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Thromb Haemost 1988; 59(02): 186-192
DOI: 10.1055/s-0038-1642751
Original Articles
Schattauer GmbH Stuttgart

The Interaction of von Willebrand Factor (vWf) with Collagen: Investigation of vWf-Binding Sites in the Collagen Molecule

C M Fitzsimmons
1   Edinburgh, Royal Infirmary, Edinburgh and Strangeways Research Laboratory, Cambridge, UK
,
C G Cockburn
1   Edinburgh, Royal Infirmary, Edinburgh and Strangeways Research Laboratory, Cambridge, UK
,
V Hornsey
*   South-East Scotland Regional Blood Transfusion Service, Royal Infirmary, Edinburgh and Strangeways Research Laboratory, Cambridge, UK
,
C V Prowse
*   South-East Scotland Regional Blood Transfusion Service, Royal Infirmary, Edinburgh and Strangeways Research Laboratory, Cambridge, UK
,
M J Barnes
1   Edinburgh, Royal Infirmary, Edinburgh and Strangeways Research Laboratory, Cambridge, UK
› Author Affiliations
Further Information

Publication History

Received 07 July 1987

Accepted after revision 11 November 1987

Publication Date:
21 May 2018 (online)

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Summary

Following fragmentation of the collagen molecule, we have examined the ability of the isolated fragments to bind vWf. In view of the importance of collagen tertiary and quaternary structure for binding, fragments were first renatured to restore triple-helical conformation and then polymerized. Results indicate the presence of specific vWf-binding sites in both the αl(I)-and α2(I)-chains of type I collagen. Cleavage of the αl(I)-chain with cyanogen bromide suggests the presence of at least four (conceivably several more) binding sites implying a wide distribution of sites along the length of the collagen type I molecule. Collagen type III appears to possess a similar wide distribution of sites. Chemical modification of specific amino acid residues indicates that interaction involves arginyl residues in collagen and carboxyl groups in vWf. Although interaction between fibronec-tin and collagen fibres also involves collagen arginyl residues and carboxyl groups in fibronectin (authors’ unpublished results), fibronectin does not compete with vWf in the binding to collagen fibres.

Keywords

Collagen - von Willebrand factor - Fibronectin
 

  • References

  • 1 Zimmermann TS, Ruggeri ZM, Fulcher CA. Factor VUI/von Willebrand Factor. Prog Hematol 1983; 13: 279-309
    PubMedGoogle Scholar
  • 2 Tschopp TB, Weiss HJ, Baumgartner HR. Decreased adhesion of platelets to subendothelium in von Willebrand’s disease. J Lab Clin Med 1974; 83: 296-300
    PubMedGoogle Scholar
  • 3 Weiss HJ, Turitto VT, Baumgartner HR. Effect of shear rate on platelet interaction with subendothelium in citrated and native blood. I. Shear dependent decrease of adhesion in von Willebrand’s disease and the Bernard-Soulier syndrome J Lab Clin Med 1978; 92: 750-764
    PubMedGoogle Scholar
  • 4 Sakariassen KS, Bolhuis PA, Sixma JJ. Human blood platelet adhesion to artery subendothelium is mediated by factor VIII- von Willibrand factor bound to the subendothelium. Nature 1979; 279: 636-638
    CrossrefPubMedGoogle Scholar
  • 5 Baumgartner HR, Tschopp TB, Meyer D. Shear rate dependent inhibition of platelet adhesion and aggregation on collagenous surfaces by antibodies to human factor VUI/von Willebrand factor. Brit J Haematol 1980; 44: 127-139
    CrossrefPubMedGoogle Scholar
  • 6 Stel HV, Sakariassen KS, de Groot PG, van Mourik JA, Sixma JJ. Von Willebrand factor in the vessel wall mediates platelet adherence. Blood 1985; 65: 85-90
    PubMedGoogle Scholar
  • 7 Turitto VT, Weiss HJ, Zimmermann TS, Sussman II. Factor VIII/ von Willebrand factor in subendothelium mediates platelet adhesion. Blood 1985; 65: 823-31
    PubMedGoogle Scholar
  • 8 Fauvel F, Grant ME, Legrand YJ, Souchon H, Tobelem G, Jackson DS, Caen JP. Interaction of blood platelets with a microfibrillar extract from adult bovine aorta: Requirement for von Willebrand factor. Proc Natl Acad Sci USA 1983; 80: 551-554
    CrossrefPubMedGoogle Scholar
  • 9 Baumgartner HR, Tschopp TB, Weiss HJ. Platelet interaction with collagen fibrils in flowing blood. II. Impaired adhesion-aggregation in bleeding disorders. A comparison with subendothelium Thromb Haemostas 1977; 37: 17-28
    PubMedGoogle Scholar
  • 10 Aihara M, Cooper HA, Wagner RH. Platelet-collagen interactions: Increase in rate of adhesion of fixed washed platelets by factor VIII- related antigen. Blood 1984; 63: 495-501
    PubMedGoogle Scholar
  • 11 Leytin VL, Gorbunova WA, Misselwitz F, Novitkov ID, Podrez EA, Plyusch OP, Likhachova EA, Repin VS, Smirnov VN. Step-by- step analysis of adhesion of human platelets to a collagen-coated surface defect in initial attachment and spreading of platelets in von Willebrand’s disease. Thromb Res 1984; 34: 51-63
    CrossrefPubMedGoogle Scholar
  • 12 Houdijk WP M, Sakariassen KS, Nievelstein PF E M, Sixma IJ. Role of Factor VUI/von Willebrand factor and fibronectin in the interaction of platelets in flowing blood with momoneric and fibrillar human collagen types I and III. J Clin Invest 1985; 75: 531-540
    CrossrefPubMedGoogle Scholar
  • 13 Girma JP, Kalafatis M, Pietu G, Lavergne JM, Chopek MW, Edgington TS, Meyer D. Mapping of distinct von Willebrand factor domains interacting with platelets GPIb and GPIIb/IIIa and with collagen using monoclonal antibodies. Blood 1986; 67: 1356-1366
    PubMedGoogle Scholar
  • 14 Houdijk WP M, Girma JP, van Mourik JA, Sixma JJ, Meyer D. Comparison of tryptic fragments of von Willebrand factor involved in binding to thrombin-activated platelets with fragments involved in ristocetin-induced binding and binding to collagen. Thromb Haemostas 1986; 56: 391-396
    PubMedGoogle Scholar
  • 15 LaDuca FM, Bettigole RE, Bell WR, Robson EB. Platelet-collagen interaction: Inhibition by ristocetin and enhancement by von Willebrand factor - platelet binding. Blood 1986; 68: 927-937
    PubMedGoogle Scholar
  • 16 Weiss HJ, Turitto VT, Baumgartner HR. Platelet adhesion and thrombus formation on subendothelium in platelets deficient in glycoproteins Ilb-IIIa, lb and storage granules. Blood 1986; 67: 322-330
    CrossrefPubMedGoogle Scholar
  • 17 Coller BS, Peerschke EI, Scudder LE, Sullivan CA. Studies with a murine monoclonal antibody that abolished ristocetin induced binding of von Willebrand factor to platelets: additional evidence in support of GPIb as a platelet receptor for von Willebrand factor. Blood 1983; 61: 99-110
    PubMedGoogle Scholar
  • 18 Ruggeri ZM, DeMarco L, Gatti L, Bader R, Montgomery RR. Platelets have more than one binding site for von Willebrand factor. J Clin Invest 1983; 72: 1-12
    CrossrefPubMedGoogle Scholar
  • 19 Plow EF, Pierschbacher MD, Ruoslahti E, Marguerie GA, Ginsberg MH. The effect of arg-gly-asp-containing peptides on fibrinogen and von Willebrand factor binding to platelets. Proc Natl Acad Sci USA 1985; 82: 8057-8061
    CrossrefPubMedGoogle Scholar
  • 20 Sarkariassen KB, Nievelstein P FE M, Coller BS, Sixma JJ. The role of platelet membrane glycoproteins lb and Ilb-IIIa in platelet adherence to human artery subendothelium. Brit J Haematol 1986; 63: 681-691
    CrossrefPubMedGoogle Scholar
  • 21 Santoro SA, Cowan JF. Thrombin enhanced adhesion of platelets to von Willebrand factor substrates. Thromb Res 1986; 43: 57-72
    CrossrefPubMedGoogle Scholar
  • 22 Furlan M. Factor VUI/von Willebrand factor: A multivalent ligand binding to platelets and collagen. Blut 1986; 52: 329-336
    CrossrefPubMedGoogle Scholar
  • 23 Legrand YJ, Rodriguez-Zeballos A, Kartalis G, Fauvel F, Caen JP. Adsorption of factor VIII antigen-activity complex by collagen. Thromb Res 1978; 13: 909-911
    CrossrefPubMedGoogle Scholar
  • 24 Nyman D. Von Willebrand factor dependent platelet aggregation and adsorption of factor VIII related antigen by collagen. Thromb Res 1980; 17: 209-214
    CrossrefPubMedGoogle Scholar
  • 25 Santoro SA. Adsorption of von Willebrand factor/factor VIII by the genetically distinct interstitial collagens. Thromb Res 1982; 21: 689-693
    PubMedGoogle Scholar
  • 26 Santoro SA. Preferential binding of high molecular weight forms of von Willebrand factor to fibrillar collagen. Biochim Biophys Acta 1983; 756: 123-126
    CrossrefPubMedGoogle Scholar
  • 27 Kessler CM, Floyd CM, Rick ME, Krizek DM, Lee SL, Gralnick HR. Collagen-factor VUI/von Willebrand factor protein interaction. Blood 1984; 63: 1291-1298
    PubMedGoogle Scholar
  • 28 Scott DM, Griffin B, Pepper DS, Barnes MJ. The binding of purified factor VUI/von Willebrand factor to collagens of differing type and form. Thromb Res 1981; 24: 467-472
    CrossrefPubMedGoogle Scholar
  • 29 Santoro SA, Cowan JF. Adsorption of von Willebrand factor by fibrillar collagen (Implications concerning the adhesion of platelets to collagen. Collagen Rel Res 1982; 2: 31-43
    CrossrefPubMedGoogle Scholar
  • 30 Morton LF, Griffin B, Pepper DS, Barnes MJ. The interaction between collagens and factor VUI/von Willebrand factor: Investigation of the structural requirements for interaction. Thromb Res 1983; 32: 545-556
    CrossrefPubMedGoogle Scholar
  • 31 Bockenstedt P, McDonagh J, Handin RI. Binding and covalent cross- linking of purified von Willebrand factor to native monomeric collagen. J Clin Invest 1986; 78: 551-556
    CrossrefPubMedGoogle Scholar
  • 32 Pareti FI, Fujimura Y, Dent JA, Holland LZ, Zimmerman TS, Ruggeri ZM. Isolation and characterisation of a collagen binding domain in human von Willebrand factor. J Biol Chem 1986; 261: 15310-15315
    PubMedGoogle Scholar
  • 33 Roth GJ, Titani K, Hoyer LW, Hickey MJ. Localisation of binding sites within human von Willebrand factor for monomeric type III collagen. Biochemistry 1986; 25: 8357-8361
    CrossrefPubMedGoogle Scholar
  • 34 Fritzsimmons CM, Cawston TE, Barnes MJ. Biologicaly reactive sites in collagen involved in its haemostatic function. Biochem Soc Trans 1986; 14: 1085-1086
    CrossrefPubMedGoogle Scholar
  • 35 Tkocz C, Kuhn K. The formation of triple-helical collagen molecules from al or a2 polypeptide chains. Europ J Biochem 1969; 7: 454-464
    PubMedGoogle Scholar
  • 36 Piez KA, Eigner EA, Lewis MS. The chromatographic separation and amino acid composition of the subunits of several collagens. Biochemistry 1963; 2: 58-66
    CrossrefPubMedGoogle Scholar
  • 37 Fujii T, Kuhn K. Isolation and characterisation of pepsin-treated type III collagen form calf skin. Hoppe-Seyler’s Z. Physiol Chem 1975; 356: 1793-1801
    PubMedGoogle Scholar
  • 38 Fitzsimmons CM, Cawston TE, Barnes MJ. The platelet reactivity of collagen type I: Evidence for multiple platelet-reactive sites in the type I collagen molecule. Thromb Haemostas 1986; 56: 95-99
    PubMedGoogle Scholar
  • 39 Rauterberg J, Allmann H, Henkel W, Fietzek PP. Isolation and characterisation of CNBr derived peptides of the al(III) chain of pepsin-solubilised calf skin collagen. Hoppe-Seyler’s Z Physiol Chem 1976; 357: 1401-1407
    PubMedGoogle Scholar
  • 40 Fitzsimmons CM, Barnes MJ. The platelet reactivity of the a2(I)- chain of type I collagen: Platelet aggregation induced by polymers of the molecule [a2(I)]3 . Thromb Res 1985; 39: 523-531
    CrossrefPubMedGoogle Scholar
  • 41 Laurell CB. Quantitative estimation of proteins by electrophoresis in agarose gel containing antibodies. Analyt Biochem 1966; 15: 45-52
    CrossrefPubMedGoogle Scholar
  • 42 Salacinski P RP, McLean C, Sykes JE C, Clement-Jones VV, Lowry PJ. Localisation of proteins, glycoproteins and peptides using a solid- phase oxidising agent, 1, 3, 4, 6-tetrachloro-3a, 6a-diphenyl glycoluril (Iodogen). Analyt Biochem 1981; 117: 136-146
    CrossrefPubMedGoogle Scholar
  • 43 Weber K, Osborn M. Proteins and sodium dodecyl sulphate: molecular weight determination on polyacrylamide gels and related procedures. In The Proteins 3rd Edn. Vol. 1 Neurath H, Hill RL. Eds. p 179-223 Academic Press; New York: 1975
    Google Scholar
  • 44 Vuento M, Vaheri A. Purification of fibronectin from human plasma by affinity chromatography under non-denaturing conditions. Biochem J 1979; 183: 331-337
    CrossrefPubMedGoogle Scholar
  • 45 Wilner GD, Nossel HL, Procupez TL. Aggregation of platelets by collagen: polar active sites of insoluble human collagen. Amer J Physiol 1971; 220: 1074-1079
    PubMedGoogle Scholar
  • 46 Santoro SA. Amino group modification inhibits ristocetin cofactor activity of human von Willebrand factor. Biochem Biophys Res Commun 1982; 108: 479-485
    CrossrefPubMedGoogle Scholar
  • 47 Jorgensen AM, Borders CL, Fish WW. Arginine residues are critical for the heparin-cofactor activity of antithrombin III. Biochem J 1985; 231: 59-63
    CrossrefPubMedGoogle Scholar
  • 48 Wang CL, Miyata T, Weksler B, Rubin AL, Stenzel KH. Collagen- derivated platelet aggregation and release. I. Effects of side-chain modification and role of arginyl residues. Biochem Biophys Acta 1978; 544: 555-567
    CrossrefPubMedGoogle Scholar
  • 49 Fersht AR, Sperling J. The charge relay system in chymotrypsin and chymotrypsinogen. J Mol Biol 1973; 74: 137-149
    CrossrefPubMedGoogle Scholar
  • 50 Morton LF, Fizsimmons CM, Rauterberg J, Barnes MJ. Platelet reactive sites in collagen. Collagens I and III posses different aggregatory sites. Biochem J 1987; 248: 483-487
    CrossrefPubMedGoogle Scholar
  • 51 Barnes MJ. The collagen-platelet interaction. In Collagen in Health and Disease. Weiss JB, Jayson MI V. (eds) p 179 Churchill Livingstone; Edinburgh: 1982
    Google Scholar
  • 52 Barnes MJ. Blood vessel wall matrix components involved in vessel wall thrombogenicity. In Biology and Pathology of Platelet-Vessel Wall Interactions Jolles G, Legrand YJ, Nurden AT. Eds p 21 Academic Press; London: 1986
    Google Scholar
  • 53 Bockenstedt P, Greenberg JM, Handin RI. Structural basis of von Willebrand factor binding to glycoprotein lb and collagen. Effects of disulphate reduction and limited proteolysis of polymeric von Willebrand factor J Clin Invest 1986; 77: 743-749
    CrossrefPubMedGoogle Scholar
  • 54 Brown JE, Bosak JO. An Elisa test for the binding of von Willebrand antigen to collagen. Thromb Res 1986; 43: 303-311
    CrossrefPubMedGoogle Scholar
  • 55 Fretto LJ, Fowler WE, McCaslin DR, Erickson HP, McKee PA. Substructure of human von Willebrand factor. Proteolysis by V8 and characterisation of two functional domains J Biol Chem 1986; 261: 15679-89
    PubMedGoogle Scholar