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The Prophenoloxidase Activating System: The Biochemistry of Its Activation and Role in Arthropod Cellular Immunity, with Special Reference to Crustaceans

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Immunity in Invertebrates

Part of the book series: Proceedings in Life Sciences ((LIFE SCIENCES))

Abstract

Although modern immunology owes its origin largely to the pioneering work of Metchnikoff [40] and his observations of phagocytosis in the water flea, Daphnia, the study of “immune” processes in invertebrates has always lagged behind that of mammals. Indeed, it is only recently that plausible theories for the discrimination of self from non-self in invertebrates have been put forward and that fundamental techniques such as the separation of the various blood cell populations have been devised. As it is, there is still debate between invertebrate immunologists as to the true biochemical/molecular basis for non-self recognition in different invertebrate phyla, and foremost amongst the mechanisms proposed to account for recognition phenomena in the arthropods are the lectins, cell surface charge and, more recently, the prophenoloxidase activating system. To help clarify the picture for arthropods, the present review aims to re-evaluate some of the earlier work conducted on arthropod cellular immunity which gave rise to these concepts, and to reinterpret the data provided by the respective authors in the light of our present understanding of the prophenoloxidase activating system in crustaceans.

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References

  1. Acton RT, Weinheimer PF (1974) Hemagglutinins; primitive receptor molecules operative in invertebrate defense mechanisms. In: Cooper EL (ed) Contemporary topics in immunology, vol 4. Plenum, London, pp 271–282

    Google Scholar 

  2. Anderson RS (1975) Phagocytosis by invertebrate blood cells in vitro: Biochemical events and other characteristics compared with vertebrate systems. In: Maramorosch K, Shope RE (eds) Invertebrate immunity. Academic Press, London, pp 153–180

    Google Scholar 

  3. Ashida M (1971) Purification and characterization of prophenoloxidase from the hemolymph of the silkworm Bombyx morí. Arch Biochem Biophys 144: 749–762

    Article  PubMed  CAS  Google Scholar 

  4. Ashida M (1981) A cane sugar factor suppressing activation of prophenoloxidase in haemolymph of the silkworm Bombyx morí. Insect Biochem 11: 57–65

    Article  CAS  Google Scholar 

  5. Ashida M, Ohnishi E (1967) Activation of prophenoloxidase in the hemolymph of the silkworm Bombyx mori. Arch Biochem Biophys 122: 411–416

    Article  PubMed  CAS  Google Scholar 

  6. Ashida M, Sóderháll K (1984) The prophenoloxidase activating system in crayfish. Comp Biochem Physiol 77B: 21–26

    Article  Google Scholar 

  7. Ashida M, Ishizaki Y, Iwahana M (1983) Activation of prophenoloxidase by bacterial cell walls or by B,l-3 glucans in plasma of the silkworm Bombyx mori. Biochem Biophys Res Commun 113: 562–568

    Article  PubMed  CAS  Google Scholar 

  8. Beresky MA, Hall DW (1977) The influence of phenylthiourea on encapsulation, melanization and survival in larvae of the mosquito Aedes aegypti parasitized by the nematode Neo-plectana carpocapsae. J Invertebr Pathol 29: 74–80

    Article  PubMed  CAS  Google Scholar 

  9. Bertheussen K (1984) Complement and lysins in invertebrates. Dev Comp Immunol Suppl 3: 173–181

    Google Scholar 

  10. Boman HG, Steiner H (1981) Humoral immunity in Cecropia pupae. In: Henle W, Hofschneider PM, Kaprowski M, Moaloe O, Melchers F, Rott R, Sweiger MG, Vogt Pk (eds) Current top¬ics in microbiology and immunology, vol 95, Springer, Berlin Heidelberg New York, pp 75–91

    Google Scholar 

  11. Bretting H, Kalthoff H, Fehr S (1978) Studies on the relationship between lectins from Axinella polypoides agglutinating bacteria and human erythrocytes. J Invertebr Pathol 32: 151–159

    Article  PubMed  CAS  Google Scholar 

  12. Brewer FD, Vinson SB (1977) Chemicals affecting the encapsulation of foreign material in an insect. J Invertebr Pathol 18: 287–289

    Article  Google Scholar 

  13. Cantacuzéne J (1923) Le probleme de l’immunité chez les invertébrés. C R Hebd Seanc Soc biol (Paris) 75th Annivers 88 (Suppl): 48–119

    Google Scholar 

  14. Cooper EL (1980) Phylogeny of cytotoxicity. Endeavour (Oxf) 4: 160–165

    Article  CAS  Google Scholar 

  15. Cornick JW, Stewart JE (1973) Interaction of the pathogen Gaffkya homari with the natural defence mechanisms of Homarus amerícanus. J Fish Res Boar Can 25: 695–709

    Article  Google Scholar 

  16. Edelman GM (1983) Cell adhesion molecules. Science 219: 450–457

    Article  PubMed  CAS  Google Scholar 

  17. Evans EE, Painter B, Evans ML, Weinheimer PF, Acton RT (1968) An induced bactericidin in the spiny lobster Panulirus argus. Proc Soc Exp Biol Med 128: 394–398

    PubMed  CAS  Google Scholar 

  18. Faye I, Wyatt GR (1980) The synthesis of antibacterial proteins in isolated fat body from Cecropia silkmoth pupae. Experientia (Basel) 36: 1325–1326

    Article  CAS  Google Scholar 

  19. Finstad CL, Litman GW, Finstad J, Good RA (1972) The evolution of the immune response XIII. The characterization of purified erythrocyte agglutinins from two invertebrate species. J Immunol 108: 1704–1711

    Google Scholar 

  20. Graham DG, Tiffany SM, Vogel FS (1978) The toxicity of melanin precursors. J Invest Dermatol 70: 113

    Article  PubMed  CAS  Google Scholar 

  21. Hall L, Soderhall K (1982) Purification and properties of a protease inhibitor from crayfish hemolymph. J Invertebr Pathol 39: 29–37

    Article  Google Scholar 

  22. Hall L, Soderhall K (1983) Isolation and properties of a protease inhibitor in crayfish ( Astacus astacus) cuticle. Comp Biochem Physiol 76B: 699–702

    Google Scholar 

  23. Hergenhahn HG, Soderhall K (1985) a2 macroglobulin-like activity in plasma of the crayfish Pacifastacus leniusculus. Comp Biochem Physiol 8IB: 833–835

    Google Scholar 

  24. Heyneman RA, Vercauteren RE (1968) Evidence for a lipid activator of prophenoloxidase in Tenebrio molitor. J Insect Physiol 14: 409–415

    Article  CAS  Google Scholar 

  25. Hultmark D, Steiner H, Rasmuson T, Boman HG (1980) Insect immunity: Purification and properties of three inducible bactericidal proteins from the hemolymph of immunized pupae of Hyalophora cecropia. Eur J Biochem 106: 7–16

    Google Scholar 

  26. Hultmark D, Engstrom A, Andersson K, Steiner H, Bennich H, Boman HG (1983) Insect immunity. Attacins, a family of antibacterial proteins from Hyalophora cecropia. EMBO J 2: 571–576

    Google Scholar 

  27. Inaba T, Suetake Y, Funatsu M (1963) Studies on tyrosinase in the housefly II. Activation of protyrosinase by SDS. Agr Biol Chem 27: 332–339

    Google Scholar 

  28. Komano H, Mizuno D, Natori S (1980) Purification of a lectin induced in the hemolymph of Sarcophaga peregrina larvae on injury. J Biol Chem 255: 2919–2924

    PubMed  CAS  Google Scholar 

  29. Lackie AM, Tackle G, Dularay B (1983) The non-recognition of negatively charged surface by locust haemocytes. In: Cooper EL, Wright RK (eds) Aspects of developmental and comparative immunology, vol 2. Pergamon, Oxford, p 54

    Google Scholar 

  30. Leonard CM, Soderhall K, Ratcliffe NA (1985) Isolation and properties of the prophenoloxidase activating system in an insect Blaberus craniifer. Insect Biochem 15: 803–810

    Article  CAS  Google Scholar 

  31. Liener IE (1976) Phytohaemagglutinins (phylolectins). Annu Rev Plant Physiol 27: 291–319

    Article  CAS  Google Scholar 

  32. Lis H, Sharon N (1973) The biochemistry of plant lectins (phytohaemagglutinins). Annu Rev Biochem 42: 541–550

    Article  PubMed  CAS  Google Scholar 

  33. Marchalonis JJ (1978) Immunity in evolution. Harvard University Press, Cambridge, p 316

    Google Scholar 

  34. Marchalonis JJ, Edelman G (1968) Isolation and characterization of a hemagglutinin from Limulus polyphemus. J Mol Biol 32: 453–465

    Article  CAS  Google Scholar 

  35. McCumber LJ, Hoffmann EM, Clem LW (1979) Recognition of viruses and xenogeneic proteins by the blue crab Callinectes sapidus: A humoral receptor of T3-bacteriophage. J Invertebr Pathol 33: 1–9

    Article  CAS  Google Scholar 

  36. McKay D, Jenkin CR (1970a) Immunity in the invertebrates: The role of serum factors in phagocytosis of erythrocytes by haemocytes of crayfish ( Parachaeraps bicarinatus ). Aust J Exp Biol Med Sci 48: 130–170

    Google Scholar 

  37. McKay, Jenkin CR (1970b) Immunity in the invertebrates: Correlation of the phagocytic activity of haemocytes with resistance to infection in the crayfish ( Parachaeraps bicarinatus ). Aust J Exp Biol Med Sci 48: 609–617

    Google Scholar 

  38. McKay D, Jenkin CR, Rowley D (1969) Immunity in the invertebrates I. Studies on the naturally occurring haemagglutinins in the fluid from invertebrates. Aust J Exp Biol Med Sci 47: 125–134

    Google Scholar 

  39. Menon IA, Haberman HF (1977) Mechanisms of action of melanins. Br J Dermatol 97: 109–112

    Article  PubMed  CAS  Google Scholar 

  40. Metchnikoff E (1884) Ueber eine Sprosskrankheit der Daphnien. Arch Pathol Anat 96: 177–195

    Article  Google Scholar 

  41. Nappi A J (1973) The role of melanization in the immune reaction of larvae of Drosophila alonquin against Pseudocoila bochei. Parasitology 66: 23–32

    Article  CAS  Google Scholar 

  42. Noguchi H (1903) On the multiplicity of the serum haemagglutinins of cold blooded animals. Zentralbl Bakteriol I Abt Orig 34: 286–288

    Google Scholar 

  43. Paterson WD, Stewart JE (1974) In vitro phagocytosis by haemocytesof the American lobster ( Homarus americanus ). J Fish Res Board Can 31: 1051–1056

    Google Scholar 

  44. Perry G, Epel D (1981) Ca2+ stimulated production of H202 from naphthoquinone oxidation in Arbacia eggs. Exp Cell Res 134: 465–470

    Article  Google Scholar 

  45. Preston JW, Taylor RL, (1970) Observations on the phenoloxidase system in the haemolymph of the cockroach Leucophaea maderae. J Insect Physiol 16: 1729–1744

    Article  CAS  Google Scholar 

  46. Pye AE (1974) Microbial activation of prophenoloxidase from immune insect larvae. Nature 251: 610–613

    Article  PubMed  CAS  Google Scholar 

  47. Ratcliffe NA, Rowley AF (1979) A comparative synopsis of the structure and function of the blood cells of insects and other invertebrates. Dev Comp Immunol 3: 189–243

    Article  PubMed  CAS  Google Scholar 

  48. Ratcliffe NA, Leonard CM, Rowley AF (1984) Prophenoloxidase activation: Non-self recognition and cell co-operation in insect immuntiy. Science 226: 557–559

    Google Scholar 

  49. Renwrantz L, Stahmer A (1983) Opsonizing properties of an isolated hemolymph agglutinin and demonstration of lectin-like recognition molecules at the surface of hemocytes from Mytilus edulis. J Comp Physiol 149: 535–546

    Article  CAS  Google Scholar 

  50. Rizki RM, Rizki TM (1979) Cell interactions in the differentiation of a melanotic tumour in Drosophila. Differentiation 12: 167–178

    Article  PubMed  CAS  Google Scholar 

  51. Rizki RM, Rizki TM (1984) Selective destruction of a host blood cell type by a parasitoid wasp. Proc Natl Acad Sci USA 81: 6154–6158

    Article  PubMed  CAS  Google Scholar 

  52. Rizki TM, Rizki AM (1983) Blood cell surface changes in Drosophila mutants with melanotic tumours. Science 220: 73–75

    Article  PubMed  CAS  Google Scholar 

  53. Rowley AF, Ratcliffe NA (1980) Insect erythrocyte agglutinins. In vitro opsonization experi-ments with Clitumnus extradentatus andPeriplaneta americanahzemocytQS. Immunology 40: 483–492

    Google Scholar 

  54. Salt G (1970) The cellular defence reactions of insects. Cambridge University Press, London

    Book  Google Scholar 

  55. Scott MT (1971) Recognition of foreignness in invertebrates II. In vitro studies of cockroach phagocytic hemocytes. Immunology 21: 817–827

    Google Scholar 

  56. Smith VJ, Ratcliffe NA (1978) Host defence reactions of the shore crab Carcinus maenas ( L) in vitro. J Mar Biol Assoc UK 58: 367–379

    Google Scholar 

  57. Smith VJ, Soderhall K (1983) B 1,3-glucan activation of crustacean haemocytes in vitro and in vivo. Biol Bull (Woods Hole) 164: 299–314

    Article  CAS  Google Scholar 

  58. Smith VJ, Soderhall K (1983) Induction of degranulation and lysis of haemocytes of the freshwater crayfish Astacus astacus by components of the prophenoloxidase activating system in vitro. Cell Tissue Res 233: 291–303

    Article  Google Scholar 

  59. Smith VJ, Soderhall K, Hamilton M (1984) Bl,3-glucan induced cellular defence reactions in the shore crab Carcinus maenas. Comp Biochem Physiol 77A: 635–639

    Article  Google Scholar 

  60. Soderhall K (1981) Fungal cell wall Bl,3-glucans induce clotting and phenoloxidase attachment to foreign surfaces of crayfish haemocyte lysate. Dev Comp Immunol 5: 565–573

    PubMed  CAS  Google Scholar 

  61. Soderhall K (1982) Prophenoloxidase activating system and melanization - a recognition sys-tem in arthropods - a review. Dev Comp Immunol 6: 601–611

    PubMed  CAS  Google Scholar 

  62. Soderhall K (1983) Bl,3-glucans enhancement of protease activity in crayfish haemocyte lysate. Comp Biochem Physiol 74B: 221–224

    Google Scholar 

  63. Soderhall K, Ajaxon R (1982) Effect of quinones and melanin on mycelial growth oi Aphanomyces spp and extracellular protease of Aphanomyces astaci a parasitic on crayfish. J Invertebr Pathol 39: 105–109

    Article  Google Scholar 

  64. Soderhall K, Hall L, (1984) Lipopolysaccharide - induced activation of prophenoloxidase activating system in crayfish haemocyte lysate. Biochim Biophys Acta 797: 99–104

    Google Scholar 

  65. Soderhall K, Smith VJ (1983) Separation of the haemocyte populations of Carcinus maenas and other marine decapods and prophenoloxidase distribution. Dev Comp Immunol 7: 229–239

    Article  PubMed  CAS  Google Scholar 

  66. Soderhall K, Smith VJ (1984) The prophenoloxidase activating system - a complement-like pathway in arthropods. In: Aist J, Roberts DW (eds) Infections processes of fungi. Rockefeller Foundation Study Bellagio Italy, pp 160–167

    Google Scholar 

  67. Soderhall K, Smith VJ (1986) The prophenoloxidase activating cascade as a recognition and defence system in arthropods. In: Gupta AP (ed) Humoral and cellular immunity in arthropods. Wiley, New York (in press)

    Google Scholar 

  68. Soderhall K, Unestam T (1979) Activation of crayfish serum prophenoloxidase: The specificity of cell wall glucan activation and activation by purified fungal glycoprotein. Can J Microbiol 25: 404–416

    Google Scholar 

  69. Soderhall K, Vey A, Ramstedt M (1984) Hemocyte lysate enhancement of fungal spore encapsulation by crayfish hemocytes. Dev Comp Immunol 8: 23–30

    Article  PubMed  CAS  Google Scholar 

  70. Soderhall K, Wingren A. Johansson M, Bertheussen K (1985) The cytotoxic reactions of haemocytes from the freshwater crayfish Astacus astacus. Cell Immunol 94: 326–332

    Article  PubMed  CAS  Google Scholar 

  71. Starkey PM, Barrett AJ (1977) a2 macroglobulin, a physiological regulator of protease activity. In: Barrett AJ (ed) Proteinases in mammalian cells and tissues. Elsevier/North Holland, Amsterdam, pp 665–696

    Google Scholar 

  72. Steiner H, Hultmark D, Engstom A, Bennich H, Boman HG (1981) Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 292: 246–248

    Article  PubMed  CAS  Google Scholar 

  73. Stephens JS (1962) Influence of active immunization on melanization of the blood of wax moth larvae. Can J Microbiol 8: 719–725

    Article  CAS  Google Scholar 

  74. Stewart JE, Zwicker BM (1972) Natural and induced bactericidal activities in the haemolymph of the lobster Homarus americanus: Products of haemocyte: plasma interactions. Can J Microbiol 18: 1499–1511

    Article  PubMed  CAS  Google Scholar 

  75. Stoltz DB, Cook DI (1983) Inhibition of host phenoloxidase activity by parasitoid hymenoptera. Experientia (Basel) 39: 1022–1024

    Article  CAS  Google Scholar 

  76. Taylor RL (1969) A suggested role for the polyphenol-phenoloxidase system in invertebrate immunity. J Invertebr Pathol 14: 427–428

    Article  PubMed  CAS  Google Scholar 

  77. Tyler A, Metz CB (1945) Natural heteroagglutinins in the serum of the spiny lobster Panulirus interruptus II. Chemical and antigenic relation to blood proteins. Biol Bull (Woods Hole) 89: 193–200

    Google Scholar 

  78. Tyson CJ, Jenkin CR (1973) The importance of opsonic factors in the removal of bacteria from the circulation of the crayfish ( Parachaeraps bicarinatus ). Aust J Exp Biol Med Sci 51: 609–615

    Google Scholar 

  79. Tyson CJ, Jenkin CR (1974a) Phagocytosis of bacteria in vitro by haemocytes from the crayfish ( Parachaeraps bicarinatus ). Aust J Exp Biol Med Sci 52: 341–348

    Google Scholar 

  80. Tyson CJ, Jenkin CR (1974b) The cytotoxic effect of haemocytes from the crayfish ( Para-chaeraps bicarinatus) on tumour cells of vertebrates. Aust J Exp Biol Med Sci 52: 915–923

    Google Scholar 

  81. Unestam T, Soderhall K (1977) Soluble fragments from fungal cell walls elicit defence reactions in crayfish. Nature 167: 45–46

    Article  Google Scholar 

  82. Vasta GR. Marchalonis JJ (1983) Humoral recognition factors in the Arthropoda: The specificity of Chelicerata serum lectins. Ann Zool 23: 157–171

    Google Scholar 

  83. Weinheimer PF, Evans EE, Stroud RM, Acton RT, Painter B (1969) Comparative immunology: A natural hemolytic system of the spiny lobster Panulirus argus. Proc Soc Exp Biol Med 130: 322–326

    Google Scholar 

  84. Yeaton RW (1981a) Invertebrate lectins I. Occurrence. Dev Comp Immunol 5: 391–402

    CAS  Google Scholar 

  85. Yeaton RW (1981b) Invertebrate lectins II. Diversity of specificity, biological synthesis and function in recognition. Dev Comp Immunol 5: 535–545

    PubMed  CAS  Google Scholar 

  86. Yoshino T (1983) Lectins and antibodies as molecular probes of molluscan hemocyte surface membranes. Dev Comp Immunol 7: 641–644

    Article  CAS  Google Scholar 

  87. Zlotkin E, Gurevitz M, Shulov A (1973) The toxic effects of phenoloxidase from the haemolymph of tenebrionid bettles. J Insect Physiol 19: 1057–1065

    Article  PubMed  CAS  Google Scholar 

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  1. Institutionen för Fysiologisk Botanik, Uppsala Universitet, Box 540, 751 21, Uppsala, Sweden

    K. Söderhäll

  2. University Marine Biological Station Millport, Isle of Cumbrae, KA28 OEG, Scotland, UK

    V. J. Smith

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  1. K. Söderhäll
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  1. Laboratoire de Pathologie Comparée, USTL, Place E. Bataillon, F-34060, Montpellier, France

    Michel Brehélin

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© 1986 Springer-Verlag Berlin Heidelberg

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Söderhäll, K., Smith, V.J. (1986). The Prophenoloxidase Activating System: The Biochemistry of Its Activation and Role in Arthropod Cellular Immunity, with Special Reference to Crustaceans. In: Brehélin, M. (eds) Immunity in Invertebrates. Proceedings in Life Sciences. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-70768-1_15

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  • DOI: https://doi.org/10.1007/978-3-642-70768-1_15

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