Thromb Haemost 1997; 77(02): 227-233
DOI: 10.1055/s-0038-1655943
Review Article
Schattauer GmbH Stuttgart

Haemostasis in Fish – An Evolutionary Perspective[*]

Andrew F Rowley
The School of Biological Sciences, University of Wales Swansea, Singleton Park, Swansea, UK
,
Darryl J Hill
The School of Biological Sciences, University of Wales Swansea, Singleton Park, Swansea, UK
,
Clare E Ray
The School of Biological Sciences, University of Wales Swansea, Singleton Park, Swansea, UK
,
Roger Munro
1   The Haematology Department, Morriston Hospital, Swansea, UK
› Author Affiliations
Further Information

Publication History

Received 05 September 1996

Accepted after revision 17 October 1996

Publication Date:
10 July 2018 (online)

The original studies referred to in this review were partially supported by the Wellcome Trust (042316/Z/94/Z). D. J. H. was supported by a studentship from the Biotechnology and Biological Sciences Research Council, UK.


 
  • References

  • 1 Ratcliffe NA, Rowley AF, Fitzgerald SW, Rhodes CP. Invertebrate immunity:basic concepts and recent advances. Int Rev Cytol 1985; 97: 183-350
  • 2 Armstrong PB. Adhesion and spreading of Limulus blood cells on artificial surfaces. J Cell Sci 1980; 44: 243-262
  • 3 Armstrong PB, Levin J. In vitro phagocytosis by Limulus blood cells. J Invertebr Pathol 1979; 34: 145-151
  • 4 Iwanaga S, Muta T, Shigenaga T, Seki N, Kawano K, Katsu T, Kawabata S. Structure-function relationships of tachyplesins and their analogues. In: Ciba Foundation Symposium 186. Antimicrobial Peptides, Boman HG, Marsh J, Goode JA, eds. Wiley J. Chichester: 1994. pp. 160-175
  • 5 Muta T, Iwanaga S. The role of hemolymph coagulation in innate immunity. Curr Opinion Immunol 1996; 08: 41-47
  • 6 Kopacek P, Hall M, Söderhäll K. Characterisation of a clotting protein isolated from plama of the fresh-water crayfish Pascifastacus leniusculus . Eur J Biochem 1993; 213: 591-597
  • 7 Boolootian RA, Giese AC. Clotting of echinoderm coelomic fluid. J exp Zool 1959; 140: 207-229
  • 8 Takahashi H, Azumi K, Yokosawa H. Hemocyte aggregation in the solitary ascidian Halocynthia roretzi: plasma factors, magnesium ions, and Met-Lys-bradykinin induce aggregation. Biol Bull Woods Hole 1994; 186: 247-253
  • 9 Takahashi H, Azumi K, Yokosawa H. A novel membrane glycoprotein involved in ascidian hemocyte aggregation and phagocytosis. Eur J Biochem 1995; 233: 778-783
  • 10 Ratcliffe NA, Rowley AF. Invertebrate Blood Cells Vols 1 & 2. Academic Press; London: 1981
  • 11 Peddie CM, Riches AC, Smith VJ. Proliferation of undifferentiated blood cells from the solitary ascidian, Ciona intestinalis in vitro. Dev Comp Immunol 1995; 19: 377-387
  • 12 Peddie CM, Smith VJ. ‘Lymphocyte-like’ cells in ascidians: precursors for vertebrate lymphocytes?. Fish Shellfish Immunol 1995; 5: 17-28
  • 13 Beck G, Habicht GS. Isolation and characterization of a primitive IL-1-like protein from an invertebrate. Proc Natl Acad Sci 1986; 83: 7429-7433
  • 14 Raftos DA, Cooper EL, Habicht GS, Beck G. Invertebrate cytokines: tunicate cell proliferation stimulated by an interleukin 1-like molecule. Proc Natl Acad Sci 1991; 88: 9518-9522
  • 15 Horton J, Ratcliffe NA. Evolution of immunity. In: Immunology. Roitt I, Brostoff J, Male D. eds. 04. Mosby; London: 1996. pp 15.01-15.22
  • 16 Rowley AF, Hunt TC, Page M, Mainwaring GM. Fish In: Vertebrate Blood Cells. Rowley AF, Ratcliffe NA. eds. Cambridge University Press; Cambridge: 1988. pp 017-128
  • 17 Bone Q, Marshall NB, Blaxter JHS. Biology of Fishes 2ndedn. Blackie Academic. 1995
  • 18 Satchell GH. Physiology and Form of Fish Circulation. Cambridge University Press; Cambridge: 1991
  • 19 Satchell GH. The venous system. In: Fish Physiology Vol 12A. Hoar WS, Randall DJ, Farrell AP. eds. Academic Press; San Diego: 1992. pp. 141-187
  • 20 Bond CE. Biology of Fishes. Saunders; Philadelphia: 1979
  • 21 Farrell AP, Johansen JA. Vasoactivity of the coronary artery of rainbow trout, steelhead trout, and dogfish: lack of support for non-prostanoid endothelium-derived relaxation factors. Can J Zool 1995; 73: 1899-1911
  • 22 Brown JA, Bucknall RM. Antidiuretic and cardiovascular actions of prostaglandin E2in the rainbow trout Salmo gairdneri . Gen Comp Endocrinol 1986; 61: 330-337
  • 23 Mustafa T, Agnisola C, Tota B. Myocardial and coronary effects of exogenous arachidonic acid on the isolated and perfused heart preparation and its metabolism in the heart of trout (Oncorhynchus mykiss). Comp Biochem Physiol 1992; 103C: 163-167
  • 24 Chiono M, Heller RS, Andazola JJ, Herman CA. Leukotriene C4binds to receptors and has positive inotropic effects in bullfrog heart. J Pharmacol Exp Ther 1991; 256: 1042-1048
  • 25 Kagström J, Holmgren S, Olson KR, Conlon JM, Jensen J. Vasoconstrictive effects of native tachykinins in the rainbow trout, Oncorhynchus mykiss . Peptides 1996; 17: 39-45
  • 26 Olsen KR, Duff DW, Farrell AP, Keen J, Kellog MD. Cardiovascular effects of endothelin in trout. Am J Physiol 1991; 260: H1214-H1225
  • 27 Poder TC, Silberberg SD, Rampe D. Contraction of reptile, amphibian and fish blood vessels by endothelin-1. Can J Physiol Pharmacol 1991; 69: 215-217
  • 28 Ellis AE. The leucocytes of fish. J Fish Biol 1977; 11: 453-491
  • 29 Zapata A, Carrato A. Ultrastructure of elasmobranch and teleost thrombocytes. Acta Zool 1980; 61: 179-182
  • 30 Daimon T, Uchida K. Ultrastructural evidence of the existence of the surface connected canalicular system in the thrombocyte of the shark (Triakis scyllia). J Anat 1985; 141: 193-200
  • 31 Hunt TC, Rowley AF. Studies on the reticuloendothelial system of the dogfish, Scyliorhinus canicula . Endocytic activity of fixed cells in the gills and peripheral blood leucocytes. Cell Tissue Res 1986; 244: 215-226
  • 32 Hill DJ, Rowley AF. The thromboxane mimetic, U-46619, induces the aggregation of fish thrombocytes. Brit J Haematol 1996; 92: 200-211
  • 33 Harrison P, Cramer EM. Platelet α-granules. Blood Rev 1993; 7: 52-62
  • 34 Pica A, Lodato A, Grimaldi MC, Corte FD. Morphology, origin and functions of the thrombocytes of elasmobranchs. Arch Ital Anat Embriol 1990; 95: 187-207
  • 35 Lewis JH. Comparative haemostasis: studies on elasmobranchs. Comp Biochem Physiol 1972; 42A: 233-240
  • 36 Belamarich FA, Fusari MH, Shepro D. In vitro studies of aggregation of non-mammalian thrombocytes. Nature 1966; 212: 1579-1580
  • 37 Stokes EE, Firkin BG. Studies on the peripheral blood of the Port Jackson shark (Heterodontus portusjacksoni) with particular reference to the thrombocyte. Brit J Haematol 1971; 20: 427-435
  • 38 Woodward JJ, Smith L, Casillas E. Thrombocyte aggregation in rainbow trout. Comp Biochem Physiol 1981; 68A: 457-466
  • 39 Lloyd-Evans P, Barrow SE, Hill DJ, Bowden LA, Rainger GE, Knight J, Rowley AF. Eicosanoid generation and effects on the aggregation of thrombocytes from the rainbow trout, Oncorhynchus mykiss . Biochim Biophys Acta 1994; 1215: 291-299
  • 40 Gotwals PJ, Painesaunders SE, Stark KA, Hynes RO. Drosophila integrins and their ligands. Curr Opin Cell Biol 1994; 6: 734-739
  • 41 Kunicki TJ, Newman PJ. Synthesis of analogs of human platelet membrane glycoprotein IIb-IIIa complex by chicken peripheral blood thrombocytes. Proc Natl Acad Sci USA 1995; 82: 7319-7323
  • 42 Hynes RO. Integrins, versatility, modulation, and signaling in cell adhesion. Cell 1992; 69: 11-25
  • 43 Herd CM, Page CP. Do platelets have a role as inflammatory cells?. In: Immunopharmacology of Platelets. Joseph M. ed. Academic Press London: 1995: 01-20
  • 44 Clawson CC, White JG. Platelet interaction with bacteria V. Ultrastructure of congenital afibrinogenemic platelets. Am J Pathol 1980; 98: 197-212
  • 45 Thuvander A, Norrgren L, Fossum C. Phagocytic cells in blood from rainbow trout, Salmo gairdneri (Richardson), characterized by flow cytometry and electron microscopy. J Fish Biol 1987; 31: 197-208
  • 46 Doolittle RF, Surgenor DM. Blood coagulation in fish. Am J Physiol 1962; 203: 964-970
  • 47 Doolittle RF, Oncley JL, Surgenor DM. Species differences in the interaction of thrombin and fibrinogen. J Biol Chem 1962; 237: 3123-3127
  • 48 Doolittle RF. Further studies on clotting and fibrinolysis in plasma from the smooth dogfish (Mustelis canis). Brit J Haematol 1993; 09: 464-470
  • 49 Doolittle RF, Cottrell BA, Riley M. Amino acid composition of the subunit chains of lamprey fibrinogen. Evolutionary significance of some structural anomalies. Biochim Biophys Acta 1976; 453: 439-452
  • 50 Doolittle RF, Wooding GL. The subunit structure of lamprey fibrinogen and fibrin. Biochim Biophys Acta 1974; 271: 277-282
  • 51 Cottrell BA, Doolittle RF. Amino acid sequences of lamprey fibrino-peptides A and B and characterisation of the junctions split by lamprey and mammalian thrombins. Biochim Biophys Acta 1976; 453: 426-438
  • 52 van Vliet KJ, Smit GL, Pieterse JJ, Schoonbee HJ, van Vliet JHJ. Thromb-elastographic diagnosis of blood coagulation in two freshwater fish species. J Fish Biol 1985; 82A: 19-21
  • 53 Banfield DK, MacGillivray RTA. Partial characterization of vertebrate prothrombin cDNAs: amplification and sequence analysis of the B chain of thrombin from nine different species. Proc Natl Acad Sci 1992; 89: 2779-2783
  • 54 Doolittle RF. The evolution of vertebrate blood coagulation: a case of Yin and Yang. Thromb Haemost 1993; 70: 24-28
  • 55 Smit GL, Schoonbee HJ. Blood coagulation factors in freshwater fish Oreochromis mossambicus . J Fish Biol 1988; 32: 673-677
  • 56 Ellis AE, Hastings TS, Munro ALS. The role of Aeromonas salmonicida extracellular products in the pathology of furunculosis. J Fish Disease 1981; 04: 41-51
  • 57 Salte R, Norberg K, Amesen JA, Ødegaard OR, Eggset G. Serine protease and glycerophospholipid:cholesterol acyltransferase of Aeromonas salmonicida work in concert in thrombus formation; in vitro the process is counteracted by plasma antithrombin andα2-macroglobulin. J Fish Disease 1992; 15: 215-227
  • 58 Salte R, Norberg K, Ødegaard OR. Do extracellular products of Aeromonas salmonicida induce thrombosis by entering the fish coagulation system at factor X?. J Fish Disease 1991; 14: 401-406
  • 59 Salte R, Norberg K, Ødegaard OR, Arnesen JA, Olli JJ. Exotoxin-induced consumptive coagulopathy in Atlantic salmon, Salmo salar L.: inhibitory effects of exogenous antithrombin and α2-macroglobulin on Aeromonas salmonicida serine protease. J Fish Disease 1993; 16: 425-435
  • 60 Ellis AE. Inhibition of the Aeromonas salmonicida extracellular protease by α2-macroglobulin in the serum of rainbow trout. Microbial Pathogenesis 1987; 03: 167-177
  • 61 Freedman SJ. The role of alpha 2-macroglobulin in furunculosis: a comparison of rainbow trout and brook trout. Comp Biochem Physiol 1991; 98B:: 549-553