Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-30T23:35:00.991Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of glycosylation of antigens on the antibody responses against Echinostoma caproni (Trematoda: Echinostomatidae)

Published online by Cambridge University Press:  14 May 2014

JAVIER SOTILLO ,
ALBA CORTÉS ,
CARLA MUÑOZ-ANTOLI ,
BERNARD FRIED ,
J. GUILLERMO ESTEBAN  and
RAFAEL TOLEDO
JAVIER SOTILLO*
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot – Valencia, Spain
ALBA CORTÉS
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot – Valencia, Spain
CARLA MUÑOZ-ANTOLI
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot – Valencia, Spain
BERNARD FRIED
Affiliation:
Department of Biology, Lafayette College, Easton, Pennsylvania 18042, USA
J. GUILLERMO ESTEBAN
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot – Valencia, Spain
RAFAEL TOLEDO
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100 Burjassot – Valencia, Spain
*
*Corresponding author: Present address: Centre for Biodiscovery and Molecular Development of Therapeutics, Building E4, James Cook University, McGregor Rd, Smithfield, QLD 4878, Australia. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In the present study, we analyse the effect of glycosylation in Echinostoma caproni (Trematoda: Echinostomatidae) antigens in antibody responses against the parasite in experimentally infected mice. It has been previously demonstrated that the mouse is a host of high compatibility with E. caproni and develops elevated responses of IgG, IgG1, IgG3 and IgM as a consequence of the infection, though the role of glycans in these responses remains unknown. To this purpose, the responses generated in mice against non-treated excretory/secretory antigens of E. caproni were compared with those observed after N-deglycosylation, O-deglycosylation and double deglycosylation of the antigens by indirect ELISA and western blot. Our results suggest that E. caproni-expressed glycans play a major role in the modulation of the immune responses. The results obtained indicate that IgG subclass responses generated in mice against E. caproni are essentially due to glycoproteins and may affect the Th1/Th2 biasing. The reactivity significantly decreased after any of the deglycosylation treatments and the N-glycans appears to be of greater importance than O-glycans. Interestingly, the IgM response increased after N-deglycosylation suggesting that carbohydrates may mask peptide antigens.

Keywords

TrematodaEchinostoma capronimousedeglycosylationglycoproteincarbohydratesimmunoglobulinwestern blot
Type
Research Article
Information
Parasitology , Volume 141 , Issue 10 , September 2014 , pp. 1333 - 1340
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Agger, M. K., Simonsen, P. E. and Vennervald, B. J. (1993). The antibody response in serum, intestinal wall and intestinal lumen of NMRI mice infected with Echinostoma caproni . Journal of Helminthology 67, 169–178.Google Scholar
Andresen, K., Simonsen, P. E., Andersen, B. J. and Birch-Andersen, A. (1989). Echinostoma caproni in mice: shedding of antigens from the surface of an intestinal trematode. International Journal for Parasitology 19, 111–118.Google Scholar
Brunet, L. R., Joseph, S., Dunne, D. W. and Fried, B. (2000). Immune responses during the acute stages of infection with the intestinal trematode Echinostoma caproni . Parasitology 120, 565–571.Google Scholar
Cummings, R. D. and Nyame, A. K. (1996). Glycobiology of schistosomiasis. FASEB Journal 10, 838–848.Google Scholar
Cummings, R. D. and Nyame, A. K. (1999). Schistosome glysoconjugates. Biochimica et Biophysica Acta 1455, 363–374.Google Scholar
Dea-Ayuela, M. A., Martinez-Fernandez, A. R. and Bolas-Fernandez, F. (2000). Comparison of IgG3 responses to carbohydrates following mouse infection or immunization with six species of Trichinella . Journal of Helminthology 74, 215–223.Google Scholar
Dell, A., Haslam, S. M., Morris, H. R. and Khoo, K. H. (1999). Immunogenic glycoconjugates implicated in parasitic nematode diseases. Biochimica et Biophysica Acta 1455, 353–362.Google Scholar
Drabek, D., Raguz, S., De Wit, T. P., Dingjan, G. M., Savelkoul, H. F., Grosveld, F. and Hendriks, R. W. (1997). Correction of the X-linked immunodeficiency phenotype by transgenic expression of human Bruton tyrosine kinase under the control of the class II major histocompatibility complex Ea locus control region. Proceedings of the National Academy of Sciences USA 94, 610–615.CrossRefGoogle ScholarPubMed
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, 1238–1247.CrossRefGoogle ScholarPubMed
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, 1271–1281.Google Scholar
Fried, B. and Huffman, J. E. (1996). The biology of the intestinal trematode Echinostoma caproni . Advances in Parasitology 38, 311–368.Google Scholar
Fried, B., Graczyk, T. K. and Tamang, L. (2004). Food-borne intestinal trematodiases in humans. Parasitology Research 93, 159–170.CrossRefGoogle ScholarPubMed
Fujino, T. and Fried, B. (1993). Expulsion of Echinostoma trivolvis (Cort, 1914) Kanev, 1985 and retention of E. caproni Richard, 1964 (Trematoda: Echinostomatidae) in C3H mice: pathological, ultrastructural, and cytochemical effects on the host intestine. Parasitology Research 79, 286–292.Google Scholar
Graczyk, T. K. (2000). Immunobiology and immunodiagnosis of echinostomes. In Echinostomes as Experimental Models for Biological Research (ed. Fried, B. and Graczyk, T.), pp. 229–244. Kluwer Academic Publishers, Dordrecht, the Netherlands.Google Scholar
Harn, D. A., McDonald, J., Atochina, O. and Da'dara, A. A. (2009). Modulation of host immune responses by helminth glycans. Immunological Reviews 230, 247–257.Google Scholar
Haslam, S. M., Restrepo, B. I., Obregon-Henao, A., Teale, J. M., Morris, H. R. and Dell, A. (2003). Structural characterization of the N-linked glycans from Taenia solium metacestodes. Molecular and Biochemical Parasitology 126, 103–107.Google Scholar
Hillyer, G. V. and Soler de Galanes, M. (1988). Identification of a 17-kDa Fasciola hepatica immunodiagnostic antigen by the enzyme linked immunoelectrotransfer blot technique. Journal of Clinical Microbiology 26, 2048–2053.CrossRefGoogle ScholarPubMed
Hokke, C. H. and Deelder, A. M. (2001). Schistosome glycoconjugates in host-parasite interplay. Glycoconjugate Journal 18, 573–587.Google Scholar
Hokke, C. H., Deelder, A. M., Hoffmann, K. F. and Wuhrer, M. (2007). Glycomics-driven discoveries in schistosome research. Experimental Parasitology 117, 275–283.Google Scholar
Maizels, R. M., Bundy, D. A., Selkirk, M. E., Smith, D. F. and Anderson, R. M. (1993). Immunological modulation and evasion by helminth parasites in human populations. Nature 365, 797–805.Google Scholar
Norden, A. P. and Strand, M. (1985). Identification of antigenic Schistosoma mansoni glycoproteins during the course of infection in mice and humans. American Journal of Tropical Medicine and Hygiene 34, 495–507.CrossRefGoogle ScholarPubMed
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, 1–13.Google Scholar
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, 182–200.Google Scholar
Perrigoue, J. G., Marshall, F. A. and Artis, D. (2008). On the hunt for helminths: innate immune cells in the recognition and response to helminth parasites. Cellular Microbiology 10, 1757–1764.Google Scholar
Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York, NY, USA.Google Scholar
Simonsen, P. E. and Andersen, B. J. (1986). Echinostoma revolutum in mice; dynamics of the antibody attack to the surface of an intestinal trematode. International Journal for Parasitology 16, 475–482.Google Scholar
Snapper, C. M., McIntyre, T. M., Mandler, R., Pecanha, L. M., Finkelman, F. D., Lees, A. and Mond, J. J. (1992). Induction of IgG3 secretion by interferon gamma: a model for T cell-independent class switching in response to T cell-independent type 2 antigens. Journal of Experimental Medicine 175, 1367–1371.CrossRefGoogle Scholar
Sotillo, J., Munoz-Antoli, C., Marcilla, A., Fried, B., Guillermo Esteban, J. and Toledo, R. (2007). Echinostoma caproni: kinetics of IgM, IgA and IgG subclasses in the serum and intestine of experimentally infected rats and mice. Experimental Parasitology 116, 390–398.CrossRefGoogle ScholarPubMed
Sotillo, J., Valero, L., Sanchez Del Pino, M. M., Fried, B., Esteban, J. G., Marcilla, A. and Toledo, R. (2008). Identification of antigenic proteins from Echinostoma caproni (Trematoda) recognized by mouse immunoglobulins M, A and G using an immunoproteomic approach. Parasite Immunology 30, 271–279.Google Scholar
Sotillo, J., Trelis, M., Cortes, A., Fried, B., Marcilla, A., Esteban, J. G. and Toledo, R. (2011). Th17 responses in Echinostoma caproni infections in hosts of high and low compatibility. Experimental Parasitology 129, 307–311.Google Scholar
Talabnin, K., Aoki, K., Saichua, P., Wongkham, S., Kaewkes, S., Boons, G. J., Sripa, B. and Tiemeyer, M. (2013). Stage-specific expression and antigenicity of glycoprotein glycans isolated from the human liver fluke, Opisthorchis viverrini . International Journal for Parasitology 43, 37–50.Google Scholar
Tawill, S., Le Goff, L., Ali, F., Blaxter, M. and Allen, J. E. (2004). Both free-living and parasitic nematodes induce a characteristic Th2 response that is dependent on the presence of intact glycans. Infection and Immunity 72, 398–407.Google Scholar
Thomas, P. G. and Harn, D. A. Jr. (2004). Immune biasing by helminth glycans. Cellular Microbiology 6, 13–22. doi: 10.1046/j.1462-5822.2003.00337.x.Google Scholar
Toledo, R. (2009). Echinostomes in the definitive host: a model for the study of host-parasite relationships. In The Biology of Echinostomes. From the Molecule to the Community (ed. Fried, B. and Toledo, R.), pp. 89–109. Springer, New York, NY, USA.Google Scholar
Toledo, R. and Fried, B. (2005). Echinostomes as experimental models for interactions between adult parasites and vertebrate hosts. Trends in Parasitology 21, 251–254.Google Scholar
Toledo, R., Espert, A. M., Munoz-Antoli, C., Marcilla, A., Fried, B. and Esteban, J. G. (2003). Development of an antibody-based capture enzyme-linked immunosorbent assay for detecting Echinostoma caproni (Trematoda) in experimentally infected rats: kinetics of coproantigen excretion. Journal of Parasitology 89, 1227–1231.Google Scholar
Trelis, M., Sotillo, J., Monteagudo, C., Fried, B., Marcilla, A., Esteban, J. G. and Toledo, R. (2011). Echinostoma caproni (Trematoda): differential in vivo cytokine responses in high and low compatible hosts. Experimental Parasitology 127, 387–397.Google Scholar
Tundup, S., Srivastava, L. and Harn, D. A. Jr. (2012). Polarization of host immune responses by helminth-expressed glycans. Annals of the New York Academy of Sciences 1253, E1–E13.Google Scholar
van Diepen, A., Van der Velden, N. S., Smit, C. H., Meevissen, M. H. and Hokke, C. H. (2012). Parasite glycans and antibody-mediated immune responses in Schistosoma infection. Parasitology 139, 1219–1230.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Sotillo Supplementary Material

Figure 1

Download Sotillo Supplementary Material(Image)
Image 2.9 MB