Cell adhesion mechanisms in platelets

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 28, Issue 3, 2008, Pages 403-413

  Varga Szabo, David ^a   Pleines, Irina ^a   Nieswandt, Bernhard ^a,b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Activation; Adhesion; Platelet; Receptors; Thrombosis

Indexed keywords

BETA1 INTEGRIN; BETA3 INTEGRIN; COLLAGEN RECEPTOR; GLYCOPROTEIN IB ALPHA; GLYCOPROTEIN IIB; GLYCOPROTEIN IIIA; GLYCOPROTEIN VI; INTEGRIN; MATRIX PROTEIN; VERY LATE ACTIVATION ANTIGEN 2; VERY LATE ACTIVATION ANTIGEN 5; VERY LATE ACTIVATION ANTIGEN 6; VON WILLEBRAND FACTOR; FIBRINOGEN RECEPTOR; PLATELET MEMBRANE GLYCOPROTEIN VI; UNCLASSIFIED DRUG;

BLOOD CLOTTING; BLOOD VESSEL INJURY; CELL SPREADING; DISULFIDE BOND; EXTRACELLULAR MATRIX; HEART INFARCTION; HEMOSTASIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; STROKE; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOGENESIS; ANIMAL; CELL ADHESION; CYTOLOGY; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR BIOLOGY; MOUSE; PHYSIOLOGY; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOCYTE ADHESIVENESS;

ANIMALS; BLOOD PLATELETS; CELL ADHESION; EXTRACELLULAR MATRIX; HUMANS; MICE; MOLECULAR BIOLOGY; PLATELET ADHESIVENESS; PLATELET AGGREGATION; PLATELET MEMBRANE GLYCOPROTEINS; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION;

EID: 40749118934     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.107.150474     Document Type: Review

References (116)

1. Italiano JE Jr, Patel-Hett S, Hartwig JH. Mechanics of proplatelet elaboration. J Thromb Haemost. 2007;5(Suppl 1):18-23.
2. Junt T, Schulze H, Chen Z, Massberg S, Goerge T, Krueger A, Wagner DD, Graf T, Italiano JE Jr, Shivdasani RA, von Andrian UH. Dynamic visualization of thrombopoiesis within bone marrow. Science. 2007;317:1767-1770.
3. Huo Y, Schober A, Forlow SB, Smith DF, Hyman MC, Jung S, Littman DR, Weber C, Ley K. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med. 2003;9:61- 67.
4. Frenette PS, Denis CV, Weiss L, Jurk K, Subbarao S, Kehrel B, Hartwig JH, Vestweber D, Wagner DD. P-Selectin glycoprotein ligand 1 (PSGL-1) is expressed on platelets and can mediate platelet-endothelial interactions in vivo. J Exp Med. 2000;191:1413-1422.
5. Massberg S, Brand K, Gruner S, Page S, Muller E, Muller I, Bergmeier W, Richter T, Lorenz M, Konrad I, Nieswandt B, Gawaz M. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J Exp Med. 2002; 196:887- 896.
6. Schober A, Manka D, von Hundelshausen P, Huo Y, Hanrath P, Sarembock IJ, Ley K, Weber C. Deposition of platelet RANTES triggering monocyte recruitment requires P-selectin and is involved in neointima formation after arterial injury. Circulation. 2002;106: 1523-1529.
7. Mause SF, von Hundelshausen P, Zernecke A, Koenen RR, Weber C. Platelet microparticles: a transcellular delivery system for RANTES promoting monocyte recruitment on endothelium. Arterioscler Thromb Vasc Biol. 2005;25:1512-1518.
8. Lindemann S, Kramer B, Seizer P, Gawaz M. Platelets, inflammation and atherosclerosis. J Thromb Haemost. 2007;5(Suppl 1):203-211.
9. 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.
10. Furie B, Furie BC. In vivo thrombus formation. J Thromb Haemost. 2007;5 Suppl 1:12-17.
11. Offermanns S. Activation of platelet function through G protein-coupled receptors. Circ Res. 2006;99:1293-1304.
12. Ruggeri ZM. Structure and function of von Willebrand factor. Thromb Haemost. 1999;82:576 -584.
13. Berndt MC, Shen Y, Dopheide SM, Gardiner EE, Andrews RK. The vascular biology of the glycoprotein Ib-IX-V complex. Thromb Haemost. 2001;86:178 -188.
14. 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.
15. 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.
16. Sporn LA, Marder VJ, Wagner DD. Inducible secretion of large, biologically potent von Willebrand factor multimers. Cell. 1986;46:185-190.
17. Ewenstein BM. Von Willebrand's disease. Annu Rev Med. 1997;48: 525-542.
18. Denis C, Methia N, Frenette PS, Rayburn H, Ullman-Cullere M, Hynes RO, Wagner DD. A mouse model of severe von Willebrand disease: defects in hemostasis and thrombosis. Proc Natl Acad Sci U S A. 1998;95:9524 -9529.
19. Jurk K, Clemetson KJ, de Groot PG, Brodde MF, Steiner M, Savion N, Varon D, Sixma JJ, Van Aken H, Kehrel BE. Thrombospondin-1 mediates platelet adhesion at high shear via glycoprotein Ib (GPIb): an alternative/backup mechanism to von Willebrand factor. FASEB J. 2003;17:1490 -1492.
20. Sakariassen KS, Nievelstein PF, Coller BS, Sixma JJ. The role of platelet membrane glycoproteins Ib and IIb-IIIa in platelet adherence to human artery subendothelium. Br J Haematol. 1986;63:681- 691.
21. George JN, Nurden AT, Phillips DR. Molecular defects in interactions of platelets with the vessel wall. N Engl J Med. 1984;311:1084 -1098.
22. Luo SZ, Mo X, Afshar-Kharghan V, Srinivasan S, Lopez JA, Li R. Gly-coprotein Ibalpha forms disulfide bonds with 2 glycoprotein Ibbeta subunits in the resting platelet. Blood. 2007;109:603- 609.
23. Ozaki Y, Asazuma N, Suzuki-Inoue K, Berndt MC. Platelet GPIb-IX-V-dependent signaling. J Thromb Haemost. 2005;3:1745-1751.
24. Lopez JA, Andrews RK, Afshar-Kharghan V, Berndt MC. Bernard-Soulier syndrome. Blood. 1998;91:4397- 4418.
25. Ware J, Russell S, Ruggeri ZM. Generation and rescue of a murine model of platelet dysfunction: the Bernard-Soulier syndrome. Proc Natl Acad Sci U S A. 2000;97:2803-2808.
26. Kato K, Martinez C, Russell S, Nurden P, Nurden A, Fiering S, Ware J. Genetic deletion of mouse platelet glycoprotein Ib{beta} produces a Bernard-Soulier phenotype with increased {alpha}-granule size. Blood. 2004;104:2339 -2344.
27. Kanaji T, Russell S, Ware J. Amelioration of the macrothrombocytopenia associated with the murine Bernard-Soulier syndrome. Blood. 2002;100: 2102-2107.
28. Ramakrishnan V, Reeves PS, DeGuzman F, Deshpande U, Ministri-Madrid K, DuBridge RB, Phillips DR. Increased thrombin responsiveness in platelets from mice lacking glycoprotein V. Proc Natl Acad Sci U S A. 1999; 96:13336 -13341.
29. Kahn ML, Diacovo TG, Bainton DF, Lanza F, Trejo J, Coughlin SR. Glyco-protein V-deficient platelets have undiminished thrombin responsiveness and do not exhibit a Bernard-Soulier phenotype. Blood. 1999;94:4112- 4121.
30. Andrews RK, Berndt MC. Platelet physiology and thrombosis. Thromb Res. 2004;114:447- 453.
31. Dai K, Bodnar R, Berndt MC, Du X. A critical role for 14-3-3zeta protein in regulating the VWF binding function of platelet glycoprotein Ib-IX and its therapeutic implications. Blood. 2005;106:1975-1981.
32. Shrimpton CN, Borthakur G, Larrucea S, Cruz MA, Dong JF, Lopez JA. Localization of the Adhesion Receptor Glycoprotein Ib-IX-V Complex to Lipid Rafts Is Required for Platelet Adhesion and Activation. J Exp Med. 2002;196:1057-1066.
33. Arthur JF, Gardiner EE, Matzaris M, Taylor SG, Wijeyewickrema L, Ozaki Y, Kahn ML, Andrews RK, Berndt MC. Glycoprotein VI is associated with GPIb-IX-V on the membrane of resting and activated platelets. Thromb Haemost. 2005;93:716 -723.
34. Wu Y, Suzuki-Inoue K, Satoh K, Asazuma N, Yatomi Y, Berndt MC, Ozaki Y. Role of Fc receptor gamma-chain in platelet glycoprotein Ib-mediated signaling. Blood. 2001;97:3836-3845.
35. Kasirer-Friede A, Cozzi MR, Mazzucato M, De Marco L, Ruggeri ZM, Shattil SJ. Signaling through GP Ib-IX-V activates alpha IIb beta 3 independently of other receptors. Blood. 2004;103:3403-3411.
36. Andrews RK, Harris SJ, McNally T, Berndt MC. Binding of purified 14-3-3 zeta signaling protein to discrete amino acid sequences within the cyto-plasmic domain of the platelet membrane glycoprotein Ib-IX-V complex. Biochemistry. 1998;37:638- 647.
37. Andrews RK, Munday AD, Mitchell CA, Berndt MC. Interaction of cal-modulin with the cytoplasmic domain of the platelet membrane glycopro-tein Ib-IX-V complex. Blood. 2001;98:681- 687.
38. Wu Y, Asazuma N, Satoh K, Yatomi Y, Takafuta T, Berndt MC, Ozaki Y. Interaction between von Willebrand factor and glycoprotein Ib activates Src kinase in human platelets: role of phosphoinositide 3-kinase. Blood. 2003; 101:3469 -3476.
39. Kasirer-Friede A, Moran B, Nagrampa-Orje J, Swanson K, Ruggeri ZM, Schraven B, Neel BG, Koretzky G, Shattil SJ. ADAP is required for normal alphaIIbbeta3 activation by VWF/GP Ib-IX-V and other agonists. Blood. 2007;109:1018 -1025.
40. 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.
41. Massberg S, Gawaz M, Gruner S, Schulte V, Konrad I, Zohlnhofer D, Heinzmann U, Nieswandt B. A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. J Exp Med. 2003;197:41- 49.
42. Bergmeier W, Piffath CL, Goerge T, Cifuni SM, Ruggeri ZM, Ware J, Wagner DD. The role of platelet adhesion receptor GPIbalpha far exceeds that of its main ligand, von Willebrand factor, in arterial thrombosis. Proc Natl Acad Sci U S A. 2006;103:16900 -16905.
43. Kleinschnitz C, Pozgajova M, Pham M, Bendszus M, Nieswandt B, Stoll G. Targeting platelets in acute experimental stroke: impact of glycoprotein Ib, VI, and IIb/IIIa blockade on infarct size, functional outcome, and intra-cranial bleeding. Circulation. 2007;115:2323-2330.
44. Bergmeier W, Piffath CL, Cheng G, Dole VS, Zhang Y, von Andrian UH, Wagner DD. Tumor necrosis factor-alpha-converting enzyme (ADAM17) mediates GPIbalpha shedding from platelets in vitro and in vivo. Circ Res. 2004;95:677- 683.
45. Vanhoorelbeke K, Ulrichts H, Van de WG, Fontayne A, Deckmyn H. Inhibition of platelet glycoprotein Ib and its antithrombotic potential. Curr Pharm Des. 2007;13:2684-2697.
46. Morton LF, Hargreaves PG, Farndale RW, Young RD, Barnes MJ. Integrin alpha 2 beta 1-independent activation of platelets by simple collagen-like peptides: collagen tertiary (triple-helical) and quaternary (polymeric) structures are sufficient alone for alpha 2 beta 1-independent platelet reactivity. Biochem J. 1995;306(Pt 2):337-344.
47. Kehrel B, Wierwille S, Clemetson KJ, Anders O, Steiner M, Knight CG, Farndale RW, Okuma M, Barnes MJ. Glycoprotein VI is a major collagen receptor for platelet activation: it recognizes the platelet-activating quaternary structure of collagen, whereas CD36, glycoprotein IIb/IIIa, and von Willebrand factor do not. Blood. 1998;91:491-499.
48. Nieswandt B, Watson SP. Platelet-collagen interaction: is GPVI the central receptor? Blood. 2003;102:449 - 461.
49. Farndale RW, Sixma JJ, Barnes MJ, de Groot PG. The role of collagen in thrombosis and hemostasis. J Thromb Haemost. 2004;2:561-573.
50. Nieswandt B, Brakebusch C, Bergmeier W, Schulte V, Bouvard D, Mokhtari-Nejad R, Lindhout T, Heemskerk JW, Zirngibl H, Fassler R. Glycoprotein VI but not alpha2beta1 integrin is essential for platelet interaction with collagen. EMBO J. 2001;20:2120 -2130.
51. Clemetson JM, Polgar J, Magnenat E, Wells TN, Clemetson KJ. The platelet collagen receptor glycoprotein VI is a member of the immuno-globulin superfamily closely related to FcalphaR and the natural killer receptors. J Biol Chem. 1999;274:29019 -29024.
52. Tsuji M, Ezumi Y, Arai M, Takayama H. A novel association of Fc receptor gamma-chain with glycoprotein VI and their co-expression as a collagen receptor in human platelets. J Biol Chem. 1997;272:23528-23531.
53. Watson SP, Gibbins J. Collagen receptor signalling in platelets: extending the role of the ITAM. Immunol Today. 1998;19:260 -264.
54. Ezumi Y, Shindoh K, Tsuji M, Takayama H. Physical and functional association of the Src family kinases Fyn and Lyn with the collagen receptor glycoprotein VI-Fc receptor gamma chain complex on human platelets. J Exp Med. 1998;188:267-276.
55. Briddon SJ, Watson SP. Evidence for the involvement of p59fyn and p53/56lyn in collagen receptor signalling in human platelets. Biochem J. 1999;338(Pt 1):203-209.
56. Watson SP, Auger JM, McCarty OJ, Pearce AC. GPVI and integrin alphaIIb beta3 signaling in platelets. J Thromb Haemost. 2005;3:1752-1762.
57. Grosse J, Braun A, Varga-Szabo D, Beyersdorf N, Schneider B, Zeitlmann L, Hanke P, Schropp P, Muhlstedt S, Zorn C, Huber M, Schmittwolf C, Jagla W, Yu P, Kerkau T, Schulze H, Nehls M, Nieswandt B. An EF hand mutation in Stim1 causes premature platelet activation and bleeding in mice. J Clin Invest. 2007;117:3540 -3550.
58. Pasquet JM, Quek L, Pasquet S, Poole A, Matthews JR, Lowell C, Watson SP. Evidence of a role for SHP-1 in platelet activation by the collagen receptor glycoprotein VI. J Biol Chem. 2000;275:28526 -28531.
59. Newman PJ, Newman DK. Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler Thromb Vasc Biol. 2003;23:953-964.
60. Dhanjal TS, Ross EA, Auger JM, McCarty OJ, Hughes CE, Senis YA, Buckley CD, Watson SP. Minimal regulation of platelet activity by PECAM-1. Platelets. 2007;18:56 - 67.
61. Wee JL, Jackson DE. The Ig-ITIM superfamily member PECAM-1 regulates the "outside-in" signaling properties of integrin alpha(IIb)beta3 in platelets. Blood. 2005;106:3816 -3823.
62. Moroi M, Jung SM, Okuma M, Shinmyozu K. A patient with platelets deficient in glycoprotein VI that lack both collagen-induced aggregation and adhesion. J Clin Invest. 1989;84:1440 -1445.
63. Boylan B, Chen H, Rathore V, Paddock C, Salacz M, Friedman KD, Curtis BR, Stapleton M, Newman DK, Kahn ML, Newman PJ. Anti-GPVI-associated ITP: an acquired platelet disorder caused by autoantibody-mediated clearance of the GPVI/FcRgamma-chain complex from the human platelet surface. Blood. 2004;104:1350 -1355.
64. Nieswandt B, Schulte V, Bergmeier W, Mokhtari-Nejad R, Rackebrandt K, Cazenave JP, Ohlmann P, Gachet C, Zirngibl H. Long-term Antithrombotic Protection by In Vivo Depletion of Platelet Glycoprotein VI in Mice. J Exp Med. 2001;193:459 -470.
65. Kato K, Kanaji T, Russell S, Kunicki TJ, Furihata K, Kanaji S, Marchese P, Reininger A, Ruggeri ZM, Ware J. The contribution of glycoprotein VI to stable platelet adhesion and thrombus formation illustrated by targeted gene deletion. Blood. 2003;102:1701-1707.
66. Lockyer S, Okuyama K, Begum S, Le S, Sun B, Watanabe T, Matsumoto Y, Yoshitake M, Kambayashi J, Tandon NN. GPVI-deficient mice lack collagen responses and are protected against experimentally induced pulmonary thromboembolism. Thromb Res. 2006;118:371-380.
67. Konishi H, Katoh Y, Takaya N, Kashiwakura Y, Itoh S, Ra C, Daida H. Platelets activated by collagen through immunoreceptor tyrosine-based activation motif play pivotal role in initiation and generation of neointimal hyperplasia after vascular injury. Circulation. 2002;105:912-916.
68. Konstantinides S, Ware J, Marchese P, Almus-Jacobs F, Loskutoff DJ, Ruggeri ZM. Distinct antithrombotic consequences of platelet glycoprotein Ibalpha and VI deficiency in a mouse model of arterial thrombosis. J Thromb Haemost. 2006;4:2014 -2021.
69. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002;110:673- 687.
70. Shattil SJ, Kashiwagi H, Pampori N. Integrin signaling: the platelet paradigm. Blood. 1998;91:2645-2657.
71. Santoro SA. Identification of a 160,000 dalton platelet membrane protein that mediates the initial divalent cation-dependent adhesion of platelets to collagen. Cell. 1986;46:913-920.
72. Nieuwenhuis HK, Akkerman JW, Houdijk WP, Sixma JJ. Human blood platelets showing no response to collagen fail to express surface glycopro-tein Ia. Nature. 1985;318:470 - 472.
73. Kehrel B, Balleisen L, Kokott R, Mesters R, Stenzinger W, Clemetson KJ, van de Loo J. Deficiency of intact thrombospondin and membrane glyco-protein Ia in platelets with defective collagen-induced aggregation and spontaneous loss of disorder. Blood. 1988;71:1074 -1078.
74. Holtkotter O, Nieswandt B, Smyth N, Muller W, Hafner M, Schulte V, Krieg T, Eckes B. Integrin alpha 2-deficient mice develop normally, are fertile, but display partially defective platelet interaction with collagen. J Biol Chem. 2002;277:10789 -10794.
75. Chen J, Diacovo TG, Grenache DG, Santoro SA, Zutter MM. The alpha(2) integrin subunit-deficient mouse: a multifaceted phenotype including defects of branching morphogenesis and hemostasis. Am J Pathol. 2002;161:337-344.
76. Gruner S, Prostredna M, Schulte V, Krieg T, Eckes B, Brakebusch C, Nieswandt B. Multiple integrin-ligand interactions synergize in shear-resistant platelet adhesion at sites of arterial injury in vivo. Blood. 2003;102:4021- 4027.
77. Takada Y, Elices MJ, Crouse C, Hemler ME. The primary structure of the alpha 4 subunit of VLA-4: homology to other integrins and a possible cell-cell adhesion function. EMBO J. 1989;8:1361-1368.
78. Emsley J, King SL, Bergelson JM, Liddington RC. Crystal structure of the I domain from integrin alpha2beta1. J Biol Chem. 1997;272:28512-28517.
79. Emsley J, Knight CG, Farndale RW, Barnes MJ, Liddington RC. Structural basis of collagen recognition by integrin alpha2beta1. Cell. 2000;101:47-56.
80. Smith C, Estavillo D, Emsley J, Bankston LA, Liddington RC, Cruz MA. Mapping the collagen-binding site in the I domain of the glycoprotein Ia/IIa (integrin alpha(2)beta(1)). J Biol Chem. 2000;275:4205- 4209.
81. Santoro SA, Walsh JJ, Staatz WD, Baranski KJ. Distinct determinants on collagen support alpha 2 beta 1 integrin-mediated platelet adhesion and platelet activation. Cell Regul. 1991;2:905-913.
82. Jung SM, Moroi M. Signal-transducing mechanisms involved in activation of the platelet collagen receptor integrin alpha(2)beta(1). J Biol Chem. 2000;275:8016 - 8026.
83. Jung SM, Moroi M. Platelet collagen receptor integrin alpha2beta1 activation involves differential participation of ADP-receptor subtypes P2Y1 and P2Y12 but not intracellular calcium change. Eur J Biochem. 2001;268:3513-3522.
84. Van de Walle GR, Vanhoorelbeke K, Majer Z, Illyes E, Baert J, Pareyn I, Deckmyn H. Two functional active conformations of the integrin {alpha}2{beta}1, depending on activation condition and cell type. J Biol Chem. 2005;280:36873-36882.
85. Van de Walle GR, Schoolmeester A, Iserbyt BF, Cosemans JM, Heemskerk JW, Hoylaerts MF, Nurden A, Vanhoorelbeke K, Deckmyn H. Activation of alphaIIbbeta3 is a sufficient but also an imperative prerequisite for activation of alpha2beta1 on platelets. Blood. 2007;109:595-602.
86. Inoue O, Suzuki-Inoue K, Dean WL, Frampton J, Watson SP. Integrin {alpha}2{beta}1 mediates outside-in regulation of platelet spreading on collagen through activation of Src kinases and PLC{gamma}2. J Cell Biol. 2003;160:769 -780.
87. Chen H, Kahn ML. Reciprocal signaling by integrin and nonintegrin receptors during collagen activation of platelets. Mol Cell Biol. 2003;23:4764 - 4777.
88. Siljander PR, Munnix IC, Smethurst PA, Deckmyn H, Lindhout T, Ouwehand WH, Farndale RW, Heemskerk JW. Platelet receptor interplay regulates collagen-induced thrombus formation in flowing human blood. Blood. 2004;103:1333-1341.
89. He L, Pappan LK, Grenache DG, Li Z, Tollefsen DM, Santoro SA, Zutter MM. The contributions of the {alpha}2{beta}1 integrin to vascular thrombosis in vivo. Blood. 2003;102:3652-3657.
90. Ruggeri ZM. Platelets in atherothrombosis. Nat Med. 2002;8:1227-1234.
91. Nurden AT. Glanzmann thrombasthenia. Orphanet J Rare Dis. 2006;1:10.
92. Hodivala-Dilke KM, McHugh KP, Tsakiris DA, Rayburn H, Crowley D, Ullman-Cullere M, Ross FP, Coller BS, Teitelbaum S, Hynes RO. Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J Clin Invest. 1999;103:229-238.
93. Ni H, Denis CV, Subbarao S, Degen JL, Sato TN, Hynes RO, Wagner DD. Persistence of platelet thrombus formation in arterioles of mice lacking both von Willebrand factor and fibrinogen. J Clin Invest. 2000;106:385-392.
94. Xiong JP, Stehle T, Diefenbach B, Zhang R, Dunker R, Scott DL, Joachimiak A, Goodman SL, Arnaout MA. Crystal structure of the extracellular segment of integrin alpha Vbeta3. Science. 2001;294:339 -345.
95. Xiong JP, Stehle T, Zhang R, Joachimiak A, Frech M, Goodman SL, Arnaout MA. Crystal structure of the extracellular segment of integrin alpha Vbeta3 in complex with an Arg-Gly-Asp ligand. Science. 2002;296:151-155.
96. Adair BD, Yeager M. Three-dimensional model of the human platelet integrin alpha IIbbeta 3 based on electron cryomicroscopy and x-ray crystallography. Proc Natl Acad Sci U S A. 2002;99:14059 -14064.
97. Carrell NA, Fitzgerald LA, Steiner B, Erickson HP, Phillips DR. Structure of human platelet membrane glycoproteins IIb and IIIa as determined by electron microscopy. J Biol Chem. 1985;260:1743-1749.
98. Weisel JW, Nagaswami C, Vilaire G, Bennett JS. Examination of the platelet membrane glycoprotein IIb-IIIa complex and its interaction with fibrinogen and other ligands by electron microscopy. J Biol Chem. 1992; 267:16637-16643.
99. Smith JW, Piotrowicz RS, Mathis D. A mechanism for divalent cation regulation of beta 3-integrins. J Biol Chem. 1994;269:960 -967.
100. Ginsberg MH, Partridge A, Shattil SJ. Integrin regulation. Curr Opin Cell Biol. 2005;17:509 -516.
101. Hughes PE, Diaz-Gonzalez F, Leong L, Wu C, McDonald JA, Shattil SJ, Ginsberg MH. Breaking the integrin hinge. A defined structural constraint regulates integrin signaling. J Biol Chem. 1996;271:6571- 6574.
102. Peterson JA, Visentin GP, Newman PJ, Aster RH. A recombinant soluble form of the integrin alpha IIb beta 3 (GPIIb-IIIa) assumes an active, ligand-binding conformation and is recognized by GPIIb-IIIa-specific monoclonal, allo-, auto-, and drug-dependent platelet antibodies. Blood. 1998;92:2053-2063.
103. Calderwood DA, Zent R, Grant R, Rees DJ, Hynes RO, Ginsberg MH. The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J Biol Chem. 1999;274:28071-28074.
104. Tadokoro S, Shattil SJ, Eto K, Tai V, Liddington RC, de Pereda JM, Ginsberg MH, Calderwood DA. Talin binding to integrin beta tails: a final common step in integrin activation. Science. 2003;302:103-106.
105. Nieswandt B, Moser M, Pleines I, Varga-Szabo D, Monkley S, Critchley D, Fassler R. Loss of talin 1 in platelets abrogates integrin activation, platelet aggregration, and thrombus formation in vitro and in vivo. J Exp Med. 2007;204:3113-3118.
106. Petrich BG, Fogelstrand P, Partridge AW, Yousefi N, Ablooglu AJ, Shattil SJ, Ginsberg MH. The antithrombotic potential of selective blockade of talin-dependent integrin alpha(IIb)beta(3) (platelet GPIIb-IIIa) activation. J Clin Invest. 2007;117:2250 -2259.
107. Larkin D, Murphy D, Reilly DF, Cahill M, Sattler E, Harriott P, Cahill DJ, Moran N. ICln, a novel integrin alphaIIbbeta3-associated protein, functionally regulates platelet activation. J Biol Chem. 2004;279:27286 -27293.
108. Naik UP, Patel PM, Parise LV. Identification of a novel calcium-binding protein that interacts with the integrin alphaIIb cytoplasmic domain. J Biol Chem. 1997;272:4651-4654.
109. Vijayan KV, Liu Y, Li TT, Bray PF. Protein phosphatase 1 associates with the integrin alphaIIb subunit and regulates signaling. J Biol Chem. 2004; 279:33039 -33042.
110. Arias-Salgado EG, Lizano S, Sarkar S, Brugge JS, Ginsberg MH, Shattil SJ. Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proc Natl Acad Sci U S A. 2003;100:13298 -13302.
111. Wonerow P, Pearce AC, Vaux DJ, Watson SP. A critical role for phospho-lipase Cgamma2 in alphaIIbbeta3-mediated platelet spreading. J Biol Chem. 2003;278:37520 -37529.
112. Quinn MJ, Byzova TV, Qin J, Topol EJ, Plow EF. Integrin alphaIIbbeta3 and its antagonism. Arterioscler Thromb Vasc Biol. 2003;23:945-952.
113. Suzuki S, Argraves WS, Pytela R, Arai H, Krusius T, Pierschbacher MD, Ruoslahti E. cDNA and amino acid sequences of the cell adhesion protein receptor recognizing vitronectin reveal a transmembrane domain and homologies with other adhesion protein receptors. Proc Natl Acad Sci U S A. 1986;83:8614 -8618.
114. Kamata T, Handa M, Sato Y, Ikeda Y, Aiso S. Membrane-proximal {alpha}/{beta} stalk interactions differentially regulate integrin activation. J Biol Chem. 2005;280:24775-24783.
115. Sonnenberg A, Modderman PW, Hogervorst F. Laminin receptor on platelets is the integrin VLA-6. Nature. 1988;336:487-489.
116. Inoue O, Suzuki-Inoue K, McCarty OJ, Moroi M, Ruggeri ZM, Kunicki TJ, Ozaki Y, Watson SP. Laminin stimulates spreading of platelets through integrin alpha6beta1-dependent activation of GPVI. Blood. 2006;107:1405-1412.