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Invertebrate blood cells: Morphological and functional aspects of the haemocytes in the pond snail Lymnaea stagnalis

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Abstract

The internal defence system (immune system) of the pond snail Lymnaea stagnalis is reviewed. Humoral defence activities are agglutination, opsonisation and inhibition of bacterial growth. Cellular defence is exerted by antigen trapping endothelial cells, foreign protein engulfing pore cells, phagocytic reticulum cells and mobile haemocytes. The haemocytes contribute most to defence and are therefore treated in more detail. There is one type of haemocyte; morphological heterogeneity of the haemocyte population is due to varying states of differentiation of the cells. Haemocytopoiesis is through mitosis of haemocytes, both in the pool of tissue-dwelling cells and in circulation. Haemocytes resemble monocytes/macrophages, they are typical phagocytes equipped with recognition factors (lectins), lysosomal enzymes and a cytotoxicity mechanism using reative oxygen intermediates. A comparison is made of the internal defence systems of the three main metazoan taxa, insects, molluscs and vertebrates.

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References

  • Adema CM (1992) Haemocyte-mediated cytotoxicity in the pond snail Lymnaea stagnalis, intermediate host of Trichobilharzia ocellata. PhD thesis, Vrije Universiteit, Amsterdam, The Netherlands

    Google Scholar 

  • Adema CM, van der Knaap WPW, Sminia T (1991a) Molluscan haemocyte-mediated cytotoxicity: the role of reactive oxygen intermediates. Rev Aquat Sci 4:210–223

    Google Scholar 

  • Adema CM, van Deutekom-Mulder EC, van der Knaap WPW et al. (1991b) Generation of oxygen radicals in haemocytes of the pond snail Lymnaea stagnalis in relation to the rate of phagocytosis. Dev Comp Immunol 15:17–26

    Article  PubMed  CAS  Google Scholar 

  • Amen RI (1992) Schistosomes modulate the defence system of their intermediate hosts. PhD thesis, Vrije Universiteit, Amsterdam, The Netherlands

    Google Scholar 

  • Boer HH, Sminia T (1976) Sieve structure of slit diaphragms of podocytes and pore cells of gastropod molluscs. Cell Tissue Res 170:221–229

    Article  PubMed  CAS  Google Scholar 

  • Dikkeboom R, van der Knaap WPW, Meuleman EA et al. (1984) Differences between blood cells of juvenile and adult specimens of the pond snail Lymnaea stagnalis. Cell Tissue Res 238:43–47

    Article  Google Scholar 

  • Dikkeboom R, van der Knaap WPW, Maaskant JJ et al. (1985) Different subpopulations of haemocytes in juvenile, adult and Trichobilharzia ocellata-infected Lymnaea stagnalis: a characterization using monoclonal antibodies. Z Parasitenkd 71:815–819

    Article  PubMed  CAS  Google Scholar 

  • Dikkeboom R, Tijnagel JMGH, Mulder EC et al. (1987) Hemocytes of the pond snail Lymnaea stagnalis generate reactive forms of oxygen. J Invertebr Pathol 49:321–331

    Article  PubMed  CAS  Google Scholar 

  • Dikkeboom R, Tijnagel JMGH, van der Knaap WPW (1988a) Monoclonal antibody recognized hamocyte subpopulations in juvenile and adult Lymnaea stagnalis: functional characteristics and lectin binding. Dev Comp Immunol 12:17–32

    Article  PubMed  CAS  Google Scholar 

  • Dikkeboom R, van der Knaap WPW, van den Bovenkamp W et al. (1988b) The production of toxic oxygen metabolites by hemocytes of different snail species. Dev Comp Immunol 12:509–520

    Article  PubMed  CAS  Google Scholar 

  • Dikkeboom R, Bayne CJ, van der Knaap WPW et al. (1989c) Possible role of reactive forms of oxygen in in vitro killing of Schistosoma mansoni sporocysts by hemocytes of Lymnaea stagnalis. Parasitol Res 75:148–154

    Article  Google Scholar 

  • Grimm-Jørgensen Y (1987) Somatostatin and calcitonin modulate gastropod internal defense mechanisms. Dev Comp Immunol 11:487–499

    Article  PubMed  Google Scholar 

  • Hughes TK Jr, Smith EM, Barnett JA et al. (1991) LPS stimulated invertebrate hemocytes: a role for immunoreactive TNF and IL-1. Dev Comp Immunol 15:117–122

    Article  PubMed  Google Scholar 

  • Jeong KH, Lie KJ, Heyneman D (1983) The ultrastructure of the amebocyte-producing organ in Biomphalaria glabrata. Dev Comp Immunol 7:217–228

    Article  PubMed  CAS  Google Scholar 

  • Johansson MW, Söderhäll K (1989) Cellular immunity in crustaceans and the proPO system. Parasitol Today 5:171–176

    Article  PubMed  CAS  Google Scholar 

  • Lever J, Bekius R (1965) On the presence of an external haemal pore in Lymnaea stagnalis L. Experienta 21:1–4

    Article  Google Scholar 

  • Mohandas A, Adema CM, van der Knaap WPW et al. (1992) The effect of haemolymph extraction on distribution of lysosomal enzymes in Lymnaea stagnalis haemocytes: a cytochemical study. Comp Haematol Int 2:61–67

    Article  CAS  Google Scholar 

  • Ratcliffe NA, Leonard C, Rowley AF (1984) Prophenoloxidase activation: nonself recognition and cell cooperation in insect immunity. Science 226:557–559

    Article  PubMed  CAS  Google Scholar 

  • Reichhart J-M, Meister M, Dimarq J-L et al. (1992) Insect immunity: developmental and inducible activity of the Drosophila diptericin promoter. EMBO J 11:1469–1477

    PubMed  CAS  Google Scholar 

  • Rondelaud D, Barthe D (1981) The development of the amoebocyte-producing organ in Lymnaea truncatula Müller infected by Fasciola hepatica L. Z Parasitenkd 65:331–341

    Article  PubMed  CAS  Google Scholar 

  • Sminia T (1972) Structure and function of blood and connective tissue cells of the fresh water pulmonate Lymnaea stagnalis studied by electron microscopy and enzyme histochemistry. Z Zellforsch 130:497–526

    Article  PubMed  CAS  Google Scholar 

  • Sminia T (1981) Gastropods. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells 1. Academic Press, London, New York, Toronto, Sydney, San Francisco, pp 191–232

    Google Scholar 

  • Sminia T, Barendsen L (1980) A comparative morphological and enzyme histochemical study on blood cells of the fresh water snails Lymnaea stagnalis, Biomphalaria glabrata, and Bulinus truncatus. J Morphol 165:31–39

    Article  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-Verlag, Berlin, Heidelberg, New York, Tokyo, pp 113–124

    Google Scholar 

  • Sminia T, Pietersma K, Scheerboom JEM (1973) Histological and ultrastructural observations on wound healing in the freshwater pulmonate Lymnaea stagnalis. Z Zellforsch 141:561–573

    Article  PubMed  CAS  Google Scholar 

  • Sminia T, Borghart-Reinders E, van de Linde AW (1974) Encapsulation of foreign material experimentally introduced into the freshwater snail Lymnaea stagnalis; an electron microscopical and autoradiographic study. Cell Tissue Res 153:307–326

    Article  PubMed  CAS  Google Scholar 

  • Sminia T, van der Knaap WPW, Kroese FGM (1979a) Fixed phagocytes in the freshwater snail Lymnaea stagnalis. Cell Tissue Res 196:545–548

    Article  PubMed  CAS  Google Scholar 

  • Sminia T, van der Knaap WPW, Edelenbosch P (1979b) The role of serum factors in phagocytosis of foreign particles by blood cells of the freshwater snail Lymnaea stagnalis. Dev Comp Immunol 3:37–44

    Article  PubMed  CAS  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  CAS  Google Scholar 

  • Sminia T, van der Knaap WPW, van Asselt LA (1983) Blood cell types and blood cell formation in gastropod molluscs. Dev Comp Immunol 7:665–668

    Article  Google Scholar 

  • Stefano GB, Leung MK, Zhao X et al. (1989) Evidence for the involvement of opioid neuropeptides in the adherence and migration of immunocompetent invertebrate hemocytes. Proc Natl Acad Sci 86:626–630

    Article  PubMed  CAS  Google Scholar 

  • van der Knaap WPW (1982) The internal defence system of the pond snail Lymnaea stagnalis. PhD Thesis, Vrije Universiteit, Amsterdam, The Netherlands

    Google Scholar 

  • van der Knaap WPW, Loker ES (1990) Immune mechanisms in trematode-snail interactions. Parasitol Today 6:175–182

    Article  PubMed  Google Scholar 

  • van der Knaap WPW, Sminia T, Kroese FGM et al. (1981a) Elimination of bacteria from the circulation of the pond snail Lymnaea stagnalis. Dev Comp Immunol 5:21–32

    Article  PubMed  Google Scholar 

  • van der Knaap WPW, Boerrigter-Barendsen LH, van den Hoeven DSP et al. (1981b) Immunocytochemical demonstration of a humoral defence factor in blood cells (amoebocytes) of the pond snail Lymnaea stagnalis. Cell Tissue Res 219:291–296

    Article  PubMed  Google Scholar 

  • van der Knaap WPW, Doderer A, Boerrigter-Barendsen LH et al. (1982) Some properties of an agglutinin in the haemolymph of the pond snail Lymnaea stagnalis. Biol Bull 162:404–412

    Article  Google Scholar 

  • van der Knaap WPW, Sminia T, Schutte R et al. (1983) Cytophylic receptors for foreigness and some factors which influence phagocytosis by invertebrate leukocytes: in vitro phagocytosis by amoebocytes of the snail Lymnaea stagnalis. Immunology 48:377–383

    PubMed  Google Scholar 

  • van der Knaap WPW, Boots AMH, Meuleman EA et al. (1985) Search for shared antigens in the schistosome-snail combination Trichobilharzia ocellata — Lymnaea stagnalis. Z Parasitenkd 71:219–226

    Article  PubMed  Google Scholar 

  • van der Knaap WPW, Meuleman EA, Sminia T (1987) Alterations in the internal defence system of the pond snail Lymnaea stagnalis induced by infection with the schistosome Trichobilharzia ocellata. Parasitol Res 73:57–65

    Article  PubMed  Google Scholar 

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Author notes

  1. C. M. Adema

    Present address: Department of Biology, University of New Mexico, Albuquerque, NM, USA

Authors and Affiliations

  1. Department of Medical Microbiology and Parasitology, Vrije Universiteit, Amsterdam, The Netherlands

    W. P. W. van der Knaap & C. M. Adema

  2. Department of Cell Biology, Faculty of Medicine, Vrije Universiteit, Amsterdam, The Netherlands

    T. Sminia

Authors
  1. W. P. W. van der Knaap
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  2. C. M. Adema
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  3. T. Sminia
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Originally presented at ECCP 93.

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van der Knaap, W.P.W., Adema, C.M. & Sminia, T. Invertebrate blood cells: Morphological and functional aspects of the haemocytes in the pond snail Lymnaea stagnalis . Comparative Haematology International 3, 20–26 (1993). https://doi.org/10.1007/BF00394923

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