Glycomics analysis of Schistosoma mansoni egg and cercarial secretions

Molecular and Cellular Proteomics

Volumn 6, Issue 9, 2007, Pages 1485-1499

  Jang Lee, Jihye ^a   Curwen, Rachel S ^b   Ashton, Peter D ^b   Tissot, Bérangère ^a   Mathieson, William ^b   Panico, Maria ^a   Dell, Anne ^a   Wilson, R Alan ^b   Haslam, Stuart M ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; CARBOHYDRATE BINDING PROTEIN; FUCOSE; GLYCAN; GLYCOCONJUGATE; GLYCOPROTEIN; MUCIN 1; N ACETYLGLUCOSAMINE;

ANIMAL CELL; ARTICLE; CARBOHYDRATE ANALYSIS; CERCARIA (TREMATODE LARVA); CONTROLLED STUDY; DEVELOPING COUNTRY; DEVELOPMENTAL STAGE; FUCOSYLATION; GLYCOSYLATION; HELMINTH; HOST; IMMUNE SYSTEM; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PUBLIC HEALTH PROBLEM; SCHISTOSOMA MANSONI; TANDEM MASS SPECTROMETRY;

AMINO ACID MOTIFS; ANIMALS; ANTIGENS, HELMINTH; CARBOHYDRATES; FUCOSE; GLYCOPROTEINS; IONS; LIGANDS; PEPTIDE-N4-(N-ACETYL-BETA-GLUCOSAMINYL) ASPARAGINE AMIDASE; POLYSACCHARIDES; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; SCHISTOSOMA MANSONI; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

SCHISTOSOMA MANSONI; VERMES;

EID: 34848863356     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M700004-MCP200     Document Type: Article

References (57)

1. King, C. H., Dickman, K., and Tisch, D. J. (2005) Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365, 1561-1569
2. van der Werf, M. J., de Vlas, S. J., Brooker, S., Looman, C. W., Nagelkerke, N. J., Habbema, J. D., and Engels, D. (2003) Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop. 86, 125-139
3. Dorsey, C. H., Cousin, C. E., Lewis, F. A., and Stirewalt, M. A. (2002) Ultrastructure of the Schistosoma mansoni cercaria. Micron 33, 279-323
4. Ashton, P. D., Harrop, R., Shah, B., and Wilson, R. A. (2001) The schistosome egg: development and secretions. Parasitology 122, 329-338
5. Hang, L. M., Warren, K. S., and Boros, D. L. (1974) Schistosoma mansoni: antigenic secretions and the etiology of egg granulomas in mice. Exp. Parasitol. 35, 288-298
6. 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? J. Infect. Dis. 183, 1238-1247 2
7. Omer Ali, P., Smithers, S. R., Bickle, Q., Phillips, S. M., Harn, D., and Simpson, A. J. (1988) Analysis of the anti-Schistosoma mansoni surface antibody response during murine infection and its potential contribution to protective immunity. J. Immunol. 140, 3273-3279
8. Omer-Ali, P., Magee, A. I., Kelly, C., and Simpson, A. J. (1986) A major role 2 for carbohydrate epitopes preferentially recognized by chronically infected mice in the determination of Schistosoma mansoni schistosomulum surface antigenicity. J. Immunol. 137, 3601-3607
9. Curwen, R. S., Ashton, P. D., Sundaralingam, S., and Wilson, R. A. (2006) Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Mol. Cell. Proteomics 5, 835-844
10. Knudsen, G. M., Medzihradszky, K. F., Lim, K. C., Hansell, E., and McKerrow, J. H. (2005) Proteomic analysis of Schistosoma mansoni cercarial secretions. Mol. Cell. Proteomics 4, 1862-1875
11. Hokke, C. H., and Deelder, A. M. (2001) Schistosome glycoconjugates in host-parasite interplay. Glycoconj. J. 18, 573-587
12. 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, 395-406
13. 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, 663-677
14. 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, 149-163
15. 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 -3GaINAcβ1 →4GIcNAcβ1 →3Galα1 - motif constitutes the repeating unit of the complex O-glycans derived from the cercarial glycocalyx of Schistosoma mansoni. J. Biol. Chem. 270, 17114-17123
16. 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. Exp. Parasitol. 96, 202-212
17. 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, GalNAcβ1-4(Fucα1-3)GlcNAc and GalNAcβ1-4(Fucα1-2Fucα1-3)GlcNAc carbohydrate epitopes: detection with monoclonal antibodies that are characterized by enzymatically synthesized neoglycoproteins. Glycobiology 10, 601-609
18. 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, 67-77
19. 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)-(β-D-GlcpA-(1 →3)) -β-D-GalpNAc-(1 → repeating units. J. Biol. Chem. 269, 31510-31517
20. Srivatsan, J., Smith, D. F., and Cummings, R. D. (1992) The human blood fluke Schistosoma mansoni synthesizes glycoproteins containing the Lewis X antigen. J. Biol. Chem. 267, 20196-20203
21. 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. Eur. J. Biochem. 225, 467-482
22. 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) IPSE/alpha-1, a major secretory glycoprotein antigen from schistosome eggs, expresses the Lewis X motif on core-difucosylated N-glycans. FEBS J. 273, 2276-2292
23. Thomas, P. G., and Harn, D. A., Jr. (2004) Immune biasing by helminth glycans. Cell. Microbiol. 6, 13-22
24. Dell, A., Reason, A. J., Khoo, K. H., Panico, M., McDowell, R. A., and Morris, H. R. (1994) Mass spectrometry of carbohydrate-containing biopolymers. Methods Enzymol. 230, 108-132
25. Schramm, G., Falcone, F. H., Gronow, A., Haisch, K., Mamat, U., Doenhoff, M. J., Oliveira, G., Galle, J., Dahinden, C. A., and Haas, H. (2003) Molecular characterization of an interleukin-4-inducing factor from Schistosoma mansoni eggs. J. Biol. Chem. 278, 18384-18392
26. Haslam, S. M., Coles, G. C., Reason, A. J., Morris, H. R., and Dell, A. (1998) The novel core fucosylation of Haemonchus contortus N-glycans is stage specific. Mol. Biochem. Parasitol. 93, 143-147
27. 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., and Dunne, D. W. (2005) Molecular characterization of omega-1: a hepatotoxic ribonuclease from Schistosoma mansoni eggs. Mol. Biochem. Parasitol. 144, 123-127
28. Kim, J. S., Soucek, J., Matousek, J., and Raines, R. T. (1995) Catalytic activity of bovine seminal ribonuclease is essential for its immunosuppressive and other biological activities. Biochem. J. 308, 547-550
29. Makarov, A. A., and Ilinskaya, O. N. (2003) Cytotoxic ribonucleases: molecular weapons and their targets. FEBS Lett. 540, 15-20
30. Olmo, N., Turnay, J., Gonzalez de Buitrago, G., Lopez de Silanes, I., Gavilanes, J. G., and Lizarbe, M. A. (2001) Cytotoxic mechanism of the ribotoxin α-sarcin. Induction of cell death via apoptosis. Eur. J. Biochem. 268, 2113-2123
31. Smith, P., Fallon, R. E., Mangan, N. E., Walsh, C. M., Saraiva, M., Sayers, J. R., McKenzie, A. N., Alcami, A., and Fallon, P. G. (2005) Schistosoma mansoni secretes a chemokine binding protein with antiinflammatory activity. J. Exp. Med. 202, 1319-1325
32. Williams, D. L., Asahi, H., Oke, T. T., da Rosa, J. L., and Stadecker, M. J. (2005) Murine immune responses to a novel schistosome egg antigen, SmEP25. Int. J. Parasitol. 35, 875-882
33. Jenkins, S. J., and Mountford, A. P. (2005) Dendritic cells activated with products released by schistosome larvae drive Th2-type immune responses, which can be inhibited by manipulation of CD40 costimulation. Infect. Immun. 73, 395-402
34. Jenkins, S. J., Hewitson, J. P., Ferret-Bernard, S., and Mountford, A. P. (2005) Schistosome larvae stimulate macrophage cytokine production through TLR4-dependent and -independent pathways. Int. Immunot. 17, 1409-1418
35. Asojo, O. A., Goud, G., Dhar, K., Loukas, A., Zhan, B., Deumic, V., Liu, S., Borgstahl, G. E., and Hotez, P. J. (2005) X-ray structure of Na-ASP-2, a pathogenesis-related-1 protein from the nematode parasite, Necator americanus, and a vaccine antigen for human hookworm infection. J. MoL Biol. 346, 801-814
36. Okano, M., Satoskar, A. R., Nishizaki, K., Abe, M., and Harn, D. A., Jr. (1999) Induction of Th2 responses and IgE is largely due to carbohydrates functioning as adjuvants on Schistosoma mansoni egg antigens. J. Immunol. 163, 6712-6717
37. Okano, M., Satoskar, A. R., Nishizaki, K., and Ham, D. A., Jr. (2001) Lacto-N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response. J. Immunol. 167, 442-450
38. Thomas, P. G., Carter, M. R., Atochina, O., Da'Dara, A. A., Piskorska, D., McGuire, E., and Harn, D. A. (2003) Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J. Immunol. 171, 5837-5841
39. van Die, I., van Vliet, S. J., Nyame, A. K., Cummings, R. D., Bank, C. M., Appelmelk, B., Geijtenbeek, T. B., and van Kooyk, Y. (2003) 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 13, 471-478
40. 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. (1996) Schistosoma mansoni excretory circulating cathodic antigen shares Lewis-x epitopes with a human granulocyte surface antigen and evokes host antibodies mediating complement-dependent lysis of granulocytes. Blood 88, 4246-4251
41. Borojevic, R., Santos-da-Silva, C., and Carvalho, E. A. (1983) Chronic schistosomiasis mansoni: splenic myelopoiesis and inhibition of neutrophil granulocytopoiesis mediated by the sera of patients. J. Infect. Dis. 148, 422-426
42. 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 Infect. 6, 1125-1132
43. Spooncer, E., Fukuda, M., Klock, J. C., Oates, J. E., and Dell, A. (1984) Isolation and characterization of polyfucosylated lactosaminoglycan from human granulocytes. J. Biol. Chem. 259, 4792-4801
44. 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 GaINAβ1-4(Fucα1-2Fucα1-3)GIcNAc. J. Infect. Dis. 185, 531-539
45. 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., and van Die, I. (2004) LaccliNAc-glycans constitute a parasite pattern for galectin-3-mediated immune recognition. J. Immunol. 173, 1902-1907
46. van Vliet, S. J., van Liempt, E., Saeland, E., Aamoudse, C. A., Appelmelk, B., Irimura, T., Geijtenbeek, T. B., Blixt, O., Alvarez, R., van Die, I., and van Kooyk, Y. (2005) Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. Int. Immunol. 17, 661-669
47. Harn, D. A., Cianci, C. M., and Caulfield, J. P. (1989) Schistosoma mansoni: immunization with cercarial glycocalyx preparation increases the adult worm burden. Exp. Parasitol. 68, 108-110
48. Garcia-Casado, G., Sanchez-Monge, R., Chrispeels, M. J., Armentia, A., Salcedo, G., and Gomez, L. (1996) Role of complex asparagine-linked glycans in the allergenicity of plant glycoproteins. Glycobiology 6, 471-477
49. Kubelka, V., Altmann, F., Staudacher, E., Tretter, V., Marz, L., Hard, K., Kamerling, J. P., and Vlegenthart, J. F. (1993) Primary structures of the N-linked carbohydrate chains from honeybee venom phospholipase A2. Eur. J. Biochem. 213, 1193-1204
50. 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 α3-fucose and core β2-xylose epitopes are strong inducers of Th2 responses in mice. Eur. J. Immunol. 33, 1271-1281
51. Tretter, V., Altmann, F., Kubelka, V., Marz, L., and Becker, W. M. (1993) Fucose α1,3-linked to the core region of glycoprotein N-glycans creates an important epitope for IgE from honeybee venom allergic individuals. Int. Arch. Allergy Immunol. 102, 259-266
52. van Die, I., Gomord, V., Kooyman, F. N., van den Berg, T. K., Cummings, R. D., and Vervelde, L. (1999) Core α1 →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 Lett. 463, 189-193
53. Weber, A., Schroder, H., Thalberg, K., and Marz, L. (1987) Specific interaction of IgE antibodies with a carbohydrate epitope of honey bee venom phospholipase A2. Allergy 42, 464-470
54. Doenhoff, M. J., Hassounah, O., Murare, H., Bain, J., and Lucas, S. (1986) The schistosome egg granuloma: immunopathology in the cause of host protection or parasite survival? Trans. R. Soc. Trop. Med. Hyg. 80, 503-514
55. Karania, D. M., Colley, D. G., Nahlen, B. L., Ourna, J. H., and Secor, W. E. (1997) Studies on schistosomiass in western Kenya: I. Evidence for immune-facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. Am. J. Trop. Med. Hyg. 56, 515-521
56. Handel, T. M., Johnson, Z., Crown, S. E., Lau, E. K., and Proudfoot, A. E. (2005) Regulation of protein function by glycosaminoglycans - as exemplified by chemokines. Annu. Rev. Biochem. 74, 385-410
57. Dessein, A., Samuelson, J. C., Butterworth, A. E., Hogan, M., Sherry, B. A., Vadas, M. A., and David, J. R. (1981) Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules. Parasitology 82, 357-374