Abstract
We have provided an account of the progress we and others have made over the last decade on the structural characterization of glycans from parasitic helminths. We hope to have illustrated a few principles and patterns governing helminth glycosylation, as well as the experimental approaches adopted and their associated strengths and limitations. Schistosomes remain the best studied systems but are still punctuated with gaps of knowledge. An important theme developed here is the regulated developmental stagespecific expression of various glycan epitopes and their interplay with immediate host environments for successful parasitism. It is anticipated that more novel or unusual structures will continuously be uncovered in the future and that despite many difficulties, current analytical techniques should be well up to meet the challenge in at least elucidating the major or key glycoconjugates from each of the diverse range of worms. The bottle neck will in fact reside in finding suitable experimental models to test their putative immunobiological functions from which the intricate host-parasite interactions can be delineated and rational vaccine design be achieved. The glycobiology of parasitic helminths is an area waiting to be more fully explored and the rewards should be sweet.
Article FootNote
The abbreviations used are: CAA, circulating anodic antigen; CCA, circulating cathodic antigen; Cer, ceramide; Con A, con-canavalin A; ES, excretory-secretory; GSL, glycosphingolipids; HexNAc, GlcNAc or GalNAc; lacNAc, N-acetyl-Iactosamine; lacdiNAc, N,N’-diacetyl-Iactosediamin; LexLewis X; mAb, monoclonal antibody.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Altmann, F., Staudacher, E., Wilson, I.B. and Marz, L., 1999, Insect cells as hosts for the expression of recombinant glycoproteinsGlycoconj J16: 109–123.
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 fromSchistosoma mansoniis a threonine-linked polysaccharide consisting of→6)-(ß-D-GlcpA-(1→3))-ß-D-GalpNAc(1→repeating unitsJBiol Chem269: 31510–31517.
Blaxter, M.L., Page, A.P., Rudin, W. and Maizels, R.M., 1992, Nematode surface coats: Actively evading immunityParasitol Today8: 243–247.
Bundy, D.A.P., 1997, This wormy world - then and nowParasitol Today13: 407–408.
Caulfield, J.P., Cianci, C.M.L., McDiarmid, S.S., Suyemitsu, T. and Schmid, K., 1987, Ultrastructure, carbohydrate, and amino acid analysis of two preparations of the cercarial glycocalyx ofSchistosoma mansoni J Parasitol73: 514–522.
Cummings, R.D., 1994, Use of lectins in analysis of glycoconjugatesMethods Enzymol230: 66–85. Cummings, R.D. and Nyame, A.K., 1996, Glycobiology of schistosomiasisFASEB J 10:838–848.
Cummings, R.D. and Nyame, A.K., 1999, Schistosome glysoconjugatesBiochim Biophys Acta1455: 363–374.
Dalton, J.P., Lewis, S.A., Aronstein, W.S. and Strand, M., 1987Schistosoma mansoni:immunogenic glycoproteins of the cercarial glycocalyxExp Parasitol63: 215–226.
Daniel, B.E., Preston, T.M. and Southgate, V.R., 1992, Thein vitrotransformation of the miracidium to the mother sporocysts ofSchistosoma margrebowiei;changes in the parasite surface and implications for interactions with snail plasma factorsParasitology104: 41–49.
Dell, A., Haslam, S.M., Morris, H.R. and Khoo, K.H., 1999, Immunogenic glycoconjugates implicated in parasitic nematode diseasesBiochim Biophys Acta1455: 353–362.
Dennis, R.D. and Wiegandt, H., 1993, Glycosphingolipids of the invertebrata as exemplified by a cestode platyhelminthTaenia crassicepsand a dipteran insectCalliphora vicina Adv Lipid Res26: 321–351.
Dissous, C., Grzych, J.M. and Capron, A., 1986Schistosoma mansonishares a protective oligosaccharide epitope with freshwater and marine snailsNature323: 443–445.
Dunne, D.W., 1990, Schistosome carbohydratesParasitol Today6: 45–48.
El Ridi, R., Velupillai, P. and Ham, D.A., 1996, Regulation of schistosome egg granuloma formation: host-soluble L- selectin enters tissue-trapped eggs and binds to carbohydrate antigens on surface membranes of miracidiaInfect Immun64: 4700–4705.
Fryer, S.E. and Bayne, C.J., 1996, Host-parasite interactions in molluscs, in:Invertebrate Immunology Progress in Molecular and Subcellular Biology series vol. 15Rinkevich, B. and Müller, W.E.G. eds., Springer-Verlag, Berlin Heidelberg, pp. 131–153.
Garcia-Casado, G., Sanchezmonge, R., Chrispeels, M.J., Armentia, A., Salcedo, G. and Gomez, L., 1996, Role of complex asparagine-linked glycans in the allergenicity of plant glycoproteins.Glycobiology6: 471–477.
Gerdt, S., Lochnit, G., Dennis, R.D. and Geyer, R., 1997, Isolation and structural analysis of three neutral glycosphingolipids from a mixed population ofCaenorhabditis elegans(Nematoda:Rhabditida)Glycobiology7: 265–275.
Gerdt, S., Dennis, R.D., Borgonie, G., Schnabel, R. and Geyer, R., 1999, Isolation, characterization and immunolocalization of phosphorylcholine-substituted glycolipids in developmental stages ofCaenorhabditis elegans EurJBiochem266: 952–963.
Harnett, W. and Parkhouse, R.M.E., 1995, Nature and function of parasitic nematode surface and excretory-secretory antigens., in:Perspectives in Nematode Physiology and Biochemistry.Sood, M.L. and Kapur, J. eds., Narenda Publishing House, Delhi, pp. 207–242.
Harnett, W., Deehan, M.R., Houston, K.M. and Harnett, M.M., 1999, Immunomodulatory properties of aphosphorylcholine-containing secreted filarial glycoprotein.Parasite Immunol21: 601–608.
Harnett, W. and Harnett, M.M., 1999, Phosphorylcholine: friend or foe of the immune system ?Immunol Today20: 125–129.
Haslam, S.M., Coles, G.C., Munn, E.A., Smith, T.S., Smith, H.F., Morris, H.R. and Dell, A., 1996Haemonchus contortusglycoproteins contain N-linked oligosaccharides with novel highly fucosylated core structuresJ Bio! Chem271: 30561–30570.
Haslam, S.M., Khoo, K.H., Houston, K.M., Harnett, W., Morris, H.R. and Dell, A., 1997, Characterisation of the phosphorylcholine-containing N-linked oligosaccharides in the excretory-secretory 62 kDa glycoprotein ofAcanthocheilonema viteae Mol Biochem Parasitol85: 53–66.
Haslam, S.M., Coles, G.C., Reason, A.J., Morris, H.R. and Dell, A., 1998, The novel core fucosylation ofHaemonchus contortusN-glycans is stage specificMol Biochem Parasitol93: 143–147.
Haslam, S.M., Houston, K.M., Harnett, W., Reason, A.J., Morris, H.R. and Dell, A., 1999, Structural studies of N-glycans of filarial parasites. Conservation of phosphorylcholine-substituted glycans among species and discovery of novel chito-oligomersJ Biol Chem274: 20953–20960.
Haslam, S.M., Coles, G.C., Morris, H.R. and Dell, A., 2000, Structural characterization of the N-glycans ofDictyocaulus viviparus:discovery of the Lewisx structure in a nematodeGlycobiology 10:223–229.
Jacobs, W., Deelder, A. and Van Marck, E., 1999, Schistosomal granuloma modulation. II. Specific immunogenic carbohydrates can modulate schistosome-egg-antigen-induced hepatic granuloma formation.Parasitol Res85: 14–18.
Johnston, L.A. and Yoshino, T.P., 1996, Analysis of lectin-and snail plasma-binding glycopeptides associated with the tegumental surface of the primary sporocysts ofSchistosoma mansoni. Parasitology112:469–479.
Kamerling, J.P. and Vliegenthart, J.F.G., 1997, Hemocyanins, in:Glycoproteins IIMontreuil, J., Vliegenthart, J.F.G. and Schachter, H. eds., Elsevier, Amsterdam, pp. 123–142.
Kang, S., Cummings, R.D. and McCall, J.W., 1993, Characterization of the N-linked oligosaccharides in glycoproteins synthesized by microfilariae ofDirofilaria immitis JParasitol79: 815–828.
Kawakami, Y., Nakamura, K., Kojima, H., Suzuki, M., Inagaki, F., Suzuki, A., Sonoki, S., Uchida, A., Murata, Y. and Tamai, Y., 1993, A novel fucosylated glycosphingolipid with a Galß1–4Glcß1–3Gal sequence in plerocercoids of the parasiteSpirometra erinacei J Biochem (Tokyo) 114:677–683.
Khoo, K.-H., Maizels, R.M., Page, A.P., Taylor, G.W., Rendell, N.B. and Dell, A., 1991, Characterization of nematode glycoproteins: the major O-glycans ofToxocaraexcretory-secretory antigens areO-methylated trisaccharidesGlycobiology 1:163–171.
Khoo, K.-H., Morris, H.R. and Dell, A., 1993, Structural characterisation of the major glycans ofToxocara canisES antigens, in:Toxocara and Toxocariasis: Clinical Epidemiological and Molecular PerspectivesLewis, J.W. and Maizels, R.M. eds., Institute of Biology, pp. 133–140.
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 -3GalNAcß1→4GlcNAcßl→3Galα1- motif constitutes the repeating unit of the complex O-glycans derived from the cercarial glycocalyx ofSchistosoma mansoni J Bio! Chem270: 17114–17123.
Khoo, K.-H., Chatterjee, D., Caulfield, J.P., Morris, H.R. and Dell, A., 1997a, Structural characterization of glycophingolipids from the eggs ofSchistosoma mansoniandSchistosoma japonicum Glycobiology7: 653–661.
Khoo, K.-H., Chatterjee, D., Caulfield, J.P., Morris, H.R. and Dell, A., 1997, Structural mapping of the glycans from the egg glycoproteins ofSchistosoma mansoniandSchistosoma japonicum:identification of novel core structures and terminal sequencesGlycobiology7: 663–677.
Khoo, K.-H., Fan, K.-C. and Lee, K.-M., 1999, Structural probing of the developmental stage-specific glycosylation profile of schistosomes, in:Sialobiology and Other Novel Forms of GlycosylationInoue, Y., Lee, Y.C. and Troy II, F.A. eds., Gakushin, Osaka, pp. 255–258.
Ko, A.I., Drager, U.C. and Ham, D.A., 1990, ASchistosoma mansoniepitope recognized by a protective monoclonal antibody is identical to the stage-specific embryonic antigen 1Proc Natl Acad Sci USA87: 4159–4163.
Köster, B. and Strand, M., 1994Schistosoma mansoni:immunolocalization of two different fucosecontaining carbohydrate epitopesParasitology108: 433–446.
Lejoly-Boisseau, H., Appriou, M., Seigneur, M., Pruvost, A., Tribouley-Duret, J. and Tribouley, J., 1999Schistosoma mansoni:in vitro adhesion of parasite eggs to the vascular endothelium. Subsequent inhibition by a monoclonal antibody directed to a carbohydrate epitopeExp Parasitol91: 20–29.
Lerouge, P., Cabanes-Macheteau, M., Rayon, C., Fischette-Lainé, A.-C., Gomord, V. and Faye, L., 1998, N-Glycoprotein biosynthesis in plants: recent developments and future trendsPlant Mol Biol38: 31–48.
Lester, R.L. and Dickson, R.C., 1993, Sphingolipids with inositolphosphate-containing head groupsAdvLipid Res26: 253–274.
Levery, S.B., Weiss, J.B., Salyan, M.E., Roberts, C.E., Hakomori, S., Magnani, J.L. and Strand, M., 1992, Characterization of a series of novel fucose-containing glycosphingolipid immunogens from eggs ofSchistosoma mansoni J Bio! Chem267: 5542–5551.
Lochnit, G., Dennis, R.D., Ulmer, A.J. and Geyer, R., 1998a, Structural elucidation and monokine-inducing activity of two biologically active zwitterionic glycosphingolipids derived from the porcine parasitic nematodeAscaris suum J Bio! Chem273: 466–474.
Lochnit, G., Nispel, S., Dennis, R.D. and Geyer, R., 1998b, Structural analysis and immunohistochemical localization of two acidic glycosphingolipids from the porcine, parasitic nematodeAscaris suum Glycobiology8: 891–899.
Lochnit, G., Dennis, R.D., Zähringer, U. and Geyer, R., 1997, Structural analysis of neutral glycosphingolipids fromAscaris suumadults (Nematoda: Ascaridida)Glycoconj J14: 389–399.
Maizels, R.M. and Selkirk, M.E., 1988, Immunobiology of nematode antigens, in:The Biology of ParasitismEnglund, P.T. and Sher, F.A. eds., Alan R. Liss, New York, pp. 285–308.
Maizels, R.M., Blaxter, M.L. and Selkirk, M.E., 1993, Forms and functions of nematode surfacesExp Parasitol77: 380–384.
Makaaru, C.K., Damian, R.T., Smith, D.F. and Cummings, R.D., 1992, The human blood flukeSchistosoma mansonisynthesizes a novel type of glycosphingolipidJ Biol Chem267: 2251–2257.
Mansour, M.H., Negm, H.I., Saad, A.H. and Taalab, N.I., 1995, Characterization ofBiomphalaria alexandrina-derivedlectins recognizing a fucosyllactose-related determinant on schistosomesMol Biochem Parasitol69: 173–184.
Nanduri, J., Dennis, J.E., Rosenberry, T.L., Mahmoud, A.A.F. and Tartakoff, A.M., 1991, Glycocalyx of bodiesversustails ofSchistosoma mansonicercarieaeJ Biol Chem266: 1341–1347.
Nyame, K., Cummings, R.D. and Damian, R.T., 1987Schistosoma mansonisynthesizes glycoproteins containing terminal 0-linked N-acetylglucosamine residuesJ Biol Chem262: 7990–7995.
Nyame, K., Cummings, R.D. and Damian, R.T., 1988a, Characterization of the high mannose asparagine-linked oligosaccharides synthesized by Schistosoma mansoni adult male wormsMol Biochem Parasitol28: 265–274.
Nyame, K., Cummings, R.D. and Damian, R.T., 1988b, Characterization of theN-and 0-linked oligosaccharides in glycoproteins synthesized bySchistosoma mansonischistosomulaJ Parasitol74: 562–572.
Nyame, K., Smith, D.F., Damian, R.T. and Cummings, R.D., 1989, Complex-type asparagine-linked oligosaccharides in glycoproteins synthesized bySchistosoma mansoniadult males contain terminal f3-linked N-acetylgalactosamineJ Biol Chem264: 3235–3243.
Nyame, A.K., Pilcher, J.B., Tsang, V.C. and Cummings, R.D., 1996Schistosoma mansoniinfection in humans and primates induces cytolytic antibodies to surface Le(x) determinants on myeloid cellsExp Parasitol82: 191–200.
Nyame, A.K., Pilcher, J.B., Tsang, V.C. and Cummings, R.D., 1997, Rodents infected withSchistosoma mansoniproduce cytolytic IgG and IgM antibodies to the Lewis x antigenGlycobiology7: 207–215.
Nyame, A.K., Debose-Boyd, R., Long, T.D., Tsang, V.C. and Cummings, R.D., 1998, Expression of Lex antigen inSchistosoma japonicumandS. haematobiumand immune responses to Lexin infected animals: lack of Lexexpression in other trematodes and nematodesGlycobiology8: 615–624.
Nyame, A.K., Leppanen, A.M., DeBose-Boyd, R. and Cummings, R.D., 1999, Mice infected withSchistosoma mansonigenerate antibodies to LacdiNAc (Ga1NAcß1→4GlcNAc) determinantsGlycobiology9: 1029–1035.
Pearce, E.J., Caspar, P., Grzych, J.M., Lewis, F.A. and Sher, A., 1991, Downregulation of Thl cytokine production accompanies induction of Th2 responses by a parasitic helminthSchistosoma mansoni J Exp Med173: 159–166.
Reason, A.J., Ellis, L.A., Appleton, J.A., Wisnewski, N., Grieve, R.B., McNeil, M., Wassom, D.L., Morris, H.R. and Dell, A., 1994, Novel tyvelose-containing tri-and tetra-antennary N-glycans in the immunodominant antigens of the intracellular parasiteTrichinella spiralis Glycobiology4: 593–603.
Samuelson, J.C. and Caulfield, J.P., 1985, The cercarial glycocalyx ofSchistosoma mansoni J Cell Biol100: 1423–1434.
Simpson, A.J.G., 1990, Schistosome surface antigens: Developmental expression and immunological functionParasitol Today6: 40–45.
Srivatsan, J., Smith, D.F. and Cummings, R.D., 1992a, The human blood flukeSchistosoma mansonisynthesizes glycoproteins containing the Lewis X antigenJ Biol Chem267: 20196–20203.
Srivatsan, J., Smith, D.F. and Cummings, R.D., 1992Schistosoma mansonisynthesizes novel biantennary Asn-linked oligosaccharides containing terminal ß-linked N-acetylgalactosamineGlycobiology2: 445–452.
Sugita, M., Mizunoma, T., Aoki, K., Dulaney, J.T., Inagaki, F., Suzuki, M., Suzuki, A., Ichikawa, S., Kushida, K., Ohta, S. and Kurimoto, A., 1996, Structural characterization of a novel glycoinositolphospholipid from the parasitic nematodeAscaris suum Biochim Biophys Acta1302: 185–192.
Tretter, V., Altmann, F., Kubelka, V., Marz, L. and Becker, W.M., 1993, Fucose a1,3-linked to the core region of glycoprotein N-glycans creates an important epitope for IgE from honeybee venom allergic individualsInt Arch Allergy Immunol102: 259–266.
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 0-linked polysaccharide chains derived from circulating cathodic antigen isolated from the human blood flukeSchistosoma mansonihave Lewis x as repeating unitEur J Biochem225: 467–482.
van Dam, G.J., Claas, F.H., Yazdanbakhsh, M., Kruize, Y.C., van Keulen, A.C., Ferreira, S.T., Rotmans, J.P. and Deelder, A.M., 1996Schistosoma mansoniexcretory circulating cathodic antigen shares Lewis-x epitopes with a human granulocyte surface antigen and evokes host antibodies mediating complement-dependent lysis of granulocytes.Blood88: 4246–4251.
Van den Eijnden, D.H., Bakker, H., Neeleman, A.P., van den Nieuwenhof, I.M. and van Die, I., 1997, Novel pathways in complex-type oligosaccharide synthesis: new vistas opened by studies in invertebratesBiochem Soc Trans25: 887–893.
van der Knaap, W.P.W. and Loker, E.S., 1990, Immune mechanisms in trematode-snail interactionsParasitol Today6: 175–182.
van Die, I., Gomord, V., Kooyman, F.N., van den Berg, T.K., Cummings, R.D. and Vervelde, L., 1999, Core αl→3-fucose is a common modification of N-glycans in parasitic helminths and constitutes an important epitope for IgE fromHaemonchus contortusinfected sheepFEBS Lett463: 189–193.
Velupillai, P. and Ham, D.A., 1994, Oligosaccharide-specific induction of interleukin 10 production by B220+ cells from schistosome-infected mice: a mechanism for regulation of CD4+ T-cell subsetsProc Nall Acad Sci USA91: 18–22.
Velupillai, P., dos Reis, E.A., dos Reis, M.G. and Ham, D.A., 2000, Lewisx-containing oligosaccharide attenuates schistosome egg antigen-induced immune depression in human schistosomiasisHuman Immunol61: 225–232.
Weiss, J.B. and Strand, M., 1985, Characterization of developmentally regulated epitopes ofSchistosoma mansoniegg glycoprotein antigensJlmmunol135: 1421–1429.
Weiss, J.B., Magnani, J.L. and Strand, M., 1986, Identification ofSchistosoma mansoniglycolipids that share immunogenic carbohydrate epitopes with glycoproteinsJ Immunol136: 4275–4282.
Wuhrer, M., Dennis, R.D., Doenhoff, M.J., Lochnit, G. and Geyer, R., 2000Schistosoma mansonicercarial glycolipids are dominated by lewis X and pseudo-lewis Y structuresGlycobiology 10:89–101.
Xu, X., Stack, R.J., Rao, N. and Caulfield, J.P., 1994Schistosoma mansoni:Fractionation and characterization of the glycocalyx and glycogen-like material from cercariaeExpParasitol79: 399–409.
Zelck, U. and Becker, W., 1990, Lectin binding to cells ofSchistosoma mansonisporocyts and surroundingBiomphalaria glabratatissueJ lnvertebr Pathol 55:93–99.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2001 Springer Science+Business Media New York
About this chapter
Cite this chapter
Khoo, KH., Dell, A. (2001). Glycoconjugates from Parasitic Helminths: Structure Diversity and Immunobiological Implications. In: Wu, A.M. (eds) The Molecular Immunology of Complex Carbohydrates —2. Advances in Experimental Medicine and Biology, vol 491. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1267-7_14
Download citation
DOI: https://doi.org/10.1007/978-1-4615-1267-7_14
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-5469-7
Online ISBN: 978-1-4615-1267-7
eBook Packages: Springer Book Archive