Antibody and cytokine responses in BALB/c mice immunized with the excreted/secreted proteins of Giardia intestinalis: The role of cysteine proteases

Annals of Tropical Medicine and Parasitology

Volumn 103, Issue 8, 2009, Pages 693-703

  Jimenez, J C ^a,b   Fontaine, J ^a   Grzych, J M ^c   Capron, M ^a   Dei Cas, E ^a,c  

^a INSTITUT PASTEUR DE LILLE   (France)

^b UNIVERSIDAD CENTRAL DE VENEZUELA   (Venezuela)

^c LILLE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CYSTEINE PROTEINASE; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 5; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY DETECTION; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME INHIBITION; FEMALE; GIARDIA LAMBLIA; HEAT TREATMENT; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOREGULATION; MOUSE; NONHUMAN; PROTEIN SECRETION; PROTEIN SYNTHESIS; SPLEEN CELL; ZYMOGRAPHY;

ANIMALS; ANTIBODIES, PROTOZOAN; CELL PROLIFERATION; CELLS, CULTURED; CYSTEINE PROTEASES; CYTOKINES; GIARDIA LAMBLIA; GIARDIASIS; IMMUNOGLOBULINS; INTERFERON-GAMMA; INTERLEUKINS; MICE; MICE, INBRED BALB C; PROTOZOAN PROTEINS; SPLEEN; TH1 CELLS; TH2 CELLS;

GIARDIA INTESTINALIS; MURINAE; MUS;

EID: 77949475927     PISSN: 00034983     EISSN: 13648594     Source Type: Journal    
DOI: 10.1179/000349809X12502035776351     Document Type: Article

References (39)

1. Adam, R. D. (2001). Biology of Giardia lamblia. Clinical Microbiology Reviews, 14, 447-475.
2. Buxbaum, L. U., Denise, H., Coombs, G. H., Alexander, J., Mottram, J. C. & Scott, P. (2003). Cysteine protease B of Leishmania mexicana inhibits host Th1 responses and protective immunity. Journal of Immunology, 171, 3711-3717.
3. Chambers, L., Brown, A., Pritchard, D. I., Sreedharan, S., Brocklehurst, K. & Kalsheker, N. A. (1998). Enzymatically active papain preferentially induces an allergic response in mice. Biochemical and Biophysical Research Communications, 253, 837-840.
4. Comoy, E. E., Pestel, J., Duez, C., Stewart, G. A., Vendeville, C., Fournier, C., Finkelman, F. D., Capron, A. & Thyphronitis ,G. (1998). The house dust mite allergen, Dermatophagoides pteronyssinus, promotes type 2 responses by modulating the balance between IL-4 and IFN-γ. Journal of Immunology, 160, 2456-2462.
5. Denise, H., McNeil, K., Brooks, D. R., Alexander, J., Coombs, G. H. & Mottram, J. C. (2003). Expression of multiple CPB genes encoding cysteine proteases is required for Leishmania mexicana virulence in vivo. Infection and Immunity, 71, 3190-3195.
6. Dirgahayu, P., Fukumoto, S., Miura, K. & Hirai, K. (2002). Excretory/secretory products from plerocercoids of Spirometra erinaceieuropaei suppress the TNF-alpha gene expression by reducing phosphorylation of ERK1/2 and p38 MAPK in macrophages. International Journal for Parasitology, 32, 1155-1162.
7. Djamiatun, K. & Faubert, G. M. (1998). Exogenous cytokines released by spleen and Peyer's patch cells removed from mice infected with Giardia muris. Parasite Immunology, 20, 27-36.
8. Eckerman, L. (2003). Mucosal defences against Giardia. Parasite Immunology, 25, 259-270.
9. Faubert, G. (2000). Immune response to Giardia duodenalis. Clinical Microbiology Reviews, 13, 35-54.
10. Geldhof, P., Claerebout, E., Knox, D., Vercauteren, L., Looszova, A. & Vercruysse, J. (2002). Vaccination of calves against Ostertagia ostergati with cysteine proteinase enriched protein fractions. Parasite Immunology, 24, 263-270.
11. Gough, L., Schulz, O., Sewell, H. F. & Shakib, F. (1999). The cysteine protease activity of the major dust mite allergen Der p 1 selectively enhances the immunoglobulin E antibody response. Journal of Experimental Medicine, 190, 1897-1901.
12. Guy, R. A., Bertrand, S. & Faubert, G. M. (1991). Modification of RPMI-1640 for use in vitro immunological studies of host-parasite interaction in giardiasis. Journal of Clinical Microbiology, 29, 627-629.
13. Hare, D. F., Jarroll, E. L. & Lindmark, D. G. (1989). Giardia lamblia: characterization of proteinase activity in trophozoites. Experimental Parasitology, 68, 168-175.
14. Hellberg, A., Nickel, R., Lotter, H., Tannich, E. & Bruchhaus, I. (2001). Overexpression of cysteine proteinase 2 in Entamoeba histolytica or Entamoeba dispar increases amoeba-induced monolayer destruction in vitro but does not augment amoebic liver abscess formation in gerbils. Cellular Microbiology, 3, 13-20.
15. Heussen, C. & Dowdle, E. B. (1980). Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Analytical Biochemistry, 102, 196-202.
16. Hewit, C. R. A., Brwon, A. P., Hart, B. J. & Pritchard, D. I. (1995). A major house dust mite allergen disrupts the immunoglobulin E network by selectively cleaving CD23: innate protection by antiprotease. Journal of Experimental Medicine, 182, 1537-1544.
17. Holland, M. J., Marcus, Y. M., Riches, P. L. & Maizels, R. M. (2000). Proteins secreted by the parasitic nematode Nippostrongylus brasiliensis act as adjuvants for Th2 responses. European Journal of Immunology, 30, 1977-1987.
18. Jimenez, J. C., Uzcanga, G., Zambrano, A., Di Prisco, M. C. & Lynch, N. R. (2000). Identification and partial characterization of excretory/secretory products with proteolytic activity in Giardia intestinalis. Journal of Parasitology, 86, 859-862.
19. Jimenez, J. C., Fontaine, J., Grzych, J.-M., Dei-Cas, E. & Capron, M. (2004). Systemic and mucosal response to oral administration of excretory/secretory antigens from Giardia intestinalis. Clinical and Diagnostic Laboratory Immunology, 11, 152-160.
20. Kaur, H., Samra, H., Ghosh, S., Vinayak, V. K. & Ganguly, N. K. (1999). Immune effector responses to an excretory-secretory product of Giardia lamblia. FEMS Immunology and Medical Microbiology, 23, 93-105.
21. Keister, D. B. (1983). Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Transactions of the Royal Society of Tropical Medicine and Hygiene, 77, 478-488.
22. Klemba, M. & Goldberg, D. E. (2002). Biological roles of proteases in parasitic protozoa. Annual Review of Biochemistry, 71, 275-305.
23. Larocque, R., Nakagaki, K., Lee, P., Abdul-Wahid, A. & Faubert ,G. M. (2003). Oral immunization of BALB/c mice with Giardia duodenalis recombinant cyst wall protein inhibits shedding of cysts. Infection and Immunity, 71, 5662-5669.
24. Lauwaet, T., Oliveira, M. J., Callewaert, B., de Bruyne, G., Saelens, X., Ankri, S., Vandenabeele, P., Mirelman, D., Mareel, M. & Leroy, A. (2003). Proteolysis of enteric cell villin by Entamoeba histolytica cysteine proteinases. Journal of Biological Chemistry, 278, 22,650-22,656.
25. Nash, T. E. & Gillin, F. D. (1983). Excretory-secretory products of Giardia lamblia. Journal of Immunology, 131, 2004-2010.
26. North, M. J., Moltram, J. C. & Coombs, G. H. (1990). Cysteine proteinases in protozoan parasites. Parasitology Today, 6, 270-275.
27. Pollock, K. G., McNeil, K. S., Mottram, J. C., Lyons, R. E., Brewer, J. M., Scott, P., Coombs, G. H. & Alexander, J. (2003). The Leishmania mexicana cysteine protease, CPB2.8, induce potent Th2 responses. Journal of Immunology, 170, 1746-1753.
28. Sajid, M. & McKerrow, J. H. (2002). Cysteine proteases of parasitic organisms. Molecular and Biochemical Parasitology, 120, 1-21.
29. Schramm, G., Falcone, F. H., Gronow, A., Haisch, K., Mamat, U., Doenhoff, M. J., Oliveira, G., Galle, J., Dahinden, C. A. & Haas, H. (2003). Molecular characterization of an interleukin-4-inducing factor from Schistosoma mansoni eggs. Journal of Biological Chemistry, 278, 18,384-18,392.
30. Shakib, F. & Gough, L. (2000). The proteolytic activity of Der p 1 selectively enhances IgE synthesis: a link between allergenicity and cysteine protease activity. Clinical and Experimental Allergy, 30, 751-752.
31. Shin, M. H., Kita, H., Park, H. Y. & Seoh, J. Y. (2001). Cysteine protease secreted by Paragonimus westermani attenuates effector functions of human eosinophils stimulated with immunoglobulin G. Infection and Immunity, 69, 1599-1604.
32. Singer, S. M. & Nash, T. E. (2000). T-cell-dependent control of acute Giardia lamblia infections in mice. Infection and Immunity, 68, 170-175.
33. Thirion, J., Wattiaux, R. & Jadot, M. (2003). The acid phosphatase positive organelles of the Giardia lamblia trophozoites contain a membrane bound cathepsin C activity. Biology of the Cell, 95, 99-105.
34. Touz, M. C., Nores, M. J., Slavin, I., Carmona, C., Conrad, J. T., Mowatt, M. R., Nash, T. E., Coronel, C. E. & Luján, H. D. (2001). The activity of a developmentally regulated cysteine proteinase is required for cyst wall formation in the primitive eukaryote. Journal of Biological Chemistry, 277, 8474-8481.
35. Venkatesan, P., Finch, R. G. & Wakelin, D. (1996). Comparison of antibody and cytokine responses to primary Giardia muris infection in H-2 congenic strains of mice. Infection and Immunity, 64, 4525-4533.
36. Ward, W., Alvarado, L., Rawlings, N. D., Engel, J. C., Franklin, C. & McKerrow, J. H. (1997). A primitive enzyme for a primitive cell: the protease required for excystation of Giardia. Cell, 89, 437-444.
37. Werries, E., Franz, A., Hippe, H. & Acil, Y. (1991). Purification and substrate specificity of two cysteine proteinases of Giardia lamblia. Journal of Protozoology, 38, 378-383.
38. Williams, A. G. & Coombs, G. H. (1995). Multiple protease activities in Giardia intestinalis trophozoites. International Journal for Parasitology, 25, 771-778.
39. Zhang, Z., Wang, L., Seydel, K. B., Li, E., Ankri, S., Mirelman, D. & Stanley Jr, S. L. (2000). Entamoeba histolytica cysteine proteinases with interleukin-1 beta converting enzyme (ICE) activity cause intestinal inflammation and tissue damage in amoebiasis. Molecular Microbiology, 37, 542-548.