Structure and function of von Willebrand factor

Thrombosis and Haemostasis

Volumn 82, Issue 2, 1999, Pages 576-584

  Ruggeri, Zaverio M ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 8; GLYCOPROTEIN IB; INTEGRIN RECEPTOR; PROTEIN SUBUNIT; VON WILLEBRAND FACTOR;

CONFERENCE PAPER; CRYSTAL STRUCTURE; EXTRACELLULAR MATRIX; HEMOSTASIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; THROMBOCYTE FUNCTION; THROMBOSIS;

EID: 0032724684     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-0037-1615883     Document Type: Conference Paper

References (115)

1. Ruggeri ZM, Saldivar E. Platelets, hemostasis and thrombosis. In: Ruggeri ZM (ed). Von Willebrand Factor and the Mechanisms of Platelet Function. Berlin, Springer; 1998:1-32.
2. Ruggeri ZM. Structure and biosynthesis of von Willebrand factor. In: Ruggeri ZM, ed. Von Willebrand Factor and the Mechanisms of Platelet Function. Berlin, Springer; 1998:33-77.
3. Ruggeri ZM, Savage B. Biological functions of von Willebrand factor. In: Ruggeri ZM, ed. Von Willebrand Factor and the Mechanisms of Platelet Function. Berlin, Springer; 1998:79-109.
4. Zimmerman TS, Ratnoff OD, Powell AE. Immunologic differentiation of classic hemophilia (Factor VIII deficiency) and von Willebrand's disease. With observations on combined deficiencies of antihemophilic factor and proaccelerin (Factor V) and on an acquired circulating anticoagulant against antihemophilic factor. J Clin Invest. 1971;50:244-254.
5. van Mourik JA, Bouma BN, La Bruyere WT, de Graaf S, Mochtar IA. Factor VIII, a series of homologous oligomers and a complex of two proteins. Thromb Res. 1974;4:155-164.
6. Ruggeri ZM, Zimmerman TS. Variant von Willebrand's disease: characterization of two subtypes by analysis of multimeric composition of factor VIII/von Willebrand factor in plasma and platelets. J Clin Invest. 1980;65:1318-1325.
7. Hoyer LW, Shainoff JR. Factor VIII-related protein circulates in normal human plasma as high molecular weight multimers. Blood. 1980;55:1056-1059.
8. Perret BA, Furlan M, Beck EA. Studies on factor VIII-related protein. II. Estimation of molecular size differences between factor VIII oligomers. Biochim Biophys Acta. 1979;578:164-174.
9. Ruggeri ZM, Zimmerman TS. The complex multimeric composition of factor VIII/von Willebrand factor. Blood. 1981;57:1140-1143.
10. 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.
11. Titani K, Kumar S, Takio K, Ericsson LH, Wade RD, Ashida K, Walsh KA, Chopek MW, Sadler JE, Fujikawa K. Amino acid sequence of human von Willebrand factor. Biochemistry. 1986;25:3171-3184.
12. Fowler WE, Fretto LJ, Hamilton KK, Erickson HP, McKee PA. Substructure of human von Willebrand factor. J Clin Invest. 1985;76:1491-1500.
13. Fowler WE, Fretto LJ. Electron microscopy of von Willebrand factor. In: Zimmerman TS, Ruggeri ZM, eds. Coagulation and Bleeding Disorders. The Role of Factor VIII and von Willebrand Factor. New York, Marcel Dekker, Inc.; 1989:181-193.
14. Zimmerman TS, Dent JA, Ruggeri ZM, Nannini LH. Subunit composition of plasma von Willebrand factor. Cleavage is present in normal individuals, increased in IIA and IIB von Willebrand disease, but minimal in variants with aberrant structure of individual oligomers (Types IIC, IID and IIE). J Clin Invest. 1986;77:947-951.
15. 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 USA. 1990;87:6306-6310.
16. Sporn LA, Marder VJ, Wagner DD. Inducible secretion of large, biologically potent von Willebrand factor multimers. Cell. 1986;46:185-190.
17. Lopez-Fernandez MF, Ginsberg MH, Ruggeri ZM, Batlle J, Zimmerman TS. Multimeric structure of platelet factor VIII/von Willebrand factor. The presence of larger multimers and their reassociation with thrombin-stimulated platelets. Blood. 1982;60:1132-1138.
18. Moake JL, Rudy CK, Troll JH, Weinstein MJ, Colannino NM, Azacar J, Seder RH, Hong SL, Deykin D. Unusually large plasma factor VIII: von Willebrand factor multimers in chronic relapsing thrombotic thrombocytopenic purpura. N Engl J Med. 1982;307:1432-1435.
19. Furlan M, Robles R, Lammle B. Partial purification and characterization of a protease from human plasma cleaving von Willebrand factor to fragments produced by in vivo proteolysis. Blood. 1996;87:4223-4234.
20. Tsai HM. Physiologic cleavage of von Willebrand factor by a plasma protease is dependent on its conformation and requires calcium ion. Blood. 1996;87:4235-4244.
21. 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.
22. Mancuso DJ, Tuley EA, Westfield LA, Worrall NK, Shelton-Inloes BB, Sorace JM, Alevy YG, Sadler JE. Structure of the gene for human von Willebrand factor. J Biol Chem. 1989;264:19514-19527.
23. Ginsburg D, Handin RI, Bonthron DT, Donlon TA, Bruns GAP, Latt SA, Orkin SH. Human von Willebrand factor (vWF): isolation of complementary DNA (cDNA) clones and chromosomal localization. Science. 1985;228:1401-1406.
24. Mancuso DJ, Tuley EA, Westfield LA, Lester-Mancuso TL, Le Beau MM, Sorace JM, Sadler JE. Human von Willebrand factor gene and pseudogene: structural analysis and differentiation by polymerase chain reaction. Biochemistry. 1991;30:253-269.
25. Jahroudi N, Lynch DC. Endothelial-cell-specific regulation of von Willebrand factor gene expression. Mol Cell Biol. 1994;14:999-1008.
26. Ferreira V, Assouline Z, Schwachtgen JL, Bahnak BR, Meyer D, Kerbiriou-Nabias D. The role of the 5′-flanking region in the cell-specific transcription of the human von Willebrand factor gene. Biochem J. 1993;293:641-648.
27. Aird WC, Jahroudi N, Weiler-Guettler H, Rayburn HB, Rosenberg RD. Human von Willebrand factor gene sequences target expression to a subpopulation of endothelial cells in transgenic mice. Proc Natl Acad Sci USA. 1995;92:4567-4571.
28. Wu QY, Drout L, Carrier JL, Rothschild C, Berard M, Rouault C, Caen JP, Meyer D. Differential distribution of von Willebrand factor in endothelial cells. Comparison between normal pigs and pigs with von Willebrand disease. Arteriosclerosis. 1987;7:47-54.
29. Bahnak BR, Wu Q-Y, Coulombel L, Assouline Z, Kerbiriou-Nabias D, Pietu G, Drouet L, Caen JP, Meyer D. Expression of von Willebrand factor in porcine vessels: heterogeneity at the level of von Willebrand factor mRNA. J Cell Physiol. 1989;138:305-310.
30. Bonthron DT, Handin RI, Kaufman RJ, Wasley LC, Orr EC, Mitsock LM, Ewenstein B, Loscalzo J, Ginsburg D, Orkin SH. Structure of pre-pro-von Willebrand factor and its expression in heterologous cells. Nature. 1986;324:270-273.
31. Verweij CL, Diergaarde PJ, Hart M, Pannekoek H. Full-length von Willebrand factor (vWF) cDNA encodes a highly repetitive protein considerably larger than the mature vWF subunit. EMBO J. 1986;5:1839-1847.
32. Wagner DD, Fay PJ, Sporn LA, Sinha S, Lawrence SO, Marder VJ. Divergent fates of von Willebrand factor and its propolypeptide (von Willebrand antigen II) after secretion from endothelial cells. Proc Natl Acad Sci USA. 1987;84:1955-1959.
33. Vischer UM, Wagner DD. von Willebrand factor proteolytic processing and multimerization precede the formation of Weibel-Palade bodies. Blood. 1994;83:3536-3544.
34. Fay PJ, Kawai Y, Wagner DD, Ginsburg D, Bonthron D, Ohlsson-Wilhelm BM, Chavin SI, Abraham GN, Handin RI, Orkin SH, Montgomery RR, Marder VJ. Propolypeptide of von Willebrand factor circulates in blood and is identical to von Willebrand antigen II. Science. 1986;232:995-998.
35. Montgomery RR, Zimmerman TS. von Willebrand's disease antigen II: a new plasma and platelet antigen deficient in severe von Willebrand's disease. J Clin Invest. 1978;61:1498-1507.
36. Shelton-Inloes BB, Titani K, Sadler JE. cDNA sequences for human von Willebrand factor reveal five types of repeated domains and five possible protein sequence polymorphisms. Biochemistry. 1986;25:3164-3171.
37. Colombatti A, Bonaldo P. The superfamily of proteins with von Willebrand factor type A-like domains: one theme common to components of extracellular matrix, hemostasis, cellular adhesion, and defense mechanisms. Blood. 1991;77:2305-2315.
38. Hunt LT, Barker WC. von Willebrand Factor shares a distinctive cystein-rich domain with thrombospondin and procollagen. Biochem Biophys Res Commun. 1987;144:876-882.
39. Ginsberg MH, Loftus JC, Plow EF. Cytoadhesins, integrins, and platelets. Thromb Haemost. 1988;59:1-6.
40. Hynes RO. Integrins: versatility, modulation and signaling in cell adhesion. Cell. 1992;69:11-25.
41. Wagner DD, Lawrence SO, Ohlsson-Wilhelm BM, Fay PJ, Marder VJ. Topology and order of formation of interchain disulfide bonds in von Willebrand factor. Blood. 1987;69:27-32.
42. Voorberg J, Fontijn R, Calafat J, Janssen H, van Mourik JA, Pannekoek H. Assembly and routing of von Willebrand factor variants: the requirements for disulfide-linked dimerization reside within the carboxy-terminal 151 amino acids. J Cell Biol. 1991;113:195-205.
43. Schneppenheim R, Brassard J, Krey S, Budde U, Kunicki TJ, Holmberg L, Ware J, Ruggeri ZM. Defective dimerization of von Willebrand factor subunits due to a Cys to Arg mutation in type IID von Willebrand disease. Proc Natl Acad Sci USA. 1996;93:3581-3586.
44. Voorberg J, Fontijn R, van Mourik JA, Pannekoek H. Domains involved in multimer assembly of von Willebrand factor (vWF): multimerization is independent of dimerization. EMBO J. 1990;9:797-803.
45. Mayadas TN, Wagner DD. Vicinal cysteines in the prosequence play a role in von Willebrand factor multimer assembly. Proc Natl Acad Sci USA. 1992;89:3531-3535.
46. Kinoshita S, Harrison J, Lazerson J, Abildgaard CF. A new variant of dominant type II von Willebrand's disease with aberrant multimeric pattern of factor VIII-related antigen (type IID). Blood. 1984;63:1369-1371.
47. Loesberg C, Gonsalves MD, Zandbergen J, Willems C, Van Aken WG, Stel HV, van Mourik JA, DeGroot PG. The effect of calcium on the secretion of factor VIII-related antigen by cultured human endothelial cells. Biochim Biophys Acta. 1983;763:160-168.
48. Wagner DD. Storage and secretion of von Willebrand factor. In: Zimmerman TS, Ruggeri ZM, eds. Coagulation and Bleeding Disorders. The Role of Factor VIII and von Willebrand Factor. New York, Marcel Dekker, Inc.; 1989:161-180.
49. Wagner DD. Cell biology of von Willebrand factor. Annu Rev Cell Biol. 1990;6:217-246.
50. v.d. Kwast TH, Stel HV, Cristen E, Bertina RM, Veerman ECI. Localization of factor VIII-procoagulant antigen: an immunohistological survey of the human body using monoclonal antibodies. Blood. 1986;67:222-227.
51. Takeuchi M, Nagura H, Kaneda T. DDAVP and epinephrine-induced changes in the localization of von Willebrand factor antigen in endothelial cells of human oral mucosa. Blood. 1988;72:850-854.
52. Hop C, Fontijn R, VanMourik JA, Pannekoek H. Polarity of constitutive and regulated von Willebrand factor secretion by transfected MDCK-II cells. Exp Cell Res. 1997;230:352-361.
53. Nachman RL, Levine R, Jaffe EA. Synthesis of factor VIII antigen by cultured guinea pig megakaryocytes. J Clin Invest. 1977;60:914-921.
54. Sporn LA, Chavin SI, Marder VJ, Wagner DD. Biosynthesis of von Willebrand protein by human megakaryocytes. J Clin Invest. 1985;76:1102-1106.
55. Bowie EJ, Solberg LA, Jr, Fass DN, Johnson CM, Knutson GJ, Stewart ML, Zoecklein LJ. Transplantation of normal bone marrow into a pig with severe von Willebrand's disease. J Clin Invest. 1986;78:26-30.
56. Koutts J, Walsh PN, Plow EF, Fenton JW, Bouma BN, Zimmerman TS. Active release of human platelet Factor VIII-related antigen by adenosine diphosphate, collagen and thrombin. J Clin Invest. 1978;62:1255-1263.
57. Roth GJ, Titani K, Hoyer LW, Hickey MJ. Localization of binding sites within human von Willebrand factor for monomeric type III collagen. Biochemistry. 1986;25:8357-8361.
58. Pareti FI, Fujimura Y, Dent JA, Holland LZ, Zimmerman TS, Ruggeri ZM. Isolation and characterization of a collagen binding domain in human von Willebrand factor. J Biol Chem. 1986;261:15310-15315.
59. 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;262:13835-13841.
60. Mohri H, Yoshioka A, Zimmerman TS, Ruggeri ZM. Isolation of the von Willebrand factor domain interacting with platelet glycoprotein Ib, heparin, and collagen, and characterization of its three distinct functional sites. J Biol Chem. 1989;264:17361-17367.
61. Cruz MA, Yuan H, Lee JR, Wise RJ, Handin RI. Interaction of the von Willebrand factor (vWF) with collagen. J Biol Chem. 1995;270:10822-10827.
62. 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;324:185-191.
63. Yamamoto H, Vermylen J, Hoylaerts MF. Exposure of von Willebrand factor to shear forces stimulates A1 domain mediated interaction with collagen. Thromb Haemost. 1997;78:642-643.
64. Mazzucato M, Spessotto 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;274:3033-3041.
65. Fujimura Y, Titani K, Holland LZ, Roberts JR, Kostel P, Ruggeri ZM, Zimmerman TS. A heparin-binding domain of human von Willebrand factor. Characterization and localization to a tryptic fragment extending from amino acid residue Val-449 to Lys-728. J Biol Chem. 1987;262:1734-1739.
66. Sobel M, Soler DF, Kermode JC, Harris RB. Localization and characterization of a heparin binding domain peptide of human von Willebrand factor. J Biol Chem. 1992;267:8857-8862.
67. Fretto LJ, Fowler WE, McCaslin DR, Erickson HP, McKee PA. Substructure of human von Willebrand factor. Proteolysis by V8 and characterization of two functional domains. J Biol Chem. 1986;261:15679-15689.
68. Fujimura Y, Titani K, Holland LZ, Russell SR, Roberts JR, Elder JH, Ruggeri ZM, Zimmerman TS. von Willebrand factor. A reduced and alkylated 52/48 kDa fragment beginning at amino acid residue 449 contains the domain interacting with platelet glycoprotein Ib. J Biol Chem. 1986;261:381-385.
69. Mohri H, Fujimura Y, Shima M, Yoshioka A, Houghten RA, Ruggeri ZM, Zimmerman TS. Structure of the von Willebrand factor domain interacting with glycoprotein Ib. J Biol Chem. 1988;263:17901-17904.
70. Scott JP, Montgomery RR, Retzinger GS. Dimeric ristocetin flocculates proteins, binds to platelets, and mediates von Willebrand factor-dependent agglutination of platelets. J Biol Chem. 1991;266:8149-8155.
71. Berndt MC, Ward CM, Booth WJ, Castaldi PA, Mazurov AV, Andrews RK. Identification of aspartic acid 514 through glutamic acid 542 as a glycoprotein Ib-IX complex receptor recognition sequence in von Willebrand factor. Mechanisms of modulation of von Willebrand factor by ristocetin and botrocetin. Biochemistry. 1992;31:11144-11151.
72. Knott HM, Berndt MC, Kralicek AV, O'Donoghue SI, King GF. Determination of the solution structure of a platelet-adhesion peptide of von Willebrand factor. Biochemistry. 1992;31:11152-11158.
73. Matsushita T, Sadler JE. Identification of amino acid residues essential for von Willebrand factor binding to platelet glycoprotein Ib. J Biol Chem. 1995;270:13406-13414.
74. Celikel R, Varughese KI, Madhusudan A, 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.
75. 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;273:10396-10401.
76. 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.
77. 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.
78. Lee J-O, Rieu P, Arnaout MA, Liddington R. Crystal structure of the A domain from the α subunit of integrin CR3 (CD11b/CD18). Cell. 1995;80:631-638.
79. 2) integrin. Proc Natl Acad Sci USA. 1995;92:10277-10281.
80. Emsley J, King SL, Bergelson JM, Liddington TC. Crystal structure of the I domain from integrin α 2β1. J Biol Chem. 1997;272:28512-28517.
81. Kamata T, Puzon W, Takada Y. Identification of putative ligand binding sites within I domain of integrin alpha 2 beta 1 (VLA-2, CD49b/CD29). J Biol Chem. 1994;269:9659-9663.
82. Pierschbacher MD, Ruoslahti E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature. 1984;309:30-33.
83. Ruoslahti E, Pierschbacher MD. New perspectives in cell adhesion: RGD and integrins. Science. 1987;238:491-497.
84. Hynes RO. Integrins: a family of cell surface receptors. Cell. 1987;48:549-554.
85. Plow EF, Srouji AH, Meyer D, Marguerie G, Ginsberg MH. Evidence that three adhesive proteins interact with a common recognition site on activated platelets. J Biol Chem. 1984;259:5385-5391.
86. Berliner S, Niiya K, Roberts JR, Houghten RA, Ruggeri ZM. Generation and characterization of peptide-specific antibodies that inhibit von Willebrand factor binding to GP IIb-IIIa without interacting with other adhesive molecules: selectivity is conferred by Pro 1743 and other amino acid residues adjacent to the sequence Arg1744-Gly1745-Asp1746. J Biol Chem. 1988;263:7500-7505.
87. Beacham DA, Wise RJ, Turci SM, Handin RI, Selective inactivation of the Arg-Gly-Asp-Ser (RGDS) binding site in von Willebrand factor by site-directed Mutagenesis. J Biol Chem. 1992;267:3409-3415.
88. Dejana E, Lampugnani MG, Giorgi M, Gaboli M, Federici AB, Ruggeri ZM. von Willebrand factor promotes endothelial cell adhesion via an Arg-Gly-Asp-dependent mechanism. J Cell Biol. 1989;109:367-375.
89. Foster PA, Fulcher CA, Marti T, Titani K, Zimmerman TS. A major factor VIII binding domain resides within the amino-terminal 272 amino acid residues of von Willebrand factor. J Biol Chem. 1987;262:8443-8446.
90. Bahou WF, Ginsburg D, Sikkink R, Litwiller R, Fass DN. A monoclonal antibody to von Willebrand factor (vWF) inhibits factor VIII binding. Localization of its antigenic determinant to a non-adecapeptide at the amino terminus of the mature vWF polypeptide. J Clin Invest. 1989;84:56-61.
91. Ginsburg D, Bockenstedt PL, Allen EA, Fox DA, Foster PA, Ruggeri ZM, Zimmerman TS, Montgomery RR, Bahou WF, Johnson TA, Yang AY. Fine mapping of monoclonal antibody epitopes on human von Willebrand factor using a recombinant peptide library. Thromb Haemost. 1992;67:166-171.
92. Tuley EA, Gaucher C, Jorieux S, Worrall NK, Sadler JE, Mazurier C. Expression of von Willebrand factor "Normandy:" an autosomal mutation that mimics hemophilia A. Proc Natl Acad Sci USA. 1991;88:6377-6381.
93. Gaucher C, Mercier B, Jorieux S, Oufkir D, Mazurier C. Identification of two point mutations in the von Willebrand factor gene of three families with the "Normandy" variant of von Willebrand disease. Br J Haematol. 1991;78:506-514.
94. Cacheris PM, Nichols WC, Ginsburg D. Molecular characterization of a unique von Willebrand disease variant. J Biol Chem. 1991;266:13499-13502.
95. Kroner PA, Friedman KD, Fahst SA, Scott JP, Montgomery RR. Abnormal binding of factor VIII is linked with the substitution of glutamine for arginine 91 in von Willebrand factor in a variant form of von Willebrand disease. J Biol Chem. 1991;266:19146-19149.
96. Gu J, Jorieux S, Lavergne JM, Ruan C, Mazurier C, Meyer D. A patient with type 2N von Willebrand disease is heterozygous for a new mutation: Gly22Glu. Demonstration of a defective expression of the second allele by the use of monoclonal antibodies. Blood. 1997;89:3263-3269.
97. Roberts DD, Williams SB, Gralnick HR, Ginsburg V. von Willebrand factor binds specifically to sulfated glycolipids. J Biol Chem. 1986;261:3306-3309.
98. Christophe O, Obert B, Meyer D, Girma J-P. The binding domain of von Willebrand factor to sulfatides is distinct from those interacting with glycoprotein Ib, heparin, and collagen and resides between amino acid residues Leu 512 and Lys 673. Blood. 1991;78:2310-2317.
99. Ribes JA, Francis CW. Multimer size dependence of von Willebrand factor binding to crosslinked or noncrosslinked fibrin. Blood. 1990;75:1460-1465.
100. Hada M, Kaminski M, Bockenstedt P, McDonagh J. Covalent crosslinking of von Willebrand Factor to fibrin. Blood. 1986;68:95-101.
101. Tangelder GJ, Slaaf DW, Arts T, Reneman RS. Wall shear rate in arterioles in vivo: least estimates from platelet velocity profiles. Am J Physiol. 1988;254:H1059-H1064
102. 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.
103. 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.
104. Back CH, Radbill JR, Crawford DW. Analysis of pulsatile viscous blood flow through diseased coronary arteries of man. J Biomech (Tokyo). 1977;10:339-353.
105. Ikeda Y, Handa M, Kawano K, Kamata T, Murata M, Araki Y, Anbo H, Kawai Y, Watanabe K, Itagaki I, Sakai K, Ruggeri ZM. The role of von Willebrand factor and fibrinogen in platelet aggregation under varying shear stress. J Clin Invest. 1991;87:1234-1240.
106. Phillips DR, Charo IF, Scarborough RM. GPIIb-IIIa: the responsive integrin. Cell. 1991;65:359-362.
107. FAK. Biochem J. 1993;296:543-547.
108. 1 integrin is a necessary co-receptor for collagen-induced activation of Syk and subsequent phosphorylation of phospholipase Cy2 in platelets. J Biol Chem. 1996;271:26668-26676.
109. Nieuwenhuis HK, Akkerman JWN, Houdijk WPM, Sixma JJ. Human blood platelets showing no response to collagen fail to express surface glycoprotein Ia. Nature. 1985;318:470-472.
110. 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.
111. Weiss HJ. Platelet physiology and abnormalities of platelet function (first of two parts). N Engl J Med. 1975;293:531-541.
112. Weiss HJ. Platelet physiology and abnormalities of platelet function (second of two parts). N Engl J Med. 1975;293:580-588.
113. Sixma JJ, Wester J. The hemostatic plug. Semin Hematol. 1977;14:265-299.
114. Kroll MH, Hellums JD, McIntire LV, Schafer AI, Moake JL. Platelets and shear stress. Blood. 1996;88:1525-1541.
115. Ruggeri ZM, Dent JA, Saldivar E. Contribution of distinct adhesive interactions to platelet aggregation in flowing blood. Blood. In press.