Thromb Haemost 2002; 87(04): 763-770
DOI: 10.1055/s-0037-1613077
Review Article
Schattauer GmbH

Reduced High Shear Platelet Adhesion to the Vascular Media: Defective von Willebrand Factor Binding to the Interstitial Collagen

Erzsebet Komorowicz
1   Section of Hematology Research, Mayo Clinic and Foundation for Education and Research, Rochester, MN
4   Visiting Scientist, from Department of Medical Biochemistry, Semmelweis University, Budapest, Hungary
,
Robert D. McBane II
2   Division of Cardiovascular Medicine, Mayo Clinic and Foundation for Education and Research, Rochester, MN
,
Jon Charlesworth
3   Electron Microscopy Facility, Mayo Clinic and Foundation for Education and Research, Rochester, MN
,
David N. Fass
1   Section of Hematology Research, Mayo Clinic and Foundation for Education and Research, Rochester, MN
› Author Affiliations
Further Information

Publication History

Received 28 August 2001

Accepted after resubmission 08 January 2002

Publication Date:
08 December 2017 (online)

Summary

Fibrillar collagen serves as a thrombogenic surface for platelet adhesion mediated by von Willebrand factor (vWf) at high shear. Although abundant throughout the arterial wall, vWf-dependent platelet deposition to artery cross-sections from perfused citrated blood is localized to the adventitia of the vessel wall. Here we describe a similarly skewed distribution of vWf-binding sites in artery cross-sections. Binding of vWf-coated fluorescent beads, as well as detection of plasma vWf bound to artery cross-section at 3350 s−1 shear rate with indirect particle-immunofluorescence or immunoelectron microscopy demonstrate vWf binding sites in the adventitia, but not in the media. A monoclonal anti-vWf antibody that interferes with vWf-binding to collagen in a microplate ELISA inhibits vWf-binding to both the adventitia and sections of collagen fibrils. Our data suggest that the media, despite its fibrillar collagen content, evidenced by electron microscopy, is defective for vWf-binding, which may explain its thromboresistant nature at high shear rates.

 
  • References

  • 1 Wester J, Sixma JJ, Geuze JJ, Van der Veen J. Morphology of the early hemostasis in human skin wounds. Influence of acetylsalicylic acid. Lab Invest 1978; 39: 298-311.
  • 2 Sawada Y, Fass DN, Katzmann JA, Bahn RC, Bowie EJW. Hemostatic plug formation in normal and von Willebrand pigs: the effect of the administration of cryoprecipitate and a monoclonal antibody to Willebrand factor. Blood 1986; 67: 1229-39.
  • 3 Hovig T, Stormorken H. Ultrastructural studies on the platelet plug formation in bleeding time wounds from normal individuals and patients with von Willebrand’s disease. Acta Pathol Microbiol Scand (Suppl) 1974; 248: 105.
  • 4 Ruggeri ZM, Ware J. The structure and function of von Willebrand factor. Thromb Haemost 1992; 67: 594-9.
  • 5 Pareti FI, Niiya K, McPherson JM, Ruggeri ZM. Isolation and characterization of two domains of human von Willebrand factor that interact with fibrillar collagen types I and III. J Biol Chem 1987; 262: 13835-41.
  • 6 Mazzucato M, Spessoto P, Masotti A, De Appollonia L, Cozzi MR, Yoshioka A, Perris R, Colombatti A, De Marco L. Identification of domains responsible for von Willebrand factor type VI collagen interaction mediating platelet adhesion under high flow. J Biol Chem 1999; 274: 3033-41.
  • 7 Siedlecki CA, Lestini BJ, Kottke-Marchant K, Eppell SJ, Wilson DL, Marchant RE. Shear-dependent changes in the three-dimensional structure of human von Willebrand factor. Blood 1996; 88: 2939-50.
  • 8 Kroll MH, Hellums JD, McIntire LV, Schafer AI, Moake JL. Platelets and shear stress. Blood 1996; 88: 1525-41.
  • 9 Turitto VT, Baumgartner HR. Initial deposition of platelets and fibrin on vascular surfaces in flowing blood. In: Hemostasis and Thrombosis. Basic Principles and Clinical Practice. 3rd ed. Colman RW, Hirsch J, Marder VJ, Salzman EW. eds. Philadelphia: J. B. Lippincott; 1994: 805-22.
  • 10 Weiss HJ, Turitto VT, Baumgartner HR. Effect of shear rate on platelet interaction with subendothelium in citrated and native blood. I. Shear ratedependent decrease of adhesion in von Willebrand’s disease and the Bernard-Soulier syndrome. J Lab Clin Med 1978; 92: 750-64.
  • 11 Houdijk WPM, Sakariassen KS, Nievelstein PFEM, Sixma JJ. Role of factor VIII-von Willebrand factor and fibronectin in the interaction of platelets in flowing blood with monomeric and fibrillar human collagen types I and III. J Clin Invest 1985; 75: 531-40.
  • 12 Badimon L, Badimon JJ, Turitto VT, Vallabhajosula S, Fuster V. Platelet thrombus formation on collagen type I. A model of deep vessel injury. Influence of blood rheology, von Willebrand factor, and blood coagulation. Circulation 1988; 78: 1431-42.
  • 13 Tsuji S, Sugimoto M, Miyata S, Kuwahara M, Kinoshita S, Yoshioka A. Real-time analysis of mural thrombus formation in various platelet aggregation disorders: distinct shear-dependent roles of platelet receptors and adhesive proteins under flow. Blood 1999; 94: 968-75.
  • 14 Van Zanten GH, De Graaf S, Slootweg PJ, Heijnen HFG, Connolly TM, De Groot PG, Sixma JJ. Increased platelet deposition on atherosclerotic coronary arteries. J Clin Invest 1994; 93: 615-32.
  • 15 Fass DN, Shi C, Specks U. Von Willebrand dependent binding of platelets to artery wall. Circulation 1995; 92 (Suppl)1: 804.
  • 16 Bowie EJW, Owen Jr CA, Zollman PE, Thompson Jr JH, Fass DN. Tests of hemostasis in swine: normal values and values in pigs affected with von Willebrand’s disease. Am J Vet Res 1973; 34: 1405-7.
  • 17 Olson JD, Brockway WJ, Fass DN, Bowie EJW, Mann KG. Purification of porcine and human ristocetin-Willebrand factor. J Lab Clin Med 1977; 89: 1278-94.
  • 18 Katzmann JA, Mujwid DK, Miller RS, Fass DN. Monoclonal antibodies to von Willebrand’s factor: reactivity with porcine and human antigens. Blood 1981; 58: 530-6.
  • 19 Bowie EJW, Fass DN, Katzmann JA. Functional studies of Willebrand factor using monoclonal antibodies. Blood 1983; 62: 146-51.
  • 20 Takami H, Nichols WL, Kaese SE, Miller RS, Katzmann JA, Bowie EJW. Monoclonal antibodies against porcine platelet membrane glycoproteins Ib and IIb/IIIa. Blood 1988; 72: 1740-7.
  • 21 Lindmark R, Thoren-Tolling K, Sjoquist J. Binding of Immunoglobulins to Protein A and immunoglobulin levels in mammalian sera. J Immunol Meth 1983; 62: 1-13.
  • 22 Brodsky B, Eikenberry EF. Characterization of fibrous forms of collagen. Methods Enzymol 1982; 82: 127-74.
  • 23 Sakariassen KS, Aarts PAMM, de Groot PG, Houdijk WPM, Sixma JJ. A perfusion chamber developed to investigate platelet interaction in flowing blood with human vessel wall cells, their extracellular matrix, and purified components. J Lab Clin Med 1983; 102: 522-35.
  • 24 Spurr AR. A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 1969; 26: 31-43.
  • 25 Badimon JJ, Lettino M, Toschi V, Fuster V, Berrozpe M, Chesebro JH, Badimon L. Local inhibition of tissue factor reduces the thrombogenicity of disrupted human atherosclerotic plaques. Circulation 1999; 99: 1780-7.
  • 26 Colman RW, Cook JJ, Niewiarowski S. Mechanisms of platelet aggregation. In: Hemostasis and Thrombosis. Basic Principles and Clinical Practice. 3rd ed. Colman RW, Hirsch J, Marder VJ, Salzman EW. eds. Philadelphia: J. B. Lippincott; 1994: 508-23.
  • 27 Kefalides NA. The biochemistry and molecular biology of extracellular matrix. In: Hemostasis and Thrombosis:Basic Principles and Clinical Practice. 3rd ed. Colman RW, Hirsch J, Marder VJ, Salzman EW. eds. Philadelpia: J. B. Lippincott; 1994: 745-61.
  • 28 Savage B, Ginsberg MH, Ruggeri ZM. Influence of fibrillar collagen structure on the mechanisms of platelet thrombus formation under flow. Blood 1999; 94: 2704-15.
  • 29 Buck RC. Collagen fibril diameter in the common carotid artery of the rat. Connective Tissue Res 1987; 16: 121-9.
  • 30 Merrilees MJ, Tiang KM, Scott L. Changes in collagen fibril diameters across artery walls including a correlation with glycosaminoglycan content. Connective Tissue Res 1987; 16: 237-57.
  • 31 Shekhonin BV, Domogatsky SP, Muzykantov GL, Idelson GL, Rukosuev VS. Distribution of type I, III, IV and V collagen in normal and atherosclerotic human arterial wall: immunomorphological characteristics. Coll Rel Res 1985; 05: 355-68.
  • 32 Roggendorf W, Opitz H, Schuppan D. Altered expression of collagen type VI in brain vessels of patients with chronic hypertension. Acta Neuropathol 1988; 77: 55-60.
  • 33 Morton LF, Barnes MJ. Collagen polymorphism in the normal and diseased blood vessel wall. Atherosclerosis 1982; 42: 41-51.
  • 34 Kauhanen P, Kovanen PT, Lassila R. Coimmobilized native macromolecular heparin proteoglycans strongly inhibit platelet-collagen interactions in flowing blood. Arterioscler Thromb Vasc Biol 2000; 20: e113-9.
  • 35 Wagner DD, Urban-Pickering M, Marder VJ. Von Willebrand factor binds to extracellular matrices independently of collagen. Proc Natl Acad Sci USA 1984; 81: 471-5.
  • 36 de Groot PG, Ottenhof-Rovers M, van Mourik JA, Sixma JJ. Evidence that the primary binding site of von Willebrand factor that mediates platelet adhesion on subendothelium is not collagen. J Clin Invest 1988; 82: 65-73.