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Thromb Haemost 1989; 62(03): 989-995
DOI: 10.1055/s-0038-1651040
Original Article
Schattauer GmbH Stuttgart

Thrombin Stimulated Platelet Accumulation on Protein Coated Glass Capillaries: Role of Adhesive Platelet α-Granule Proteins

Juliette N Mulvihill
INSERM U.311. Biologie et Pharmacologie des Interactions du Sang avec les Vaisseaux et les Biomatériaux, Centre Régional de Transfusion Sanguine, Strasbourg, France
,
J Andrew Davies
*   University Department of Medicine, The General Infirmary, Leeds, United Kingdom
,
Florence Toti
INSERM U.311. Biologie et Pharmacologie des Interactions du Sang avec les Vaisseaux et les Biomatériaux, Centre Régional de Transfusion Sanguine, Strasbourg, France
,
Jean-Marie Freyssinet
INSERM U.311. Biologie et Pharmacologie des Interactions du Sang avec les Vaisseaux et les Biomatériaux, Centre Régional de Transfusion Sanguine, Strasbourg, France
,
Jean-Pierre Cazenave
INSERM U.311. Biologie et Pharmacologie des Interactions du Sang avec les Vaisseaux et les Biomatériaux, Centre Régional de Transfusion Sanguine, Strasbourg, France
› Author Affiliations
Further Information

Publication History

Received: 13 November 1988

Accepted after revision 11 July 1989

Publication Date:
30 June 2018 (online)

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Summary

The generation of trace amounts of thrombin at artificial surfaces in contact with blood is likely to be a contributing factor in thrombosis on biomaterials. Using an in vitro capillary perfusion system, platelet accumulation on glass surfaces, uncoated or precoated with purified bovine collagen or human plasma proteins, was determined in the presence or absence of preadsorbed purified human thrombin. Static adsorption for 15 min at 22° C from solutions of thrombin 100 NIH units (33 μg)/ml gave surface concentrations in the range 0.019-0.101 μg/cm2. Protein coated capillaries, thrombin treated or untreated, were perfused for 2 min at 37° C with suspensions of washed 111In-labeled human platelets in Tyrode's-albumin buffer containing 40% washed red blood cells, under conditions of controlled, non pulsatile laminar flow (50 s−1 or 2,000 s−1). Platelet accumulation was increased in the presence of surface adsorbed thrombin on uncoated and albumin or fibrinogen coated glass but little affected on fibronectin or collagen coated glass. On von Willebrand factor (vWF) coated glass, thrombin enhancement was observed only at high shear forces. In experiments using antibodies against human platelet α-granule proteins, thrombin stimulated platelet deposition in uncoated glass capillaries was inhibited at 2,000 s−1 by anti-vWF and to a lesser extent by anti-fibrinogen but not by antithrombospondin antibodies.

Keywords

Platelet accumulation - Capillary perfusion - Thrombin - Adhesive α-granule protein - Biomaterials
 

  • References

  • 1 Salzman EW, Merrill EW. Interaction of blood with artificial surfaces. In: Hemostasis and Thrombosis. Basic Principles and Clinical Practice. 2nd ed Colman RW, Hirsh J, Marder VJ, Salzman EW. (eds) J. B. Lippincott Company; Philadelphia: 1987. pp 1335-1347
    Google Scholar
  • 2 Cazenave JP. Interaction of platelets with surfaces. In: Blood-Surface Interactions: Biological Principles Underlying Haemocompatibility with Artificial Materials. Cazenave JP, Davies JA, Kazatchkine MD, van Aken WG. (eds). Elsevier; Amsterdam: 1986. pp 89-105
    Google Scholar
  • 3 van Mourik JA, van Aken WG. Initiation of blood coagulation and fibrinolysis. In: Blood-Surface Interactions: Biological Principles Underlying Haemocompatibility with Artificial Materials. Cazenave JP, Davies JA, Kazatchkine MD, van Aken WG. (eds). Elsevier; Amsterdam: 1986. pp 61-73
    Google Scholar
  • 4 Jenkins CS P, Packham MA, Guccione MA, Mustard JF. Modification of platelet adherence to protein-coated surfaces. J Lab Clin Med 1973; 81: 280-290
    PubMedGoogle Scholar
  • 5 Mosher DF. Influence of proteins on platelet-surface interactions. In: Interaction of the Blood with Natural and Artificial Surfaces. Salzman EW. (ed). Marcel Dekker; New York: 1981. pp 85-101
    Google Scholar
  • 6 Zucker MB, Vroman L. Platelet adhesion induced by fibrinogen adsorbed to glass. Proc Soc Exp Biol Med 1969; 131: 318-320
    CrossrefPubMedGoogle Scholar
  • 7 Zimmerman TS, Ruggeri ZM. Von Willebrand's disease. In: Progress in Hemostasis and Thrombosis. Spaet TH. (ed). Grune and Stratton; Orlando, FL: 1982. (Vol; 6). pp 203-236
    Google Scholar
  • 8 Packham MA, Mustard JF. Platelet adhesion. In: Progress in Hemostasis and Thrombosis. Spaet TH. (ed). Grune and Stratton; Orlando, FL: 1984. (Vol; 7). pp 211-288
    Google Scholar
  • 9 Baumgartner HR. Platelet interaction with collagen in flowing blood. I. Reaction of human platelets with α-chymotrypsin-digested subendothelium. Thromb Haemostas 1977; 37: 1-16
    PubMedGoogle Scholar
  • 10 Plow EF, Ginsberg MH, Marguerie GA. Expression and function of adhesive proteins on the platelet surface. In: Biochemistry of Platelets. Phillips DR, Shuman MA. (eds). Academic Press; Orlando, FL: 1986. pp 225-256
    Google Scholar
  • 11 Niewiarowski S, Holt JC. Platelet a-granule proteins: biochemical and pathological aspects. In: The Platelets: Physiology and Pharmacology. Longenecker GL. (ed). Academic Press; Orlando, FL: 1985. pp 49-83
    Google Scholar
  • 12 Adams GA. Platelet adhesion: past and present. In: The Platelets: Physiology and Pharmacology. Longenecker GL. (ed). Academic Press; Orlando, FL: 1985. pp 15-47
    Google Scholar
  • 13 Cazenave JP, Hemmendinger S, Beretz A, Sutter-Bay A, Launay J. L agregation plaquettaire: outil d'investigation clinique et d'etude pharmacologique. Méthodologie. Ann Biol Clin 1983; 41: 167-179
    PubMedGoogle Scholar
  • 14 Ruoslahti E, Hayman EG, Pierschbacher M, Engvall E. Fibronectin: purification, immunochemical properties and biological activities. In: Methods in Enzymology (Vol; 82). Structural and Contractile Proteins, Part A: Extracellular Matrix.. Cunningham LW, Frederiksen DW. (eds). Academic Press; New York: 1982. pp 803-831
    Google Scholar
  • 15 Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-685
    CrossrefPubMedGoogle Scholar
  • 16 Kekwick RA, Mackay ME, Nance MH, Record BR. The purification of human fibrinogen. Biochem J 1955; 60: 671-683
    PubMedGoogle Scholar
  • 17 Regoeczi E. The clottability of iodinated fibrinogen. J Nucl Biol Med 1971; 15: 37-41
    PubMedGoogle Scholar
  • 18 Cazenave JP, Packham MA, Mustard JF. Adherence of platelets to a collagen-coated surface: development of a quantitative method. J Lab Clin Med 1973; 82: 987-990
    PubMedGoogle Scholar
  • 19 Owen WG, Jackson CM. Activation of prothrombin with Oxyuranus scutellatus scutellatus (Taipan-snake) venom. Thromb Res 1973; 3: 705-714
    CrossrefPubMedGoogle Scholar
  • 20 Poison A, von Wechmar MB, Fazakerley G. Antibodies to proteins from yolk of immunized hens. Immunol Comm 1980; 9: 495-514
    PubMedGoogle Scholar
  • 21 Goding JW. Purification, fragmentation and isotopic labelling of monoclonal antibodies. In: Monoclonal Antibodies: Principles and Practice 2nd ed. Academic Press; London: 1986. pp 104-141
    Google Scholar
  • 22 Towbin H, Gordon J. Immunoblotting and clot immunoblotting. Current status and outlook. J Immunol Methods 1984; 72: 313-340
    CrossrefPubMedGoogle Scholar
  • 23 Mulvihill JN, Huisman HG, Cazenave JP, van Mourik JA, van Aken WG. The use of monoclonal antibodies to human platelet membrane glycoprotein IIb-IIIa to quantitate platelet deposition on artificial surfaces. Thromb Haemostas 1987; 58: 724-731
    PubMedGoogle Scholar
  • 24 Mulvihill JN, Cazenave JP. Interactions des plaquettes sanguines avec les biomatériaux hemocompatibles. Bull Soc Chim France 1985; 4: 551-554
    PubMedGoogle Scholar
  • 25 Coller BS. Von Willebrand disease. In: Hemostasis and Thrombosis. Basic Principles and Clinical Practice. 2nd ed. Colman RW, Hirsh J, Marder VJ, Salzman EW. (eds). J. B. Lippincott Company; Philadelphia: 1987. pp 60-96
    Google Scholar
  • 26 Stiirzebecher J. Inhibitors of thrombin. In: The Thrombin (Vol; 1.). Machovich R. (ed). CRC Press; Florida: 1984. pp 131-160
    Google Scholar
  • 27 Regoeczi E. Iodine-Labeled Plasma Proteins. CRC Press; Florida: 1984. pp 49-56
    Google Scholar
  • 28 Mustard JF, Perry DW, Ardlie NG, Packham MA. Preparation of suspensions of washed platelets from humans. Br J Haematol 1972; 22: 193-204
    CrossrefPubMedGoogle Scholar
  • 29 Cazenave JP, Blondowska D, Richardson M, Kinlough-Rathbone RL, Packham MA, Mustard JF. Quantitative radioisotopic measurement and scanning electron microscopic study of platelet adherence to a collagen-coated surface and to subendothelium with a rotating probe device. J Lab Clin Med 1979; 93: 60-70
    PubMedGoogle Scholar
  • 30 Eber M, Cazenave JP, Grob JC, Abecassis J, Methlin G. 111Indium labelling of human washed platelets; kinetics and in vivo sequestration sites. In: Blood Cells in Nuclear Medicine, Part I Cell Kinetics and Bio-distribution.. Hardeman MR, Najean Y. (eds). Martinus Nijhoff Publishers; Boston: 1984. pp 29-43
    Google Scholar
  • 31 Dryjski M, Swedenborg J, Wasiutynski A. Uptake and inactivation of thrombin on aortic endothelium and neo-intima. Eur Surg Res 1985; 17: 1-9
    PubMedGoogle Scholar
  • 32 Basmadjian D, Sefton MV. A model of thrombin inactivation in heparinized and non heparinized tubes with consequences for thrombus formation. J Biomed Mater Res 1986; 20: 633-651
    CrossrefPubMedGoogle Scholar
  • 33 Hanson SR, Harker LA. Interruption of acute platelet-dependent thrombosis by the synthetic antithrombin D-phenylalanyl-L-prolyl-L-arginyl-chloromethyl ketone. Proc Natl Acad Sci USA 1988; 85: 3184-3188
    CrossrefPubMedGoogle Scholar
  • 34 Turitto VT, Weiss HJ, Baumgartner HR. Platelet interaction with rabbit subendothelium in von Willebrand's disease: altered thrombus formation distinct from defective platelet adhesion. J Clin Invest 1984; 74: 1730-1741
    CrossrefPubMedGoogle Scholar
  • 35 Waugh DF, Baughman DJ. Thrombin adsorption and possible relations to thrombus formation. J Biomed Mater Res 1969; 3: 145-164
    CrossrefPubMedGoogle Scholar
  • 36 Feuerstein IA, Dickson VM. Adhesion and aggregation of thrombin prestimulated human platelets on surface-bound fibrinogen: evidence for involvement of ADP and arachidonic acid pathways. Thromb Haemostas 1983; 50: 679-685
    PubMedGoogle Scholar
  • 37 Feuerstein IA, Skupny-Gamham LE. Adhesion and aggregation of thrombin prestimulated human platelets: evaluation of surface-bound fibrinogen and surface-bound albumin. Thromb Res 1986; 43: 497-505
    CrossrefPubMedGoogle Scholar
  • 38 Adams GA, Feuerstein IA. Kinetics of platelet adhesion and aggregation on protein-coated surfaces: morphology and release from dense granules. ASAIO J 1981; 4: 90-99
    PubMedGoogle Scholar
  • 39 Poot A, Beugeling T, Cazenave JP, Bantjes A, van Aken WG. Platelet deposition in a capillary perfusion model: quantitative and morphological aspects. Biomaterials 1988; 9: 126-132
    CrossrefPubMedGoogle Scholar
  • 40 Weiss HJ, Turitto VT, Baumgartner HR. Effect of shear rate on platelet interaction with subendothelium in citrated and native blood. I. Shear rate-dependent decrease of adhesion in von Willebrand's disease and the Bernard-Soulier syndrome. J Lab Clin Med 1978; 92750-92764
    PubMedGoogle Scholar
  • 41 Cazenave JP, Mulvihill JN. Capillary perfusion system for quantitative evaluation of protein adsorption and platelet adhesion to artificial surfaces. In: Proteins at Interfaces: Physicochemical and Biochemical Studies. Brash JL, Horbett TA. (eds). American Chemical Society; Washington D C: 1987. pp 537-550
    Google Scholar
  • 42 Fressinaud E, Baruch D, Rothschild C, Baumgartner HR, Meyer D. Platelet von Willebrand factor: evidence for its involvement in platelet adhesion to collagen. Blood 1987; 70: 1214-1217
    PubMedGoogle Scholar
  • 43 Fujimoto T, Ohara S, Hawiger J. Thrombin-induced exposure and prostacyclin inhibition of the receptor for factor VHI/von Willebrand factor on human platelets. J Clin Invest 1982; 69: 1212-1222
    CrossrefPubMedGoogle Scholar
  • 44 Rand JH, Gordon RE, Sussman II, Chu SV, Solomon V. Electron microscopic localization of factor-VUI-related antigen in adult human blood vessels. Blood 1982; 60: 627-634
    PubMedGoogle Scholar
  • 45 Dejana E, Cazenave JP, Hatton MW C, Richardson M, Groves HM, Kinlough-Rathbone RL, Packham MA, Mustard JF. The effect of thrombin on platelet accumulation on the vessel wall - influence of heparin and aspirin. Thromb Haemostas 1983; 50: 567-571
    PubMedGoogle Scholar
  • 46 Nurden AT, Hasitz M, Rosa JP. Inhibition of thrombin-induced platelet aggregation by a rabbit antibody against human platelet thrombospondin. Thromb Haemostas 1983; 50: 401
    PubMedGoogle Scholar
  • 47 Leung LL K. Role of thrombospondin in platelet aggregation. J Clin Invest 1984; 74: 1764-1772
    CrossrefPubMedGoogle Scholar