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Possible role of reactive forms of oxygen in in vitro killing ofSchistosoma mansoni sporocysts by hemocytes ofLymnaea stagnalis

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Abstract

The interactions between sporocysts ofSchistosoma mansoni and hemocytes of the pond snailLymnaea stagnalis were studied in an in vitro system. All sporocysts were encapsulated and killed in the hemolymph of juvenile or adult snails within 24 h; the killing patterns of both age groups were not very different. The separation of hemolymph into hemocytes and plasma and subsequent incubation of sporocysts showed that the cells, not the plasma, were responsible for parasite killing. The possible involvement of reactive oxygen intermediates and the enzyme peroxidase in the cytotoxic mechanism was studied. Chemiluminescence (CL) could not be detected during the hemocyteparasite encounter. Histochemical staining with nitroblue tetrazolium (indicative for superoxide) and diaminobenzidine (indicative for hydrogen peroxide) showed that oxygen intermediates were produced by snail hemocytes that encapsulated sporocysts. Histochemistry also suggested the presence of peroxidase activity at the hemocyte-sporocyst interface. The cytotoxic mechanism underlying parasite killing by hemocytes and the role of reactive forms of oxygen and peroxidase are discussed.

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References

  • Bayne CJ, Buckley PM, DeWan PC (1980a) Macrophage-like hemocytes of resistantBiomphalaria glabrata are cytotoxic for sporocysts ofSchistosoma mansoni in vitro. J Parasitol 66:413–419

    PubMed  Google Scholar 

  • Bayne CJ, Buckley PM, deWan PC (1980b)Schistosoma mansoni: cytotoxicity of hemocytes from susceptible snail hosts for sporocysts in plasma from resistantBiomphalaria glabrata. Exp Parasitol 50:409–416

    PubMed  Google Scholar 

  • Boswell CA, Bayne CJ (1985)Schistosoma mansoni: lectin dependent cytotoxicity of hemocytes from susceptible host snails,Biomphalaria glabrata. Exp Parasitol 60:133–138

    PubMed  Google Scholar 

  • Chernin E (1963) Observations on hearts explanted in vitro from the snailAustralorbis glabratus. J Parasitol 49:353–364

    PubMed  Google Scholar 

  • Dean DA, Wistar R, Murrell KD (1974) Combined in vitro effects of rat antibody and neutrophilic leukocytes on schistosomula ofSchistosoma mansoni. Am J Trop Med Hyg 23:420–428

    PubMed  Google Scholar 

  • Dikkeboom R, Van der Knaap WPW, Meuleman EA, Sminia T (1984) Differences between blood cells of juvenile and adult specimens of the pond snailLymnaea stagnalis. Cell Tissue Res 238:43–47

    Google Scholar 

  • Dikkeboom R, Van der Knaap WPW, Meuleman EA, Sminia T (1985) A comparative study on the internal defence system of juvenile and adultLymnaea stagnalis. Immunology 55:547–553

    PubMed  Google Scholar 

  • Dikkeboom R, Tijnagel JMGH, Mulder EC, Van der Knaap WPW (1987) Hemocytes of the pond snailLymnaea stagnalis generate reactive forms of oxygen. J Invertebr Pathol 49:321–331

    PubMed  Google Scholar 

  • Hafeman DG, Lucas ZJ (1979) Polymorphonuclear leukocytemediated, antibody-dependent, cellular cytotoxicity against tumor cells: dependence on oxygen and the respiratory burst. J Immunol 123:55–62

    PubMed  Google Scholar 

  • Harris KR, Cheng TC (1975) The encapsulation process inBiomphalaria glabrata experimentally infected with the metastrongylidAngiostrongylus cantonensis: enzyme histochemistry. J Invertebr Pathol 26:367–374

    PubMed  Google Scholar 

  • Incani RN, McLaren DJ (1983) Ultrastructural observations on the in vitro interaction of rat neutrophils with schistosomula ofSchistosoma mansoni in the presence of antibody and/or complement. Parasitology 86:345–357

    PubMed  Google Scholar 

  • Kazura JW, Fanning M, Blumer JL (1981) Role of cell-generated hydrogen peroxide in granulocyte-mediated killing of schistosomula ofSchistosoma mansoni in vitro. J Clin Invest 67:93–102

    PubMed  Google Scholar 

  • Klebanoff SJ (1968) Myeloperoxidase-halide-hydrogen peroxide anti-bacterial system. J Bacteriol 95:2131–2138

    PubMed  Google Scholar 

  • Klebanoff SJ (1982) Oxygen-dependent cytotoxic mechanisms of phagocytes. In: Gallin JI, Fauci AS (eds) Advances in host defense mechanisms, vol 1. Raven Press, New York, pp 111–162

    Google Scholar 

  • Leventhal R, Soulsby EJL (1972) Nitroblue tetrazolium reduction as an indicator of lysosomal activity at a larval surface. J Parasitol 58:1016–1017

    PubMed  Google Scholar 

  • Loker ES, Bayne CJ (1986) Immunity to trematode larvae in the snailBiomphalaria. In: Lackie AM (ed) Immune mechanisms in invertebrate vectors. Oxford University Press, Oxford, pp 199–220

    Google Scholar 

  • Mellink JJ, Van den Bovenkamp W (1985) In vitro culture of intramolluscan stages of the avian schistosomeTrichobilharzia ocellate. Z Parasitenkd 71:337–351

    PubMed  Google Scholar 

  • Meuleman EA, Lyaruu DM, Khan MA, Holzmann PJ, Sminia T (1978) Ultrastructural changes in the body wall ofSchistosoma mansoni during the transformation of the miracidium into the mother sporocyst in the snail hostBiomphalaria pfeifferi. Z Parasitenkd 56:227–242

    PubMed  Google Scholar 

  • Meuleman EA, Bayne CJ, Van der Knaap WPW (1987) Immunological aspects of snail-trematode interactions. In: Cooper EL, Langlet C, Bierne J (eds) Developmental and comparativ immunology. Alan Liss Inc., New York, pp 113–127

    Google Scholar 

  • Meuleman EA, Van der Knaap WPW, Mulder EC (1988) Hemocyte responses to schistosome inLymnaea stagnalis. Trop Geogr Med (in press)

  • Shozawa A (1986) A reducing factor produced by hemocytes ofBiomphalaria glabrata and its role in the host defense. Proceedings of ISDCI Conference 1986 (West Berlin). Dev Comp Immunol 10:636 (abstract)

    Google Scholar 

  • Sminia T (1972) Structure and function of blood and connective tissue cells of the freshwater pulmonateLymnaea stagnalis studied by electron microscopy and enzyme histochemistry. Z Zellforsch 130:479–526

    Google Scholar 

  • Sminia T, Barendsen LH (1980) A comparative morphological and enzyme histochemical study on blood cells of the freshwater snailsLymnaea stagnalis, Biomphalaria glabrata, andBulinus truncatus. J Morphol 165:31–39

    Google Scholar 

  • Sminia T, Van der Knaap WPW (1986) Immunorecognition in invertebrates with special reference to molluscs. In: Brehélin M (ed) Immunity in invertebrates. Springer, Berlin, pp 112–124

    Google Scholar 

  • Sminia T, Borghart-Reinders E, Van de Linde AW (1974) Encapsulation of foreign materials experimentally introduced into the freshwater snailLymnaea stagnalis. An electron microscopic and autoradiographic study. Cell Tissue Res 153:307–326

    PubMed  Google Scholar 

  • Sminia T, Van der Knaap WPW, Boerrigter-Barendsen LH (1982) Peroxidase-positive blood cells in snails. J Reticuloendothel Soc 31:399–404

    PubMed  Google Scholar 

  • Stibbs HH, Owczarzak A, Bayne CJ, DeWan PC (1979) Schistosome sporocyst-killing amoebae isolated fromBiomphalaria glabrata. J Invertebr Pathol 33:159–170

    PubMed  Google Scholar 

  • Van der Knaap WPW, Sminia T, Schutte R, Boerrigter-Barendsen LH (1983) Cytophilic receptors for foreignness and some factors which influence phagocytosis by invertebrate leucocytes: in vitro phagocytosis by amoebocytes of the pond snailLymnaea stagnalis. Immunology 48:377–383

    PubMed  Google Scholar 

  • Van der Knaap WPW, Meuleman EA (1986) Interaction between the immune system of lymnaeid snails and trematode parasites. In: Lackie AM (ed) Immune mechanisms in invertebrate vectors. Oxford University Press, Oxford, pp 179–198

    Google Scholar 

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Authors and Affiliations

  1. Laboratory of Medical Parasitology, Faculty of Medicine, Free University, P. O. Box 7161, 1007 MC, Amsterdam, The Netherlands

    Ronald Dikkeboom, Wil P. W. van der Knaap & Jolanda M. G. H. Tijnagel

  2. Department of Zoology, Oregon State University, 97331, Corvallis, OR, USA

    Christopher J. Bayne

Authors
  1. Ronald Dikkeboom
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  2. Christopher J. Bayne
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  3. Wil P. W. van der Knaap
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  4. Jolanda M. G. H. Tijnagel
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Dikkeboom, R., Bayne, C.J., van der Knaap, W.P.W. et al. Possible role of reactive forms of oxygen in in vitro killing ofSchistosoma mansoni sporocysts by hemocytes ofLymnaea stagnalis . Parasitol Res 75, 148–154 (1988). https://doi.org/10.1007/BF00932715

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