Glycoconjugates from Parasitic Helminths: Structure Diversity and Immunobiological Implications

  • Kay-Hooi Khoo
  • Anne Dell
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 491)

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.

Keywords

Polysaccharide Neutropenia Inositol Mannose Monosaccharide 

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References

  1. Altmann, F., Staudacher, E., Wilson, I.B. and Marz, L., 1999, Insect cells as hosts for the expression of recombinant glycoproteinsGlycoconj J16: 109–123.PubMedCrossRefGoogle Scholar
  2. 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.Google Scholar
  3. Blaxter, M.L., Page, A.P., Rudin, W. and Maizels, R.M., 1992, Nematode surface coats: Actively evading immunityParasitol Today8: 243–247.PubMedCrossRefGoogle Scholar
  4. Bundy, D.A.P., 1997, This wormy world - then and nowParasitol Today13: 407–408.CrossRefGoogle Scholar
  5. 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.PubMedCrossRefGoogle Scholar
  6. 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.Google Scholar
  7. Cummings, R.D. and Nyame, A.K., 1999, Schistosome glysoconjugatesBiochim Biophys Acta1455: 363–374.PubMedCrossRefGoogle Scholar
  8. Dalton, J.P., Lewis, S.A., Aronstein, W.S. and Strand, M., 1987Schistosoma mansoni:immunogenic glycoproteins of the cercarial glycocalyxExp Parasitol63: 215–226.Google Scholar
  9. 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.PubMedCrossRefGoogle Scholar
  10. Dell, A., Haslam, S.M., Morris, H.R. and Khoo, K.H., 1999, Immunogenic glycoconjugates implicated in parasitic nematode diseasesBiochim Biophys Acta1455: 353–362.PubMedCrossRefGoogle Scholar
  11. 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.PubMedGoogle Scholar
  12. Dissous, C., Grzych, J.M. and Capron, A., 1986Schistosoma mansonishares a protective oligosaccharide epitope with freshwater and marine snailsNature323: 443–445.PubMedCrossRefGoogle Scholar
  13. Dunne, D.W., 1990, Schistosome carbohydratesParasitol Today6: 45–48.PubMedCrossRefGoogle Scholar
  14. 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.PubMedGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. 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.Google Scholar
  19. 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.Google Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. Harnett, W. and Harnett, M.M., 1999, Phosphorylcholine: friend or foe of the immune system ?Immunol Today20: 125–129.PubMedCrossRefGoogle Scholar
  22. 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.Google Scholar
  23. 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.PubMedCrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. 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.PubMedCrossRefGoogle Scholar
  26. 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.PubMedCrossRefGoogle Scholar
  27. 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.PubMedCrossRefGoogle Scholar
  28. 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.PubMedCrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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.Google Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. 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.Google Scholar
  34. 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.CrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.PubMedCrossRefGoogle Scholar
  37. 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.Google Scholar
  38. 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.PubMedCrossRefGoogle Scholar
  39. Köster, B. and Strand, M., 1994Schistosoma mansoni:immunolocalization of two different fucosecontaining carbohydrate epitopesParasitology108: 433–446.PubMedCrossRefGoogle Scholar
  40. 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.PubMedCrossRefGoogle Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. Lester, R.L. and Dickson, R.C., 1993, Sphingolipids with inositolphosphate-containing head groupsAdvLipid Res26: 253–274.Google Scholar
  43. 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.Google Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Lochnit, G., Dennis, R.D., Zähringer, U. and Geyer, R., 1997, Structural analysis of neutral glycosphingolipids fromAscaris suumadults (Nematoda: Ascaridida)Glycoconj J14: 389–399.PubMedCrossRefGoogle Scholar
  47. 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.Google Scholar
  48. Maizels, R.M., Blaxter, M.L. and Selkirk, M.E., 1993, Forms and functions of nematode surfacesExp Parasitol77: 380–384.PubMedCrossRefGoogle Scholar
  49. 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.PubMedGoogle Scholar
  50. 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.PubMedCrossRefGoogle Scholar
  51. 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.PubMedGoogle Scholar
  52. Nyame, K., Cummings, R.D. and Damian, R.T., 1987Schistosoma mansonisynthesizes glycoproteins containing terminal 0-linked N-acetylglucosamine residuesJ Biol Chem262: 7990–7995.PubMedGoogle Scholar
  53. 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.CrossRefGoogle Scholar
  54. 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.CrossRefGoogle Scholar
  55. 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.PubMedGoogle Scholar
  56. 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.PubMedCrossRefGoogle Scholar
  57. 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.PubMedCrossRefGoogle Scholar
  58. 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.PubMedCrossRefGoogle Scholar
  59. 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.PubMedCrossRefGoogle Scholar
  60. 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.PubMedCrossRefGoogle Scholar
  61. 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.PubMedCrossRefGoogle Scholar
  62. Samuelson, J.C. and Caulfield, J.P., 1985, The cercarial glycocalyx ofSchistosoma mansoni J Cell Biol100: 1423–1434.PubMedCrossRefGoogle Scholar
  63. Simpson, A.J.G., 1990, Schistosome surface antigens: Developmental expression and immunological functionParasitol Today6: 40–45.PubMedCrossRefGoogle Scholar
  64. 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.Google Scholar
  65. Srivatsan, J., Smith, D.F. and Cummings, R.D., 1992Schistosoma mansonisynthesizes novel biantennary Asn-linked oligosaccharides containing terminal ß-linked N-acetylgalactosamineGlycobiology2: 445–452.PubMedCrossRefGoogle Scholar
  66. 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.PubMedCrossRefGoogle Scholar
  67. 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.PubMedCrossRefGoogle Scholar
  68. 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.PubMedCrossRefGoogle Scholar
  69. 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.PubMedGoogle Scholar
  70. 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.PubMedGoogle Scholar
  71. van der Knaap, W.P.W. and Loker, E.S., 1990, Immune mechanisms in trematode-snail interactionsParasitol Today6: 175–182.PubMedCrossRefGoogle Scholar
  72. 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.PubMedCrossRefGoogle Scholar
  73. 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.CrossRefGoogle Scholar
  74. 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.CrossRefGoogle Scholar
  75. Weiss, J.B. and Strand, M., 1985, Characterization of developmentally regulated epitopes ofSchistosoma mansoniegg glycoprotein antigensJlmmunol135: 1421–1429.Google Scholar
  76. Weiss, J.B., Magnani, J.L. and Strand, M., 1986, Identification ofSchistosoma mansoniglycolipids that share immunogenic carbohydrate epitopes with glycoproteinsJ Immunol136: 4275–4282.PubMedGoogle Scholar
  77. 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.PubMedCrossRefGoogle Scholar
  78. 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.Google Scholar
  79. Zelck, U. and Becker, W., 1990, Lectin binding to cells ofSchistosoma mansonisporocyts and surroundingBiomphalaria glabratatissueJ lnvertebr Pathol 55:93–99.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2001

Authors and Affiliations

  • Kay-Hooi Khoo
    • 1
  • Anne Dell
    • 2
  1. 1.Institute of Biological ChemistryAcademia SinicaTaipei Taiwan
  2. 2.Department of Biochemistry, Imperial College of ScienceTechnology and MedicineLondonUK

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