Hostname: page-component-84b7d79bbc-2l2gl Total loading time: 0 Render date: 2024-07-31T09:14:04.167Z Has data issue: false hasContentIssue false

Cleavage of immunoglobulin G by excretory–secretory cathepsin S-like protease of Spirometra mansoni plerocercoid

Published online by Cambridge University Press:  06 April 2009

Y. Kong
Affiliation:
Department of Parasitology, College of Medicine, Chung-Ang University, Seoul 156-756, Korea
Y.-B. Chung
Affiliation:
Department of Parasitology, College of Medicine, Chung-Ang University, Seoul 156-756, Korea
S.-Y. Cho
Affiliation:
Department of Parasitology, College of Medicine, Chung-Ang University, Seoul 156-756, Korea
S.-Y. Kang
Affiliation:
Department of Parasitology, College of Medicine, Chung-Ang University, Seoul 156-756, Korea

Extract

When immunoglobulin G (IgG) was incubated with Spirometra mansoni plerocercoid (sparganum), it was cleaved into Fab and Fc fragments. Fab/c fragments were also hydrolysed. The digestion was accelerated by dithiothreitol (DTT), indicating that cleavage of IgG heavy chain was due to a cysteine protease secreted into the medium. The responsible enzyme, of Mr 27 (± 0·8) kDa, was purified by a series of thiopropyl affinity, Sephacryl S-300 HR and DEAE-anion exchange chromatographies, either from worm extracts or from excretory–secretory products (ESP). The purified, thiol-dependent protease showed an optimal activity at pH 5·7 with 0·1 M sodium acetate but was active over the pH range 4·5–8·0. Its activity was inhibited completely by 10−5 M L-trans-epoxysuccinylleucylamido(4-guanidino) butane (E-64) and 1 mM iodoacetamide (IAA), but by only 53% using the specific cathepsin L inhibitor, Z-Phe-Phe-CHN2 (5 × 10−5 M). Partial NH2-terminal amino acid sequence was Leu-Pro-Asp-Ser-Val-Asn-Trp-Arg-Glu-Gly-Ala-Val-Thr-Ala-Val which showed 80% homology to human cathepsin S. Immunoblot analysis showed that sera from infected patients exhibited IgE antibody reaction. It is proposed that cleavage of immunoglobulin by an excreted–secreted, cathepsin S-like, allergenic protease is a mechanism of immune evasion used by the sparganum.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1994

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

Auriault, C., Joseph, M., Dessaint, J. P. & Capron, A. (1980). Interaction of rat macrophage resulting from cleavage of IgG by Schistosoma larvae proteases. Immunology Letters 2, 135–9.CrossRefGoogle Scholar
Auriault, C., Ouaissi, M. A., Torpier, G., Eisen, H. & Capron, A. (1981). Proteolytic cleavage of IgG bound to the Fc receptor of Schistosoma mansoni schistosomula. Parasite Immunology 3, 3344.CrossRefGoogle Scholar
Barrett, A. J. (1986). An introduction to the proteinases. In Proteinase Inhibitors, 1st Edn. (ed. Barrett, A. J. & Salvesen, G.), pp. 322, Amsterdam: Elsevier Scientific Publishers.Google Scholar
Beynon, R. J. & Bond, J. S. (1989). Proteolytic Enzymes: A Practical Approach, 1st Edn.Oxford: IRL Press.Google Scholar
Brömme, D., Bonneau, P. R., Lachance, P., Wiederanders, B., Kirschke, H., Peters, C., Thomas, D. Y., Storer, A. C. & Vernet, T. (1993). Functional expression of human cathepsin S in Saccharomyces cerevisiae: Purification and characterization of the recombinant enzyme. Journal of Biological Chemistry 268, 4832–8.CrossRefGoogle ScholarPubMed
Carmona, C., Dowd, A. J., Smith, A. M. & Dalton, J. P. (1993). Cathepsin L proteinase secreted by Fasciola hepatica in vitro prevents antibody-mediated eosinophil attachment to newly excysted juveniles. Molecular and Biochemical Parasitology 62, 918.CrossRefGoogle ScholarPubMed
Chamow, S. M., Peers, D. H., Byrn, R. A., Mulkerrin, M. G., Harris, R. J., Wang, W.-C., Bjorkman, P. J., Capron, D. J. & Ashkenazi, A. (1990). Enzymatic cleavage of a CD4 immunoadhesin generates crystallizable, biologically active Fd-like fragments. Biochemistry 29, 9885–91.CrossRefGoogle ScholarPubMed
Chang, K. H., Cho, S. Y., Chi, J. G., Kim, W. S., Han, M. C., Kim, C. W., Myung, H. & Choi, K. S. (1987). Cerebral sparganosis: CT characteristics. Radiology 165, 505–10.CrossRefGoogle ScholarPubMed
Chapman, C. B. & Mitchell, G. F. (1982). Proteolytic cleavage of immunoglobulin by enzymes released by Fasciola hepatica. Veterinary Parasitology 11, 165–78.CrossRefGoogle ScholarPubMed
Chappell, C. L. & Dresden, M. H. (1986). Schistosoma mansoni: Proteinase activity of ‘hemoglobinase’ from the digestive tracts of adult worms. Experimental Parasitology 61, 160–7.CrossRefGoogle Scholar
Chi, J. G., Chi, H. S. & Lee, S. H. (1980). Histopathologic study on human sparganosis. Korean Journal of Parasitology 18, 1523.CrossRefGoogle Scholar
Cho, S. Y. (1987). Diphyllobothriasis and sparganosis. In Oxford Textbook of Medicine, 2nd Edn. (ed. Weatherall, D. J., Ledingham, J. G. G. & Warrell, D. A.), pp. 5.5695.571. Oxford: Oxford University Press.Google Scholar
Cho, S. Y., Chung, Y. B. & Kong, Y. (1992). Component proteins and protease activities in excretory–secretory product of sparganum. Korean Journal of Parasitology 30, 227–30.CrossRefGoogle ScholarPubMed
Cohen, L. W., Coghlan, V. M. & Dihel, L. C. (1986). Cloning and sequencing of papain-encoding cDNA. Gene 48, 219–27.CrossRefGoogle ScholarPubMed
Eakin, A. E., Mils, A. A., Harth, G., McKerrow, J. H. & Craik, C. S. (1992). The sequence, organization, and expression of the major cysteine protease (Cruzain) from Trypanosoma cruzi. Journal of Biological Chemistry 267, 7411–20.CrossRefGoogle ScholarPubMed
Fersht, A. (1985). Enzyme Structure and Mechanism, 1st Edn.San Francisco: W. H. Freeman and Company.Google Scholar
Fukase, T., Matsuda, Y., Akihama, S. & Itagaki, H. (1985). Purification and some properties of cysteine protease of Spirometra erinacei plerocercoid (Cestoda: Diphyllobothriidae). Japanese Journal of Parasitology 34, 351–60.Google Scholar
Goose, J. (1978). Possible role of excretory/secretory products in evasion of host defenses by Fasciola hepatica. Nature, London 275, 216–17.CrossRefGoogle ScholarPubMed
Gotz, B. & Klinkert, M. Q. (1993). Expression and partial characterization of a cathepsin B-like enzyme (Sm31) and a proposed ‘hemoglobinase’ (Sm32) from Schistosoma mansoni. The Biochemical Journal 290, 801–6.CrossRefGoogle Scholar
Joseph, L., Chang, L. C., Stamenkovich, D. & Sukhatme, V. P. (1988). Complete nucleotide and deduced amino acid sequences of human and murine preprocathepsin L: An abundant transcript induced by transformation of fibroblasts. Journal of Clinical Investigation 81, 1621–9.CrossRefGoogle ScholarPubMed
Karrer, K. M., Peiffer, S. L. & Ditomas, M. E. (1993). Two distinct gene subfamilies within the family of cysteine protease genes. Proceedings of the National Academy of Sciences, USA 90, 3063–7.CrossRefGoogle ScholarPubMed
Kinet, J. P. (1989). Antibody-cell interactions: Fc receptors. Cell 57, 351–4.CrossRefGoogle ScholarPubMed
Kirschke, H., Schmidt, I. & Wiederanders, B. (1986). Cathepsin S: The cysteine proteinase from bovine lymphoid tissue is distinct from cathepsin L (EC 3.4.22.15). The Biochemical Journal 240, 455–9.CrossRefGoogle ScholarPubMed
Kong, Y., Chung, Y. B., Cho, S. Y., Choi, S. H. & Kang, S.Y. (1994). Characterization of three neutral proteases of Spirometra mansoni plerocercoid. Parasitology 108, 359–68.CrossRefGoogle ScholarPubMed
Laemmli, U. K. (1970). Cleavage of structural proteins during assembly of the head of the bacteriophage T4. Nature, London 227, 681–5.CrossRefGoogle ScholarPubMed
Lowry, O. H., Rosebrough, N., Farr, A. L. & Randall, R. J. (1951). Protein measurement with Folin phenol reagent. Journal of Biological Chemistry 193, 265–75.CrossRefGoogle ScholarPubMed
Luaces, A. L., Osorio, L. M. & Barrett, A. J. (1993). A new test for infection by Entamoeba histolytica. Parasitology Today 9, 6971.CrossRefGoogle ScholarPubMed
Mage, M. G. (1980). Preparation of Fab fragments from IgGs of different animal species. Methods in Enzymology 70, 142–50.CrossRefGoogle ScholarPubMed
Maizels, R. M., Bundy, D. A. P., Selkirk, M. E., Smith, D. F. & Anderson, R. M. (1993). Immunological modulation and evasion by helminth parasites in human population. Nature, London 365, 797805.CrossRefGoogle Scholar
Marikovsky, M., Arnon, R. & Fishelson, Z. (1988). Proteases secreted by transforming schistosomula of Schistosoma mansoni promote resistance to killing by complement. Journal of Immunology 141, 273–8.CrossRefGoogle ScholarPubMed
Matsudaira, T. (1987). Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membrane. Journal of Biological Chemistry 262, 10035–8.CrossRefGoogle Scholar
Matuura, T., Nakamura, T. & Sugane, K. (1991). A gene encoding a cysteine protease in plerocercoids of Spirometra erinacei. Japanese Journal of Parasitology 40 (Suppl.), 58.Google Scholar
McKerrow, J. H., Jones, P., Sage, H. & Piano-Heiss, H. (1985). Proteinase from invasive larvae of the trematode parasite Schistosoma mansoni degrade connective tissue and basement membrane molecules. The Biochemical Journal 231, 4751.CrossRefGoogle Scholar
Mineura, K. & Mori, T. (1980). Sparganosis in the brain: Case report. Journal of Neurosurgery 52, 588–90.CrossRefGoogle ScholarPubMed
Osaki, Y. (1990). Ultrastructural studies on the plerocercoid of Spirometra erinacei in experimental sparganosis. Parasitology Research 76, 466–72.CrossRefGoogle ScholarPubMed
Pamer, E. G., Davis, C. E., Eakin, A. E. & So, M. (1990). Cloning and sequencing of the major cysteine protease cDNA from Trypanosoma brucei rhodesiense. Nucleic Acid Research 18, 6141.CrossRefGoogle Scholar
Song, C. Y. & Chappell, C. L. (1993). Purification and partial characterization of cysteine proteinase from Spirometra mansoni plerocercoids. Journal of Parasitology 79, 517–24.CrossRefGoogle ScholarPubMed
Smith, A. M., Dowd, A. J., McGonigle, S., Keegan, P. S., Brennan, G., Trudgett, A. & Dalton, J. P. (1993). Purification of a cathepsin L-like proteinase secreted by adult Fasciola hepatica. Molecular and Biochemical Parasitology 62, 18.CrossRefGoogle ScholarPubMed
Sutton, B. J. & Gould, H. J. (1993). The human IgE network. Nature, London 366, 421–8.CrossRefGoogle ScholarPubMed
Takio, K., Towatari, T., Katunuma, N., Teller, D. C. & Titani, K. (1983). Homology of amino acid sequences of rat liver cathepsins B and H with that of papain. Proceedings of the National Academy of Sciences, USA 80, 3666–70.CrossRefGoogle Scholar
Tamashiro, W. K., Rao, M. & Scott, A. L. (1987). Proteolytic cleavage of IgG and other protein substrates by Dirofilaria immitis microfilarial enzymes. Journal of Parasitology 73, 149–54.CrossRefGoogle ScholarPubMed
Tsang, V. C. W., Peralta, J. M. & Simons, A. R. (1983). Enzyme-linked immunoelectrotransfer blot techniques (EITB) for studying specificities of antigen and antibodies separated by gel electrophoresis. Methods in Enzymology 92, 377–91.CrossRefGoogle ScholarPubMed
Wiederanders, B., Brömme, D., Kirschke, H., Kalkkinen, N., Rinne, A., Paquette, T. & Toothman, P. (1991). Primary structure of bovine cathepsin S. Comparison to cathepsin L, H, B and papain. FEBS Letters 286, 189–92.CrossRefGoogle Scholar
Wiederanders, B., Brömme, D., Kirschke, H., Von Figura, K., Schmidt, B. & Peters, C. (1992). Phylogenetic conservation of cysteine proteases: Cloning and expression of a cDNA coding for human cathepsin S. Journal of Biological Chemistry 267, 13708–13.CrossRefGoogle ScholarPubMed