Mechanisms of Antigen Processing in Invertebrates: Are There Receptors?

  • L. Tučková
  • M. Bilej
Part of the Advances in Comparative and Environmental Physiology book series (COMPARATIVE, volume 23)

Abstract

The ability to recognize self and non-self exists in all animal species. Unicellular animals, such as protozoans, which often engulf living microorganisms, must discriminate between them and nutrition proteins, to prevent damage to their own proteins during digestive processes. The mechanism of discrimination at this level is unknown. One can assume that the specificity is based on substrate specificity of the proteolytic enzymes (Valembois et al. 1973; Ratcliffe et al. 1984, 1991; Tučková etal. 1986a). The main defense mechanisms in multicellular invertebrates are certainly represented by innate factors. Microorganisms that break the outer protective barrier and invade the host are mainly eliminated by phagocytosis which can be potentiated by humoral factors. Moreover, body fluids (e.g. hemolymph, celomic fluid) contain antibacterial molecules that probably prevent the multiplication of these bacteria.

Keywords

Sugar Carbohydrate Polysaccharide Electrophoresis Serine 

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References

  1. Alonso-Bedate M, Sequeros E (1985) Suggested regulatory mechanisms for caudal regeneration in Allolobophora molleri (Annelida;Oligochaeta). Comp Biochem Physiol 81 A: 225–228Google Scholar
  2. Anderson RS (1980) Antibacterial activity in the coelomic fluid of a polychaete annelid, Glycera dibranchiata. Biol Bull 159: 259–268Google Scholar
  3. Anderson RS, Chain BM (1982) Antibacterial activity in the coelomic fluid of a marine annelid Glycera dibranchiata. J Invertebr Pathol 40: 320–326Google Scholar
  4. Ando K, Natori S (1988) Molecular cloning, sequencing, and characterization of cDNA for Sarcotoxin IIA, an inducible antibacterial protein of Sarcophaga peregrina (flesh fly). Biochemistry 27: 1715–1721PubMedGoogle Scholar
  5. Ashida M, Yoshida H (1988) Limited proteolysis of prophenoloxidase during activation by microbial products in insect plasma and effect of phenoloxidase on electrophoretic mobilities of plasma proteins. Insect Biochem 18: 11–19Google Scholar
  6. Baba K, Okada M, Kawano T, Komano H, Natori S (1987) Purification of Sarcotoxin III, a new antibacterial protein of Sarcophaga peregrina. J Biochem 102: 69–74PubMedGoogle Scholar
  7. Banerjee A, Datta PK, Basu PS, Datta TK (1991) Characterization of a naturally occurring protease inhibitor in the hemolymph of the scorpion, Heterometrus bengalensis. Dev Comp Immunol 15: 213–218PubMedGoogle Scholar
  8. Bang FB (1973) A survey of phagocytosis as a protective mechanism against disease among invertebrates. In: Braun W, Unger J (eds) Non-specific factors influencing host resistance. Karger, Basel, pp 2–10Google Scholar
  9. Bilej M, Větvička V, Tučková L, Trebichavsky I, Koukal M, Šima P (1990a) Phagocytosis of synthetic particles in earthworms. Effect of antigenic stimulation and opsonization. Folia Biol (Prague) 36: 273–280Google Scholar
  10. Bilej M, Tučková L, Rejnek J, Větvička V (1990b) In vitro antigen-binding properties of coelomocytes of Eisenia foetida ( Annelida ). Immunol Lett 26: 183–188PubMedGoogle Scholar
  11. Bilej M, Scheerlinck JP, VandenDriessche T, De Baetselier P, Větvička V (1991a) The flow cytometric analysis of in vitro phagocytic activity of earthworm coelomocytes (Eisenia foetida; Annelida ). Cell Biol Int Rep 14: 831–837Google Scholar
  12. Bilej M, De Baetselier P, Trebichavsky I, Větvička V (1991b) Phagocytosis of synthetic particles in earthworms: absence of oxidative burst and possible role of lytic enzymes. Folia Biol (Prague) 37: 227–233Google Scholar
  13. Bilej M, Rossmann P, VandenDriessche T, Scheerlinck JP, De Baetselier P, Tučková L, Větvička V, Rejnek J (1991c) Detection of antigen in the coelomocytes of the earthworm Eisenia foetida ( Annelida ). Immunol Lett 29: 241–246PubMedGoogle Scholar
  14. Bilej M, Šima P, Slipka J (1992a) Repeated antigenic challenge induces earthworm celomocyte proliferation. Immunol Lett 32: 181–184PubMedGoogle Scholar
  15. Bilej M, Rejnek J, Tučková L (1992b) The interaction of staphylococcal protein A with free coelomocytes of annelids. Cell Biol Int Rep 16: 481–485PubMedGoogle Scholar
  16. Bilej M, Tučková L, Rejnek J (1993) The fate of protein antigen in earthworms: study in vitro. Immunol Lett 35: 1–6PubMedGoogle Scholar
  17. Bilej M, Tučková L, Rossmann P (1994) A new approach to in vitro studies of antigenic response in earthworms. Dev Comp Immunol 18: 363–367PubMedGoogle Scholar
  18. Boman HG, Steiner H (1981) Humoral immunity in cecropia pupae. Curr Top Microbiol Immunol 94 /95: 75–89PubMedGoogle Scholar
  19. Boman HG, Faye I, v. Hofstein P, Kockum K, Lee JY, Xanthopoulos KG (1985) On the primary structures of lysozyme, cecropins and attacins from Hyalophora cecropia. Dev Comp Immunol 9: 551–558PubMedGoogle Scholar
  20. Cameron GR (1932) Inflammation in earthworms. J Pathol 35: 933–972Google Scholar
  21. Casteels P, Ampe C, Jacobs F, Vaeck M, Tempst P (1989) Apidaecins: antibacterial peptides from honeybees. EMBO J 8: 2387–2391PubMedGoogle Scholar
  22. Chain BM, Anderson RS (1983a) Antibacterial activity of the coelomic fluid of the polychaete, Glycera dibranchiata. I. The kinetics of the bactericidal reaction: Biol Bull 164: 28–40Google Scholar
  23. Chain BM, Anderson RS (1983b) Antibacterial activity of the coelomic fluid of the polychaete, Glycera dibranchiata. II. Partial purification and biochemical characterization of the active factor. Biol Bull 164: 41–49Google Scholar
  24. Cooper EL (1965) Rejection of body-wall xenograft exchanged between Lumbricus terrestris and Eisenia foetida Am Zool 5: 665Google Scholar
  25. Cooper EL (1970) Transplantation immunity in helminths and annelids. Transplant Proc 2: 216–221PubMedGoogle Scholar
  26. Cooper EL (1973) Evolution of cellular immunity. In: Braun W, Unger J (eds) Non-specific factors influencing host resistance. Karger, Basel, pp 11–23Google Scholar
  27. Cooper EL, Roch P (1986) Second-set allograft responses in the earthworm Lumbricus terrestris. Kinetics and characteristics. Transplantation 41: 514–520PubMedGoogle Scholar
  28. Cooper EL, Stein EA (1981) Oligochaetes. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells, vol 1. Academic Press, London, pp 75–140Google Scholar
  29. Cooper EL, Acton RT, Weinheimer PF, Evans EE (1969) Lack of bacteriocidal response in the earthworm Lumbricus terrestris after immunization wtih bacterial antigens. J Invertebr Pathol 14: 402–406PubMedGoogle Scholar
  30. Çotuk A, Dales RP (1984a) The effect of the coelomic fluid of the earthworm Eisenia foetida Sav. on certain bacteria and the role of the coelomocytes in the internal defence. Comp Biochem Physiol 78A: 271–275Google Scholar
  31. Çotuk A, Dales RP (1984b) Lysozyme activity in the coelomic fluid and coelomocytes of the earthworm Eiseniafoetida Sav. in relation to bacterial infection. Comp Biochem Physiol 78 A: 469–474Google Scholar
  32. Dales RP, Dixon LJR (1980) Responses of polychaete annelids to bacterial infection. Comp Biochem Physiol 67A: 391–396Google Scholar
  33. Dales RP, Kalaç Y (1992) Phagocytic defence by the earthworm Eisenia foetida against certain pathogenic bacteria. Comp Biochem Physiol 101A: 487–490Google Scholar
  34. Faulhaber LM, Karp RD (1991) A diphasic immune response against injected bacteria in the American cockroach. Dev Comp Immunol (Suppl) 1: 47Google Scholar
  35. Golding DW (1974) Regeneration and growth control in Nereis. III. Separation of wound healing and segment regeneration by experimental endocrine manipulation. J Embryol Exp Morphol 32: 99–109PubMedGoogle Scholar
  36. Gotz P, Trenczek T (1991) Antibacterial proteins in insects other than Lepidoptera and Diptera and some other invertebrates. In: Gupta AP (ed) Immunology of insects and other arthropods. CRC Press, Boca Raton, pp 323–346Google Scholar
  37. Goudswaard J, van der Dponk JA, Noordzig A, van Dam RH, Vaerman JP (1978) Protein A reactivity of various mammalian immunoglobulins. Scand J Immunol 8: 21–28PubMedGoogle Scholar
  38. Herlant-Meewis H (1966) Les cellules neurosecretrices de la chaine nerveuse d’Eisenia foetida. Z Zellforsch 69: 319–325PubMedGoogle Scholar
  39. Herlant-Meewis H, Deligne J (1964) Regeneration in annelids. In: Abercrombie M, Brachet J (eds) Advances in morphogenesis, vol 4. Academic Press, New York, pp 155–215Google Scholar
  40. Hildemann WH (1981) Immunophylogeny: from sponges, to hagfish to mice. In: Hildemann WH (ed) Frontiers in immunogenetics. Elsevier, Amsterdam, pp 3–19Google Scholar
  41. Hirigoyenberry F, Lassalle F, Lassègues M (1990) Antibacterial activity of Eiseniafetida Andrei coelomic fluid: transcription and translation regulation of lysozyme and proteins evidenced after bacterial infestation. Comp Biochem Physiol 95B: 71–75Google Scholar
  42. Hrženjak T, Hrzenjak M, Kašuba V, Efenberger-Marinculic P, Levanat S (1992) A new source of biologically active compounds-earthworm tissue (Eisenia foetida, Lumbricus rubellus). Comp Biochem Physiol 102A: 441–447Google Scholar
  43. Jackson AD, Smith VJ, Peddie CM (1993) In vitro phenoloxidase activity in the blood of Ciona intestinalis and other ascidians. Dev Comp Immunol 17: 97–108PubMedGoogle Scholar
  44. Janda V, Bohuslav P (1934) Sur l’explantation du tissu de la paroi intistinale et des amibocytes de Lumbricus terrestris L. et des cellules d’epithelium intestinal d’Anodonta cygnea L. Publ Fac Sci Univ Charles 133: 1–23 (in Czech with French Summary)Google Scholar
  45. Janeway CA (1992) The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol Today 13: 11–16PubMedGoogle Scholar
  46. Jolles P, Zuili S (1960) Purification et etude comparee de nouveaux lysozymes extraits du poumon de poule et de Nephthys hombergi. Biochim Biophys Acta 39: 212–217PubMedGoogle Scholar
  47. Karp RD (1985) Preliminary characterization of the inducible humoral factor in the American cockroach (Periplaneta americana). Dev Comp Immunol 9: 569–575PubMedGoogle Scholar
  48. Kauschke E, Mohrig W (1987) Comparative analysis of hemolytic and hemagglutinating activities in the coelomic fluid of Eisenia foetida and Lumbricus terrestris ( Annelida, Lumbricidae). Dev Comp Immunol 11: 331–342PubMedGoogle Scholar
  49. Keilin ND (1925) Parasitic autotomy of the host as a mode of liberation of coelomic parasites from the body of the earthworm. Parasitology 17: 170–172Google Scholar
  50. Komano H, Kasama E, Nagasawa Y, Nakanishi Y, Matsuyama K, Ando KI, Natori S (1987) Purification of Sarcophaga (fleshfly) lectin and detection of sarcotoxins in the culture medium of NIH-Sape-4, an embryonic cell line of Sarcophaga peregrina. Biochem J 248: 217–222PubMedGoogle Scholar
  51. Lambert J, Keppi E, Dimarqo JL, Wicker C, Reichhart JM, Dunbar B, Lepage P, Van Dorsselaer A, Hoffmann J, Fothergill J, Hoffmann D (1989) Insect immunity: isolation from immune blood of the dipteran Phormia terranovae of two insect antibacterial peptides with sequence homology to rabbit lung macrophage bactericidal peptides. Proc Natl Acad Sci USA 86: 262–266PubMedGoogle Scholar
  52. Langone JJ (1982) Protein A and related receptors. Adv Immunol 32: 158–241Google Scholar
  53. Lassalte F, Lassègues M, Roch P (1988) Protein analysis of earthworms coelomic fluid-IV. Evidence, activity, induction and purification of Eiseniafetida andrei lysozyme ( Annelidae ). Comp Biochem Physiol 91B: 187–192Google Scholar
  54. Laulan A, Morel A, Lestage J, Delaage M, Chateaureynaud-Duprat P (1985) Evidence of synthesis by Lumbricus terrestris of specific substance in response to an immunization with a synthetic hapten. Immunology 56: 751–758PubMedGoogle Scholar
  55. Laulan A, Lestage J, Bouc AM, Chateaureynaud-Duprat P (1988) The phagocytic activity of Lumbricus terrestris coelomocytes is enhanced by the vertebrate opsonins: IgG and complement C3b fragment. Dev Comp Immunol 12: 269–278PubMedGoogle Scholar
  56. Leipner C, Tučková L, Rejnek J, Langner J (1993) Serine proteases in coelomic fluids of annelidsEisenia foetida and Lumbricus terrestris. Comp Biochem Physiol 105B: 637–641Google Scholar
  57. Marchalonis J, Atwell JL, Goding JW (1978) 7S immunoglobulins of monotreme, the Echidna Tachyglossus acutaetus: two distinct isotypes which bind A protein of Staphylococcus aureus. Immunology 34: 97–103PubMedGoogle Scholar
  58. Metchnikoff EE (1887) Sur la lutte des cellules de Forganisme contre l’invasion des microbes. Ann Inst Pasteur 1: 322–340Google Scholar
  59. Mihara H, Sumi H, Yoneta T, Mizumoto H, Ikeda R, Seiki M, Maruyama M (1991) A novel fibrinolytic enzyme extracted from the earthworm Lumbricus rubellus. Jpn J Physiol 41: 461–472PubMedGoogle Scholar
  60. Mohrig W, Kauschke E, Ehlers M (1984) Rosette formation of the coelomocytes of the earthworm Lumbricus terrestris L. with sheep erythrocytes. Dev Comp Immunol 8: 471–476PubMedGoogle Scholar
  61. Nagasawa H, Sawaki K, Fujii Y, Kobayashi M, Segawa T, Suzuki R, Inatomi H (1991) Inhibition by lombricine from earthworm (Lumbricus terrestris) of the growth of spontaneous mammary tumours in SHN mice. Anticancer Res 11: 1061–1064PubMedGoogle Scholar
  62. Olive PJW (1974) Cellular aspects of regeneration influence in Nereis diversicolor. J Embryol Exp Morphol 32: 111–131PubMedGoogle Scholar
  63. Perin JP, Jolles P (1972) The lysozyme from Nephthys hombergi (annelid). Biochim Biophys Acta 263: 683–689PubMedGoogle Scholar
  64. Peucellier G (1983) Purification and characterization of proteases from the polychaete annelid Sabellaria alveolata. Eur J Biochem 136: 435–445Google Scholar
  65. Porchet-Hennere E, M’Berri M (1987) Cellular reaction of the polychaete annelid Nereis diversicolor against coelomic parasites. J Invertebr Pathol 50: 58–66Google Scholar
  66. Ratcliffe NA, Leonard C, Rowley AF (1984) Prophenoloxidase activation: nonself recognition and cell cooperation in insect immunity. Science 226: 557–559PubMedGoogle Scholar
  67. Ratcliffe NA, Rowley AF, Fitzgerald SW, Rhodes CP (1985) Invertebrate immunity: basic concepts and recent advances. Int Rev Cytol 97: 183–349Google Scholar
  68. Ratcliffe NA, Brookman JL, Rowley AF (1991) Activation of the prophenoloxidase in locusts by bacterial lipopolysaccharides. Dev Comp Immunol 15: 33–39PubMedGoogle Scholar
  69. Rejnek J, Tučková L, Šima P, Kostka J (1986) The proteins in Lumbricus terrestris and Eisenia foetida coelomic fluids and on coelomocytes reacting with sheep and goat IgG molecules. Dev Comp Immunol 10: 467–475Google Scholar
  70. Rejnek J, Tučková L, Zikan J, Tomana M (1991) The interaction of a protein from the coelomic fluid of earthworms with staphylococcal protein A. Dev Comp Immunol 15: 269–277PubMedGoogle Scholar
  71. Rejnek J, Tučková L, Šima P, Bilej M (1993) The fate of protein antigen in earthworms: study invivo. Immunol Lett 36: 131–136PubMedGoogle Scholar
  72. Richman DD, Cleveland PH, Oxman MN, Johnson KM (1982) The binding of staphylococcal protein A by the sera of different species. J Immunol 128: 2300–2305PubMedGoogle Scholar
  73. Roch P (1977) Reactavite in vitro des leucocytes du lombricien Eisenia fetida Sav. a quelques substance mitogeniques. CR Acad Sci Ser D 284: 705–712Google Scholar
  74. Roch P (1979) Protein analysis of earthworm coelomic fluid: I-polymorphic system of the natural hemolysin of Eisenia fetida andrei. Dev Comp Immunol 3: 599–608PubMedGoogle Scholar
  75. Roch P, Cooper EL (1983) A β2-microglobulin-like molecule on earthworm (L. terrestris) leukocyte membranes. Dev Comp Immunol 7: 633–636Google Scholar
  76. Roch P, Valembois P, Du Pasquier L (1975) Response of earthworm leukocytes to concanavalin A and transplantation antigens. In: Hildemann WH, Benedict AA (eds) Immunologic phylogeny. Plenum Press, New York, pp 45–54Google Scholar
  77. Roch P, Valembois P, Davant N, Lassègues M (1981) Protein analysis of earthworm coelomic fluid. II. Isolation and biochemical characterisation of the Eisenia fetida andrei factor ( EFAF ). Comp Biochem Physiol 69B: 829–836Google Scholar
  78. Roch P, Cooper EL, Eskinazi DP (1983) Serological evidences for a membrane structure related to human β2-microglobulin expressed by certain earthworm leukocytes. Eur J Immunol 13: 1037–1042PubMedGoogle Scholar
  79. Roch P, Davant N, Lassègues M (1984) Isolation of agglutinins from lysins in earthworm coelomic fluid by gel filtration followed by chromatofocusing. J Chromatogr 290: 231–235Google Scholar
  80. Roch P, Lassègues M, Valembois P (1991a) Antibacterial activity of Eisenia fetida andrei coelomic fluid. III. Relationship within the polymorphic hemolysins. Dev Comp Immunol. 15: 27–32PubMedGoogle Scholar
  81. Roch P, Stabili L, Pagliara P (1991b) Purification of three serine proteases from the coelomic cells of earthworms (Eisenia fetida). Comp Biochem Physiol 98B: 597–602Google Scholar
  82. Schrevel J (1969) Recherches sur le cycle des Lucodinidae Gregarines parasites d’annelides polychetes. Protistologica 5: 561–588Google Scholar
  83. Schrevel J (1970) Contribution a l’etude des Selenidiidae parasites d’ annelides polychetes. I. Cycles biologiques. Protistologica 6: 389–426Google Scholar
  84. Schrevel J (1971) Contribution a F etude des Selenidiidae parasites d’ annelides polychetes. II. Ultrastructure de quelques trophozoites. Protistologica 7: 439–450Google Scholar
  85. Schubert I, Messner B (1971) Untersuchungen fiber das Vorkommen von Lysozym bei Anneliden. Zool Jahrb Physiol 76: 36–50Google Scholar
  86. Shalev A, Goldenberg PZ, Huebner E (1980) Evidence for an H-Y cross-reactive antigen in invertebrates. Differentiation 16: 77–80PubMedGoogle Scholar
  87. Shalev A, Greenberg AH, Logdberg L, Bjorck L (1981) β2-Microglobulin-like molecules in low vertebrates and invertebrates. J Immunol 127: 1186–1191PubMedGoogle Scholar
  88. Shalev A, Segal S, Eli MB (1985) Evolutionary conservation of brain Thy-1 glycoprotein in vertebrates and invertebrates. Dev Comp Immunol 9: 497–506PubMedGoogle Scholar
  89. Sinkora M, Bilej M, Tučková L, Romanovsky A (1993) Hemolytic function of opsonizing protein of earthworm’s coelomic fluid. Cell Biol Int 17: 935–939PubMedGoogle Scholar
  90. Soderhall K, Smith VJ (1986) The prophenoloxidase activating system: the biochemistry of its activation and role in arthropod cellular immunity, with special reference to crustaceans. In: Brehelin M (ed) Immunity in invertebrates. Springer, Berlin Heidelberg New York, pp 208–223Google Scholar
  91. Stein E, Cooper EL (1981) The role of opsonins in phagocytosis by coelomocytes of the earthworm Lumbricus terrestris. Dev Comp Immunol 5: 415–425PubMedGoogle Scholar
  92. Stein EA, Cooper EL (1983) Carbohydrate and glycoprotein inhibitors of naturally occurring and induced agglutinins in the earthworm Lumbricus terrestris. Comp Biochem Physiol 76B: 197–206Google Scholar
  93. Stein EA, Cooper EL (1988) In vitro agglutinin production by earthworm leukocytes. Dev Comp Immunol 12: 531–548PubMedGoogle Scholar
  94. Stein EA, Avtalion RR, Cooper EL (1977) The coelomocytes of the earthworm Lumbricus terrestris: morphology and phagocytic properties. J Morphol 153: 467–476PubMedGoogle Scholar
  95. Stein EA, Wojdani A, Cooper EL (1982) Agglutinins in the earthworm Lumbricus terrestris: naturally occurring and induced. Dev Comp Immunol 6: 407–421PubMedGoogle Scholar
  96. Stein EA, Younai S, Cooper EL (1986) Bacterial agglutinins of the earthworm, Lumbricus terrestris. Comp Biochem Physiol 84B: 409–415Google Scholar
  97. Stein EA, Younai S, Cooper EL (1990) Separation and partial purification of agglutinins from coelomic fluid of the earthworm, Lumbricus terrestris. Comp Biochem Physiol 97B: 701–705Google Scholar
  98. Sun SC, Lindstrom I, Boman HG, Faye I, Schmidt O (1990) Hemolin: an insect-immune protein belonging to the immunoglobulin superfamily. Science 250: 1729–1732PubMedGoogle Scholar
  99. Takahashi T, Iwase T, Kobayashi K, Rejnek J, Mestecky J, Moro I (1992) Phylogeny of the immunoglobulin joining (J) chain. 7th Int Congr Mucosal Immunology, Prague, Czechoslovakia, 16–20 Aug 1992, Czechoslovak Immunological Society, Prague, 234 ppGoogle Scholar
  100. Toupin J, Lamoureux G (1976) Coelomocytes of earthworms: phytohemagglutinin (PHA) responsiveness. In: Wright RK, Cooper EL (eds) Phylogeny of thymus and bone marrowbursa cells. Elsevier, Amsterdam, pp 19–27Google Scholar
  101. Tučková L, Bilej M (1994) Antigen processing in earthworms. Immunol Lett 41: 273–277PubMedGoogle Scholar
  102. Tučková L, Rejnek J, Šíma P, Ondrejova R (1986a) Lytic activities in coelomic fluids of Eisenia foetida and Lumbricus terrestris. Dev Comp Immunol 10: 181–189PubMedGoogle Scholar
  103. Tučková L, Rejnek J, Šíma P (1986b) Lytic activites in coelomic fluid of annelids E. foetida and L. terrestris. 6th Int Congr Immunol Toronto, National Research Council Canada, 1: 52. 4 (Abstr)Google Scholar
  104. Tučková L, Rejnek J, Šíma P (1988) Response to parenteral stimulation in earthworms L. terrestris and E. foetida. Dev Comp Immunol 12: 287–296PubMedGoogle Scholar
  105. Tučková L, Rejnek J, Bilej M, Pospíšil R (1991a) Characterization of antigen-binding protein in earthworms Lumbricus terrestris and Eisenia foetida. Dev Comp Immunol 15: 263–268PubMedGoogle Scholar
  106. Tučková L, Rejnek J, Bilej M, Hájková H, Romanovský A (1991b) Monoclonal antibodies to antigen binding protein of annelids (Lumbricus terrestris). Comp Biochem Physiol 100B: 19–23Google Scholar
  107. Vaillier J, Cadoret MA, Roch P, Valembois P (1985) Protein analysis of earthworm coelomic fluid. III. Isolation and characterization of several bacteriostatic molecules from Eisenia foetida andrei. Dev Comp Immunol 9: 11–20PubMedGoogle Scholar
  108. Valembois P (1963) Recherches sur la nature de la reaction antigreffe chez le lombricien Eisenia foetida. C R Acad Sci D (Paris) 257: 3489–3490Google Scholar
  109. Valembois P, Roch P, Du Pasquier L (1973) Dégradation in vitro de protéine éntrangére par les macrophages du Lombricien Eisenia fetida Sav. C R Acad Sci Paris Sér III 277: 57–60Google Scholar
  110. Valembois P, Roch P, Boiledieu D (1980) Natural and induced cytotoxicities in sipunculids and annelids. In: Manning MJ (ed) Phylogeny of immunological memory. Elsevier, Amsterdam, pp 47–55Google Scholar
  111. Valembois P, Roch P, Lassègues M, Cassand P (1982) Antibacterial activity of the hemolytic system from the earthworm Eisenia fetida andrei. J Invertebr Pathol 40: 21–27Google Scholar
  112. Valembois P, Roch P, Lassègues M (1986) Antibacterial molecules in annelids. In: Brehelin M (ed) Immunity in invertebrates. Springer, Berlin Heidelberg New York, pp 74–93Google Scholar
  113. Valembois P, Seymour J, Roch P (1991) Evidence and cellular localization of an oxidative activity in the coelomic fluid of the earthworm Eisenia fetida andrei. J Invertebr Pathol 57: 177–183Google Scholar
  114. Valembois P, Lassègues M, Roch P (1992) Formation of brown bodies in the coelomic cavity of the earthworm Eisenia fetida andrei and attendant changes in shape and adhesive capacity of constitutive cells. Dev Comp Immunol 16: 95–101PubMedGoogle Scholar
  115. Větvička V, Šima P, Cooper EL, Bilej M, Roch P (1994) Immunology of annelids. CRC Press, Boca RatonGoogle Scholar
  116. Villaro AC, Sesma P, Alegría D, Vázquez JJ, Lopez J (1985) Relationship of symbiotic microorganisms to metanephridium: phagocytic activity in the metanephridinal epithelium of two species of Oligochaeta. J Morphol 186: 307–314Google Scholar
  117. Vivier E, Henneré E (1964) Cytologic, cycle et aflinites de la Coccidie Coelotropha durchoni nomen novum (= Eucoccidium durchoni Vivier), parasite de Nereis diversicolor O. F. Müller ( Annelide Polychete ). Bull Biol Fr Belg 1: 154–206Google Scholar
  118. Voburka Z, Mareš M, Větvička V, Bilej M, Baudyš M, Fusek M (1992) New trypsin inhibitors are present in the coelomic fluid of the earthworm Lumbricus terrestris. Biochem Int 27: 679–685PubMedGoogle Scholar
  119. Wojdani A, Stein EA, Lemmi CA, Cooper EL (1982) Agglutinins and proteins in the earthworm, Lumbricus terrestris, before and after injection of erythrocytes, carbohydrates, and other materials. Dev Comp Immunol 6: 613–624PubMedGoogle Scholar
  120. Zikán J, ŠÍma P, Prokešova L, Hadge D (1980) Binding of nonmammalian immunoglobulins to staphylococcal protein A. Folia Biol (Prague) 26: 261–266Google Scholar
  121. Zwilling R, Neurath H (1981) Invertebrate proteases. In: Lorand L (ed) Methods in enzymology, vol 80. Academic Press, New York, pp 633–664Google Scholar

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© Springer-Verlag Berlin Heidelberg 1996

Authors and Affiliations

  • L. Tučková
    • 1
  • M. Bilej
    • 1
  1. 1.Department of Immunology, Institute of MicrobiologyAcademy of Sciences of the Czech RepublicPrague 4Czech Republic

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