Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-05-06T00:34:04.527Z Has data issue: false hasContentIssue false

Schistosomicidal activities of Lymnaea stagnalis haemocytes: the role of oxygen radicals

Published online by Cambridge University Press:  06 April 2009

C. M. Adema
Affiliation:
Department of Medical Microbiology and Parasitology, Vrije Universiteit Amsterdam, van der Boechorststraat 7, 1081 BT Amsterdam, The Netherlands
E. C. Van Deutekom-Mulder
Affiliation:
Department of Medical Microbiology and Parasitology, Vrije Universiteit Amsterdam, van der Boechorststraat 7, 1081 BT Amsterdam, The Netherlands
W. P. W. Van Der Knaap
Affiliation:
Department of Medical Microbiology and Parasitology, Vrije Universiteit Amsterdam, van der Boechorststraat 7, 1081 BT Amsterdam, The Netherlands
T. Sminia
Affiliation:
Department of Histology, Faculty of Medicine, Vrije Universiteit Amsterdam, van der Boechorststraat 7, 1081 BT Amsterdam, The Netherlands

Summary

Macrophage-like defence cells (haemocytes) of the pond snail Lymnaea stagnalis mediate cytotoxicity through reactive oxygen intermediates (ROIs). This activity is NADPH-oxidase dependent, as in mammalian phagocytes during the respiratory burst. In this study, mother sporocysts of schistosomes, the compatible Trichobilharzia ocellata and the incompatible Schistosoma mansoni evoke in vitro ROI activities (detected by luminol dependent chemiluminescence, LDCL) from L. stagnalis haemocytes. S. mansoni is encapsulated by haemocytes and eliminated, whereas T. ocellata escapes encapsulation and survives. Both schistosomes were equally susceptible to in vitro oxidative damage from exposure to hydrogen peroxide and to ROIs generated by a xanthine/xanthine oxidase system. Protocatechuic acid, a specific antagonist of NADPH-oxidase, delayed the killing of T. ocellata and S. mansoni sporocysts by haemocytes of resistant snails (Biomphalaria glabrata and L. stagnalis, respectively). We conclude that ROIs take part in haemocyte-mediated cytotoxicity. However, neither a snail's capability to generate ROIs, nor a schistosome's susceptibility to ROIs, determine snail/schistosome incompatibility. Snail/schistosome compatibility is rather determined by the parasite's ability modulate haemocyte behaviour such that effective encapsulation and the generation of lethal concentrations of ROIs are prevented.

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

Adema, C. M., Van Deutekom-Mulder, E. C., Van Den Knaap, W. P. W. & Sminia, T. (1991). Generation of oxygen radicals in hemocytes of the snail Lymnaea stagnalis in relation to the rate of phagocytosis. Developmental and Comparative Immunology 15, 1726.Google Scholar
Adema, C. M., Van Deutekom-Mulder, E. C., Van Der Knaap, W. P. W. & Sminia, T. (1993). NADPH-oxidase: the probable source of reactive oxygen intermediate killing generation in haemocytes of the gastropod Lymnaea stagnalis. Journal of Leukocyte Biology 54, 379–83.Google Scholar
Bayne, C. J., Buckley, P. M. & Dewan, P. C. (1980). Macrophage-like hemocytes of resistant Biomphalaria glabrata are cytotoxic for sporocysts of Schistosoma mansoni in vitro. Journal of Parasitology 66, 413–19.CrossRefGoogle Scholar
Callahan, H. L., Crouch, R. K. & James, E. R. (1990). Hydrogen peroxide is the most toxic oxygen species for Onchocerca cervicalis microfilariae. Parasitology 100, 407–15.Google Scholar
Connors, V. A. & Yoshino, T. P. (1990). In vitro effect of larval Schistosoma mansoni excretory–secretory products on phagocytosis-stimulated superoxide production in hemocytes from Biomphalaria glabrata. Journal of Parasitology 76, 895902.CrossRefGoogle ScholarPubMed
Dahlgren, C. & Stendahl, O. (1983). Role of myeloperoxidase in luminol-dependent chemiluminescence of polymorphonuclear leucocytes. Infection and Immunity 39, 736–41.CrossRefGoogle Scholar
Dikkeboom, R., Bayne, C. J., Van Der Knaap, W. P. W. & Tijnagel, J. M. G. H. (1988 a). Possible role of reactive forms of oxygen in in vitro killing of Schistosoma mansoni sporocysts by hemocytes of Lymnaea stagnalis. Parasitology Research 75, 148–54.Google Scholar
Dikkeboom, R., Tijnagel, J. M. G. H., Mulder, E. C. & Van Der Knaap, W. P. W. (1987). Haemocytes of the pond snail Lymnaea stagnalis generate reactive forms of oxygen. Journal of Invertebrate Pathology 49, 321–31.Google Scholar
Dikkeboom, R., Van Der Knaap, W. P. W., Van Den Bovenkamp, W., Tijnagel, J. M. G. H. & Bayne, C. J. (1988 b). The production of toxic oxygen metabolites by hemocytes of different snail species. Developmental and Comparative Immunology 12, 509–20.Google Scholar
Farber, J. L., Kyle, M. E. & Coleman, J. B. (1990). Biology of disease: mechanisms of cell injury by activated oxygen species. Laboratory Investigation 62, 670–9.Google Scholar
Leippe, M. & Renwrantz, L. (1985). On the capability of bivalve and gastropod haemocytes to secrete cytotoxic molecules. Journal of Invertebrate Pathology 46, 209–10.CrossRefGoogle Scholar
McKerrow, J. H., Jeong, K. H. & Beckstead, J. H. (1985). Enzyme histochemical comparison of Biomphalaria glabrata amoebocytes with human granuloma macrophages. Journal of Leukocyte Biology 37, 341–7.Google Scholar
McLaren, D. J. & James, S. L. (1985). Ultrastructural studies of the killing of schistosomula of Schistosoma mansoni by activated macrophages in vitro. Parasite Immunology 7, 315–31.Google Scholar
Mellink, J. J. & Van Den Bovenkamp, W. (1985). In vitro culture of intra-molluscan stages of the avian schistosome Trichobilharzia ocellata. Zeitschrift für Parasitenkunde 71, 337–51.Google Scholar
Meuleman, E. A., Huyer, A. R. & Mooij, J. H. (1984). Maintenance of the life-cycle of Trichobilharzia ocellata via the duck Anas platyrhynchos and the pond snail Lymnaea stagnalis. Netherlands Journal of Zoology 34, 414–17.Google Scholar
Mjoji, G. M., Smith, J. M. & Prichard, R. K. (1988). Antioxidant systems in Schistosoma mansoni: evidence for their role in protection of the adult worms against oxidant killing. International Journal for Parasitology 18, 667–73.Google Scholar
Nathan, C. F., Arrick, B. A., Murray, H. W., De Santis, N. M. & Cohn, Z. A. (1981). Tumor-cell anti-oxidant defenses – inhibition of the glutathione redox cycle enhances macrophage-mediated cytolysis. Journal of Experimental Medicine 153, 766–82.Google Scholar
Schallig, H. D. F. H., Schut, A., Van Der Knaap, W. P. W. & De Jong-Brink, M. (1990). A simplified medium for the in vitro culture of mother sporocysts of the schistosome Trichobilharzia ocellata. Parasitology Research 76, 278–9.CrossRefGoogle Scholar
Shozawa, A. (1986). A reducing factor produced by haemocytes of Biomphalaria glabrata and its role in the host defence. Developmental and Comparative Immunology 10, 636.Google Scholar
Simons, J. M., 'T hart, B. A., Ip Vai Ching, T. R. A. M., Van Dijk, H. & Labadie, R. P, (1990). Metabolic activation of natural phenols into selective oxidative burst antagonists by activated human neutrophils. Free Radical Biology and Medicine 8, 251–8.Google Scholar
Sminia, T. (1972). Structure and function of blood and connective tissue cells of the freshwater pulmonate Lymnaea stagnalis studied by electron microscopy and enzyme histochemistry. Zeitschrift für Zellforschung und Mikroskopische Anatomie 130, 479526.Google Scholar
Sminia, T. & Barendsen, L. (1980). A comparative morphological and enzyme histochemical study on blood cells of the freshwater snails Lymnaea stagnalis, Biomphalaria glabrata, and Bulinus truncatus. Journal of Morphology 165, 31–9.Google Scholar
Sminia, T., Van Der Knaap, W. P. W. & Boerrigter-Barendsen, L. H. (1982). Peroxidase-positive blood cells in snails. Journal of the Reticuloendothelial Society 31, 399404.Google Scholar
Stibbs, H. H., Owczarzak, A., Bayne, C. J. & Dewan, P. C. (1979). Schistosome sporocyst-killing amoebae isolated from Biomphalaria glabrata. Journal of Invertebrate Pathology 33, 159–70.Google Scholar
Van Der Knaap, W. P. W. & Loker, E. S. (1990). Immune mechanisms in trematode–snail interactions. Parasitology Today 6, 175–82.Google Scholar
Van Der Knaap, W. P. W., Sminia, T., Schutte, R. & Boerrigter-Barendsen, L. H. (1983). Cytophilic receptors for foreignness and some factors which influence phagocytosis by invertebrate leucocytes: in vitro phagocytosis by amoebocytes of the snail Lymnaea stagnalis. Immunology 48, 377–83.Google Scholar
Vilim, V. & Wilhelm, J. (1989). What do we measure by luminol-dependent chemiluminescence of phagocytes? Free Radical Biology and Medicine 6, 623–9.Google Scholar
Weiss, S. J. (1989). Tissue destruction by phagocytes. New England Journal of Medicine 320, 365–76.Google Scholar
Wishkovsky, A. (1988). Chemiluminescence: an advanced tool for measuring phagocytosis. American Fisheries Society Special Publication 18, 292–7.Google Scholar
Yazdanbakhsh, M., Eckman, C. M. & Roos, D. (1987). Killing of schistosomula by taurine chloramine and taurine bromamine. American Journal of Tropical Medicine and Hygiene 37, 106–10.Google Scholar
Yoshino, T. P. (1988). Phospholipase C-like activity in phagocytic cells of the Asian clam, Corbicula fluminea, and its possible role in cell-mediated cytolytic reactions. Journal of Invertebrate Pathology 51, 3240.CrossRefGoogle Scholar