Seminars in Hematology
Volume 42, Issue 1 , Pages 5-14 , January 2005

New perspectives on von Willebrand factor functions in hemostasis and thrombosis

  • Grazia Loredana Mendolicchio

      Affiliations

    • Roon Research Laboratory for Arteriosclerosis and Thrombosis, Division of Experimental Thrombosis and Hemostasis, Department of Molecular and Experimental Medicine, The Scripps Research Institute, La Jolla, CA
    • ,
  • Zaverio M. Ruggeri

      Affiliations

    • Roon Research Laboratory for Arteriosclerosis and Thrombosis, Division of Experimental Thrombosis and Hemostasis, Department of Molecular and Experimental Medicine, The Scripps Research Institute, La Jolla, CA
    • Corresponding Author InformationAddress correspondence to Zaverio M. Ruggeri, MD, The Scripps Research Institute, MEM-175, 10550 N Torrey Pines Rd, La Jolla, CA 92037

References 

  1. Andrews RK , Gardiner EE , Shen Y , Whisstock JC , Berndt MC . Glycoprotein Ib-IX-V . Int J Biochem Cell Biol . 2003;35:1170–1174
  2. Ruggeri ZM . Platelets in atherothrombosis . Nat Med . 2002;8:1227–1234
  3. Rosenberg JB , Foster PA , Kaufman RJ , Vokac EA , Moussalli M , Kroner PA , et al.   Intracellular trafficking of factor VIII to von Willebrand factor storage granules . J Clin Invest . 1998;101:613–624
  4. Nogami K , Shima M , Nishiya K , Hosokawa K , Saenko EL , Sakurai Y , et al.   A novel mechanism of factor VIII protection by von Willebrand factor from activated protein C-catalyzed inactivation . Blood . 2002;99:3993–3998
  5. Castaman G , Federici AB , Rodeghiero F , Mannucci PM . Von Willebrand’s disease in the year 2003 (Towards the complete identification of gene defects for correct diagnosis and treatment) . Haematologica . 2003;88:94–108
  6. Federici AB , Budde U , Rand JH . Acquired von Willebrand syndrome 2004 (International Registry-diagnosis and management from online to bedside) . Hamostaseologie . 2004;24:50–55
  7. Ruggeri ZM , Ware J , Ginsburg D . von Willebrand factor . In:  Loscalzo J ,  Schafer A editor. Thrombosis and Hemorrhage . Philadelphia, PA: Lippincott Williams & Wilkins; 2003;p. 246–265
  8. Budde U , Schneppenheim R . Von Willebrand factor and von Willebrand disease . Rev Clin Exp Hematol . 2001;5:335–368
  9. Titani K , Kumar S , Takio K , Ericsson LH , Wade RD , Ashida K , et al.   Amino acid sequence of human von Willebrand factor . Biochemistry . 1986;25:3171–3184
  10. Fowler WE , Fretto LJ . Electron microscopy of von Willebrand factor. The Role of Factor VIII and von Willebrand Factor . In:  Zimmerman TS ,  Ruggeri ZM editor. Coagulation and Bleeding Disorders . New York, NY: Dekker; 1989;p. 181–193
  11. Mayadas TN , Wagner DD . von Willebrand factor biosynthesis and processing . Ann NY Acad Sci . 1991;614:153–166
  12. Katsumi A , Tuley EA , Bodo I , Sadler JE . Localization of disulfide bonds in the cystine knot domain of human von Willebrand factor . J Biol Chem . 2000;275:25585–25594
  13. Mayadas TN , Wagner DD . Vicinal cysteines in the prosequence play a role in von Willebrand factor multimer assembly . Proc Natl Acad Sci U S A . 1992;89:3531–3535
  14. Haberichter SL , Jozwiak MA , Rosenberg JB , Christopherson PA , Montgomery RR . The von Willebrand factor propeptide (VWFpp) traffics an unrelated protein to storage . Arterioscler Thromb Vasc Biol . 2002;22:921–926
  15. Haberichter SL, Merricks EP, Fahs SA, Christopherson PA, Nichols TC, Montgomery RR: Re-establishment of VWF-dependent Weibel-Palade bodies in VWD endothelial cells. Blood Epub ahead of print Aug 26, 2004
  16. Cramer EM , Breton-Gorius J , Beesley JE , Martin JF . Ultrastructural demonstration of tubular inclusions coinciding with von Willebrand factor in pig megakaryocytes . Blood . 1988;71:1533–1538
  17. Fay PJ , Kawai Y , Wagner DD , Ginsburg D , Bonthron D , Ohlsson-Wilhelm BM , et al.   Propolypeptide of von Willebrand factor circulates in blood and is identical to von Willebrand antigen II . Science . 1986;232:995–998
  18. Bowie EJ , Solberg LA , Fass DN , Johnson CM , Knutson GJ , Stewart ML , et al.   Transplantation of normal bone marrow into a pig with severe von Willebrand’s disease . J Clin Invest . 1986;78:26–30
  19. Gerritsen HE , Robles R , Lämmle B , Furlan M . Partial amino acid sequence of purified von Willebrnad factor-cleaving protease . Blood . 2001;98:1654–1661
  20. Fujikawa K , Suzuki H , McMullen B , Chung D . Purification of human von Willebrand factor-cleaving protease and its identification as a new member of the metalloproteinase family . Blood . 2001;98:1662–1666
  21. Dent JA , Berkowitz SD , Ware J , Kasper CK , Ruggeri ZM . Identification of a cleavage site directing the immunochemical detection of molecular abnormalities in type IIA von Willebrand factor . Proc Natl Acad Sci U S A . 1990;87:6306–6310
  22. Dent JA , Galbusera M , Ruggeri ZM . Heterogeneity of plasma von Willebrand factor multimers resulting from proteolysis of the constituent subunit . J Clin Invest . 1991;88:774–782
  23. Celikel R , Varughese KI , Madhusudan  , Yoshioka A , Ware J , Ruggeri ZM . Crystal structure of von Willebrand factor A1 domain in complex with the function blocking NMC-4 Fab . Nat Struct Biol . 1998;5:189–194
  24. Huizinga EG , Tsuji S , Romijn RA , Schiphorst ME , de Groot PG , Sixma JJ , et al.   Structures of glycoprotein Ibα and its complex with von Willebrand factor A1 domain . Science . 2002;297:1176–1179
  25. Dumas JJ , Kumar R , McDonagh T , Sullivan F , Stahl ML , Somers WS , et al.   Crystal structure of the wild-type von Willebrand factor A1-glycoprotein Ibα complex reveals conformation differences with a complex bearing von Willebrand disease mutations . J Biol Chem . 2004;279: 23327-22334
  26. Ruggeri ZM , Pareti FI , Mannucci PM , Ciavarella N , Zimmerman TS . Heightened interaction between platelets and factor VIII/von Willebrand factor in a new subtype of von Willebrand’s disease . N Engl J Med . 1980;302:1047–1051
  27. Celikel R , Ruggeri ZM , Varughese KI . von Willebrand factor conformation and adhesive function is modulated by an internalized water molecule . Nat Struct Biol . 2000;7:881–884
  28. Goto S , Salomon DR , Ikeda Y , Ruggeri ZM . Characterization of the unique mechanism mediating the shear-dependent binding of soluble von Willebrand factor to platelets . J Biol Chem . 1995;270:23352–23361
  29. Siediecki 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;88:2939–2950
  30. Howard MA , Firkin BG . Ristocetin—A new tool in the investigation of platelet aggregation . Thromb Haemost . 1971;26:362–369
  31. Brinkhous KM , Read MS , Fricke WA , Wagner RH . Botrocetin (venom coagglutinin) (Reaction with a broad spectrum of multimeric forms of factor VIII macromolecular complex) . Proc Natl Acad Sci U S A . 1983;80:1463–1466
  32. Fukuda K , Doggett TA , Bankston LA , Cruz MA , Diacovo TG , Liddington RC . Structural basis of von Willebrand factor activation by the snake toxin botrocetin . Structure . 2002;10:943–950
  33. Azuma H , Sugimoto M , Ruggeri ZM , Ware J . A role for von Willebrand factor proline residues 702–704 in ristocetin-mediated binding to platelet glycoprotein Ib . Thromb Haemost . 1993;69:192–196
  34. Mazzucato M, Spessotto P, Masotti A, De Appollonia L, Cozzi MR, Yoshioka A, et al  Identification of domains responsible for von Willebrand factor type VI collagen interaction mediating platelet adhesion under high flow . J Biol Chem . 1999;274:3033–3041
  35. Wu D , Vanhoorelbeke K , Cauwenberghs N , Meiring M , Depraetere H , Kotze HF , et al.   Inhibition of the von Willebrand (VWF)-collagen interaction by an antihuman VWF monoclonal antibody results in abolition of in vivo arterial platelet thrombus formation in baboons . Blood . 2002;99:3623–3628
  36. 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;86:848–854
  37. Huizinga EG , van der Plas RM , Kroon J , Sixma JJ , Gros P . Crystal structure of the A3 domain of human von Willebrand factor (Implications for collagen binding) . Structure . 1997;5:1147–1156
  38. Bienkowska J , Cruz MA , Handin RI , Liddington RC . The von Willebrand factor A3 domain does not contain a metal ion-dependent adhesion site motif . J Biol Chem . 1997;272:25162–25167
  39. Romijn RAP , Bouma B , Wuyster W , Gros P , Kroon J , Sixma JJ , et al.   Identification of the collagen-binding site of the von Willebrand factor A3-domain . J Biol Chem . 2001;276:9985–9991
  40. Romijn RA , Westein E , Bouma B , Schiphorst ME , Sixma JJ , Lenting PJ , et al.   Mapping the collagen-binding site in the von Willebrand factor-A3 domain . J Biol Chem . 2003;278:15035–15039
  41. Nishida N , Sumikawa H , Sakakura M , Shimba N , Takahashi H , Terasawa H , et al.   Collagen-binding mode of vWF-A3 domain determined by a transferred cross-saturation experiment . Nat Struct Biol . 2003;10:53–58
  42. Back CH , Radbill JR , Crawford DW . Analysis of pulsatile viscous blood flow through diseased coronary arteries of man . J Biomech . 1977;10:339–353
  43. Strony J , Beaudoin A , Brands D , Adelman B . Analysis of shear stress and hemodynamic factors in a model of coronary artery stenosis and thrombosis . Am J Physiol . 1993;265:H1787–H1796
  44. Mailhac A , Badimon JJ , Fallon JT , Fernandez-Ortiz A , Meyer B , Chesebro JH , et al.   Effect of an eccentric severe stenosis on fibrin(ogen) deposition on severely damaged vessel wall in arterial thrombosis. Relative contribution of fibrin(ogen) and platelets . Circulation . 1994;90:988–996
  45. Ruggeri ZM , Mannucci PM , Federici AB , Lombardi R , Zimmerman TS . Multimeric composition of factor VIII/von Willebrand factor following administration of DDAVP (Implications for pathophysiology and therapy of von Willebrand’s disease subtypes) . Blood . 1982;59:1272–1278
  46. Levy GG , Nichols WC , Lian EC , Foroud T , McClintock JN , McGee BM , et al.   Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura . Nature . 2001;413:488–494
  47. Zheng X , Chung D , Takayama TK , Majerus EM , Sadler JE , Fujikawa K . Structure of von Willebrand factor-cleaving protease (ADAMTS13), a metalloprotease involved in thrombotic thrombocytopenic purpura . J Biol Chem . 2001;276:41059–41063
  48. Moake JL . Thrombotic microangiopathies . N Engl J Med . 2002;347:589–600
  49. Ajzenberg N , Denis CV , Veyradier A , Girma J-P , Meyer D , Baruch D . Complete defect in vWF-cleaving protease activity associated with increased shear-induced platelet aggregation in thrombotic microangiopathy . Thromb Haemost . 2002;87:808–811
  50. Dong J-F , Moake JL , Nolasco L , Bernardo A , Arceneaux W , Shrimpton CN , et al.   ADAMTS-13 rapidly cleaves newly secreted ultra-large von Willebrand factor multimers on the endothelial surface under flowing conditions . Blood . 2002;100:4033–4039
  51. Blot E , Deecaudin D , Veyradier A , Bardier A , Zagame O-L , Pouillart P . Cancer-related thrombotic microangiopathy secondary to von Willebrand factor-cleaving protease deficiency . Thromb Res . 2002;106:127–130
  52. Xie L , Chesterman CN , Hogg PJ . Control of von Willebrand factor multimer size by thrombospondin-1 . J Exp Med . 2001;193:1341–1349
  53. Savage B , Almus-Jacobs F , Ruggeri ZM . Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow . Cell . 1998;94:657–666
  54. Savage B , Saldivar E , Ruggeri ZM . Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor . Cell . 1996;84:289–297
  55. Ruggeri ZM , Bader R , De Marco L . Glanzmann thrombasthenia (Deficient binding of von Willebrand factor to thrombin-stimulated platelets) . Proc Natl Acad Sci U S A . 1982;79:6038–6041
  56. Ruggeri ZM , De Marco 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
  57. Clemetson KJ , Clemetson JM . Platelet collagen receptors . Thromb Haemost . 2001;86:189–197
  58. Nieswandt B , Watson SP . Platelet-collagen interaction (is GPVI the central receptor?) . Blood . 2003;102:449–461
  59. Savage B , Sixma JJ , Ruggeri ZM . Functional self-association of von Willebrand factor during platelet adhesion under flow . Proc Natl Acad Sci U S A . 2002;99:425–430
  60. Goto S, Sakai H, Goto M, Ono M, Ikeda Y, Handa S, et al. Enhanced shear-induced platelet aggregation in acute myocardial infarction . Circulation . 1999;99:608–613
  61. Ruggeri ZM , Dent JA , Saldivar E . Contribution of distinct adhesive interactions to platelet aggregation in flowing blood . Blood . 1999;94:172–178
  62. Zareba W , Pancio G , Moss AJ , Kalaria VG , Marder VJ , Weiss HJ , et al.   Increased level of von Willebrand factor is significantly and independently associated with diabetes in postinfarction patients . Thromb Haemost . 2001;86:791–799
  63. Theilmeier G , Michiels C , Spaepen E , Vreys I , Collen D , Vermylen J , et al.   Endothelial von Willebrand factor recruits platelets to atherosclerosis-prone sites in response to hypercholesterolemia . Blood . 2002;99:4486–4493
  64. Methia N , Andre P , Denis CV , Economopoulos M , Wagner DD . Localized reduction of atherosclerosis in von Willebrand factor-deficient mice . Blood . 2001;98:1424–1428
  65. Kasirer-Friede A , Ware J , Leng L , Marchese P , Ruggeri ZM , Shattil SJ . Lateral clustering of platelet GP Ib-IX complexes leads to up-regulation of the adhesive function of integrin αIIbβ3 . J Biol Chem . 2002;277:11949–11956
  66. Kasirer-Friede A , Cozzi MR , Mazzucato M , De Marco L , Ruggeri ZM , Shattil SJ . Signaling through GP Ib-IX-V activates αIIbβ3 independently of other receptors . Blood . 2004;103:3403–3411
  67. Mazzucato M , Pradella P , Cozzi MR , De Marco L , Ruggeri ZM . Sequential cytoplasmic calcium signals in a two-stage platelet activation process induced by the glycoprotein Ibα mechanoreceptor . Blood . 2002;100:2793–2800
  68. Yap CL , Anderson KE , Hughan SC , Dopheide SM , Salem HH , Jackson SP . Essential role for phosphoinositide 3-kinase in shear-dependent signaling between platelet glycoprotein Ib/V/IX and integrin αIIbβ3 . Blood . 2002;99:151–158
  69. Mazzucato M, Cozzi MR, Pradella P, Ruggeri ZM, De Marco L: Distinct roles of two ADP receptors in von Willebrand factor-mediated platelet signaling and activation under flow. Blood Epub ahead of print July 29, 2004
  70. Falati S , Edmead CE , Poole AW . Glycoprotein Ib-V-IX, a receptor for von Willebrand factor, couples physically and functionally to the Fc receptor γ-chain, Fyn, and Lyn to activate human platelets . Blood . 1999;94:1648–1656
  71. Torti M , Bertoni A , Canobbio I , Sinigaglia F , Lapetina EG , Balduini C . Rap 1B and Rap2B translocation to the cytoskeleton by von Willebrand factor involves FcgammaII receptor-mediated protein tyrosine physphorylation . J Biol Chem . 1999;274:13690–13697
  72. Wu Y , Suzuki-Inoue K , Satoh K , Asazuma N , Yatomi Y , Berndt MC , et al.   Role of Fc receptor gamma-chain in platelet glycoprotein Ib-mediated signaling . Blood . 2001;97:3836–3845
  73. Sullam PM , Hyun W , Szollosi J , Foss WM , Lopez JA . Physical proximity and functional interplay of the glycoprotein Ib-IX-V complex and the Fc receptor FcΨRIIa on the platelet plasma membrane . J Biol Chem . 1998;273:5331–5336
  74. Lefkovits J , Plow EF , Topol EJ . Platelet glycoprotein IIb/IIIa receptors in cardiovascular medicine . N Engl J Med . 1995;332:1553–1559
  75. Goto S , Ikeda Y , Saldivar E , Ruggeri ZM . Distinct mechanisms of platelet aggregation as a consequence of different shearing flow conditions . J Clin Invest . 1998;101:479–486
  76. Ni H , Subbarao S , Denis C , Degen JL , Hynes RO , Wagner DD . Distinct roles of von Willebrand factor and fibrinogen in thrombus growth in arterioles . Thromb Haemost . 1999;82(suppl):411; (abstr)
  77. Ni H, Denis CV, Subbarao S, Degen JL, Sato TN, Hynes RO, et al. Persistence of platelet thrombus formation in arterioles of mice lacking both von Willebrand factor and fibrinogen . J Clin Invest . 2000;106:385–392
  78. Ni H , Yuen PS , Papalia JM , Trevithick JE , Sakai T , Fassler R , et al.   Plasma fibronectin promotes thrombus growth and stability in injured arterioles . Proc Natl Acad Sci U S A . 2003;100:2415–2419
  79. Andre P , Prasad KS , Denis CV , He M , Papalia JM , Hynes RO , et al.   CD40L stabilizes arterial thrombi by a β3 integrin-dependent mechanism . Nat Med . 2002;8:247–252

PII: S0037-1963(04)00211-2

doi: 10.1053/j.seminhematol.2004.09.006

Seminars in Hematology
Volume 42, Issue 1 , Pages 5-14 , January 2005

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