Plasma von Willebrand factor, thrombosis, and the endothelium: The first 30 years

Andrew D. Blann

doi:10.1160/TH05-07-0527

Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 2006; 95(01): 49-55
DOI: 10.1160/TH05-07-0527

Review Article

Schattauer GmbH

Plasma von Willebrand factor, thrombosis, and the endothelium: The first 30 years

Andrew D. Blann

¹Haemostasis, Thrombosis and Vascular Biology Unit, University Department of Medicine, City Hospital, Birmingham, United Kingdom

› Institutsangaben

Abstract

Summary

“It is quite useless to argue the questions concerning the development of intimal scleroses if we study and discuss the late stages of the disease alone. If we wish to gain insight into the complex question of arterio-sclerosis we must attempt to follow the lesion from its earliest beginning” (Klotz and Manning, J Path Bact 1911: 16; 211–20).

Over thirty years ago Boneu and colleagues publisheda report of raised levels of plasma vonWillebrand factor (vWf) in patients with arteritis, diabetes and sepsis. They concluded that raised levels of this molecule indicate endothelial damage, and may possibly be a contributory factor in thrombosis in arterial disease. The former aspect of this conclusion is now accepted, and numerous studies on the risk factors for atherosclerosis provide mechanisms for this damage. Other studies have demonstrated raised levels in cancer and in connective tissue disease. Numerous long-term follow-up studies have also demonstrated that increased vWf predicts major cardiovascular end points. However, the link between these studies, and the latter aspect of Boneu’s conclusion, that raised vWf contributes to thrombosis is,although attractive, nevertheless unproven. Despite this, vWf remains the most important plasma marker of endothelial damage/dysfunction and as such attracts clinical attention.

Keywords

Endothelium - vonWillebrand factor - thrombosis - atherosclerosis

Volltext

Referenzen

References
1 Cines DB, Pollak ES, Buck CA. et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 1998; 91: 3527-61.
2 Jaffe EA. Cell biology of endothelial cells. Hum Pathology 1987; 18: 234-9.
3 Blann AD, Lip GYH. The endothelium in atherothrombotic disease: assessment of function, mechanisms and clinical implications. Blood Coag Fibrinolys 1998; 09: 297-306.
4 Brinkhous KM, Koller F, Biggs R. et al. Vascular factors and thrombosis. Thromb Diathesis Haemorrhagica 1970; 40 Suppl: 1-399.
5 Mustard JF, Packham MA. The role of blood and platelets in atherosclerosis and the complications of atherosclerosis. Thromb Diathes Haemorrh 1975; 33: 444-56.
6 Boneu B, Abbal M, Plante J. et al. Factor VIII-complex and endothelial damage. Lancet 1975; 01: 1430.
7 Ross R, Glomset JA. The pathogenesis of atherosclerosis. New Eng J Med 1976; 295: 369-77 420–5.
8 Ross R. The pathogenesis of atherosclerosis - An update. New Engl J Med 1986; 314: 488-500.
9 Ruggeri ZM, Zimmerman TS. The complex multimeric composition of factor VIII/von Willebrand factor. Blood 1981; 57: 1140-3.
10 Wagner DD. Cell biology of von Willebrand factor. Annual Rev Cell Biol 1990; 06: 217-46.
11 Ruggeri ZM. Von Willebrand factor, platelets and endothelial cell interactions. J Thromb Haemost 2003; 01: 1335-42.
12 Siedlecki CA, Lestini BJ, Kottke-Marchant KK. et al. Shear-dependent changes in the three-dimensional structure of human von Willebrand factor. Blood 1996; 88: 2939-50.
13 Blann A. von Willebrand factor and the endothelium in vascular disease. Br J Biomed Sci 1993; 50: 125-34.
14 Pinsky DJ, Naka Y, Liao H. et al. Hypoxia-induced exocytosis of endothelial cell Weibel-Palade bodies. A mechanism for rapid neutrophil recruitment after cardiac preservation. J Clin Invest 1996; 97: 493-500.
15 Mannucci PM. Desmopressin (DDAVP) in the treatment of bleeding disorders: the first 20 years. Blood 1997; 90: 2515-21.
16 Sporn LA, Chavin SI, Marder VJ. et al. Biosynthesis of von Willebrand protein by human megakaryocytes. J Clin Invest 1985; 76: 1102-6.
17 Bowie EJ, Solberg Jr LA, Fass DN. et al. Transplantation of normal bone marrow into a pig with severe von Willebrand’s disease. J Clin Invest 1986; 78: 26-30.
18 Mannucci PM. Platelet von Willebrand factor in inherited and acquired bleeding disorders. Proc Natl Acad Sci USA 1995; 92: 2428-32.
19 Bennett B, Ratnoff OD. Changes in antihemophilic factor (AHF, factor VIII) procoagulant activity and AHF-like antigen in normal pregnancy, and following exercise and pneumoencephalography. J Clin Lab Med 1972; 80: 256-63.
20 Stormorken H, Erikssen J. Plasma antithrombin III and factor VIII antigen in relation to angiographicfindings, angina and blood groups in middle aged men. Thromb Haemost 1977; 38: 874-80.
21 Elwood PC, Beswick AD, O’Brien JR. et al. Interrelationships between haemostatic tests and the effects of some dietary determinants in the Caerphilly cohort of older men. Blood Coagul Fibrinolysis 1993; 04: 529-36.
22 Pottinger BE, Read RC, Paleolog EM. et al. von Willebrand factor is an acute phase reactant in man. Thromb Res 1989; 53: 38794.
23 Harvey PJ, Keightley AM, Lam YM. et al. A single nucleotide polymorphism at nucleotide -1793 in the von Willebrand factor (VWF) regulatory region is associated with plasma VWF:Ag levels. Br J Haematol 2000; 109: 349-53.
24 Greaves M, Pickering C, Knight G. et al. Changes in the factor VIII complex in diabetic ketoacidosis: evidence of endothelial cell damage?. Diabetologia 1987; 30: 1605.
25 Blann AD, Bushell D, Davies A. et al. von Willebrand factor, the endothelium and obesity. Int J Obesity 1993; 17: 723-5.
26 Blann AD, Davis A, Miller JP. et al. von Willebrand factor and soluble E-selectin in hyperlipidaemia: Relationship to vascular disease and the risk factors for atherosclerosis. AmJ Haem 1997; 55: 15-23.
27 Smith FB, Lowe GD, Fowkes FG. et al. Smoking, haemostatic factors and lipid peroxides in a population case control study of peripheral arterial disease. Atherosclerosis 1993; 102: 155-62.
28 Blann AD, Steele C, McCollum CN. Influence of smoking on soluble adhesion molecules and endothelial cell markers. Thromb Res 1997; 85: 433-8.
29 Vaziri ND, Smith DH, Winer RL. et al. Coagulation and inhibitory and fibrinolytic proteins in essential hypertension. J Am Soc Nephrol 1993; 04: 222-8.
30 Blann AD, Naqvi T, Waite M. et al. von Willebrand factor and endothelial damage in essential hypertension. J Hum Hypertens 1993; 07: 107-11.
31 Christe M, Delley A, Marbet GA. et al. Fibrinogen, factor VIII related antigen, antithrombin III and alpha 2-antiplasmin in peripheral arterial disease. Thromb Haemost 1984; 52: 240-2.
32 Haines AP, Howarth D, North WRS. et al. Haemostatic variables and the outcome of myocardial infarction. Thromb Haemost 1983; 50: 800-3.
33 Mettinger KL. A study of hemostasis in ischemic cerebrovascular disease. I. Abnormalities in factor VIII and antithrombin. Thromb Res 1982; 26: 183-92.
34 Gustafsson C, Blomback M, Britton M. et al. Coagulation factors and the increased risk of stroke in nonvalvular atrial fibrillation. Stroke 1990; 21: 47-51.
35 Campbell PM, LeRoy EC. Pathogenesis of systemic sclerosis: a vascular hypothesis. Seminars Arth Rheum 1975; 04: 351-67.
36 Rothschild BM, Masi AT. Pathogenesis of rheumatoid arthritis: a vascular hypothesis. Seminars Arth Rheum 1982; 12: 11-31.
37 Blann AD, Hopkins J, Winkles J. et al. Plasma and serum von Willebrand Factor antigen levels in connective tissue disorders. Annals Clin Biochem 1992; 29: 67-71.
38 Erhardt CC, Mumford PA, Venables PJW. et al. Factors predicting a poor life prognosis in rheumatoid arthritis: an eight year prospective study. Annals Rheum Dis 1989; 48: 7-13.
39 Lip GYH, Chin BSP, Blann AD. Cancer and the prothrombotic state. Lancet Oncology 2002; 03: 27-34.
40 Blomback M, Hedlund PO, Sawe U. Changes in blood coagulation and fibrinolysis in patients on different treatment regimens for prostatic cancer. Predictors for cardiovascular complications? Thromb Res 1988; 49: 111-21.
41 Gadducci A, Baicchi U, Marrai R. et al. Pretreatment plasma levels of fibrinopeptide-A (FPA), D-dimer (DD), and von Willebrand factor (vWF) in patients with operable cervical cancer: influence of surgical-pathological stage, tumor size, histologic type, and lymph node status. Gynecol Oncol 1993; 49: 354-8.
42 Gadducci A, Baicchi U, Marrai R. et al. Pretreatment plasma levels of fibrinopeptide-A (FPA), D-dimer (DD), and von Willebrand factor (vWF) in patients with ovarian carcinoma. Gynecol Oncol 1994; 53: 352-6.
43 Zietek Z, Iwan-Zietek I, Paczulski R. et al. von Willebrand factor antigen in blood plasma of patients with urinary bladder carcinoma. Thromb Res 1996; 83: 399-402.
44 Byrne GJ, Ghellal A, Iddon J. et al. Serum soluble vascular cell adhesion molecule-1: role as a surrogate marker of angiogenesis. J Natl Cancer Inst 2000; 92: 1329-36.
45 Blann AD, Gurney D, Wadley M. et al. Increased soluble P-selectin in patients with haematological and breast cancer: a comparison with fibrinogen, plasminogen activator inhibitor and von Willebrand factor. Blood Coagul Fibrinolysis 2001; 12: 43-50.
46 Ikeda M, Furukawa H, Imamura H. et al. Surgery for gastric cancer increases plasma levels of vascular endothelial growth factor and von Willebrand factor. Gastric Cancer 2002; 05: 137-41.
47 Mordes DB, Lazarchick J, Colwell JA. et al. Elevated glucose concentrations increase factor VIIIR:Ag levels in human umbilical vein endothelial cells. Diabetes 1983; 32: 876-8.
48 Meigs JB, Mittleman MA, Nathan DM. et al. Hyperinsulinemia, hyperglycemia, and impaired haemostasis: the Framingham Offspring Study. JAMA 2000; 283: 221-8.
49 Blann AD, Burrows G, McCollum CN. Oxidised and native low-density lipoproteins induce the release of von Willebrand factor from human endothelial cells in vitro . BrJ Biomed Sci 2003; 60: 155-60.
50 Kalra J, Chaudhary AK, Prasad K. Increased production of oxygen free radicals in cigarette smokers. Int J Exp Pathol 1991; 72: 1-7.
51 Paleolog EM, Carew MA, Pearson JD. Effects of tumour necrosis factor and interleukin-1 on von Willebrand factor secretion from human vascular endothelial cells. Int J Radiat Biol 1991; 60: 279-85.
52 Tannenbaum SH, Gralnick HR. Gamma-interferon modulates von Willebrand factor release by cultured human endothelial cells. Blood 1990; 75: 2177-84.
53 Booth F, Allington MJ, Cederholm-Williams SA. An in vitro model for the study of acute release of vWf from human endothelial cells. BrJ Haematol 1987; 67: 71-8.
54 Greaves M, Malia RG, Milford AWard. et al. Elevated von Willebrand factor antigen in systemic sclerosis: relationship to visceral disease. Br J Rheumatol 1988; 27: 281-5.
55 Federici AB, Fox RI, Espinoza LR. et al. Elevation of von Willebrand factor is independent of erythrocyte sedimentation rate and persists after glucocorticoid treatment in giant cell arteritis. Arthritis Rheum 1984; 27: 1046-9.
56 Woolf AD, Wakerley G, Wallington TB. et al. Factor VIII related antigen in the assessment of vasculitis. Ann Rheum Dis 1987; 46: 441-7.
57 Nicolson GL, Custead SE. Effects of chemotherapeutic drugs on platelet and metastatic tumor cell-endothelial cell interactions as a model for assessing vascular endothelial integrity. Cancer Res 1985; 45: 331-6.
58 Sporn LA, Rubin P, Marder VJ. et al. Irradiation induces release of von Willebrand protein from endothelial cells in culture. Blood 1984; 64: 567-70.
59 Angles-Cano E, Sultan Y, Clauvel JP. Predisposing factors to thrombosis in systemic lupus erythematosus: possible relation to endothelial cell damage. J Lab Clin Med 1979; 94: 312-23.
60 Jilma B, Blann A, Pernerstorfer T. et al. Regulation of adhesion molecules during human endotoxemia. No acute effects of aspirin. Am J Respir Crit Care Med 1999; 159: 857-63.
61 Reinhart K, Bayer O, Brunkhorst F. et al. Markers of endothelial damage in organ dysfunction and sepsis. Crit Care Med 2002; 30 (Suppl. 05) S302-12.
62 van Mourik JA, Boertjes R, Huisveld IA. et al. von Willebrand factor propeptide in vascular disorders: A tool to distinguish between acute and chronic endothelial cell perturbation. Blood 1999; 94: 179-85.
63 Blann AD, Lip GY, McCollum CN. Changes in von Willebrand factor and soluble ICAM, but not soluble VCAM, soluble E selectin or soluble thrombomodulin, reflect the natural history of the progression of atherosclerosis. Atherosclerosis 2002; 165: 389-91.
64 Blann AD, Lip GY, McCollum CN. Influence of the risk factors for atherosclerosis on levels of soluble adhesion molecules and endothelial markers in peripheral vascular disease. Thromb Haemost 2002; 88: 366-7.
65 Blann AD, McCollum CN, Lip GY. Relationship between plasma markers of endothelial cell integrity and the Framingham cardiovascular disease risk-factor scores in apparently healthy individuals. Blood Coagul Fibrinolysis 2002; 13: 513-8.
66 Hergesell O, Andrassy K, Nawroth P. Elevated levels of markers of endothelial cell damage and markers of activated coagulation in patients with systemic necrotizing vasculitis. Thromb Haemost 1996; 75: 892-8.
67 Uchiyama T, Matsumoto M, Kobayashi N. Studies on the pathogenesis of coagulopathy in patients with arterial thromboembolism and malignancy. Thromb Res 1990; 59: 955-65.
68 Erem C, Ersoz HO, Karti SS. et al. Blood coagulation and fibrinolysis in patients with hyperthyroidism. J Endocrinol Invest 2002; 25: 345-50.
69 Pearson JD. Markers of endothelial cell perturbation and damage. Br J Rheum 1993; 32: 6512.
70 Augustin HG, Kozian DH, Johnson RC. Differentiation of endothelial cells: Analysis of the constitutive and activated endothelial cell phenotypes. Bioassays 1994; 16: 901-6.
71 Blann AD. Viewpoint: Endothelial cell activation, injury, damage and dysfunction: separate entities or mutual terms. Blood Coag Fibrinolysis 2000; 11: 623-30.
72 Yarnell J, McCrum E, Rumley A. et al. Association of European population levels of thrombotic risk and inflammatory factors with risk of coronary heart disease: the MONICA Optional haemostatic Study. Eur HeartJ 2005; 26: 332-42.
73 Felmeden DC, Blann AD, Spencer CGC. et al. A comparison of flow mediated dilatation and von Willebrand factor as markers of endothelial cell function in health and in hypertension: relationship to cardiovascular risk and the effects of treatment. Blood Coag Fibrinolysis 2003; 14: 425-31.
74 Blann AD, Woywodt A, Bertolini F. et al. Circulating endothelial cells: biomarker of vascular disease. Thromb Haemost 2005; 93: 228-35.
75 Morange PE, Simon C, Alessi MC. et al. Endothelial cell markers and the risk of coronary heart disease. Circulation 2004; 109: 1343-8.
76 Lee KW, Lip GY, Tayebjee M. et al. Circulating endothelial cells, von Willebrand factor, interleukin-6, and prognosis in patients with acute coronary syndromes. Blood 2005; 105: 526-32.
77 Stehouwer CDA, Gall MA, Twisk JWR. et al. Increased urinary albumin excretion, endothelial dysfunction and chronic low grade inflammation in type 2 diabetes. Diabetes 2002; 51: 1157-62.
78 Thompson SG, Kienast J, Pyke SDM, et al. for the ECAT group. Hemostatic factors and the risk of myocardial infarction or sudden death in patients with angina pectoris. New Engl J Med 1995; 332: 635-41.
79 Wallberg-Jonsson S, Dahlen GH, Nilsson TK. et al. Tissue plasminogen activator, plasminogen activator inhibitor-1 and von Willebrand factor in rheumatoid arthritis. Clin Rheumatol 1993; 12: 318-24.
80 Blann AD, Sheeran T, Emery P. Increased levels of von Willebrand factor are a poor prognostic factor in systemic sclerosis and are unrelated to tissue autoantibodies. Br J Biomed Sci 1997; 54: 5-9.
81 Whincup PH, Danesh J, Walker M. et al. Von Willebrand factor and coronary heart disease. Prospective study and meta-analysis. Eur Heart J 2002; 23: 1764-70.
82 Moake JL, Turner NA, Stathopoulos NA. et al. Involvement of large plasma von Willebrand factor (vWF) multimers and unusually large vWF forms derived from endothelial cells in shear stress-induced platelet aggregation. J Clin Invest 1986; 78: 1456-61.
83 Methia N, Andre P, Denis CV. et al. Localized reduction of atherosclerosis in von Willebrand factordeficient mice. Blood 2001; 98: 1424-8.
84 Brinkhous KM, Reddick RL, Read MS. et al. von Willebrand factor and animal models: contributions to gene therapy, thrombotic thrombocytopenic purpura, and coronary artery thrombosis. Mayo Clin Proc 1991; 66: 733-42.
85 Chung DW, Fujikawa K. Processing of von Willebrand factor by ADAMTS-13. Biochemistry 2002; 41: 10065-70.
86 Dong JF, Moake JL, Nolasco L. et al. ADAMTS-13 rapidly cleaves newly secreted ultralarge von Wille-brand factor multimers on the endothelial surface under flowing conditions. Blood 2002; 100: 4033-9.
87 Terrell DR, Williams LA, Vesely SK. et al. The incidence of thrombotic thrombocytopenic purpura-hemolytic uremic syndrome: all patients, idiopathic patients, and patients with severe ADAMTS-13 deficiency. J Thromb Haemost 2005; 03: 1432-6.
88 Ruggeri ZM. The role of von Willebrand factor and fibrinogen in the inititation of platelet adhesion to thrombogenic surfaces. Thromb Haemost 1996; 76: 460-8.
89 Mannucci PM, Canciani MT, Rota L. et al. Response of factor VIII/von Willebrand factor to DDAVP in healthy subjects and patients with haemophilia A and von Willebrand’s disease. Br J Haematol 1981; 47: 283-93.
90 Paramo JA, Beloqui O, Colina I. et al. Independent association of von Willebrand factor with surrogate markers of atherosclerosis in middle aged asymptomatic subjects. J Thromb Haemost 2005; 03: 662-4.
91 Ruggeri ZM. Von Willebrand factor as a target for antithrombotic intervention. Circulation 1992; 86 supple III III 26-9.
92 Sobel M, Bird KE, Tyler-Cross R. et al. Heparins designed to specifically inhibit interactions with von Willebrand factor. Circulation 1996; 93: 992-9.
93 Kageyama S, Yamamoto H, Nakazawa H. et al. Pharmacokinetics and pharmacodynamics ofAJW200, a humanized monoclonal antibody to von Willebrand factor, in monkeys. Arterioscler Thromb Vasc Biol 2002; 22: 187-92.
94 Ray KK, Morrow DA, Gibson CM. et al. Predictors of the rise in vWF after ST elevation myocardial infarction: implications for treatment strategies and clinical outcome: An ENTIRE-TIMI 23 substudy. Eur Heart J 2005; 26: 440-6.
95 Blann AD, Waite MA. von Willebrand factor and soluble E-selectin in hypertension: Influence of treatment and value in predicting the progression of atherosclerosis. Coronary Artery Disease 1996; 07: 143-7.
96 Bickel C, Rupprecht HJ, Blankenberg S. AtheroGene Group. et al. Influence of HMG-CoA reductase inhibitors on markers of coagulation, systemic inflammation and soluble cell adhesion. Int J Cardiol 2002; 82: 25-31.
97 Blann AD, Jackson P, Bath PM. et al. von Willebrand factor, a possible indicator of endothelial cell damage, decreases during long-term compliance with a lipid-lowering diet. J Intern Med 1995; 237: 557-61.
98 Charles MA, Morange P, Eschwege E. et al. Effect of weight change and metformin on fibrinolysis and the von Willebrand factor in obese nondiabetic subjects: the BIGPRO1 Study. Biguanides and the Prevention of the Risk of Obesity. Diabetes Care 1998; 21: 1967-72.
99 Johansson L, Jansson JH, Stegmayr B. et al. Haemostatic factors as risk markers for intracerebral haemorrhage: a prospective incidence case-referent study. Stroke 2004; 35: 826-30.
100 Sramek A, Bucciarelli P, Federici AB. et al. Patients with type 3 severe von Willebrand disease are not protected against atherosclerosis: results from a multicenter study in 47 patients. Circulation 2004; 109: 740-4.
101 Jelenska MM, Palester-Chlebowczyk M, Grochowiecki R. et al. Can low level of von Willebrand factor decrease the risk of thrombosis in families with antithrombin or protein C deficiency?. Thromb Haemost 1999; 81: 846-7.
102 Aird WC. Spatial and temporal dynamics of the endothelium. J Thromb Haemost 2005; 03: 1392-406.
103 Koster T, Blann AD, Briet E. et al. Role of clotting factor VIII in effect of von Willebrand factor on occurrence of deep vein thrombosis. Lancet 1995; 345: 152-5.
104 Yamamoto K, de Waard V, Fearns C. et al. Tissue distribution and regulation of murine von Willebrand factor gene expression in vivo . Blood 1998; 92: 2791-801.
105 De Reuck J, Vandekerckhove T, Bosma G. et al. Steroid treatment in acute ischaemic stroke. A comparative retrospective study of 556 cases. Eur Neurol 1988; 28: 70-2.
106 Pui CH, Jackson CW, Chesney CM. et al. Involvement of von Willebrand factor in thrombosis following asparaginase-prednisone-vincristine therapy for leukemia. AmJ Hematol 1987; 25: 291-8.
107 Maxwell SR, Moots RJ, Kendall MJ. Corticosteroids: do they damage the cardiovascular system?. Postgrad Med J 1994; 70: 863-70.
108 Jilma B, Cvitko T, Winter-Fabry A. et al. High dose dexamethasone increases circulating P-selectin and von Willebrand factor levels in healthy men. Thromb Haemost 2005; 94: 797-801.