific nephropathy leading to end-stage renal failure. Kidney International 31, 1006–11.CrossRefGoogle ScholarPubMed
Spooncer, E., Fukuda, M., Klock, J. C., Gates, J. E. & Dell, A. (1984). Isolation and characterization of polyfucosylated lactosaminoglycan from human granulocytes. Journal of Biological Chemistry 259, 4792–801.CrossRefGoogle ScholarPubMed
Towbin, H., Staehelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences, USA 76, 4350–4.CrossRefGoogle ScholarPubMed
Van Dam, C. 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
Van Lieshout, L., Polderman, A. M., De Vlas, S. J., De Caluwé, P., Krijger, F. W., Gryseels, B. & Deelder, A. M. (1995). Analysis of worm burden variation in human Schistosoma mansoni infections by determination of serum levels of Circulating Anodic Antigen and Circulating Cathodic Antigen. Journal of Infectious Diseases (in the Press).CrossRefGoogle ScholarPubMed