Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T15:53:42.077Z Has data issue: false hasContentIssue false
  • English
  • Français

Schistosoma mansoni: praziquantel-induced tegumental lesion exposes actin of surface spines and allows binding of actin depolymerizing factor, gelsolin

Published online by Cambridge University Press:  06 April 2009

E. Linder  and
C. Thors
E. Linder
Affiliation:
Department of Parasitology, National Bacteriological Laboratory, S105 21 Stockholm, Sweden
C. Thors
Affiliation:
Department of Parasitology, National Bacteriological Laboratory, S105 21 Stockholm, Sweden
Get access Rights & Permissions [Opens in a new window]

Extract

Praziquantel is widely used for treatment of schistosomiasis. Elimination of intravascular worms involves a combination of drug-induced changes at the worm surface and a host immune response against exposed parasite components. Loss of spines is a typical feature of schistosomes obtained from praziquantel-treated infected animals. The mechanism for this is unknown. We have considered the possibility that praziquantel treatment involves exposure of surface spines consisting of ‘paracrystalline’ actin and a subsequent host response against actin through mechanisms established in the host independently from schistosomal infection. Drug-induced exposure of actin was demonstrated by fluorescence microscopy using anti-actin antibodies and phallacidin, an actin-binding mushroom toxin. Actin spines remained intact at the schistosome surface after in vitro exposure, but spine morphology was lost after in vivo exposure to praziquantel. Disintegration of spines in vivo was associated with binding of host antibodies. In vitro spine destruction could be seen in the presence of normal human serum. The effect was linked to calcium-dependent binding of actin depolymerizing factor, gelsolin.

Keywords

Schistosoma mansoniactinactin depolymerizationautoantibodiesdrug-effectsurface membranepraziquantel
Type
Research Article
Information
Parasitology , Volume 105 , Issue 1 , August 1992 , pp. 71 - 79
Copyright
Copyright © Cambridge University Press 1992

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

Abbas, M. K. & Cain, G. D. (1987). Actin and intermediate-sized filaments of the spines and cytoskeleton of Schistosoma mansoni. Parasitology Research 73, 66–74.CrossRefGoogle ScholarPubMed
Andrews, P. (1985). Praziquantel: mechanisms of antischistosomal activity. Pharmacology and Therapeutics 29, 129–56.CrossRefGoogle Scholar
Barak, L. S., Yocum, R. R., Nothnagel, E. A., Demarco, E. F. & Webb, W. W. (1980). Fluorescence staining of the actin cytoskeleton in living cells with 7-nitrobenz-2-oxa-l,3-diazole phallacidin. Proceedings of the National Academy of Sciences, USA 77, 980–4.CrossRefGoogle Scholar
Becker, B., Melhorn, H., Andrews, P. & Eckert, J. (1980). Light and electron microscopic studies on the effect of praziquantel on Schistosoma mansoni, Dicrocoelium dendriticum and Fasciola hepatica(Trematoda) in vitro. Zeitschrift für Parasitenkunde 63, 113–28.CrossRefGoogle ScholarPubMed
Brindley, P. J. & Sher, A. (1987). The chemotherapeutic effect of praziquantel against Schistosoma mansoni is dependent on host antibody response. Journal of Immunology 139, 215–20.CrossRefGoogle ScholarPubMed
Brindley, P. J., Strand, M., Norden, A. P. & Sher, A. (1989). Role of host antibody in the chemotherapeutic action of praziquantel against Schistosoma mansoni: identification of target antigens. Molecular and Biochemical Parasitology 34, 99–108.CrossRefGoogle ScholarPubMed
Chaponnier, C., Borgia, R., Rungger-Brändle, E., Well, R. & Gabbiani, G. (1979). An actin-destabilizing factor is present in human plasma. Experientia 35, 1039–40.CrossRefGoogle ScholarPubMed
Cohen, C., Reinhardt, B., Castellani, I., Norton, P. & Stirewalt, M. (1982). Schistosome surface spines are ‘crystals’ of actin. Journal of Cell Biology 95, 987–8.CrossRefGoogle ScholarPubMed
Cooker, C. M. & Von Lichtenberg, F. (1976). A revised method for isolation of Schistosoma mansoni eggs for biological experimentation. Proceedings of the Society for Experimental Biology and Medicine 92, 780–2.CrossRefGoogle Scholar
Davis, A. H., Blanton, R. & Klich, P. (1985). Stage and sex specific differences in actin gene expression in Schistosoma mansoni. Molecular and Biochemical Parasitology 17, 289–98.CrossRefGoogle ScholarPubMed
Doenhoff, M. J. & Bain, J. (1978). The immune-dependence of schistosomicidal chemotherapy: relative lack of efficacy of an antimonial in Schistosoma mansoni-infected mice deprived of their T-cells and the demonstration of drug-antiserum synergy. Clinical and Experimental Immunology 33, 232–8.Google ScholarPubMed
Doenhoff, M., Modha, J. & Lambertucci, J. R. (1988). Anti-schistosome therapy is enhanced by antibodies specific for a parasite esterase. Immunology 65, 507–10.Google ScholarPubMed
Gabbiani, G., Ryan, G. B., Lamelin, J.-P., Vassalli, P., Majno, G., Bouvier, C. A., Cruchaud, A. & Lushcer, E. F. (1973). Human smooth muscle autoantibody. American Journal of Pathology 72, 473–84.Google ScholarPubMed
Grabar, P. (1983). Autoantibodies and the physiological role of immunoglobulins. Immunology Today 4, 337–42.CrossRefGoogle ScholarPubMed
Harnett, w. & Kusel, J. R. (1986). Increased exposure of parasite antigens at the surface of adult male Schistosoma mansoni exposed to praziquantel in vitro. Parasitology 93, 401–5.CrossRefGoogle ScholarPubMed
Hockley, D. J. (1973). Ultrastructure of the tegument of Schistosoma. Advances in Parasitology 11, 233–305.CrossRefGoogle ScholarPubMed
Kreis, T. E. (1987). Microtubules containing detyrosinated tubulin are less dynamic. EMBO Journal 6, 2597–601.CrossRefGoogle ScholarPubMed
Kurki, P., Virtanen, I., Stenman, S. & Linder, E. (1977). Human smooth muscle autoantibodies reacting with intermediate (100Å) filaments. Nature, London 268, 240–1.CrossRefGoogle Scholar
Kurki, E., Linder, E., Miettinen, A. & Alfthan, O. (1978 a). Smooth muscle antibodies of actin and ‘nonactin’ specificity. Clinical Immunology and Immunopathology 9, 443–53.CrossRefGoogle ScholarPubMed
Kurki, P., Virtanen, I., Stenman, S. & Linder, E. (1978 b). Smooth muscle antibodies reacting with microtubular antigens. Protides of the Biological Fluids 26, 629–32.Google Scholar
Kurki, P., Miettinen, A., Linder, E., Pikkarainen, P., Vouristo, M. & Salaspuro, M. P. (1980). Different types of smooth muscle antibodies in chronic active hepatitis and primary biliary cirrhosis; their diagnostic and prognostic significance. Gut 21, 878–84.CrossRefGoogle ScholarPubMed
Laemmli, U. K. & Favre, M. (1973). Maturation of the head of bacteriophage T4 I. DNA packing event. Journal of Molecular Biology 80, 575–99.CrossRefGoogle Scholar
Macgregor, A. N. & Shore, S. J. (1990). Immunocytochemistry of cytoskeletal proteins in adult Schistosoma mansoni. International Journal for Parasitology 20, 279–84.CrossRefGoogle ScholarPubMed
Mclaren, D. J. (1980). Schistosoma mansoni: the parasite surface in relation to host immunity. Research Studies Press, Chichester pp. 163–5, 184–9.Google Scholar
Matsumoto, Y., Perry, G., Levine, R. J. C., Blanton, R., Mahmoud, A. A. F. & Aikawa, M. (1988). Paramyosin and actin in schistosomal teguments. Nature, London 333, 76–8.CrossRefGoogle ScholarPubMed
Melhorn, H., Becker, B., Andrews, P., Thomas, H. & Frenkel, J. K. (1981). In vivo and in vitro experiments on the effects of praziquantel on Schiztosoma mansoni. Arzneimittelforschung 31, 544–54.Google Scholar
Modha, J., Lambertucci, J. R., Doenhoff, M. J. & Mclaren, D. J. (1990). Immune dependence of schistosomicidal chemotherapy: an ultrastructural study of Schistosoma mansoni adult worms exposed to praziquantel and immune serum in vivo. Parasite Immunology 12, 321–34.CrossRefGoogle ScholarPubMed
Norberg, R., Thorstensson, R., Utter, G. & Fagraeus, A. (1979). F-actin depolymerizing activity of human serum. European Journal of Biochemistry 100, 575–83.CrossRefGoogle ScholarPubMed
Norden, A. P., Aronstein, W. S. & Strand, M. (1982). Schistosoma mansoni: identification, characterization and purification of the spine glcoprotein by monoclonal antibody. Experimental Parasitology 54, 432–42.CrossRefGoogle Scholar
Ohsawa, M. & Kimura, H. (1989). Formation of vitamin D-binding protein-actin and binary and ternary plasma gelsolin–actin complexes in human serum. Biochimica et Biophysica Acta 992, 195–200.CrossRefGoogle ScholarPubMed
Pollard, T. D. & Cooper, J. A. (1986). Actin and actinbinding proteins. A critical evaluation of mechanisms and functions. Annual Review of Biochemistry 55, 987–1035.CrossRefGoogle ScholarPubMed
Sabah, A. A., Fletcher, C., Webbe, G. & Doenhoff, M. J. (1986 a). Schistosoma mansoni: reduced efficacy of chemotherapy in infected T-cell-deprived mice. Experimental Parasitology 60, 348–56.CrossRefGoogle Scholar
Sabah, A. A., Fletcher, C., Webbe, G. & Doenhoff, M. J. (1986 b). Schistosoma mansoni: chemotherapy of infections of different ages. Experimental Parasitology 61, 294–303.CrossRefGoogle ScholarPubMed
Shaw, M. K. & Erasmus, D. A. (1983 a). Schistosoma mansoni: dose-related tegumental surface changes after in vivo treatment with praziquantel. Zeitschrift für Parasitenkunde 69, 643–53.CrossRefGoogle ScholarPubMed
Shaw, M. K. & Erasmus, D. A. (1983 b). Schistosoma mansoni: the effects of a subcurative dose of praziquantel on the ultrastructure of worms in vivo. Zeitschrift für Parasitenkunde 69, 73–90.CrossRefGoogle ScholarPubMed
Skalli, O., Ropraz, P., Trzeciak, A. & Benzonana, G. (1986). A monoclonal antibody against a-smooth muscle actin: a new probe for smooth muscle differentiation. Cell Biology 103, 2787–96.CrossRefGoogle Scholar
Smithers, S. R. & Terry, R. J. (1965). Infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695–700.CrossRefGoogle ScholarPubMed
Towbin, H., Staehelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences, USA 76, 4350–4.CrossRefGoogle ScholarPubMed