Von Willebrand factor, Jedi knight of the bloodstream

Blood

Volumn 124, Issue 9, 2014, Pages 1412-1425

  Springer, Timothy A ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RISTOCETIN; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE;

BIOSYNTHESIS; BLOOD CLOTTING; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; GAIN OF FUNCTION MUTATION; HUMAN; HYDRODYNAMICS; HYDROGEN BOND; PRIORITY JOURNAL; REVIEW; RISK FACTOR; THROMBOCYTE; THROMBOCYTE MEMBRANE; VON WILLEBRAND DISEASE; AMINO ACID SEQUENCE; ANIMAL; BIOPHYSICS; BLOOD; BLOOD RHEOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HEMOSTASIS; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; THROMBOSIS; TRANSMISSION ELECTRON MICROSCOPY;

AMINO ACID SEQUENCE; ANIMALS; BIOPHYSICAL PHENOMENA; HEMORHEOLOGY; HEMOSTASIS; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; THROMBOSIS; VON WILLEBRAND DISEASES; VON WILLEBRAND FACTOR;

EID: 84907369365     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-05-378638     Document Type: Review

References (112)

1. Zhou YF, Eng ET, Nishida N, Lu C, Walz T, Springer TA. A pH-regulated dimeric bouquet in the structure of von Willebrand factor. EMBO J. 2011;30(19):4098-4111.
2. Zhou YF, Eng ET, Zhu J, Lu C, Walz T, Springer TA. Sequence and structure relationships within von Willebrand factor. Blood. 2012;120(2):449-458.
3. Wagner DD. Cell biology of von Willebrand factor. Annu Rev Cell Biol. 1990;6:217-246.
4. Sadler JE. New concepts in von Willebrand disease. Annu Rev Med. 2005;56:173-191.
5. Yee A, Kretz CA. Von Willebrand factor: form for function. Semin Thromb Hemost. 2014;40(1): 17-27.
6. Huang RH, Wang Y, Roth R, et al. Assembly of Weibel-Palade body-like tubules from Nterminal domains of von Willebrand factor. Proc Natl Acad Sci USA. 2008;105(2): 482-487.
7. Shiltagh N, Kirkpatrick J, Cabrita LD, et al. Solution structure of the major factor VIII binding region on von Willebrand factor. Blood. 2014; 123(26):4143-4151.
8. O'Leary JM, Hamilton JM, Deane CM, Valeyev NV, Sandell LJ, Downing AK. Solution structure and dynamics of a prototypical chordinlike cysteine-rich repeat (von Willebrand factor type C module) from collagen IIA. J Biol Chem. 2004;279(51):53857-53866.
9. Zhang JL, Qiu LY, Kotzsch A, et al. Crystal structure analysis reveals how the Chordin family member crossveinless 2 blocks BMP-2 receptor binding. Dev Cell. 2008;14(5):739-750.
10. Titani K, Kumar S, Takio K, et al. Amino acid sequence of human von Willebrand factor. Biochemistry. 1986;25(11):3171-3184.
11. Nowak AA, Canis K, Riddell A, Laffan MA, McKinnon TA. O-linked glycosylation of von Willebrand factor modulates the interaction with platelet receptor glycoprotein Ib under static and shear stress conditions. Blood. 2012;120(1): 214-222.
12. Carew JA, Quinn SM, Stoddart JH, Lynch DC. O-linked carbohydrate of recombinant von Willebrand factor influences ristocetin-induced binding to platelet glycoprotein 1b. J Clin Invest. 1992;90(6):2258-2267.
13. Nowak AA, McKinnon TA, Hughes JM, Chion AC, Laffan MA. The O-linked glycans of human von Willebrand factor modulate its interaction with ADAMTS-13. J Thromb Haemost. 2014;12(1):54-61.
14. Badirou I, Kurdi M, Legendre P, et al. In vivo analysis of the role of O-glycosylations of von Willebrand factor. PLoS ONE. 2012;7(5): e37508.
15. De Luca M, Facey DA, Favaloro EJ, et al. Structure and function of the von Willebrand factor A1 domain: analysis with monoclonal antibodies reveals distinct binding sites involved in recognition of the platelet membrane glycoprotein Ib-IX-V complex and ristocetindependent activation. Blood. 2000;95(1): 164-172.
16. Flood VH, Friedman KD, Gill JC, et al. Limitations of the ristocetin cofactor assay in measurement of von Willebrand factor function. J Thromb Haemost. 2009;7(11):1832-1839.
17. Flood VH, Gill JC, Morateck PA, et al. Common VWF exon 28 polymorphisms in African Americans affecting the VWF activity assay by ristocetin cofactor. Blood. 2010;116(2):280-286.
18. Dong JF, Berndt MC, Schade A, McIntire LV, Andrews RK, López JA. Ristocetin-dependent, but not botrocetin-dependent, binding of von Willebrand factor to the platelet glycoprotein Ib-IX-V complex correlates with shear-dependent interactions. Blood. 2001;97(1):162-168.
19. Berriman JA, Li S, Hewlett LJ, et al. Structural organization of Weibel-Palade bodies revealed by cryo-EM of vitrified endothelial cells. Proc Natl Acad Sci USA. 2009;106(41):17407-17412.
20. Erent M, Meli A, Moisoi N, et al. Rate, extent and concentration dependence of histamine-evoked Weibel-Palade body exocytosis determined from individual fusion events in human endothelial cells. J Physiol. 2007;583(Pt 1):195-212.
21. Cramer EM, Caen JP, Drouet L, Breton-Gorius J. Absence of tubular structures and immunolabeling for von Willebrand factor in the platelet a-granules from porcine von Willebrand disease. Blood. 1986;68(3):774-778.
22. Michaux G, Abbitt KB, Collinson LM, Haberichter SL, Norman KE, Cutler DF. The physiological function of von Willebrand's factor depends on its tubular storage in endothelial Weibel-Palade bodies. Dev Cell. 2006;10(2):223-232.
23. Cookson EA, Conte IL, Dempster J, Hannah MJ, Carter T. Characterisation of Weibel-Palade body fusion by amperometry in endothelial cells reveals fusion pore dynamics and the effect of cholesterol on exocytosis. J Cell Sci. 2013; 126(Pt 23):5490-5499.
24. Vischer UM, Wagner DD. von Willebrand factor proteolytic processing and multimerization precede the formation of Weibel-Palade bodies. Blood. 1994;83(12):3536-3544.
25. Nightingale TD, White IJ, Doyle EL, et al. Actomyosin II contractility expels von Willebrand factor from Weibel-Palade bodies during exocytosis. J Cell Biol. 2011;194(4):613-629.
26. Fowler WE, Fretto LJ, Hamilton KK, Erickson HP, McKee PA. Substructure of human von Willebrand factor. J Clin Invest. 1985;76(4): 1491-1500.
27. Slayter H, Loscalzo J, Bockenstedt P, Handin RI. Native conformation of human von Willebrand protein. Analysis by electron microscopy and quasi-elastic light scattering. J Biol Chem. 1985; 260(14):8559-8563.
28. Dong JF, Moake JL, Nolasco L, et al. ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions. Blood. 2002; 100(12):4033-4039.
29. De Gennes PG. Scaling Concepts in Polymer Physics. Ithaca, NY: Cornell University Press; 1979.
30. Batlle J, Lopez-Fernandez MF, Lopez-Borrasca A, et al. Proteolytic degradation of von Willebrand factor after DDAVP administration in normal individuals. Blood. 1987;70(1):173-176.
31. Springer TA. Biology and physics of von Willebrand factor concatamers. J Thromb Haemost. 2011;9(suppl 1):130-143.
32. Savage B, Sixma JJ, Ruggeri ZM. Functional self-association of von Willebrand factor during platelet adhesion under flow. Proc Natl Acad Sci USA. 2002;99(1):425-430.
33. Ulrichts H, Vanhoorelbeke K, Girma JP, Lenting PJ, Vauterin S, Deckmyn H. The von Willebrand factor self-association is modulated by a multiple domain interaction. J Thromb Haemost. 2005;3(3):552-561.
34. Siedlecki CA, Lestini BJ, Kottke-Marchant KK, Eppell SJ, Wilson DL, Marchant RE. Sheardependent changes in the three-dimensional structure of human von Willebrand factor. Blood. 1996;88(8):2939-2950.
35. Schneider SW, Nuschele S, Wixforth A, et al. Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. Proc Natl Acad Sci USA. 2007;104(19):7899-7903.
36. Ruggeri ZM, Mendolicchio GL. Adhesion mechanisms in platelet function. Circ Res. 2007; 100(12):1673-1685.
37. Savage B, Saldívar E, Ruggeri ZM. Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell. 1996;84(2):289-297.
38. Savage B, Almus-Jacobs F, Ruggeri ZM. Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow. Cell. 1998;94(5):657-666.
39. Ruggeri ZM, Orje JN, Habermann R, Federici AB, Reininger AJ. Activation-independent platelet adhesion and aggregation under elevated shear stress. Blood. 2006;108(6): 1903-1910.
40. Smith DE, Babcock HP, Chu S. Single-polymer dynamics in steady shear flow. Science. 1999; 283(5408):1724-1727.
41. De Gennes PG. Coil-stretch transition of dilute flexible polymers under ultrahigh velocity gradients. J Chem Phys. 1974;60(12):5030.
42. Alexander-Katz A, Schneider MF, Schneider SW, Wixforth A, Netz RR. Shear-flow-induced unfolding of polymeric globules. Phys Rev Lett. 2006;97(13):138101.
43. Zhang X, Halvorsen K, Zhang CZ, Wong WP, Springer TA. Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor. Science. 2009;324(5932):1330-1334.
44. Sing CE, Alexander-Katz A. Elongational flow induces the unfolding of von Willebrand factor at physiological flow rates. Biophys J. 2010;98(9): L35-L37.
45. Sing CE, Alexander-Katz A. Giant nonmonotonic stretching response of a self-associating polymer in shear flow. Phys Rev Lett. 2011;107(19): 198302.
46. Doyle PS, Ladoux B, Viovy JL. Dynamics of a tethered polymer in shear flow. Phys Rev Lett. 2000;84(20):4769-4772.
47. Ulrichts H, Udvardy M, Lenting PJ, et al. Shielding of the A1 domain by the D9D3 domains of von Willebrand factor modulates its interaction with platelet glycoprotein Ib-IX-V. J Biol Chem. 2006;281(8):4699-4707.
48. Zhou YF, Springer TA. Highly reinforced structure of a C-terminal dimerization domain in von Willebrand factor. Blood. 2014;123(12): 1785-1793.
49. Wu T, Lin J, Cruz MA, Dong JF, Zhu C. Force-induced cleavage of single VWFA1A2A3 tridomains by ADAMTS-13. Blood. 2010;115(2): 370-378.
50. Ying J, Ling Y, Westfield LA, Sadler JE, Shao JY. Unfolding the A2 domain of von Willebrand factor with the optical trap. Biophys J. 2010; 98(8):1685-1693.
51. Jakobi AJ, Mashaghi A, Tans SJ, Huizinga EG. Calcium modulates force sensing by the von Willebrand factor A2 domain. Nat Commun. 2011;2:385.
52. Xu AJ, Springer TA. Calcium stabilizes the von Willebrand factor A2 domain by promoting refolding. Proc Natl Acad Sci USA. 2012; 109(10):3742-3747.
53. Xu AJ, Springer TA. Mechanisms by which von Willebrand disease mutations destabilize the A2 domain. J Biol Chem. 2013;288(9): 6317-6324.
54. Zhang Q, Zhou Y-F, Zhang C-Z, Zhang X, Lu C, Springer TA. Structural specializations of A2, a force-sensing domain in the ultralarge vascular protein von Willebrand factor. Proc Natl Acad Sci USA. 2009;106(23):9226-9231.
55. Zhou M, Dong X, Baldauf C, et al. A novel calcium-binding site of von Willebrand factor A2 domain regulates its cleavage by ADAMTS13. Blood. 2011;117(17):4623-4631.
56. Gao W, Anderson PJ, Majerus EM, Tuley EA, Sadler JE. Exosite interactions contribute to tension-induced cleavage of von Willebrand factor by the antithrombotic ADAMTS13 metalloprotease. Proc Natl Acad Sci USA. 2006; 103(50):19099-19104.
57. Zanardelli S, Crawley JT, Chion CK, Lam JK, Preston RJ, Lane DA. ADAMTS13 substrate recognition of von Willebrand factor A2 domain. J Biol Chem. 2006;281(3):1555-1563.
58. Luken BM, Winn LY, Emsley J, Lane DA, Crawley JT. The importance of vicinal cysteines, C1669 and C1670, for von Willebrand factor A2 domain function. Blood. 2010;115(23): 4910-4913.
59. Morioka Y, Casari C, Wohner N, et al. Expression of a structurally constrained von Willebrand factor variant triggers acute thrombotic thrombocytopenic purpura in mice. Blood. 2014;123(21):3344-3353.
60. Tersteeg C, de Maat S, De Meyer SF, et al. Plasmin cleavage of von Willebrand factor as an emergency bypass for ADAMTS13 deficiency in thrombotic microangiopathy. Circulation. 2014; 129(12):1320-1331.
61. Sadler JE. Von Willebrand factor, ADAMTS13, and thrombotic thrombocytopenic purpura. Blood. 2008;112(1):11-18.
62. Zarpellon A, Celikel R, Roberts JR, et al. Binding of a-thrombin to surface-anchored platelet glycoprotein Ib(α) sulfotyrosines through a two-site mechanism involving exosite I. Proc Natl Acad Sci USA. 2011;108(21):8628-8633.
63. McEwan PA, Yang W, Carr KH, et al. Quaternary organization of GPIb-IX complex and insights into Bernard-Soulier syndrome revealed by the structures of GPIbb and a GPIbb/GPIX chimera. Blood. 2011;118(19):5292-5301.
64. Huizinga EG, Tsuji S, Romijn RA, et al. Structures of glycoprotein Iba and its complex with von Willebrand factor A1 domain. Science. 2002;297(5584):1176-1179.
65. Blenner MA, Dong X, Springer TA. Structural basis of regulation of von Willebrand factor binding to glycoprotein Ib. J Biol Chem. 2014; 289(9):5565-5579.
66. Dumas JJ, Kumar R, McDonagh T, et al. Crystal structure of the wild-type von Willebrand factor A1-glycoprotein Iba complex reveals conformation differences with a complex bearing von Willebrand disease mutations. J Biol Chem. 2004;279(22):23327-23334.
67. Miura S, Li CQ, Cao Z, Wang H, Wardell MR, Sadler JE. Interaction of von Willebrand factor domain A1 with platelet glycoprotein Iba-(1-289). Slow intrinsic binding kinetics mediate rapid platelet adhesion. J Biol Chem. 2000;275(11): 7539-7546.
68. Othman M, Kaur H, Emsley J. Platelet-type von Willebrand disease: new insights into the molecular pathophysiology of a unique platelet defect. Semin Thromb Hemost. 2013;39(6): 663-673.
69. Casari C, Du V, Wu Y-P, et al. Accelerated uptake of VWF/platelet complexes in macrophages contributes to VWD type 2B-associated thrombocytopenia. Blood. 2013; 122(16):2893-2902.
70. Yago T, Lou J, Wu T, et al. Platelet glycoprotein Iba forms catch bonds with human WT vWF but not with type 2B von Willebrand disease vWF. J Clin Invest. 2008;118(9):3195-3207.
71. Kim J, Zhang CZ, Zhang X, Springer TA. A mechanically stabilized receptor-ligand flex-bond important in the vasculature. Nature. 2010; 466(7309):992-995.
72. Ju L, Dong JF, Cruz MA, Zhu C. The N-terminal flanking region of the A1 domain regulates the force-dependent binding of von Willebrand factor to platelet glycoprotein Iba. J Biol Chem. 2013; 288(45):32289-32301.
73. Holmberg L, Dent JA, Schneppenheim R, Budde U, Ware J, Ruggeri ZM. von Willebrand factor mutation enhancing interaction with platelets in patients with normal multimeric structure. J Clin Invest. 1993;91(5):2169-2177.
74. Shen Y, Romo GM, Dong JF, et al. Requirement of leucine-rich repeats of glycoprotein (GP) Iba for shear-dependent and static binding of von Willebrand factor to the platelet membrane GP Ib-IX-V complex. Blood. 2000;95(3):903-910.
75. Shen Y, Cranmer SL, Aprico A, et al. Leucinerich repeats 2-4 (Leu60-Glu128) of platelet glycoprotein Iba regulate shear-dependent cell adhesion to von Willebrand factor. J Biol Chem. 2006;281(36):26419-26423.
76. Nishida N, Sumikawa H, Sakakura M, et al. Collagen-binding mode of vWF-A3 domain determined by a transferred cross-saturation experiment. Nat Struct Biol. 2003;10(1):53-58.
77. Brondijk TH, Bihan D, Farndale RW, Huizinga EG. Implications for collagen I chain registry from the structure of the collagen von Willebrand factor A3 domain complex. Proc Natl Acad Sci USA. 2012;109(14):5253-5258.
78. Hoylaerts MF, Yamamoto H, Nuyts K, Vreys I, Deckmyn H, Vermylen J. von Willebrand factor binds to native collagen VI primarily via its A1 domain. Biochem J. 1997;324(Pt 1):185-191.
79. Bonnefoy A, Romijn RA, Vandervoort PA, VAN Rompaey I, Vermylen J, Hoylaerts MF. von Willebrand factor A1 domain can adequately substitute for A3 domain in recruitment of flowing platelets to collagen. J Thromb Haemost. 2006; 4(10):2151-2161.
80. Rastegar-Lari G, Villoutreix BO, Ribba AS, Legendre P, Meyer D, Baruch D. Two clusters of charged residues located in the electropositive face of the von Willebrand factor A1 domain are essential for heparin binding. Biochemistry. 2002;41(21):6668-6678.
81. Sadler JE, Budde U, Eikenboom JC, et al; Working Party on von Willebrand Disease Classification. Update on the pathophysiology and classification of von Willebrand disease: a report of the Subcommittee on von Willebrand Factor. J Thromb Haemost. 2006;4(10):2103-2114.
82. Larsen DM, Haberichter SL, Gill JC, Shapiro AD, Flood VH. Variability in platelet- and collagenbinding defects in type 2M von Willebrand disease. Haemophilia. 2013;19(4):590-594.
83. Hampshire DJ, Goodeve AC. The international society on thrombosis and haematosis von Willebrand disease database: an update. Semin Thromb Hemost. 2011;37(5):470-479.
84. Riddell AF, Gomez K, Millar CM, 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(16):3489-3496.
85. Flood VH, Lederman CA, Wren JS, 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(6):1431-1433.
86. Vincentelli A, Susen S, Le Tourneau T, et al. Acquired von Willebrand syndrome in aortic stenosis. N Engl J Med. 2003;349(4):343-349.
87. Sanders YV, Eikenboom J, de Wee EM, et al; WiN Study Group. Reduced prevalence of arterial thrombosis in von Willebrand disease. J Thromb Haemost. 2013;11(5):845-854.
88. Qureshi W, Hassan S, Dabak V, Kuriakose P. Thrombosis in Von Willebrand disease. Thromb Res. 2012;130(5):e255-e258.
89. Lotta LA, Tuana G, Yu J, et al. Next-generation sequencing study finds an excess of rare, coding single-nucleotide variants of ADAMTS13 in patients with deep vein thrombosis. J Thromb Haemost. 2013;11(7):1228-1239.
90. Lambers M, Goldenberg NA, Kenet G, et al. Role of reduced ADAMTS13 in arterial ischemic stroke: a pediatric cohort study. Ann Neurol. 2013;73(1):58-64.
91. Chauhan AK, Motto DG, Lamb CB, et al. Systemic antithrombotic effects of ADAMTS13. J Exp Med. 2006;203(3):767-776.
92. Zhao BQ, Chauhan AK, Canault M, et al. von Willebrand factor-cleaving protease ADAMTS13 reduces ischemic brain injury in experimental stroke. Blood. 2009;114(15):3329-3334.
93. Donadelli R, Orje JN, Capoferri C, Remuzzi G, Ruggeri ZM. Size regulation of von Willebrand factor-mediated platelet thrombi by ADAMTS13 in flowing blood. Blood. 2006;107(5):1943-1950.
94. Sixma JJ, Wester J. The hemostatic plug. Semin Hematol. 1977;14(3):265-299.
95. 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(3):298-311.
96. Zucker MB. Platelet agglutination and vasoconstriction as factors in spontaneous hemostasis in normal, thrombocytopenic, heparinized and hypoprothrombinemic rats. Am J Physiol. 1947;148(2):275-288.
97. Guyton AC. Textbook of Medical Physiology. 8th ed. Philadelphia, PA: W.B. Saunders Company; 1991.
98. Cruz WO. The significance of a smooth muscle component in hemostasis. Proc Soc Exp Biol Med. 1965;119:876-880.
99. Arfors KE, Bergqvist D. Influence of blood flow velocity on experimental haemostatic plug formation. Thromb Res. 1974;4(3):447-461.
100. Nesbitt WS, Westein E, Tovar-Lopez FJ, et al. A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med. 2009;15(6):665-673.
101. Ni H, Denis CV, Subbarao S, et al. Persistence of platelet thrombus formation in arterioles of mice lacking both von Willebrand factor and fibrinogen. J Clin Invest. 2000;106(3):385-392.
102. Brill A, Fuchs TA, Chauhan AK, et al. von Willebrand factor-mediated platelet adhesion is critical for deep vein thrombosis in mouse models. Blood. 2011;117(4):1400-1407.
103. De Meyer SF, Stoll G, Wagner DD, Kleinschnitz C. von Willebrand factor: an emerging target in stroke therapy. Stroke. 2012;43(2):599-606.
104. Momi S, Tantucci M, Van Roy M, Ulrichts H, Ricci G, Gresele P. Reperfusion of cerebral artery thrombosis by the GPIb-VWF blockade with the Nanobody ALX-0081 reduces brain infarct size in guinea pigs. Blood. 2013;121(25): 5088-5097.
105. Marti T, Rösselet SJ, Titani K, Walsh KA. Identification of disulfide-bridged substructures within human von Willebrand factor. Biochemistry. 1987;26(25):8099-8109.
106. Katsumi A, Tuley EA, Bodó I, Sadler JE. Localization of disulfide bonds in the cystine knot domain of human von Willebrand factor. J Biol Chem. 2000;275(33):25585-25594.
107. Huizinga EG, Martijn van der Plas R, Kroon J, Sixma JJ, Gros P. Crystal structure of the A3 domain of human von Willebrand factor: implications for collagen binding. Structure. 1997;5(9):1147-1156.
108. Emsley J, Cruz M, Handin R, Liddington R. Crystal structure of the von Willebrand factor A1 domain and implications for the binding of platelet glycoprotein Ib. J Biol Chem. 1998; 273(17):10396-10401.
109. Bienkowska J, Cruz M, Atiemo A, Handin R, Liddington R. The von Willebrand factor A3 domain does not contain a metal ion-dependent adhesion site motif. J Biol Chem. 1997;272(40): 25162-25167.
110. Zenner HL, Collinson LM, Michaux G, Cutler DF. High-pressure freezing provides insights into Weibel-Palade body biogenesis. J Cell Sci. 2007;120(Pt 12):2117-2125.
111. Loirat C, Girma JP, Desconclois C, Coppo P, Veyradier A. Thrombotic thrombocytopenic purpura related to severe ADAMTS13 deficiency in children. Pediatr Nephrol. 2009; 24(1):19-29.
112. Arya M, Anvari B, Romo GM, et al. Ultralarge multimers of von Willebrand factor form spontaneous high-strength bonds with the platelet glycoprotein Ib-IX complex: studies using optical tweezers. Blood. 2002;99(11): 3971-3977.