Skip to main content
SpringerLink
Log in

Excreted/secreted glycoproteins of G. intestinalis play an essential role in the antibody response

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

In the present work, glycoproteins in the excretory/secretory products of G. intestinalis were identified and the reactivity in serum of immunized mice with these molecules was evaluated by western blotting before and after chemical treatment or enzymatic deglycosylation. Glycoproteins of 58 and 63 kDa were revealed in E/S products after periodic acid-Schiff (PAS) stain. Studies of carbohydrate specificity using digoxigenin-labeled lectins, revealed the presence of O-glycans and N-glycans. Chemical treatment of excretory/secretory products with sodium meta-periodate or enzymatic deglycosylation with N-glycosidase F reduced the reactivity in serum for proteins of 36, 58 and 63 kDa, respectively. These results show the presence of glycoproteins in E/S products of G. intestinalis and suggest that the antibody response is directed against glycoepitopes. The expression of carbohydrate moieties in the E/S-G. intestinalis may play an essential role in the antibody response and may be a target for serodiagnosis or immune intervention in human giardiasis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adam RD (2001) The biology of Giardia lamblia. Clin Microbiol Rev 14:447–475

    Article  PubMed  CAS  Google Scholar 

  • Céu Sousa M, Gonçalves CA, Bairos VA, Poires-da-Silva J (2001) Adherence of Giardia lamblia trophozoites to INT-407 human intestinal cells. Clin Diagn Lab Immunol 8:258–265

    Article  Google Scholar 

  • Flanagan PA (1992) Giardia-diagnosis, clinical course and epidemiology: a review. Epidemiol Infect 109:1–22

    PubMed  CAS  Google Scholar 

  • Guimaraes S, Sogayar MI, Franco M (2003) Analysis of proteins from membrane and soluble fractions of Giardia duodenalis trophozoites of two Brazilian axenic strains. Rev Inst Med Trop Sao Paulo 44:239–244

    Google Scholar 

  • Guha-Niyogi A, Sullivan DR, Turco SJ (2001) Glycoconjugate structures of parasitic protozoa. Glycobiology 11:45R–59R

    Article  PubMed  CAS  Google Scholar 

  • Guy RA, Bertrand S, Faubert GM (1991) Modification of RPMI-1640 for use in vitro immunological studies of host-parasite interaction in giardiasis. J Clin Microbiol 29:627–629

    PubMed  CAS  Google Scholar 

  • Hiltpold A, Frey M, Hulsmeier A, Köhler P (2000) Glycosylation and palmitoylation are common modifications of Giardia variant surface proteins. Mol Biochem Parasitol 109:61–65

    Article  PubMed  CAS  Google Scholar 

  • Jarvis LM, Pritchard DI (1992) An evaluation of the role of carbohydrate epitopes in immunity to Trichinella spiralis. Parasite Immunol 14:489–501

    PubMed  CAS  Google Scholar 

  • Jimenez JC, Fontaine J, Grzych JM, Dei-Cas E, Capron M (2004) Systemic and mucosal responses to oral administration of excretory/secretory (E-S) antigens from Giardia intestinalis. Clin Diagn Lab Immunol 11:152–160

    Article  PubMed  Google Scholar 

  • Karr CD, Jarroll EL (2004) Cyst wall synthase: N-acetylgalactosaminyltransferase activity is induced to form the novel N-acetylgalactosamine polysaccharide in the Giardia cyst wall. Microbiology 150(Pt 5):1237–1243

    Article  PubMed  CAS  Google Scholar 

  • Kaur H, Ghosh S, Samra H, Vinayak VK, Ganguly NK (2001) Identification and characterization of an excretory-secretory product from Giardia lamblia. Parasitology 123(Pt 4):347–356

    Article  PubMed  CAS  Google Scholar 

  • Kaur H, Samra H, Ghosh S, Vinayak V, Ganguly NK (1999) Immune effector response to an excretory-secretory product of Giardia lamblia. FEMS Immunol Med Microbiol 23:93–105

    Article  PubMed  CAS  Google Scholar 

  • Keister DB (1983) Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 77:487–488

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Lloyd D, Ralphs JR, Harris JC (2002) Giardia intestinalis, a eukaryote without hydrogenosomes, produces hydrogen. Microbiology 148(Pt 3):727–733

    PubMed  CAS  Google Scholar 

  • Magne D, Favennec L, Chochillon C (1991) Role of cytoskeleton and surface lectins in Giardia duodenalis attachment to Caco2 cells. Parasitol Res 77:659–662

    Article  PubMed  CAS  Google Scholar 

  • Moncada DC, Kammanadiminti SJ, Chadee K (2003) Mucin and Toll-like receptors in host defence against intestinal parasites. Trends Parasitol 19:305–310

    Article  PubMed  CAS  Google Scholar 

  • Morelle W, Jimenez JC, Cienieski-Bernard C, Dei-Cas E, Michalski J.-C (2005) Characterization of the N-linked glycans of Giardia intestinalis. Glycobiology 15:549–559

    Article  PubMed  CAS  Google Scholar 

  • Nash TE, Gillin FD, Smith PD (1983) Excretory-secretory products of Giardia lamblia. J Immunol 131:2004–2010

    PubMed  CAS  Google Scholar 

  • Ortega-Barria E, Ward HD, Evans JE, Pereira ME (1990) N-acetyl-d-glucosamine is present in cysts and trophozoites of Giardia lamblia and serves as receptor for wheatgerm agglutinin. Mol Biochem Parasitol 43:151–165

    Article  PubMed  CAS  Google Scholar 

  • Paget TA, James SL (1994) The mucolytic activity of polyamines and mucosal invasion. Biochem Soc Trans 22:394S

    PubMed  CAS  Google Scholar 

  • Papanastasiou P, Mc Conville MJ, Ralton J, Köhler P (1997) The variant-specific surface protein of Giardia, VSP4A1, is a glycosylated and palmitoylated protein. Biochem J 322:49–56

    Google Scholar 

  • Pegado MGF, de Souza W (1994) Role of the surface components in the process of interaction of Giardia duodenalis with epithelial cells in vitro. Parasitol Res 80:320–326

    Article  PubMed  CAS  Google Scholar 

  • Schalling Henk DFH, van Leeuwen AW (1996) Carbohydrate epitopes on Haemonchus contotrtus antigens. Parasitol Res 82:38–42

    Article  Google Scholar 

  • Towbin H, Staehlin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Nat Acad Sci USA 76:4350–4354

    Article  PubMed  CAS  Google Scholar 

  • Ward HD, Lev BI, Kane AV, Keusch GT, Pereira ME (1987) Identification and characterization of taglin, a mannose 6-phosphate binding, trypsin-activated lectin from Giardia lamblia. Biochemistry 29:8669–8675

    Article  Google Scholar 

  • Ward HD, Alray J, Lev BI, Keusch GT, Pereira ME (1988) Biology of Giardia lamblia. Detection of N-acetyl-d-glucosamine as the only surface saccharide moiety and identification of two distinct subsets of the trophozoites by lectin binding. J Exp Med 167:73–88

    Article  PubMed  CAS  Google Scholar 

  • Woodward M, Young W Jr, Bloogood R (1985) Detection of monoclonal antibodies specific for carbohydrate epitopes using periodate oxidation. J Immunol Methods 78:143–153

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was developed in the framework of collaboration between ECOPA (EA-3609—Lille-2 University) groups at the Institute Pasteur of Lille (IFR-17) and UMR 8576 Laboratory of Structural and Functional Glycobiology (CNRS and University of Lille 1), France. Juan C. Jiménez was supported by a fellowship from “Fondo Nacional de Ciencia, Tecnología” e Innovación (FONACIT) and “Consejo de Desarrollo Científico y Humanístico” (Universidad Central de Venezuela). We thank Dr. Marian Ulrich for her critical revision and correction on the manuscript.

Author information

Authors and Affiliations

  1. Laboratory of Immunopathology, Institute of Biomedicine, Faculty of Medicine, Central University of Venezuela, Caracas, Venezuela

    J. C. Jiménez

  2. UMR 8576 Laboratory of Structural and Functional Glycobiology (CNRS and University of Lille 1), Lille, France

    W. Morelle & J-C. Michalsky

  3. Ecology of Parasitism Group EA-3609 CHU Hôpital Universitaire de Lille, Institut Fédératif de Recherche No. 17, Institut Pasteur of Lille, Lille, France

    J. C. Jiménez & E. Dei-Cas

Authors
  1. J. C. Jiménez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. Morelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J-C. Michalsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Dei-Cas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. C. Jiménez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiménez, J.C., Morelle, W., Michalsky, JC. et al. Excreted/secreted glycoproteins of G. intestinalis play an essential role in the antibody response. Parasitol Res 100, 715–720 (2007). https://doi.org/10.1007/s00436-006-0339-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-006-0339-0

Keywords

Search

Navigation