Von Willebrand factor: At the crossroads of bleeding and thrombosis

International Journal of Hematology

Volumn 95, Issue 4, 2012, Pages 353-361

  Denis, Cécile V ^a,b   Lenting, Peter J ^a,b  

^a Dept Environ Med Natl Inst Publ HIth   (Norway)

^b UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Hemostasis; Thrombosis; Von Willebrand disease; Von Willebrand factor

Indexed keywords

VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE;

ACQUIRED VON WILLEBRAND DISEASE; AORTA STENOSIS; ARTICLE; BLEEDING; BRAIN ISCHEMIA; CARDIOVASCULAR RISK; DISEASE ASSOCIATION; HEART DISEASE; HEMOSTASIS; HUMAN; HYPERTROPHIC OBSTRUCTIVE CARDIOMYOPATHY; MOLECULAR PATHOLOGY; NONHUMAN; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RISK FACTOR; SHEAR STRESS; THROMBOSIS; THROMBOTIC THROMBOCYTOPENIC PURPURA; VEIN THROMBOSIS; VON WILLEBRAND DISEASE;

ANIMALS; HEMORRHAGE; HUMANS; MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; THROMBOSIS; VON WILLEBRAND FACTOR;

EID: 84862904873     PISSN: 09255710     EISSN: 18653774     Source Type: Journal    
DOI: 10.1007/s12185-012-1041-x     Document Type: Article

References (79)

1. Reininger AJ. Function of von Willebrand factor in haemostasis and thrombosis. Haemophilia. 2008;14(SUPPL. 5):11-26.
2. Ruggeri ZM. Platelet adhesion under flow. Microcirculation. 2009;16:58-83.
3. Lenting PJ, Van Schooten CJ, Denis CV. Clearance mechanisms of von Willebrand factor and factor VIII. J Thromb Haemost. 2007;5:1353-60.
4. Denis CV. Molecular and cellular biology of von Willebrand factor. Int J Hematol. 2002;75:3-8.
5. Ruggeri ZM, Zimmerman TS. The complex multimeric composition of factor VIII/von Willebrand factor. Blood. 1981;57: 1140-3.
6. Furlan M. von Willebrand factor: molecular size and functional activity. Ann Hematol. 1996;72:341-8.
7. Barr J, Motto D. Modulation of von Willebrand factor by ADAMTS13. In: Federici AB, Lee CA, Berntorp EE, Lillicrap D, Montgomery RR, editors. Von Willebrand disease: basic and clinical aspects. Chichester: Wiley-Blackwell; 2011. p. 49-62.
8. Springer TA. Biology and physics of von Willebrand factor concatamers. J Thromb Haemost. 2011;9(SUPPL. 1):130-43.
9. Sadler JE, Budde U, Eikenboom JC, Favaloro EJ, Hill FG, Holmberg L, et al. Update on the pathophysiology and classification of von Willebrand disease: a report of the subcommittee on von Willebrand Factor. J Thromb Haemost. 2006;4:2103-14.
10. Schneppenheim R, Budde U. Phenotypic and genotypic diagnosis of von Willebrand disease: a 2004 update. Semin Hematol. 2005; 42:15-28.
11. Schneppenheim R, Budde U. von Willebrand factor: the complex molecular genetics of a multidomain and multifunctional protein. J Thromb Haemost. 2011;9(SUPPL. 1):209-15.
12. Rayes J, Hommais A, Legendre P, Tout H, Veyradier A, Obert B, et al. Effect of von Willebrand disease type 2B and type 2M mutations on the susceptibility of von Willebrand factor to ADAMTS-13. J Thromb Haemost. 2007;5:321-8.
13. Federici AB, Mannucci PM, Castaman G, Baronciani L, Bucciarelli P, Canciani MT, et al. Clinical and molecular predictors of thrombocytopenia and risk of bleeding in patients with von Willebrand disease type 2B: a cohort study of 67 patients. Blood. 2009;113:526-34.
14. Rayes J, Hollestelle MJ, Legendre P, Marx I, de Groot PG, Christophe OD, et al. Mutation and ADAMTS13-dependent modulation of disease severity in a mouse model for von Willebrand disease type 2B. Blood. 2010;115:4870-7.
15. Nishino M, Girma JP, Rothschild C, Fressinaud E, Meyer D. New variant of von Willebrand disease with defective binding to factor VIII. Blood. 1989;74:1591-9.
16. Flood VH, Lederman CA, Wren JS, Christopherson PA, Friedman KD, Hoffmann RG, et al. Absent collagen binding in a VWF A3 domain mutant: utility of the VWF:CB in diagnosis of VWD. J Thromb Haemost. 2010;8:1431-3.
17. Ribba AS, Loisel I, Lavergne JM, Juhan-Vague I, Obert B, Cherel G, et al. Ser968Thr mutation within the A3 domain of von Willebrand factor (VWF) in two related patients leads to a defective binding of VWF to collagen. Thromb Haemost. 2001; 86:848-54.
18. Riddell AF, Gomez K, Millar CM, Mellars G, Gill S, Brown SA, et al. Characterization of W1745C and S1783A: 2 novel mutations causing defective collagen binding in the A3 domain of von Willebrand factor. Blood. 2009;114:3489-96.
19. Marx I, Christophe OD, Lenting PJ, Rupin A, Vallez MO, Verbeuren TJ, et al. Altered thrombus formation in von Willebrand factor-deficient mice expressing von Willebrand factor variants with defective binding to collagen or GPIIbIIIa. Blood. 2008;112: 603-9.
20. Casonato A, Pontara E, Sartorello F, Cattini MG, Sartori MT, Padrini R, et al. Reduced von Willebrand factor survival in type Vicenza von Willebrand disease. Blood. 2002;99:180-4.
21. Lenting PJ, Westein E, Terraube V, Ribba AS, Huizinga EG, Meyer D, et al. An experimental model to study the in vivo survival of von Willebrand factor. Basic aspects and application to the R1205H mutation. J Biol Chem. 2004;279:12102-9.
22. Pruss CM, Golder M, Bryant A, Hegadorn CA, Burnett E, Laverty K, et al. Pathologic mechanisms of type 1 VWD mutations R1205H and Y1584C through in vitro and in vivo mouse models. Blood. 2011;117:4358-66.
23. Denis CV, Christophe OD, Oortwijn BD, Lenting PJ. Clearance of von Willebrand factor. Thromb Haemost. 2008;99:271-8.
24. Haberichter SL, Castaman G, Budde U, Peake I, Goodeve A, Rodeghiero F, et al. Identification of type 1 von Willebrand disease patients with reduced von Willebrand factor survival by assay of the VWF propeptide in the European study: molecular and clinical markers for the diagnosis and management of type 1 VWD (MCMDM-1VWD). Blood. 2008;111:4979-85.
25. Van Schooten CJ, Tjernberg P, Westein E, Terraube V, Castaman G, Mourik JA, et al. Cysteine-mutations in von Willebrand factor associated with increased clearance. J Thromb Haemost. 2005; 3:2228-37.
26. Federici AB, Bucciarelli P, Castaman G, Baronciani L, Canciani MT, Mazzucconi MG, et al. Management of inherited von Willebrand disease in Italy: results from the retrospective study on 1234 patients. Semin Thromb Hemost. 2011;37:511-21.
27. Castaman G, Tosetto A, Federici AB, Rodeghiero F. Bleeding tendency and efficacy of anti-haemorrhagic treatments in patients with type 1 von Willebrand disease and increased von Willebrand factor clearance. Thromb Haemost. 2011;105:647-54.
28. Shetty S, Kasatkar P, Ghosh K. Pathophysiology of acquired von Willebrand disease: a concise review. Eur J Haematol. 2011;87: 99-106.
29. Tiede A, Rand JH, Budde U, Ganser A, Federici AB. How I treat the acquired von Willebrand syndrome. Blood. 2011;117: 6777-85.
30. Budde U, Scharf RE, Franke P, Hartmann-Budde K, Dent J, Ruggeri ZM. Elevated platelet count as a cause of abnormal von Willebrand factor multimer distribution in plasma. Blood. 1993; 82:1749-57.
31. Richard C, Cuadrado MA, Prieto M, Batlle J, Lopez Fernandez MF, Rodriguez Salazar ML, et al. Acquired von Willebrand disease in multiple myeloma secondary to absorption of von Willebrand factor by plasma cells. Am J Hematol. 1990;35:114-7.
32. Gill JC, Wilson AD, Endres-Brooks J, Montgomery RR. Loss of the largest von Willebrand factor multimers from the plasma of patients with congenital cardiac defects. Blood. 1986;67:758-61.
33. Warkentin TE, Moore JC, Morgan DG. Aortic stenosis and bleeding gastrointestinal angiodysplasia: is acquired von Willebrand's disease the link? Lancet. 1992;340:35-7.
34. Vincentelli A, Susen S, Le Tourneau T, Six I, Fabre O, Juthier F, et al. Acquired von Willebrand syndrome in aortic stenosis. N Engl J Med. 2003;349:343-9.
35. Banerjee AK. Angiodysplasia associated with hypertrophic obstructive cardiomyopathy (HOCM). Br J Clin Pract. 1990;44: 326-7.
36. Le Tourneau T, Susen S, Caron C, Millaire A, Marechaux S, Polge AS, et al. Functional impairment of von Willebrand factor in hypertrophic cardiomyopathy: relation to rest and exercise obstruction. Circulation. 2008;118:1550-7.
37. Slaughter MS. Hematologic effects of continuous flow left ventricular assist devices. J Cardiovasc Transl Res. 2010;3:618-24.
38. Pareti FI, Lattuada A, Bressi C, Zanobini M, Sala A, Steffan A, et al. Proteolysis of von Willebrand factor and shear stressinduced platelet aggregation in patients with aortic valve stenosis. Circulation. 2000;102:1290-5.
39. Zhang X, Halvorsen K, Zhang CZ, Wong WP, Springer TA. Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor. Science. 2009;324:1330-4.
40. van Schie MC, van Loon JE, de Maat MP, Leebeek FW. Genetic determinants of von Willebrand factor levels and activity in relation to the risk of cardiovascular disease: a review. J Thromb Haemost. 2011;9:899-908.
41. De Meyer SF, De Maeyer B, Deckmyn H, Vanhoorelbeke K. Von Willebrand factor: drug and drug target. Cardiovasc Hematol Disord: Drug Targets. 2009;9:9-20.
42. Jager A, van Hinsbergh VW, Kostense PJ, Emeis JJ, Yudkin JS, Nijpels G, et al. von Willebrand factor, C-reactive protein, and 5-year mortality in diabetic and nondiabetic subjects: the Hoorn Study. Arterioscler Thromb Vasc Biol. 1999;19:3071-8.
43. Wiman B, Andersson T, Hallqvist J, Reuterwall C, Ahlbom A, de Faire U. Plasma levels of tissue plasminogen activator/plasminogen activator inhibitor-1 complex and von Willebrand factor are significant risk markers for recurrent myocardial infarction in the Stockholm Heart Epidemiology Program (SHEEP) study. Arterioscler Thromb Vasc Biol. 2000;20:2019-23.
44. Klemm T, Mehnert AK, Siegemund A, Wiesner TD, Gelbrich G, Bluher M, et al. Impact of the Thr789Ala variant of the von Willebrand factor levels, on ristocetin co-factor and collagen binding capacity and its association with coronary heart disease in patients with diabetes mellitus type 2. Exp Clin Endocrinol Diabetes. 2005;113:568-72.
45. Lacquemant C, Gaucher C, Delorme C, Chatellier G, Gallois Y, Rodier M, et al. Association between high von willebrand factor levels and the Thr789Ala vWF gene polymorphism but not with nephropathy in type I diabetes. The GENEDIAB Study Group and the DESIR Study Group. Kidney Int. 2000;57:1437-43.
46. van der Meer IM, Brouwers GJ, Bulk S, Leebeek FW, van der Kuip DA, Hofman A, et al. Genetic variability of von Willebrand factor and risk of coronary heart disease: the Rotterdam Study. Br J Haematol. 2004;124:343-7.
47. Smith NL, Rice KM, Bovill EG, Cushman M, Bis JC, McKnight B, et al. Genetic variation associated with plasma von Willebrand factor levels and the risk of incident venous thrombosis. Blood. 2011;117:6007-11.
48. Antoni G, Oudot-Mellakh T, Dimitromanolakis A, Germain M, Cohen W, Wells P, et al. Combined analysis of three genomewide association studies on vWF and FVIII plasma levels. BMC Med Genet. 2011;12:102.
49. Smith NL, Chen MH, Dehghan A, Strachan DP, Basu S, Soranzo N, et al. Novel associations of multiple genetic loci with plasma levels of factor VII, factor VIII, and von Willebrand factor: The CHARGE (Cohorts for Heart and Aging Research in Genome Epidemiology) Consortium. Circulation. 2010;121:1382-92.
50. van Loon JE, Leebeek FW, Deckers JW, Dippel DW, Poldermans D, Strachan DP, et al. Effect of genetic variations in syntaxinbinding protein-5 and syntaxin-2 on von Willebrand factor concentration and cardiovascular risk. Circ Cardiovasc Genet. 2010; 3:507-12.
51. Koster T, Blann AD, Briet E, Vandenbroucke JP, Rosendaal FR. Role of clotting factor VIII in effect of von Willebrand factor on occurrence of deep-vein thrombosis. Lancet. 1995;345:152-5.
52. Tsai AW, Cushman M, Rosamond WD, Heckbert SR, Tracy RP, Aleksic N, et al. Coagulation factors, inflammation markers, and venous thromboembolism: the longitudinal investigation of thromboembolism etiology (LITE). Am J Med. 2002;113:636-42.
53. Takahashi M, Yamashita A, Moriguchi-Goto S, Marutsuka K, Sato Y, Yamamoto H, et al. Critical role of von Willebrand factor and platelet interaction in venous thromboembolism. Histol Histopathol. 2009;24:1391-8.
54. Chauhan AK, Kisucka J, Lamb CB, Bergmeier W, Wagner DD. von Willebrand factor and factor VIII are independently required to form stable occlusive thrombi in injured veins. Blood. 2007; 109:2424-9.
55. Brill A, Fuchs TA, Chauhan AK, Yang JJ, De Meyer SF, Kollnberger M, et al. von Willebrand factor-mediated platelet adhesion is critical for deep vein thrombosis in mouse models. Blood. 2011;117:1400-7.
56. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA. 2010;107:15880-5.
57. Fuchs TA, Bhandari AA, Wagner DD. Histones induce rapid and profound thrombocytopenia in mice. Blood. 2011;118:3708-14.
58. Brill A, Fuchs TA, Savchenko A, Thomas GM, Martinod K, De Meyer SF, et al. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost. 2011 (Epub ahead of print).
59. Moake JL, Rudy CK, Troll JH, Weinstein MJ, Colannino NM, Azocar J, et al. Unusually large plasma factor VIII:von Willebrand factor multimers in chronic relapsing thrombotic thrombocytopenic purpura. N Engl J Med. 1982;307:1432-5.
60. Levy GG, Motto DG, Ginsburg D. ADAMTS13 turns 3. Blood. 2005;106:11-7.
61. Crawley JT, de Groot R, Xiang Y, Luken BM, Lane DA. Unraveling the scissile bond: how ADAMTS13 recognizes and cleaves von Willebrand factor. Blood. 2011;118:3212-21.
62. Lenting PJ, Pegon JN, Groot E, de Groot PG. Regulation of von Willebrand factor-platelet interactions. Thromb Haemost. 2010; 104:449-55.
63. De Ceunynck K, Rocha S, Feys HB, De Meyer SF, Uji-i H, Deckmyn H, et al. Local elongation of endothelial cell-anchored von Willebrand factor strings precedes ADAMTS13 proteinmediated proteolysis. J Biol Chem. 2011;286:36361-7.
64. Schneider SW, Nuschele S, Wixforth A, Gorzelanny C, Alexander-Katz A, Netz RR, et al. Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. Proc Natl Acad Sci U S A. 2007;104:7899-903.
65. Lenting PJ, Rastegarlari G. ADAMTS-13: double trouble for von Willebrand factor. J Thromb Haemost. 2010;8:2775-7.
66. Ganderton T, Berndt MC, Chesterman CN, Hogg PJ. Hypothesis for control of von Willebrand factor multimer size by intramolecular thiol-disulphide exchange. J Thromb Haemost. 2007;5: 204-6.
67. Li Y, Choi H, Zhou Z, Nolasco L, Pownall HJ, Voorberg J, et al. Covalent regulation of ULVWF string formation and elongation on endothelial cells under flow conditions. J Thromb Haemost. 2008;6:1135-43.
68. Yeh HC, Zhou Z, Choi H, Tekeoglu S, May W 3rd, Wang C, et al. Disulfide bond reduction of von Willebrand factor by ADAMTS-13. J Thromb Haemost. 2010;8:2778-88.
69. Fu X, Chen J, Gallagher R, Zheng Y, Chung DW, Lopez JA. Shear stress-induced unfolding of VWF accelerates oxidation of key methionine residues in the A1A2A3 region. Blood. 2011;118: 5283-91.
70. Chen J, Fu X, Wang Y, Ling M, McMullen B, Kulman J, et al. Oxidative modification of von Willebrand factor by neutrophil oxidants inhibits its cleavage by ADAMTS13. Blood. 2010;115: 706-12.
71. Lancellotti S, De Filippis V, Pozzi N, Peyvandi F, Palla R, Rocca B, et al. Formation of methionine sulfoxide by peroxynitrite at position 1606 of von Willebrand factor inhibits its cleavage by ADAMTS-13: A new prothrombotic mechanism in diseases associated with oxidative stress. Free Radic Biol Med. 2010;48: 446-56.
72. De Filippis V, Lancellotti S, Maset F, Spolaore B, Pozzi N, Gambaro G, et al. Oxidation of Met1606 in von Willebrand factor is a risk factor for thrombotic and septic complications in chronic renal failure. Biochem J. 2011 (Epub ahead of print).
73. Hulstein JJ, de Groot PG, Silence K, Veyradier A, Fijnheer R, Lenting PJ. A novel nanobody that detects the gain-of-function phenotype of von Willebrand factor in ADAMTS13 deficiency and von Willebrand disease type 2B. Blood. 2005;106:3035-42.
74. Hulstein JJ, Lenting PJ, de Laat B, Derksen RH, Fijnheer R, de Groot PG. beta2-Glycoprotein I inhibits von Willebrand factor dependent platelet adhesion and aggregation. Blood. 2007;110: 1483-91.
75. de Laat B, de Groot PG, Derksen RH, Urbanus RT, Mertens K, Rosendaal FR, et al. Association between beta2-glycoprotein I plasma levels and the risk of myocardial infarction in older men. Blood. 2009;114:3656-61.
76. De Meyer SF, Stoll G, Wagner DD and Kleinschnitz C. von Willebrand factor: an emerging target in stroke therapy. Stroke. 2011 (Epub ahead of print).
77. Kleinschnitz C, De Meyer SF, Schwarz T, Austinat M, Vanhoorelbeke K, Nieswandt B, et al. Deficiency of von Willebrand factor protects mice from ischemic stroke. Blood. 2009;113: 3600-3.
78. De Meyer SF, Schwarz T, Deckmyn H, Denis CV, Nieswandt B, Stoll G, et al. Binding of von Willebrand factor to collagen and glycoprotein Ibalpha, but not to glycoprotein IIb/IIIa, contributes to ischemic stroke in mice-brief report. Arterioscler Thromb Vasc Biol. 2010;30:1949-51.
79. Chen J, Reheman A, Gushiken FC, Nolasco L, Fu X, Moake JL, et al. N-acetylcysteine reduces the size and activity of von Willebrand factor in human plasma and mice. J Clin Invest. 2011; 121:593-603.