Schistosoma mansoni egg glycoproteins and C-type lectins of host immune cells: Molecular partners that shape immune responses

Experimental Parasitology

Volumn 132, Issue 1, 2012, Pages 14-21

  Meevissen, Moniek H J ^a   Yazdanbakhsh, Maria ^a   Hokke, Cornelis H ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

C Type lectins; Eggs; Glycosylation; Immunomodulation; Schistosoma mansoni; Trematode

Indexed keywords

CD209 ANTIGEN; CYTOKINE; FRUCTOSE; GALACTOSE; GAMMA INTERFERON; GLYCAN; GLYCOPROTEIN; GLYCOSYLTRANSFERASE; INTERCELLULAR ADHESION MOLECULE 3; INTERLEUKIN 4; INTERLEUKIN 5; LECTIN; MACROPHAGE C TYPE LECTIN 1; MACROPHAGE C TYPE LECTIN 2; MANNOSE; MANNOSE RECEPTOR; N ACETYLGLUCOSAMINE; PARASITE ANTIGEN; PATTERN RECOGNITION RECEPTOR; PROTEIN SIGNR1; PROTEIN SIGNR3; SIALYL LEWIS X ANTIGEN; SOLUBLE EGG ANTIGEN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ANTIGEN PRESENTING CELL; ARTICLE; BINDING AFFINITY; CYTOKINE RESPONSE; ENZYME ACTIVITY; HOST PARASITE INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; SIGNAL TRANSDUCTION; TH2 CELL;

ANIMALS; ANTIGENS, HELMINTH; GLYCOPROTEINS; HELMINTH PROTEINS; HUMANS; LECTINS, C-TYPE; OVUM; POLYSACCHARIDES; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; TH2 CELLS;

SCHISTOSOMA; SCHISTOSOMA MANSONI; TREMATODA;

EID: 84865543385     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2011.05.005     Document Type: Article

References (80)

1. Asahi H., Hernandez H.J., Stadecker M.J. A novel 62-kilodalton egg antigen from Schistosoma mansoni induces a potent CD4(+) T helper cell response in the C57BL/6 mouse. Infection and Immunity 1999, 67:1729-1735.
2. Ashton P.D., Harrop R., Shah B., Wilson R.A. The schistosome egg: development and secretions. Parasitology 2001, 122:329-338.
3. Bashirova A.A., Geijtenbeek T.B., van Duijnhoven G.C., van Vliet S.J., Eilering J.B., Martin M.P., Wu L., Martin T.D., Viebig N., Knolle P.A., Kewalramani V.N., van Kooyk Y., Carrington M. A dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal endothelial cells and promotes HIV-1 infection. The Journal of Experimental Medicine 2001, 193:671-678.
4. Breuilh L., Vanhoutte F., Fontaine J., van Stijn C.M., Tillie-Leblond I., Capron M., Faveeuw C., Jouault T., van Die I., Gosset P., Trottein F. Galectin-3 modulates immune and inflammatory responses during helminthic infection: impact of galectin-3 deficiency on the functions of dendritic cells. Infection and Immunity 2007, 75:5148-5157.
5. Cambi A., de Lange F., van Maarseveen N.M., Nijhuis M., Joosten B., van Dijk E.M., de Bakker B.I., Fransen J.A., Bovee-Geurts P.H., van Leeuwen F.N., van Hulst N.F., Figdor C.G. Microdomains of the C-type lectin DC-SIGN are portals for virus entry into dendritic cells. The Journal of Cell Biology 2004, 164:145-155.
6. Cervi L., MacDonald A.S., Kane C., Dzierszinski F., Pearce E.J. Cutting edge: dendritic cells copulsed with microbial and helminth antigens undergo modified maturation, segregate the antigens to distinct intracellular compartments, and concurrently induce microbe-specific Th1 and helminth-specific Th2 responses. Journal of Immunology 2004, 172:2016-2020.
7. Chensue S.W., Warmington K., Ruth J., Lincoln P., Kuo M.C., Kunkel S.L. Cytokine responses during mycobacterial and schistosomal antigen-induced pulmonary granuloma formation. Production of Th1 and Th2 cytokines and relative contribution of tumor necrosis factor. The American Journal of Pathology 1994, 145:1105-1113.
8. de Bakker B.I., de Lange F., Cambi A., Korterik J.P., van Dijk E.M., van Hulst N.F., Figdor C.G., Garcia-Parajo M.F. Nanoscale organization of the pathogen receptor DC-SIGN mapped by single-molecule high-resolution fluorescence microscopy. ChemPhysChem 2007, 8:1473-1480.
9. de Jong E.C., Vieira P.L., Kalinski P., Schuitemaker J.H., Tanaka Y., Wierenga E.A., Yazdanbakhsh M., Kapsenberg M.L. Microbial compounds selectively induce Th1 cell-promoting or Th2 cell-promoting dendritic cells in vitro with diverse the cell-polarizing signals. Journal of Immunology 2002, 168:1704-1709.
10. 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., van Hellemond J.J. The proteome of the insoluble Schistosoma mansoni eggshell skeleton. International Journal for Parasitology 2011, 41:523-532.
11. Donnelly S., Stack C.M., O'Neill S.M., Sayed A.A., Williams D.L., Dalton J.P. Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages. The FASEB Journal 2008, 22:4022-4032.
12. Drickamer K., Taylor M.E. Biology of animal lectins. Annual Review of Cell Biology 1993, 9:237-264.
13. Eberl M., Langermans J.A., Vervenne R.A., Nyame A.K., Cummings R.D., Thomas A.W., Coulson P.S., Wilson R.A. Antibodies to glycans dominate the host response to schistosome larvae and eggs: is their role protective or subversive?. The Journal of Infectious Diseases 2001, 183:1238-1247.
14. Everts B., Perona-Wright G., Smits H.H., Hokke C.H., van der Ham A.J., Fitzsimmons C.M., Doenhoff M.J., van der B.J., Mohrs K., Haas H., Mohrs M., Yazdanbakhsh M., Schramm G. Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. The Journal of Experimental Medicine 2009, 206:1673-1680.
15. Faveeuw C., Angeli V., Fontaine J., Maliszewski C., Capron A., Van Kaer L., Moser M., Capron M., Trottein F. Antigen presentation by CD1d contributes to the amplification of Th2 responses to Schistosoma mansoni glycoconjugates in mice. Journal of Immunology 2002, 169:906-912.
16. Fitzsimmons C.M., Schramm G., Jones F.M., Chalmers I.W., Hoffmann K.F., Grevelding C.G., Wuhrer M., Hokke C.H., Haas H., Doenhoff M.J., Dunne D.W. Molecular characterization of omega-1: a hepatotoxic ribonuclease from Schistosoma mansoni eggs. Molecular and Biochemical Parasitology 2005, 144:123-127.
17. Galustian C., Park C.G., Chai W., Kiso M., Bruening S.A., Kang Y.S., Steinman R.M., Feizi T. High and low affinity carbohydrate ligands revealed for murine SIGN-R1 by carbohydrate array and cell binding approaches, and differing specificities for SIGN-R3 and langerin. International Immunology 2004, 16:853-866.
18. Geijtenbeek T.B., Torensma R., van Vliet S.J., van Duijnhoven G.C., Adema G.J., van Kooyk Y., Figdor C.G. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 2000, 100:575-585.
19. Gringhuis S.I., den Dunnen J., Litjens M., van der Vlist M., Geijtenbeek T.B. Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nature Immunology 2009, 10:1081-1088.
20. Guo Y., Feinberg H., Conroy E., Mitchell D.A., Alvarez R., Blixt O., Taylor M.E., Weis W.I., Drickamer K. Structural basis for distinct ligand-binding and targeting properties of the receptors DC-SIGN and DC-SIGNR. Nature Structural and Molecular Biology 2004, 11:591-598.
21. Harris N., Super M., Rits M., Chang G., Ezekowitz R.A. Characterization of the murine macrophage mannose receptor: demonstration that the downregulation of receptor expression mediated by interferon-gamma occurs at the level of transcription. Blood 1992, 80:2363-2373.
22. Haslam S.M., Coles G.C., Morris H.R., Dell A. Structural characterization of the N-glycans of Dictyocaulus viviparus: discovery of the Lewis(x) structure in a nematode. Glycobiology 2000, 10:223-229.
23. Higashi N., Fujioka K., Denda-Nagai K., Hashimoto S., Nagai S., Sato T., Fujita Y., Morikawa A., Tsuiji M., Miyata-Takeuchi M., Sano Y., Suzuki N., Yamamoto K., Matsushima K., Irimura T. The macrophage C-type lectin specific for galactose/N-acetylgalactosamine is an endocytic receptor expressed on monocyte-derived immature dendritic cells. The Journal of Biological Chemistry 2002, 277:20686-20693.
24. Jang-Lee J., Curwen R.S., Ashton P.D., Tissot B., Mathieson W., Panico M., Dell A., Wilson R.A., Haslam S.M. Glycomics analysis of Schistosoma mansoni egg and cercarial secretions. Molecular and Cellular Proteomics 2007, 6:1485-1499.
25. Jankovic D., Kullberg M.C., Caspar P., Sher A. Parasite-induced Th2 polarization is associated with down-regulated dendritic cell responsiveness to Th1 stimuli and a transient delay in T lymphocyte cycling. Journal of Immunology 2004, 173:2419-2427.
26. Kane C.M., Cervi L., Sun J., McKee A.S., Masek K.S., Shapira S., Hunter C.A., Pearce E.J. Helminth antigens modulate TLR-initiated dendritic cell activation. Journal of Immunology 2004, 173:7454-7461.
27. Kariuki T.M., Farah I.O., Wilson R.A., Coulson P.S. Antibodies elicited by the secretions from schistosome cercariae and eggs are predominantly against glycan epitopes. Parasite Immunology 2008, 30:554-562.
28. Karrar A., Broome U., Uzunel M., Qureshi A.R., Sumitran-Holgersson S. Human liver sinusoidal endothelial cells induce apoptosis in activated T cells: a role in tolerance induction. Gut 2007, 56:243-252.
29. Khoo K.H., Chatterjee D., Caulfield J.P., Morris H.R., Dell A. Structural mapping of the glycans from the egg glycoproteins of Schistosoma mansoni and Schistosoma japonicum: identification of novel core structures and terminal sequences. Glycobiology 1997, 7:663-677.
30. Knolle P.A., Gerken G. Local control of the immune response in the liver. Immunological Reviews 2000, 174:21-34.
31. Koppel E.A., Ludwig I.S., Appelmelk B.J., van Kooyk Y., Geijtenbeek T.B. Carbohydrate specificities of the murine DC-SIGN homologue mSIGNR1. Immunobiology 2005, 210:195-201.
32. Lee R.T., Hsu T.L., Huang S.K., Hsieh S.L., Wong C.H., Lee Y.C. Survey of immune-related, mannose/fucose-binding C-type lectin receptors reveals widely divergent sugar-binding Specificities. Glycobiology 2011, 21:512-520.
33. Linehan S.A. The mannose receptor is expressed by subsets of APC in non-lymphoid organs. BMC Immunology 2005, 6:4.
34. Lozach P.Y., Lortat-Jacob H., de Lacroix d.L., Staropoli I., Foung S., Amara A., Houles C., Fieschi F., Schwartz O., Virelizier J.L., Arenzana-Seisdedos F., Altmeyer R. DC-SIGN and L-SIGN are high affinity binding receptors for hepatitis C virus glycoprotein E2. The Journal of Biological Chemistry 2003, 278:20358-20366.
35. MacDonald A.S., Straw A.D., Bauman B., Pearce E.J. CD8- dendritic cell activation status plays an integral role in influencing Th2 response development. Journal of Immunology 2001, 167:1982-1988.
36. Mathieson W., Wilson R.A. A comparative proteomic study of the undeveloped and developed Schistosoma mansoni egg and its contents: the miracidium, hatch fluid and secretions. International Journal for Parasitology 2010, 40:617-628.
37. Meevissen M.H., Balog C.I., Koeleman C.A., Doenhoff M.J., Schramm G., Haas H., Deelder A.M., Wuhrer M., Hokke C.H. Targeted glycoproteomic analysis reveals that kappa-5 is a major, uniquely glycosylated component of Schistosoma mansoni egg antigens. Molecular and Cellular Proteomics 2011.
38. Meevissen M.H., Wuhrer M., Doenhoff M.J., Schramm G., Haas H., Deelder A.M., Hokke C.H. Structural characterization of glycans on omega-1, a major Schistosoma mansoni egg glycoprotein that drives Th2 responses. Journal of Proteome Research 2010, 9:2630-2642.
39. Meyer S., Tefsen B., Imberty A., Geyer R., van, Die I. The C-type lectin L-SIGN differentially recognizes glycan antigens on egg glycosphingolipids and soluble egg glycoproteins from Schistosoma mansoni. Glycobiology 2007, 17:1104-1119.
40. Mitchell D.A., Fadden A.J., Drickamer K. A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR. Subunit organization and binding to multivalent ligands. The Journal of Biological Chemistry 2001, 276:28939-28945.
41. Nagaoka K., Takahara K., Minamino K., Takeda T., Yoshida Y., Inaba K. Expression of C-type lectin, SIGNR3, on subsets of dendritic cells, macrophages, and monocytes. Journal of Leukocyte Biology 2010, 88:913-924.
42. Neill P.J., Smith J.H., Doughty B.L., Kemp M. The ultrastructure of the Schistosoma mansoni egg. The American Journal of Tropical Medicine and Hygiene 1988, 39:52-65.
43. Nyame A.K., Debose-Boyd R., Long T.D., Tsang V.C., Cummings R.D. Expression of Lex antigen in Schistosoma japonicum and S. haematobium and immune responses to Lex in infected animals: lack of Lex expression in other trematodes and nematodes. Glycobiology 1998, 8:615-624.
44. Nyame A.K., Lewis F.A., Doughty B.L., Correa-Oliveira R., Cummings R.D. Immunity to schistosomiasis: glycans are potential antigenic targets for immune intervention. Experimental Parasitology 2003, 104:1-13.
45. Okano M., Satoskar A.R., Nishizaki K., Abe M., Harn D.A. Induction of Th2 responses and IgE is largely due to carbohydrates functioning as adjuvants on Schistosoma mansoni egg antigens. Journal of Immunology 1999, 163:6712-6717.
46. Okano M., Satoskar A.R., Nishizaki K., Harn D.A. Lacto-N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response. Journal of Immunology 2001, 167:442-450.
47. Park C.G., Takahara K., Umemoto E., Yashima Y., Matsubara K., Matsuda Y., Clausen B.E., Inaba K., Steinman R.M. Five mouse homologues of the human dendritic cell C-type lectin, DC-SIGN. International Immunology 2001, 13:1283-1290.
48. Pearce E.J. Priming of the immune response by schistosome eggs. Parasite Immunology 2005, 27:265-270.
49. Pearce E.J., MacDonald A.S. The immunobiology of schistosomiasis. Nature Reviews Immunology 2002, 2:499-511.
50. Powlesland A.S., Ward E.M., Sadhu S.K., Guo Y., Taylor M.E., Drickamer K. Widely divergent biochemical properties of the complete set of mouse DC-SIGN-related proteins. The Journal of Biological Chemistry 2006, 281:20440-20449.
51. Robijn M.L., Koeleman C.A., Hokke C.H., Deelder A.M. Schistosoma mansoni eggs excrete specific free oligosaccharides that are detectable in the urine of the human host. Molecular and Biochemical Parasitology 2007, 151:162-172.
52. Robijn M.L., Koeleman C.A., Wuhrer M., Royle L., Geyer R., Dwek R.A., Rudd P.M., Deelder A.M., Hokke C.H. Targeted identification of a unique glycan epitope of Schistosoma mansoni egg antigens using a diagnostic antibody. Molecular and Biochemical Parasitology 2007, 151:148-161.
53. Robijn M.L., Wuhrer M., Kornelis D., Deelder A.M., Geyer R., Hokke C.H. Mapping fucosylated epitopes on glycoproteins and glycolipids of Schistosoma mansoni cercariae, adult worms and eggs. Parasitology 2005, 130:67-77.
54. Saunders S.P., Walsh C.M., Barlow J.L., Mangan N.E., Taylor P.R., McKenzie A.N., Smith P., Fallon P.G. The C-type lectin SIGNR1 binds Schistosoma mansoni antigens in vitro, but SIGNR1-deficient mice have normal responses during schistosome infection. Infection and Immunity 2009, 77:399-404.
55. Schramm G., Falcone F.H., Gronow A., Haisch K., Mamat U., Doenhoff M.J., Oliveira G., Galle J., Dahinden C.A., Haas H. Molecular characterization of an interleukin-4-inducing factor from Schistosoma mansoni eggs. The Journal of Biological Chemistry 2003, 278:18384-18392.
56. Schramm G., Gronow A., Knobloch J., Wippersteg V., Grevelding C.G., Galle J., Fuller H., Stanley R.G., Chiodini P.L., Haas H., Doenhoff M.J. IPSE/alpha-1: a major immunogenic component secreted from Schistosoma mansoni eggs. Molecular and Biochemical Parasitology 2006, 147:19.
57. Schramm G., Hamilton J.V., Balog C.I., Wuhrer M., Gronow A., Beckmann S., Wippersteg V., Grevelding C.G., Goldmann T., Weber E., Brattig N.W., Deelder A.M., Dunne D.W., Hokke C.H., Haas H., Doenhoff M.J. Molecular characterisation of kappa-5, a major antigenic glycoprotein from Schistosoma mansoni eggs. Molecular and Biochemical Parasitology 2009, 166:4-14.
58. Schramm G., Mohrs K., Wodrich M., Doenhoff M.J., Pearce E.J., Haas H., Mohrs M. Cutting edge: IPSE/alpha-1, a glycoprotein from Schistosoma mansoni eggs, induces IgE-dependent, antigen-independent IL-4 production by murine basophils in vivo. Journal of Immunology 2007, 178:6023-6027.
59. Singh S.K., Streng-Ouwehand I., Litjens M., Weelij D.R., Garcia-Vallejo J.J., van Vliet S.J., Saeland E., van Kooyk Y. Characterization of murine MGL1 and MGL2 C-type lectins: distinct glycan specificities and tumor binding properties. Molecular Immunology 2009, 46:1240-1249.
60. Smith P., Fallon R.E., Mangan N.E., Walsh C.M., Saraiva M., Sayers J.R., McKenzie A.N., Alcami A., Fallon P.G. Schistosoma mansoni secretes a chemokine binding protein with antiinflammatory activity. The Journal of Experimental Medicine 2005, 202:1319-1325.
61. Steinfelder S., Andersen J.F., Cannons J.L., Feng C.G., Joshi M., Dwyer D., Caspar P., Schwartzberg P.L., Sher A., Jankovic D. The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). The Journal of Experimental Medicine 2009, 206:1681-1690.
62. Tanne A., Ma B., Boudou F., Tailleux L., Botella H., Badell E., Levillain F., Taylor M.E., Drickamer K., Nigou J., Dobos K.M., Puzo G., Vestweber D., Wild M.K., Marcinko M., Sobieszczuk P., Stewart L., Lebus D., Gicquel B., Neyrolles O. A murine DC-SIGN homologue contributes to early host defense against Mycobacterium tuberculosis. The Journal of Experimental Medicine 2009, 206:2205-2220.
63. Taylor M.E., Bezouska K., Drickamer K. Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor. The Journal of Biological Chemistry 1992, 267:1719-1726.
64. Taylor M.E., Drickamer K. Structural requirements for high affinity binding of complex ligands by the macrophage mannose receptor. The Journal of Biological Chemistry 1993, 268:399-404.
65. Thomas P.G., Carter M.R., Atochina O., Da'Dara A.A., Piskorska D., McGuire E., Harn D.A. Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. Journal of Immunology 2003, 171:5837-5841.
66. Thomas P.G., Carter M.R., Da'Dara A.A., DeSimone T.M., Harn D.A. A helminth glycan induces APC maturation via alternative NF-kappa B activation independent of I kappa B alpha degradation. Journal of Immunology 2005, 175:2082-2090.
67. Tsuiji M., Fujimori M., Ohashi Y., Higashi N., Onami T.M., Hedrick S.M., Irimura T. Molecular cloning and characterization of a novel mouse macrophage C-type lectin, mMGL2, which has a distinct carbohydrate specificity from mMGL1. The Journal of Biological Chemistry 2002, 277:28892-28901.
68. van de Vijver K.K., Deelder A.M., Jacobs W., Van Marck E.A., Hokke C.H. LacdiNAc- and LacNAc-containing glycans induce granulomas in an in vivo model for schistosome egg-induced hepatic granuloma formation. Glycobiology 2006, 16:237-243.
69. van de Vijver K.K., Hokke C.H., van Remoortere A., Jacobs W., Deelder A.M., Van Marck E.A. Glycans of Schistosoma mansoni and keyhole limpet haemocyanin induce hepatic granulomas in vivo. International Journal for Parasitology 2004, 34:951-961.
70. van den Berg T.K., Honing H., Franke N., van Remoortere A., Schiphorst W.E., Liu F.T., Deelder A.M., Cummings R.D., Hokke C.H., van Die I. LacdiNAc-glycans constitute a parasite pattern for galectin-3-mediated immune recognition. Journal of Immunology 2004, 173:1902-1907.
71. van der Kleij D., van Remoortere A., Schuitemaker J.H., Kapsenberg M.L., Deelder A.M., Tielens A.G., Hokke C.H., Yazdanbakhsh M. 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. The Journal of Infectious Diseases 2002, 185:531-539.
72. van Die I., van Vliet S.J., Nyame A.K., Cummings R.D., Bank C.M., Appelmelk B., Geijtenbeek T.B., van Kooyk Y. The dendritic cell-specific C-type lectin DC-SIGN is a receptor for Schistosoma mansoni egg antigens and recognizes the glycan antigen Lewis x. Glycobiology 2003, 13:471-478.
73. van Liempt E., Bank C.M., Mehta P., Garcia-Vallejo J.J., Kawar Z.S., Geyer R., Alvarez R.A., Cummings R.D., Kooyk Y., van Die I. Specificity of DC-SIGN for mannose- and fucose-containing glycans. FEBS Letters 2006, 580:6123-6131.
74. van Liempt E., van Vliet S.J., Engering A., Garcia Vallejo J.J., Bank C.M., Sanchez-Hernandez M., van Kooyk Y., van Die I. Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Molecular Immunology 2007, 44:2605-2615.
75. van Remoortere A., Hokke C.H., van dam G.J., van Die I., Deelder A.M., van den Eijnden D.H. 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 2000, 10:601-609.
76. van Vliet S.J., van Liempt E., Saeland E., Aarnoudse C.A., Appelmelk B., Irimura T., Geijtenbeek T.B., Blixt O., Alvarez R., van Die I., van Kooyk Y. Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. International Immunology 2005, 17:661-669.
77. Varki A., Cummings R.D., Esko J.D., Freeze H.H., Stanley P., Bertozzi C.R., Hart G.W., Etzler M.E. Essentials of glycobiology 2009, Cold Spring Harbor Laboratory Press, New York. second ed.
78. Vella A.T., Pearce E.J. CD4+ Th2 response induced by Schistosoma mansoni eggs develops rapidly, through an early, transient, Th0-like stage. Journal of Immunology 1992, 148:2283-2290.
79. Williams D.L., Asahi H., Oke T.T., da Rosa J.L., Stadecker M.J. Murine immune responses to a novel schistosome egg antigen, SmEP25. International Journal for Parasitology 2005, 35:875-882.
80. Wuhrer M., Balog C.I., Catalina M.I., Jones F.M., Schramm G., Haas H., Doenhoff M.J., Dunne D.W., Deelder A.M., Hokke C.H. IPSE/alpha-1, a major secretory glycoprotein antigen from schistosome eggs, expresses the Lewis X motif on core-difucosylated N-glycans. The FEBS Journal 2006, 273:2276-2292.