Skip to main content Accessibility help

Parasite glycans and antibody-mediated immune responses in Schistosoma infection



Schistosome infections in humans are characterized by the development of chronic disease and high re-infection rates after treatment due to the slow development of immunity. It appears that anti-schistosome antibodies are at least partially mediating protective mechanisms. Efforts to develop a vaccine based on immunization with surface-exposed or secreted larval or worm proteins are ongoing. Schistosomes also express a large number of glycans as part of their glycoprotein and glycolipid repertoire, and antibody responses to those glycans are mounted by the infected host. This observation raises the question if glycans might also form novel vaccine targets for immune intervention in schistosomiasis. This review summarizes current knowledge of antibody responses and immunity in experimental and natural infections with Schistosoma, the expression profiles of schistosome glycans (the glycome), and antibody responses to individual antigenic glycan motifs. Future directions to study anti-glycan responses in schistosomiasis in more detail in order to address more precisely the possible role of glycans in antibody-mediated immunity are discussed.


Corresponding author

*Correspondence to: Dr Angela van Diepen, Department of Parasitology, Center of Infectious Diseases, Leiden University Medical Center, PO Box 9600, 2300 RC Leiden, The Netherlands. Tel.: +31-71-5265064 (office) Tel.: +31-71-5265062 (secr.). Fax: +31-71-5266907. E-mail:


Hide All
Al-Sherbiny, M., Osman, A., Barakat, R., El, M. H., Bergquist, R. and Olds, R. (2003). In vitro cellular and humoral responses to Schistosoma mansoni vaccine candidate antigens. Acta Tropica 88, 117130.
Amiri, P., Haak-Frendscho, M., Robbins, K., McKerrow, J. H., Stewart, T. and Jardieu, P. (1994). Anti-immunoglobulin E treatment decreases worm burden and egg production in Schistosoma mansoni-infected normal and interferon gamma knockout mice. Journal of Experimental Medicine 180, 4351.
Anderson, S., Coulson, P. S., Ljubojevic, S., Mountford, A. P. and Wilson, R. A. (1999). The radiation-attenuated schistosome vaccine induces high levels of protective immunity in the absence of B cells. Immunology 96, 2228.
Astronomo, R. D. and Burton, D. R. (2010). Carbohydrate vaccines: developing sweet solutions to sticky situations? Nature Reviews Drug Discovery 9, 308324.
Bergwerff, A. A., Thomas-Oates, J. E., Van Oostrum, J., Kamerling, J. P. and Vliegenthart, J. F. (1992). Human urokinase contains GalNAc beta (1-4)[Fuc alpha (1-3)]GlcNAc beta (1-2) as a novel terminal element in N-linked carbohydrate chains. FEBS Letters 314, 389394.
Bergwerff, A. A., van Dam, G. J., Rotmans, J. P., Deelder, A. M., Kamerling, J. P. and Vliegenthart, J. F. (1994). The immunologically reactive part of immunopurified circulating anodic antigen from Schistosoma mansoni is a threonine-linked polysaccharide consisting of –> 6)-(beta-D-GlcpA-(1 –> 3))-beta-D-GalpNAc-(1 –> repeating units. Journal of Biological Chemistry 269, 3151031517.
Bergwerff, A. A., van Oostrum, J., Kamerling, J. P. and Vliegenthart, J. F. (1995). The major N-linked carbohydrate chains from human urokinase. The occurrence of 4-O-sulfated, (alpha 2-6)-sialylated or (alpha 1-3)-fucosylated N-acetylgalactosamine(beta 1-4)-N-acetylglucosamine elements. European Journal of Biochemistry 228, 10091019.
Bickle, Q. D. (2009). Radiation-attenuated schistosome vaccination–a brief historical perspective. Parasitology 136, 16211632.
Bickle, Q. D., Andrews, B. J., Doenhoff, M. J., Ford, M. J. and Taylor, M. G. (1985). Resistance against Schistosoma mansoni induced by highly irradiated infections: studies on species specificity of immunization and attempts to transfer resistance. Parasitology 90, 301312.
Black, C. L., Muok, E. M., Mwinzi, P. N., Carter, J. M., Karanja, D. M., Secor, W. E. and Colley, D. G. (2010). Increases in levels of schistosome-specific immunoglobulin E and CD23(+) B cells in a cohort of Kenyan children undergoing repeated treatment and reinfection with Schistosoma mansoni. Journal of Infectious Diseases 202, 399405.
Blixt, O., Head, S., Mondala, T., Scanlan, C., Huflejt, M. E., Alvarez, R., Bryan, M. C., Fazio, F., Calarese, D., Stevens, J. et al. (2004). Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proceedings of the National Academy of Sciences, USA 101, 1703317038.
Bochner, B. S., Alvarez, R. A., Mehta, P., Bovin, N. V., Blixt, O., White, J. R. and Schnaar, R. L. (2005). Glycan array screening reveals a candidate ligand for Siglec-8. Journal of Biological Chemistry 280, 43074312.
Butterworth, A., Dunne, D., Fulford, A., Capron, M., Khalife, J., Capron, A., Koech, D., Ouma, J. and Sturrock, R. (1988 a). Immunity in human schistosomiasis mansoni: cross-reactive IgM and IgG2 anti-carbohydrate antibodies block the expression of immunity. Biochimie 70, 10531063.
Butterworth, A. E., Fulford, A. J., Dunne, D. W., Ouma, J. H. and Sturrock, R. F. (1988 b). Longitudinal studies on human schistosomiasis. Philosophical Transactions of the Royal Society B Biological Sciences 321, 495511.
Butterworth, A. E., Remold, H. G., Houba, V., David, J. R., Franks, D., David, P. H. and Sturrock, R. F. (1977). Antibody-dependent eosinophil-mediated damage to 51Cr-labeled schistosomula of Schistosoma mansoni: mediation by IgG, and inhibition by antigen-antibody complexes. Journal of Immunology 118, 22302236.
Butterworth, A. E., Sturrock, R. F., Houba, V., Mahmoud, A. A., Sher, A. and Rees, P. H. (1975). Eosinophils as mediators of antibody-dependent damage to schistosomula. Nature 256, 727729.
Caldas, I. R., Campi-Azevedo, A. C., Oliveira, L. F., Silveira, A. M., Oliveira, R. C. and Gazzinelli, G. (2008). Human schistosomiasis mansoni: immune responses during acute and chronic phases of the infection. Acta Tropica 108, 109117.
Capron, M., Rousseaux, J., Mazingue, C., Bazin, H. and Capron, A. (1978). Rat mast cell-eosinophil interaction in antibody-dependent eosinophil cytotoxicity to Schistosoma mansoni schistosomula. Journal of Immunology 121, 25182525.
Correa-Oliveira, R., Caldas, I. R. and Gazzinelli, G. (2000). Natural versus drug-induced resistance in Schistosoma mansoni infection. Parasitology Today 16, 397399.
De Andres, B., Rakasz, E., Hagen, M., McCormik, M. L., Mueller, A. L., Elliot, D., Metwali, A., Sandor, M., Britigan, B. E., Weinstock, J. V. and Lynch, R. G. (1997). Lack of Fc-epsilon receptors on murine eosinophils: implications for the functional significance of elevated IgE and eosinophils in parasitic infections. Blood 89, 38263836.
De Boer, A. R., Hokke, C. H., Deelder, A. M. and Wuhrer, M. (2007). General microarray technique for immobilization and screening of natural glycans. Analytical Chemistry 79, 81078113.
De Boer, A. R., Hokke, C. H., Deelder, A. M. and Wuhrer, M. (2008). Serum antibody screening by surface plasmon resonance using a natural glycan microarray. Glycoconjugate Journal 25, 7584.
De Oliveira Fraga, L. A., Lamb, E. W., Moreno, E. C., Chatterjee, M., Dvorak, J., Delcroix, M., Sajid, M., Caffrey, C. R. and Davies, S. J. (2010). Rapid induction of IgE responses to a worm cysteine protease during murine pre-patent schistosome infection. BMC Immunology 11, 56.
Deelder, A. M., van Dam, G. J., Kornelis, D., Fillie, Y. E. and van Zeyl, R. J. (1996). Schistosoma: analysis of monoclonal antibodies reactive with the circulating antigens CAA and CCA. Parasitology 112, 2135.
Dell, A., Morris, H. R., Easton, R. L., Panico, M., Patankar, M., Oehniger, S., Koistinen, R., Koistinen, H., Seppala, M. and Clark, G. F. (1995). Structural analysis of the oligosaccharides derived from glycodelin, a human glycoprotein with potent immunosuppressive and contraceptive activities. Journal of Biological Chemistry 270, 2411624126.
Dewalick, S., Bexkens, M. L., van Balkom, B. W., Wu, Y. P., Smit, C. H., Hokke, C. H., de Groot, P. G., Heck, A. J., Tielens, A. G. and van Hellemond, J. J. (2011). The proteome of the insoluble Schistosoma mansoni eggshell skeleton. International Journal for Parasitology 41, 523532.
Dunne, D. W., Butterworth, A. E., Fulford, A. J., Kariuki, H. C., Langley, J. G., Ouma, J. H., Capron, A., Pierce, R. J. and 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, 14831494.
Dunne, D. W., Richardson, B. A., Jones, F. M., Clark, M., Thorne, K. J. and Butterworth, A. E. (1993). The use of mouse/human chimaeric antibodies to investigate the roles of different antibody isotypes, including IgA2, in the killing of Schistosoma mansoni schistosomula by eosinophils. Parasite Immunology 15, 181185.
Dunne, D. W., Webster, M., Smith, P., Langley, J. G., Richardson, B. A., Fulford, A. J., Butterworth, A. E., Sturrock, R. F., Kariuki, H. C. and Ouma, J. H. (1997). The isolation of a 22 kDa band after SDS-PAGE of Schistosoma mansoni adult worms and its use to demonstrate that IgE responses against the antigen(s) it contains are associated with human resistance to reinfection. Parasite Immunology 19, 7989.
Eberl, M., Langermans, J. A., Vervenne, R. A., Nyame, A. K., Cummings, R. D., Thomas, A. W., Coulson, P. S. and Wilson, R. A. (2001). Antibodies to glycans dominate the host response to schistosome larvae and eggs: is their role protective or subversive? Journal of Infectious Diseases 183, 12381247.
El, R. R., Ozaki, T. and Kamiya, H. (1998). Schistosoma mansoni infection in IgE-producing and IgE-deficient mice. Journal of Parasitology 84, 171174.
Farias, L. P., Cardoso, F. C., Miyasato, P. A., Montoya, B. O., Tararam, C. A., Roffato, H. K., Kawano, T., Gazzinelli, A., Correa-Oliveira, R., Coulson, P. S., Wilson, R. A., Oliveira, S. C. and Leite, L. C. (2010). Schistosoma mansoni Stomatin like protein-2 is located in the tegument and induces partial protection against challenge infection. PLoS Neglected Tropical Diseases 4, e597.
Faveeuw, C., Mallevaey, T., Paschinger, K., Wilson, I. B., Fontaine, J., Mollicone, R., Oriol, R., Altmann, F., Lerouge, P., Capron, M. and Trottein, F. (2003). Schistosome N-glycans containing core alpha 3-fucose and core beta 2-xylose epitopes are strong inducers of Th2 responses in mice. European Journal of Immunology 33, 12711281.
Fenwick, A., and Webster, J. P. (2006). Schistosomiasis: challenges for control, treatment and drug resistance. Current Opinion in Infectious Diseases 19, 577582.
Fitzsimmons, C. M., McBeath, R., Joseph, S., Jones, F. M., Walter, K., Hoffmann, K. F., Kariuki, H. C., Mwatha, J. K., Kimani, G., Kabatereine, N. B., Vennervald, B. J., Ouma, J. H. and Dunne, D. W. (2007). Factors affecting human IgE and IgG responses to allergen-like Schistosoma mansoni antigens: Molecular structure and patterns of in vivo exposure. International Archives of Allergy and Immunology 142, 4050.
Ford, M. J., Bickle, Q. D., Taylor, M. G. and Andrews, B. J. (1984). Passive transfer of resistance and the site of immune-dependent elimination of the challenge infection in rats vaccinated with highly irradiated cercariae of Schistosoma mansoni. Parasitology 89, 461482.
Fox, N., Damjanov, I., Knowles, B. B. and Solter, D. (1983). Immunohistochemical localization of the mouse stage-specific embryonic antigen 1 in human tissues and tumors. Cancer Research 43, 669678.
Fukuda, M. N., Dell, A., Oates, J. E., Wu, P., Klock, J. C. and Fukuda, M. (1985). Structures of glycosphingolipids isolated from human granulocytes. The presence of a series of linear poly-N-acetyllactosaminylceramide and its significance in glycolipids of whole blood cells. Journal of Biological Chemistry 260, 10671082.
Fulford, A. J., Butterworth, A. E., Sturrock, R. F. and Ouma, J. H. (1992). On the use of age-intensity data to detect immunity to parasitic infections, with special reference to Schistosoma mansoni in Kenya. Parasitology, 105, 219227.
Gray, D. J., Ross, A. G., Li, Y. S. and McManus, D. P. (2011). Diagnosis and management of schistosomiasis. British Medical Journal, 342:d2651. doi: 10.1136/bmj.d2651., d2651.
Gryseels, B., Polman, K., Clerinx, J. and Kestens, L. (2006). Human schistosomiasis. The Lancet 368, 11061118.
Hagan, P., Blumenthal, U. J., Dunn, D., Simpson, A. J. and Wilkins, H. A. (1991). Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349, 243245.
Hakomori, S., Nudelman, E., Levery, S., Solter, D. and Knowles, B. B. (1981). The hapten structure of a developmentally regulated glycolipid antigen (SSEA-1) isolated from human erythrocytes and adenocarcinoma: a preliminary note. Biochemical and Biophysical Research Communications 100, 15781586.
Harn, D. A., McDonald, J., Atochina, O. and Da'dara, A. A. (2009). Modulation of host immune responses by helminth glycans. Immunological Reviews 230, 247257.
Harrison, R. A., Bickle, Q. D., Kiare, S., James, E. R., Andrews, B. J., Sturrock, R. F., Taylor, M. G. and Webbe, G. (1990). Immunization of baboons with attenuated schistosomula of Schistosoma haematobium: levels of protection induced by immunization with larvae irradiated with 20 and 60 krad. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 8999.
Hokke, C. H. and Deelder, A. M. (2001). Schistosome glycoconjugates in host-parasite interplay. Glycoconjugate Journal 18, 573587.
Hokke, C. H., Deelder, A. M., Hoffmann, K. F. and Wuhrer, M. (2007 a). Glycomics-driven discoveries in schistosome research. Experimental Parasitology, 117, 275283.
Hokke, C. H., Fitzpatrick, J. M. and Hoffmann, K. F. (2007 b). Integrating transcriptome, proteome and glycome analyses of Schistosoma biology. Trends in Parasitology 23, 165174.
Hokke, C. H. and Yazdanbakhsh, M. (2005). Schistosome glycans and innate immunity. Parasite Immunology 27, 257264.
Hotez, P. J., Bethony, J. M., Diemert, D. J., Pearson, M. and Loukas, A. (2010). Developing vaccines to combat hookworm infection and intestinal schistosomiasis. Nature Reviews Microbiology 8, 814826.
Huang, H. H., Tsai, P. L. and Khoo, K. H. (2001). Selective expression of different fucosylated epitopes on two distinct sets of Schistosoma mansoni cercarial O-glycans: identification of a novel core type and Lewis X structure. Glycobiology 11, 395406.
Jang-Lee, J., Curwen, R. S., Ashton, P. D., Tissot, B., Mathieson, W., Panico, M., Dell, A., Wilson, R. A. and Haslam, S. M. (2007). Glycomics analysis of Schistosoma mansoni egg and cercarial secretions. Molecular & Cellular Proteomics 6, 14851499.
Jankovic, D., Wynn, T. A., Kullberg, M. C., Hieny, S., Caspar, P., James, S., Cheever, A. W. and Sher, A. (1999). Optimal vaccination against Schistosoma mansoni requires the induction of both B cell- and IFN-gamma-dependent effector mechanisms. Journal of Immunology 162, 345351.
Jiz, M., Friedman, J. F., Leenstra, T., Jarilla, B., Pablo, A., Langdon, G., Pond-Tor, S., Wu, H. W., Manalo, D., Olveda, R., Acosta, L. and Kurtis, J. D. (2009). Immunoglobulin E (IgE) responses to paramyosin predict resistance to reinfection with Schistosoma japonicum and are attenuated by IgG4. Infection & Immunity 77, 20512058.
Kabatereine, N. B., Vennervald, B. J., Ouma, J. H., Kemijumbi, J., Butterworth, A. E., Dunne, D. W. and Fulford, A. J. (1999). Adult resistance to schistosomiasis mansoni: age-dependence of reinfection remains constant in communities with diverse exposure patterns. Parasitology 118, 101105.
Kantelhardt, S. R., Wuhrer, M., Dennis, R. D., Doenhoff, M. J., Bickle, Q. and Geyer, R. (2002). Fuc(alpha1–>3)GalNAc-: the major antigenic motif of Schistosoma mansoni glycolipids implicated in infection sera and keyhole-limpet haemocyanin cross-reactivity. Biochemical Journal 366, 217223.
Kariuki, T. M., Farah, I. O., Wilson, R. A. and Coulson, P. S. (2008). Antibodies elicited by the secretions from schistosome cercariae and eggs are predominantly against glycan epitopes. Parasite Immunology 30, 554562.
Khalife, J., Dunne, D. W., Richardson, B. A., Mazza, G., Thorne, K. J., Capron, A. and Butterworth, A. E. (1989). Functional role of human IgG subclasses in eosinophil-mediated killing of schistosomula of Schistosoma mansoni. Journal of Immunology 142, 44224427.
Khoo, K. H., Chatterjee, D., Caulfield, J. P., Morris, H. R. and Dell, A. (1997). Structural mapping of the glycans from the egg glycoproteins of Schistosoma mansoni and Schistosoma japonicum: identification of novel core structures and terminal sequences. Glycobiology 7, 663677.
Khoo, K. H., Huang, H. H. and Lee, K. M. (2001). Characteristic structural features of schistosome cercarial N-glycans: expression of Lewis X and core xylosylation. Glycobiology 11, 149163.
Khoo, K. H., Sarda, S., Xu, X., Caulfield, J. P., McNeil, M. R., Homans, S. W., Morris, H. R. and Dell, A. (1995). A unique multifucosylated -3GalNAc beta 1–>4GlcNAc beta 1–>3Gal alpha 1- motif constitutes the repeating unit of the complex O-glycans derived from the cercarial glycocalyx of Schistosoma mansoni. Journal of Biological Chemistry 270, 1711417123.
King, C. L., Xianli, J., Malhotra, I., Liu, S., Mahmoud, A. A. and Oettgen, H. C. (1997). Mice with a targeted deletion of the IgE gene have increased worm burdens and reduced granulomatous inflammation following primary infection with Schistosoma mansoni. Journal of Immunology 158, 294300.
Koster, B. and Strand, M. (1994). Schistosoma mansoni: immunolocalization of two different fucose-containing carbohydrate epitopes. Parasitology 108, 433446.
Leenstra, T., Acosta, L. P., Wu, H. W., Langdon, G. C., Solomon, J. S., Manalo, D. L., Su, L., Jiz, M., Jarilla, B., Pablo, A. O., McGarvey, S. T., Olveda, R. M., Friedman, J. F. and Kurtis, J. D. (2006). T-helper-2 cytokine responses to Sj97 predict resistance to reinfection with Schistosoma japonicum. Infection & Immunity 74, 370381.
Li, Y., Sleigh, A. C., Ross, A. G., Li, Y., Zhang, X., Williams, G. M., Yu, X., Tanner, M. and McManus, D. P. (2001). Human susceptibility to Schistosoma japonicum in China correlates with antibody isotypes to native antigens. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 441448.
Lonardi, E., Balog, C. I., Deelder, A. M. and Wuhrer, M. (2010). Natural glycan microarrays. Expert Reviews of Proteomics 7, 761774.
Mangold, B. L. and Dean, D. A. (1986). Passive transfer with serum and IgG antibodies of irradiated cercaria-induced resistance against Schistosoma mansoni in mice. Journal of Immunology 136, 26442648.
McManus, D. P. and Loukas, A. (2008). Current status of vaccines for schistosomiasis. Clinical Microbiology Reviews 21, 225242.
Meevissen, M. H., Balog, C. I., Koeleman, C. A., Doenhoff, M. J., Schramm, G., Haas, H., Deelder, A. M., Wuhrer, M. and Hokke, C. H. (2011 a). Targeted glycoproteomic analysis reveals that kappa-5 is a major, uniquely glycosylated component of Schistosoma mansoni egg antigens. Molecular & Cellular Proteomics 10, M110.
Meevissen, M. H., Wuhrer, M., Doenhoff, M. J., Schramm, G., Haas, H., Deelder, A. M. and Hokke, C. H. (2010). Structural characterization of glycans on omega-1, a major Schistosoma mansoni egg glycoprotein that drives Th2 responses. Journal of Proteome Research 9, 26302642.
Meevissen, M. H., Yazdanbakhsh, M. and Hokke, C. H. (2011 b). Schistosoma mansoni egg glycoproteins and C-type lectins of host immune cells: Molecular partners that shape immune responses. Experimental Parasitology. doi:
Muller-Graf, C. D., Collins, D. A., Packer, C. and Woolhouse, M. E. (1997). Schistosoma mansoni infection in a natural population of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 115, 621627.
Mutapi, F., Hagan, P., Woolhouse, M. E., Mduluza, T. and Ndhlovu, P. D. (2003). Chemotherapy-induced, age-related changes in antischistosome antibody responses. Parasite Immunology 25, 8797.
Mutapi, F., Ndhlovu, P. D., Hagan, P., Spicer, J. T., Mduluza, T., Turner, C. M., Chandiwana, S. K. and Woolhouse, M. E. (1998). Chemotherapy accelerates the development of acquired immune responses to Schistosoma haematobium infection. Journal of Infectious Diseases 178, 289293.
Mutapi, F., Ndhlovu, P. D., Hagan, P. and Woolhouse, M. E. (1997). A comparison of humoral responses to Schistosoma haematobium in areas with low and high levels of infection. Parasite Immunology 19, 255263.
Mutapi, F., Winborn, G., Midzi, N., Taylor, M., Mduluza, T. and Maizels, R. M. (2007). Cytokine responses to Schistosoma haematobium in a Zimbabwean population: contrasting profiles for IFN-gamma, IL-4, IL-5 and IL-10 with age. BMC Infectious Diseases 7, 139.
Naus, C. W., van Dam, G. J., Kremsner, P. G., Krijger, F. W. and Deelder, A. M. (1998). Human IgE, IgG subclass, and IgM responses to worm and egg antigens in schistosomiasis haematobium: a 12-month study of reinfection in Cameroonian children. Clinical Infectious Diseases 26, 11421147.
Naus, C. W., van Remoortere, A., Ouma, J. H., Kimani, G., Dunne, D. W., Kamerling, J. P., Deelder, A. M. and Hokke, C. H. (2003). Specific antibody responses to three schistosome-related carbohydrate structures in recently exposed immigrants and established residents in an area of Schistosoma mansoni endemicity. Infection & Immunity 71, 56765681.
Nyame, A. K., Kawar, Z. S. and Cummings, R. D. (2004). Antigenic glycans in parasitic infections: implications for vaccines and diagnostics. Archives of Biochemistry and Biophysics 426, 182200.
Nyame, A. K., Leppanen, A. M., Bogitsh, B. J. and Cummings, R. D. (2000). Antibody responses to the fucosylated LacdiNAc glycan antigen in Schistosoma mansoni-infected mice and expression of the glycan among schistosomes. Experimental Parasitology 96, 202212.
Nyame, A. K., Leppanen, A. M., DeBose-Boyd, R. and Cummings, R. D. (1999). Mice infected with Schistosoma mansoni generate antibodies to LacdiNAc (GalNAc beta 1–>4GlcNAc) determinants. Glycobiology 9, 10291035.
Nyame, A. K., Lewis, F. A., Doughty, B. L., Correa-Oliveira, R. and Cummings, R. D. (2003). Immunity to schistosomiasis: glycans are potential antigenic targets for immune intervention. Experimental Parasitology 104, 113.
Nyame, A. K., Pilcher, J. B., Tsang, V. C. and Cummings, R. D. (1997). Rodents infected with Schistosoma mansoni produce cytolytic IgG and IgM antibodies to the Lewis x antigen. Glycobiology 7, 207215.
Nyame, A. K., Pilcher, J. B., Tsang, V. C. and Cummings, R. D. (1996). Schistosoma mansoni infection in humans and primates induces cytolytic antibodies to surface Le(x) determinants on myeloid cells. Experimental Parasitology 82, 191200.
Okano, M., Satoskar, A. R., Nishizaki, K. and Harn, D. A. Jr. (2001). Lacto-N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response. Journal of Immunology, 167, 442450.
Ouma, J. H., Fulford, A. J., Kariuki, H. C., Kimani, G., Sturrock, R. F., Muchemi, G., Butterworth, A. E. and Dunne, D. W. (1998). The development of schistosomiasis mansoni in an immunologically naive immigrant population in Masongaleni, Kenya. Parasitology 117, 123132.
Oyelaran, O. and Gildersleeve, J. C. (2007). Application of carbohydrate array technology to antigen discovery and vaccine development. Expert Review of Vaccines 6, 957969.
Oyelaran, O., McShane, L. M., Dodd, L. and Gildersleeve, J. C. (2009). Profiling human serum antibodies with a carbohydrate antigen microarray. Journal of Proteome Research 8, 43014310.
Pinot de Moira, A., Fulford, A. J., Kabatereine, N. B., Ouma, J. H., Booth, M. and Dunne, D. W. (2010). Analysis of complex patterns of human exposure and immunity to Schistosomiasis mansoni: the influence of age, sex, ethnicity and IgE. PLoS Neglected Tropical Diseases 4, e820.
Ribeiro de, J. A., Araujo, I., Bacellar, O., Magalhaes, A., Pearce, E., Harn, D., Strand, M. and Carvalho, E. M. (2000). Human immune responses to Schistosoma mansoni vaccine candidate antigens. Infection & Immunity 68, 27972803.
Richter, D., Incani, R. N. and Harn, D. A. (1996). Lacto-N-fucopentaose III (Lewis x), a target of the antibody response in mice vaccinated with irradiated cercariae of Schistosoma mansoni. Infection & Immunity 64, 18261831.
Robijn, M. L., Koeleman, C. A., Wuhrer, M., Royle, L., Geyer, R., Dwek, R. A., Rudd, P. M., Deelder, A. M. and Hokke, C. H. (2007). Targeted identification of a unique glycan epitope of Schistosoma mansoni egg antigens using a diagnostic antibody. Molecular and Biochemical Parasitology 151, 148161.
Robijn, M. L., Wuhrer, M., Kornelis, D., Deelder, A. M., Geyer, R. and Hokke, C. H. (2005). Mapping fucosylated epitopes on glycoproteins and glycolipids of Schistosoma mansoni cercariae, adult worms and eggs. Parasitology 130, 6777.
Satti, M. Z., Lind, P., Vennervald, B. J., Sulaiman, S. M., Daffalla, A. A. and Ghalib, H. W. (1996). Specific immunoglobulin measurements related to exposure and resistance to Schistosoma mansoni infection in Sudanese canal cleaners. Clinical & Experimental Immunology 106, 4554.
Shalaby, K. A., Yin, L., Thakur, A., Christen, L., Niles, E. G. and LoVerde, P. T. (2003). Protection against Schistosoma mansoni utilizing DNA vaccination with genes encoding Cu/Zn cytosolic superoxide dismutase, signal peptide-containing superoxide dismutase and glutathione peroxidase enzymes. Vaccine 22, 130136.
Siddiqui, A. A., Phillips, T., Charest, H., Podesta, R. B., Quinlin, M. L., Pinkston, J. R., Lloyd, J. D., Pompa, J., Villalovos, R. M. and Paz, M. (2003). Enhancement of Sm-p80 (large subunit of calpain) induced protective immunity against Schistosoma mansoni through co-delivery of interleukin-2 and interleukin-12 in a DNA vaccine formulation. Vaccine 21, 28822889.
Singh, S. K., Stephani, J., Schaefer, M., Kalay, H., Garcia-Vallejo, J. J., den Haan, J., Saeland, E., Sparwasser, T. and van Kooyk, Y. (2009). Targeting glycan modified OVA to murine DC-SIGN transgenic dendritic cells enhances MHC class I and II presentation. Molecular Immunology 47, 164174.
Singh, S. K., Streng-Ouwehand, I., Litjens, M., Kalay, H., Burgdorf, S., Saeland, E., Kurts, C., Unger, W. W. and van Kooyk, Y. (2011). Design of neo-glycoconjugates that target the mannose receptor and enhance TLR-independent cross-presentation and Th1 polarization. European Journal of Immunology 41, 916925.
Smith, D. F., Song, X. and Cummings, R. D. (2010). Use of glycan microarrays to explore specificity of glycan-binding proteins. Methods in Enzymology 480, 417444.
Song, X., Lasanajak, Y., Xia, B., Heimburg-Molinaro, J., Rhea, J. M., Ju, H., Zhao, C., Molinaro, R. J., Cummings, R. D. and Smith, D. F. (2011). Shotgun glycomics: a microarray strategy for functional glycomics. Nature Methods 8, 8590.
Spooncer, E., Fukuda, M., Klock, J. C., Oates, J. E. and Dell, A. (1984). Isolation and characterization of polyfucosylated lactosaminoglycan from human granulocytes. Journal of Biological Chemistry 259, 47924801.
Steinmann, P., Keiser, J., Bos, R., Tanner, M. and Utzinger, J. (2006). Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. The Lancet Infectious Diseases 6, 411425.
Tran, M. H., Pearson, M. S., Bethony, J. M., Smyth, D. J., Jones, M. K., Duke, M., Don, T. A., McManus, D. P., Correa-Oliveira, R. and Loukas, A. (2006). Tetraspanins on the surface of Schistosoma mansoni are protective antigens against schistosomiasis. Nature Medicine 12, 835840.
Utzinger, J., N'goran, E. K., Caffrey, C. R. and Keiser, J. (2010). From innovation to application: Social-ecological context, diagnostics, drugs and integrated control of schistosomiasis. Acta Tropica 120 (Suppl. 1), S121S137.
Van Dam, G. J., Bergwerff, A. A., Thomas-Oates, J. E., Rotmans, J. P., Kamerling, J. P., Vliegenthart, J. F. and 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, 467482.
Van den Biggelaar, A. H., Borrmann, S., Kremsner, P. and Yazdanbakhsh, M. (2002). Immune responses induced by repeated treatment do not result in protective immunity to Schistosoma haematobium: interleukin (IL)-5 and IL-10 responses. Journal of Infectious Diseases 186, 14741482.
Van den Eijnden, D. H., Neeleman, A. P., van der Knaap, W. P., Bakker, H., Agterberg, M. and van Die, I. (1995). Novel glycosylation routes for glycoproteins: the lacdiNAc pathway. Biochemical Society Transactions 23, 175179.
Van der Kleij, D., van Remoortere, A., Schuitemaker, J. H., Kapsenberg, M. L., Deelder, A. M., Tielens, A. G., Hokke, C. H. and Yazdanbakhsh, M. (2002). Triggering of innate immune responses by schistosome egg glycolipids and their carbohydrate epitope GalNAc beta 1-4(Fuc alpha 1-2Fuc alpha 1–3)GlcNAc. Journal of Infectious Diseases 185, 531539.
Van der Kleij, D., Tielens, A. G. and Yazdanbakhsh, M. (1999). Recognition of schistosome glycolipids by immunoglobulin E: possible role in immunity. Infection & Immunity 67, 59465950.
Van Die, I. and Cummings, R. D. (2010). Glycan gimmickry by parasitic helminths: a strategy for modulating the host immune response? Glycobiology 20, 212.
Van Die, I., Gomord, V., Kooyman, F. N., van den Berg, T. K., Cummings, R. D. and Vervelde, L. (1999). Core alpha1–>3-fucose is a common modification of N-glycans in parasitic helminths and constitutes an important epitope for IgE from Haemonchus contortus infected sheep. FEBS Letters, 463, 189193.
Van, Die, I., van Stijn, C. M., Geyer, H. and Geyer, R. (2010). Structural and functional analysis of glycosphingolipids of Schistosoma mansoni. Methods in Enzymology 480, 117140.
Van Kuik, J. A., de Waard, P., Vliegenthart, J. F., Klein, A., Carnoy, C., Lamblin, G. and Roussel, P. (1991). Isolation and structural characterization of novel neutral oligosaccharide-alditols from respiratory-mucus glycoproteins of a patient suffering from bronchiectasis. 2. Structure of twelve hepta-to-nonasaccharides, six of which possess the GlcNAc beta(1––3)[Gal beta(1––4)GlcNAc beta(1––6)]Gal beta(1––3)GalNAc-ol common structural element. European Journal of Biochemistry 198, 169182.
Van Montfort, T., Eggink, D., Boot, M., Tuen, M., Hioe, C. E., Berkhout, B. and Sanders, R. W. (2011). HIV-1 N-glycan composition governs a balance between dendritic cell-mediated viral transmission and antigen presentation. Journal of Immunology 187, 46764685.
Van Remoortere, A., Bank, C. M., Nyame, A. K., Cummings, R. D., Deelder, A. M. and van Die, I. (2003 a). Schistosoma mansoni-infected mice produce antibodies that cross-react with plant, insect, and mammalian glycoproteins and recognize the truncated biantennaryN-glycan Man3GlcNAc2-R. Glycobiology 13, 217225.
Van Remoortere, A., Hokke, C. H., van Dam, G. J., van Die, I., Deelder, A. M. and van den Eijnden, D. H. (2000). Various stages of schistosoma express Lewis(x), LacdiNAc, GalNAcbeta1-4 (Fucalpha1-3)GlcNAc and GalNAcbeta1-4(Fucalpha1-2Fucalpha1-3)GlcNAc carbohydrate epitopes: detection with monoclonal antibodies that are characterized by enzymatically synthesized neoglycoproteins. Glycobiology 10, 601609.
Van Remoortere, A., van Dam, G. J., Hokke, C. H., van den Eijnden, D. H., van Die, I. and Deelder, A. M. (2001). Profiles of immunoglobulin M (IgM) and IgG antibodies against defined carbohydrate epitopes in sera of Schistosoma-infected individuals determined by surface plasmon resonance. Infection & Immunity 69, 23962401.
Van Remoortere, A., Vermeer, H. J., van Roon, A. M., Langermans, J. A., Thomas, A. W., Wilson, R. A., van Die, I., van den Eijnden, D. H., Agoston, K., Kerekgyarto, J., Vliegenthart, J. F., Kamerling, J. P., van Dam, G. J., Hokke, C. H. and Deelder, A. M. (2003 b). Dominant antibody responses to Fucalpha1-3GalNAc and Fucalpha1-2Fucalpha1-3GlcNAc containing carbohydrate epitopes in Pan troglodytes vaccinated and infected with Schistosoma mansoni. Experimental Parasitology 105, 219225.
Van Roon, A. M., van de Vijver, K. K., Jacobs, W., van Marck, E. A., van Dam, G. J., Hokke, C. H. and Deelder, A. M. (2004). Discrimination between the anti-monomeric and the anti-multimeric Lewis X response in murine schistosomiasis. Microbes and Infection 6, 11251132.
Van Stijn, C. M., Meyer, S., van den Broek, M., Bruijns, S. C., van Kooyk, Y., Geyer, R. and van Die, I. (2010). Schistosoma mansoni worm glycolipids induce an inflammatory phenotype in human dendritic cells by cooperation of TLR4 and DC-SIGN. Molecular Immunology 47, 15441552.
Velupillai, P., dos Reis, E. A., dos Reis, M. G. and Harn, D. A. (2000). Lewis(x)-containing oligosaccharide attenuates schistosome egg antigen-induced immune depression in human schistosomiasis. Human Immunology 61, 225232.
Vereecken, K., Naus, C. W., Polman, K., Scott, J. T., Diop, M., Gryseels, B. and Kestens, L. (2007). Associations between specific antibody responses and resistance to reinfection in a Senegalese population recently exposed to Schistosoma mansoni. Tropical Medicine & International Health 12, 431444.
Viana, I. R., Correa-Oliveira, R., Carvalho, O. S., Massara, C. L., Colosimo, E., Colley, D. G. and Gazzinelli, G. (1995). Comparison of antibody isotype responses to Schistosoma mansoni antigens by infected and putative resistant individuals living in an endemic area. Parasite Immunology 17, 297304.
Wachholz, P. A. and Durham, S. R. (2004). Mechanisms of immunotherapy: IgG revisited. Current Opinion in Allergy and Clinical Immunology 4, 313318.
Walter, K., Fulford, A. J., McBeath, R., Joseph, S., Jones, F. M., Kariuki, H. C., Mwatha, J. K., Kimani, G., Kabatereine, N. B., Vennervald, B. J., Ouma, J. H. and Dunne, D. W. (2006). Increased human IgE induced by killing Schistosoma mansoni in vivo is associated with pretreatment Th2 cytokine responsiveness to worm antigens. Journal of Immunology 177, 54905498.
Webster, M., Fallon, P. G., Fulford, A. J., Butterworth, A. E., Ouma, J. H., Kimani, G. and Dunne, D. W. (1997 a). Effect of praziquantel and oxamniquine treatment on human isotype responses to Schistosoma mansoni: elevated IgE to adult worm. Parasite Immunology 19, 333335.
Webster, M., Fallon, P. G., Fulford, A. J., Butterworth, A. E., Ouma, J. H., Kimani, G. and Dunne, D. W. (1997 b). IgG4 and IgE responses to Schistosoma mansoni adult worms after treatment. Journal of Infectious Diseases 175, 493494.
Webster, M., Fulford, A. J., Braun, G., Ouma, J. H., Kariuki, H. C., Havercroft, J. C., Gachuhi, K., Sturrock, R. F., Butterworth, A. E. and Dunne, D. W. (1996). Human immunoglobulin E responses to a recombinant 22·6-kilodalton antigen from Schistosoma mansoni adult worms are associated with low intensities of reinfection after treatment. Infection & Immunity 64, 40424046.
Wilkins, H. A., Blumenthal, U. J., Hagan, P., Hayes, R. J. and Tulloch, S. (1987). Resistance to reinfection after treatment of urinary schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 2935.
Woolhouse, M. E. (1998). Patterns in parasite epidemiology: the peak shift. Parasitology Today 14, 428434.
Woolhouse, M. E., Taylor, P., Matanhire, D. and Chandiwana, S. K. (1991). Acquired immunity and epidemiology of Schistosoma haematobium. Nature 351, 757759.
Wuhrer, M., Balog, C. I., Catalina, M. I., Jones, F. M., Schramm, G., Haas, H., Doenhoff, M. J., Dunne, D. W., Deelder, A. M. and Hokke, C. H. (2006 a). IPSE/alpha-1, a major secretory glycoprotein antigen from schistosome eggs, expresses the Lewis X motif on core-difucosylated N-glycans. FEBS Journal 273, 22762292.
Wuhrer, M., Dennis, R. D., Doenhoff, M. J., Lochnit, G. and Geyer, R. (2000). Schistosoma mansoni cercarial glycolipids are dominated by Lewis X and pseudo-Lewis Y structures. Glycobiology 10, 89101.
Wuhrer, M., Kantelhardt, S. R., Dennis, R. D., Doenhoff, M. J., Lochnit, G. and Geyer, R. (2002). Characterization of glycosphingolipids from Schistosoma mansoni eggs carrying Fuc(alpha1-3)GalNAc-, GalNAc(beta1-4)[Fuc(alpha1-3)]GlcNAc- and Gal(beta1-4)[Fuc(alpha1-3)]GlcNAc- (Lewis X) terminal structures. European Journal of Biochemistry 269, 481493.
Wuhrer, M., Koeleman, C. A., Deelder, A. M. and Hokke, C. H. (2006 b). Repeats of LacdiNAc and fucosylated LacdiNAc on N-glycans of the human parasite Schistosoma mansoni. FEBS Journal 273, 347361.
Wuhrer, M., Koeleman, C. A., Fitzpatrick, J. M., Hoffmann, K. F., Deelder, A. M. and Hokke, C. H. (2006 c). Gender-specific expression of complex-type N-glycans in schistosomes. Glycobiology 16, 9911006.
Yan, S. B., Chao, Y. B. and van Halbeek, H. (1993). Novel Asn-linked oligosaccharides terminating in GalNAc beta (1–>4)[Fuc alpha (1–>3)]GlcNAc beta (1–>.) are present in recombinant human protein C expressed in human kidney 293 cells. Glycobiology 3, 597608.
Yole, D. S., Reid, G. D. and Wilson, R. A. (1996). Protection against Schistosoma mansoni and associated immune responses induced in the vervet monkey Cercopithecus aethiops by the irradiated cercaria vaccine. American Journal of Tropical Medicine and Hygiene 54, 265270.
Zhang, Z., Wu, H., Chen, S., Hu, L., Xie, Z., Qiu, Y., Su, C., Cao, J. P., Wu, Y., Zhang, S. and Wu, G. (1997). Association between IgE antibody against soluble egg antigen and resistance to reinfection with Schistosoma japonicum. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 606608.


Parasite glycans and antibody-mediated immune responses in Schistosoma infection



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed