New insights into the haemostatic function of platelets

British Journal of Haematology

Volumn 147, Issue 4, 2009, Pages 415-430

  Wei, Andrew H ^a,b   Schoenwaelder, Simone M ^a   Andrews, Robert K ^a   Jackson, Shaun P ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b ALFRED HOSPITAL   (Australia)

Author keywords

Bleeding; Function; Inherited; Mouse model; Platelets

Indexed keywords

ADENOSINE DIPHOSPHATE; BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 12; GLYCOPROTEIN IB ALPHA; GLYCOPROTEIN VI; KININOGEN; PADGEM PROTEIN; THROMBIN; THROMBOSPONDIN; THROMBOXANE A2; VERY LATE ACTIVATION ANTIGEN 2; VERY LATE ACTIVATION ANTIGEN 5; VERY LATE ACTIVATION ANTIGEN 6; VON WILLEBRAND FACTOR;

BERNARD SOULIER DISEASE; CALCIUM SIGNALING; CHEDIAK HIGASHI SYNDROME; FRAMESHIFT MUTATION; GENE DELETION; GLANZMANN DISEASE; GREY PLATELET SYNDROME; GRISCELLI SYNDROME; HUMAN; MISSENSE MUTATION; NONHUMAN; OCULAR ALBINISM; PRIORITY JOURNAL; QUEBEC PLATELET DISORDER; REVIEW; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOCYTE DYSFUNCTION; THROMBOCYTE FUNCTION; THROMBOCYTOPENIA; VON WILLEBRAND DISEASE; WISKOTT ALDRICH SYNDROME;

ANIMALS; BLOOD PLATELET DISORDERS; BLOOD PLATELETS; HEMOSTASIS; HUMANS; MICE; PLATELET ADHESIVENESS; PLATELET AGGREGATION; PLATELET STORAGE POOL DEFICIENCY;

EID: 70350435452     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2009.07819.x     Document Type: Review

References (130)

1. Albrecht, C., McVey, J.H., Elliott, J.I., Sardini, A., Kasza, I., Mumford, A.D., Naoumova, R.P., Tuddenham, E.G., Szabo, K. Higgins, C.F. (2005) A novel missense mutation in ABCA1 results in altered protein trafficking and reduced phosphatidylserine translocation in a patient with Scott syndrome. Blood, 106, 542 549.
2. André, P., Delaney, S.M., LaRocca, T., Vincent, D., DeGuzman, F., Jurek, M., Koller, B., Phillips, D.R. Conley, P.B. (2003) P2Y12 regulates platelet adhesion/activation, thrombus growth, and thrombus stability in injured arteries. Journal of Clinical Investigation, 112, 398 406.
3. Andrews, R., Gardiner, E., Shen, Y., Whisstock, J. Berndt, M. (2003) Glycoprotein Ib-IX-V. International Journal of Biochemistry and Cell Biology, 35, 1170 1174.
4. Arai, M., Yamamoto, N., Moroi, M., Akamatsu, N., Fukutake, K. Tanoue, K. (1995) Platelets with 10 percent of the normal amount of glycoprotein VI have an impaired response to collagen that results in a mild bleeding tendency. British Journal of Haematology, 89, 124 130.
5. Barbosa, M., Nguyen, Q., Tchernev, V., Ashley, J., Detter, J., Blaydes, S., Brandt, S., Chotai, D., Hodgman, C. Solari, R. (1996) Identification of the homologous beige and Chediak-Higashi syndrome genes. Nature, 382, 262 265.
6. Beguin, S., Keularts, I., Al Dieri, R., Bellucci, S., Caen, J. Hemker, H. (2004) Fibrin polymerization is crucial for thrombin generation in platelet-rich plasma in a VWF-GPIb-dependent process, defective in Bernard-Soulier syndrome. Journal of Thrombosis and Haemostasis, 2, 170 176.
7. Bergmeier, W., Piffath, C., Goerge, T., Cifuni, S., Ruggeri, Z., Ware, J. Wagner, D. (2006) The role of platelet adhesion receptor GPIbα far exceeds that of its main ligand, von Willebrand factor, in arterial thrombosis. Proceedings of the National Academy of Sciences of the United States of America, 103, 16900 16905.
8. Bergmeier, W., Goerge, T., Wang, H., Crittenden, J.R., Baldwin, A.C.W., Cifuni, S.M., Housman, D.E., Graybiel, A.M. Wagner, D.D. (2007) Mice lacking the signaling molecule CalDAG-GEFI represent a model for leukocyte adhesion deficiency type III. Journal of Clinical Investigation, 117, 1699 1707.
9. Bergmeier, W., Oh-hora, M., McCarl, C.-A., Roden, R.C., Bray, P.F. Feske, S. (2009) R93W mutation in Orai1 causes impaired calcium influx in platelets. Blood, 113, 675 678.
10. Bizzozero, G. (1882) Ueber einen neuen Forrnbestandteil des blutes und dessen rolle bei der thrombose und blut gerinnung (On a new blood particle and its role in thrombosis and blood coagulation). Virchows Archiv für pathologische Anatomie und Physiologie und für klinische Medizin, 90, 261 332.
11. Blake, R.A., Schieven, G.L. Watson, S.P. (1994) Collagen stimulates tyrosine phosphorylation of phospholipase C-gamma 2 but not phospholipase C-gamma 1 in human platelets. FEBS Letters, 353, 212 216.
12. Born, G.V.R. (1962) Aggregation of blood platelets by adenosine diphosphate and its reversal. Nature, 194, 927 929.
13. Boylan, B., Chen, H., Rathore, V., Paddock, C., Salacz, M., Friedman, K., Curtis, B., Stapleton, M., Newman, D. Kahn, M. (2004) Anti-GPVI-associated ITP: an acquired platelet disorder caused by autoantibody-mediated clearance of the GPVI/FcR gamma-chain complex from the human platelet surface. Blood, 104, 1350 1355.
14. Braun, A., Varga-Szabo, D., Kleinschnitz, C., Pleines, I., Bender, M., Austinat, M., Bosl, M., Stoll, G. Nieswandt, B. (2009) Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation. Blood, 113, 2056 2063.
15. Cheli, Y., Jensen, D., Marchese, P., Habart, D., Wiltshire, T., Cooke, M., Fernandez, J., Ware, J., Ruggeri, Z. Kunicki, T. (2007) The Modifier of Hemostasis (MH) locus on chromosome 4 controls in vivo hemostasis of Gp6-/- mice. Blood, 111, 1266 1273.
16. Chintala, S., Tan, J., Gautam, R., Rusiniak, M., Guo, X., Li, W., Gahl, W., Huizing, M., Spritz, R. Hutton, S. (2007) The Slc35d3 gene, encoding an orphan nucleotide sugar transporter, regulates platelet-dense granules. Blood, 109, 1533 1540.
17. Cho, M.J., Pestina, T.I., Steward, S.A., Lowell, C.A., Jackson, C.W. Gartner, T.K. (2002) Role of the Src family kinase Lyn in TxA2 production, adenosine diphosphate secretion, Akt phosphorylation, and irreversible aggregation in platelets stimulated with gamma-thrombin. Blood, 99, 2442 2447.
18. Chrzanowska-Wodnicka, M., Smyth, S.S., Schoenwaelder, S.M., Fischer, T.H. White, G.C. (2005) Rap1b is required for normal platelet function and hemostasis in mice. Journal of Clinical Investigation, 115, 680 687.
19. Coughlin, S. (2005) Protease-activated receptors in hemostasis, thrombosis and vascular biology. Journal of Thrombosis and Haemostasis, 3, 1800 1814.
20. Crittenden, J., Bergmeier, W., Zhang, Y., Piffath, C., Liang, Y., Wagner, D., Housman, D. Graybiel, A. (2004) CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nature Medicine, 10, 982 986. (Pubitemid 39273740)
21. Daly, M., Dawood, B., Lester, W., Peake, I., Rodeghiero, F., Goodeve, A., Makris, M., Wilde, J., Mumford, A. Watson, S. (2009) Identification and characterisation of a novel P2Y12 variant in a patient diagnosed with type 1 von Willebrand disease in the European MCMDM-1VWD study. Blood, 113, 4110 4113.
22. Denis, C.V. Wagner, D.D. (2007) Platelet adhesion receptors and their ligands in mouse models of thrombosis. Arteriosclerosis, Thrombosis, and Vascular Biology, 27, 728 739.
23. Denis, C., Methia, N., Frenette, P.S., Rayburn, H., Ullman-Cullere, M., Hynes, R.O. Wagner, D.D. (1998) A mouse model of severe von Willebrand disease: defects in hemostasis and thrombosis. Proceedings of the National Academy of Sciences of the United States of America, 95, 9524 9529.
24. Derry, J., Ochs, H. Francke, U. (1994) Isolation of a novel gene mutated in Wiskott-Aldrich syndrome Published erratum appears in 1994 Cell 79: following 922 Cell, 78, 635 644.
25. Diamandis, M., Paterson, A.D., Rommens, J.M., Veljkovic, D.K., Blavignac, J., Bulman, D.E., Waye, J.S., Derome, F., Rivard, G.E. Hayward, C.P.M. (2009) Quebec platelet disorder is linked to the urokinase plasminogen activator gene (PLAU) and increases expression of the linked allele in megakaryocytes. Blood, 113, 1543 1546.
26. Dong, F., Li, S., Pujol-Moix, N., Luban, N., Shin, S., Seo, J., Ruiz-Saez, A., Demeter, J., Langdon, S. Kelley, M. (2005) Genotype-phenotype correlation in MYH9-related thrombocytopenia. British Journal of Haematology, 130, 620 627.
27. Dunkley, S., Arthur, J.F., Evans, S., Gardiner, E.E., Shen, Y. Andrews, R.K. (2007) A familial platelet function disorder associated with abnormal signalling through the glycoprotein VI pathway. British Journal of Haematology, 137, 569 577.
28. Enayat, M., Guilliatt, A., Lester, W., Wilde, J., Williams, M. Hill, F. (2006) Distinguishing between type 2B and pseudo-von Willebrand disease and its clinical importance. British Journal of Haematology, 133, 664 666.
29. Fabre, J.E., Nguyen, M.T., Latour, A., Keifer, J.A., Audoly, L.P., Coffman, T.M. Koller, B.H. (1999) Decreased platelet aggregation, increased bleeding time and resistance to thromboembolism in P2Y1-deficient mice. Nature Medicine, 5, 1199 1202.
30. Falati, S., Gross, P., Merrill-Skoloff, G., Furie, B.C. Furie, B. (2002) Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nature Medicine, 8, 1175 1181.
31. Feng, S., Resendiz, J., Lu, X. Kroll, M. (2003) Filamin A binding to the cytoplasmic tail of glycoprotein Ibα regulates von Willebrand factor-induced platelet activation. Blood, 102, 2122 2129.
32. Fontana, G., Ware, J. Cattaneo, M. (2009) Haploinsufficiency of the platelet P2Y12 gene in a family with congenital bleeding diathesis. Haematologica, 94, 581 584.
33. Foster, C.J., Prosser, D.M., Agans, J.M., Zhai, Y., Smith, M.D., Lachowicz, J.E., Zhang, F.L., Gustafson, E., Monsma, Jr., F.J. Wiekowski, M.T. (2001) Molecular identification and characterization of the platelet ADP receptor targeted by thienopyridine antithrombotic drugs. Journal of Clinical Investigation, 107, 1591 1598.
34. Gabbeta, J., Yang, X., Kowalska, M.A., Sun, L., Dhanasekaran, N. Rao, A.K. (1997) Platelet signal transduction defect with Gα subunit dysfunction and diminished Gaq in a patient with abnormal platelet responses. Proceedings of the National Academy of Sciences of the United States of America, 94, 8750 8755.
35. q gene expression in platelets but not neutrophils. Thrombosis and Haemostasis, 87, 129 133.
36. Gahl, W.A., Brantly, M., Kaiser-Kupfer, M.I., Iwata, F., Hazelwood, S., Shotelersuk, V., Duffy, L.F., Kuehl, E.M., Troendle, J. Bernardini, I. (1998) Genetic defects and clinical characteristics of patients with a form of oculocutaneous albinism (Hermansky-Pudlak Syndrome). New England Journal of Medicine, 338, 1258 1265.
37. Gissen, P., Johnson, C., Morgan, N., Stapelbroek, J., Forshew, T., Cooper, W., McKiernan, P., Klomp, L., Morris, A. Wraith, J. (2004) Mutations in VPS33B, encoding a regulator of SNARE-dependent membrane fusion, cause arthrogryposis-renal dysfunction-cholestasis (ARC) syndrome. Nature Genetics, 36, 400 404.
38. Gunay-Aygun, M., Huizing, M. Gahl, W. (2004) Molecular defects that affect platelet dense granules. Seminars in Thrombosis and Hemostasis, 30, 537 547.
39. Hallberg, L., Hogdahl, A., Nilsson, L. Rybo, G. (1966) Menstrual blood loss - a population study. Variation at different ages and attempts to define normality. Acta Obstetricia et Gynecologica Scandinavica, 45, 320 351.
40. Hamilton, J., Cornelissen, I. Coughlin, S. (2004) Impaired hemostasis and protection against thrombosis in protease-activated receptor 4-deficient mice is due to lack of thrombin signaling in platelets. Journal of Thrombosis and Haemostasis, 2, 1429 1435.
41. Heath, K., Campos-Barros, A., Toren, A., Rozenfeld-Granot, G., Carlsson, L., Savige, J., Denison, J., Gregory, M., White, J. Barker, D. (2001) Nonmuscle myosin heavy chain IIA mutations define a spectrum of autosomal dominant macrothrombocytopenias: May-Hegglin anomaly and Fechtner, Sebastian, Epstein, and Alport-like syndromes. American Journal of Human Genetics, 69, 1033 1045.
42. Higuchi, W., Fuse, I., Hattori, A. Aizawa, Y. (1999) Mutations of the platelet Thromboxane A2 (TXA2) receptor in patients characterized by the absence of TXA2-induced platelet aggregation despite normal TXA2 binding activity. Thrombosis and Haemostasis, 82, 1528 1531.
43. Hirata, T., Kakizuka, A., Ushikubi, F., Fuse, I., Okuma, M. Narumiya, S. (1994) Arg60 to Leu mutation of the human thromboxane A2 receptor in a dominantly inherited bleeding disorder. Journal of Clinical Investigation, 94, 1662 1667.
44. Hodivala-Dilke, K.M., McHugh, K.P., Tsakiris, D.A., Rayburn, H., Crowley, D., Ullman-Culleré, M., Ross, F.P., Coller, B.S., Teitelbaum, S. Hynes, R.O. (1999) ß3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. Journal of Clinical Investigation, 103, 229 238.
45. Hollopeter, G., Jantzen, N.M., Vincent, D., Li, G., England, L., Ramakrishnan, V., Yang, R.B., Nurden, P., Nurden, A. Jullus, D. (2001) Identification of the platelet ADP receptor targeted by antithrombotic drugs. Nature (London), 409, 202 207. (Pubitemid 32144286)
46. Holtkotter, O., Nieswandt, B., Smyth, N., Muller, W., Hafner, M., Schulte, V., Krieg, T. Eckes, B. (2002) Integrin α2-deficient mice develop normally, are fertile, but display partially defective platelet interaction with collagen. Journal of Biological Chemistry, 277, 10789 10794.
47. Jackson, S. (2007) The growing complexity of platelet aggregation. Blood, 109, 5087.
48. Jain, S., Zuka, M., Liu, J., Russell, S., Dent, J., Guerrero, J., Forsyth, J., Maruszak, B., Gartner, T., Felding-Habermann, B. Ware, J. (2007) Platelet glycoprotein Ibα supports experimental lung metastasis. Proceedings of the National Academy of Sciences of the United States of America, 104, 9024 9028.
49. James, A.H. (2007) More than menorrhagia: a review of the obstetric and gynaecological manifestations of von Willebrand disease. Thrombosis Research, 120 (Suppl. 1 S17 S20.
50. Jandrot-Perrus, M., Dumont, B., Lasne, D., Rothschild, R., Grandchamp, B. Ajzenberg, N. (2008) Absent collagen-induced platelet activation in a patient double heterozygous for two GPVI mutations. Blood (ASH Annual Meeting Abstracts), 112, Abstract 88.
51. Jung, J., Bohn, G., Allroth, A., Boztug, K., Brandes, G., Sandrock, I., Schaffer, A., Rathinam, C., Kollner, I. Beger, C. (2006) Identification of a homozygous deletion in the AP3B1 gene causing Hermansky-Pudlak syndrome, type 2. Blood, 108, 362 369.
52. Kahn, M., Diacovo, T., Bainton, D., Lanza, F., Trejo, J. Coughlin, S. (1999) Glycoprotein V-deficient platelets have undiminished thrombin responsiveness and do not exhibit a Bernard-Soulier phenotype. Blood, 94, 4112 4121.
53. Kanaji, T., Russell, S. Ware, J. (2002) Amelioration of the macrothrombocytopenia associated with the murine Bernard-Soulier syndrome. Blood, 100, 2102 2107.
54. Kato, K., Kanaji, T., Russell, S., Kunicki, T.J., Furihata, K., Kanaji, S., Marchese, P., Reininger, A., Ruggeri, Z.M. Ware, J. (2003) The contribution of glycoprotein VI to stable platelet adhesion and thrombus formation illustrated by targeted gene deletion. Blood, 102, 1701 1707.
55. Kato, K., Martinez, C., Russell, S., Nurden, P., Nurden, A., Fiering, S. Ware, J. (2004) Genetic deletion of mouse platelet glycoprotein Ibß produces a Bernard-Soulier phenotype with increased a-granule size. Blood, 104, 2339 2344.
56. Kojima, H., Moroi, M., Jung, S., Goto, S., Tamura, N., Kozuma, Y., Suzukawa, K. Nagasawa, T. (2006) Characterization of a patient with glycoprotein (GP) VI deficiency possessing neither anti-GPVI autoantibody nor genetic aberration. Journal of Thrombosis and Haemostasis, 4, 2433 2442.
57. Kujovich, J.L. (2005) von Willebrand's disease and menorrhagia: prevalence, diagnosis, and management. American Journal of Hematology, 79, 220 228.
58. Kulkarni, S., Dopheide, S.M., Yap, C.L., Ravanat, C., Freund, M., Mangin, P., Heel, K.A., Street, A., Harper, I.S., Lanza, F. Jackson, S.P. (2000) A revised model of platelet aggregation. Journal of Clinical Investigation, 105, 783 791.
59. Langenbach, R., Morham, S.G., Tiano, H.F., Loftin, C.D., Ghanayem, B.I., Chulada, P.C., Mahler, J.F., Lee, C.A., Goulding, E.H. Kluckman, K.D. (1995) Prostaglandin synthase 1 gene disruption in mice reduces arachidonic acid-induced inflammation and indomethacin-induced gastric ulceration. Cell, 83, 483 492.
60. Law, D., Nannizzi-Alaimo, L., Ministri, K., Hughes, P., Forsyth, J., Turner, M., Shattil, S., Ginsberg, M., Tybulewicz, V. Phillips, D. (1999) Genetic and pharmacological analyses of syk function in alpha IIbbeta 3 signaling in platelets. Blood, 93, 2645 2652.
61. Lee, N.C., Dicker, R.C., Rubin, G.L. Ory, H.W. (1984) Confirmation of the preoperative diagnoses for hysterectomy. American Journal of Obstetrics and Gynecology, 150, 283 287.
62. Lee, S.B., Rao, A.K., Lee, K.H., Yang, X., Bae, Y.S. Rhee, S.G. (1996) Decreased expression of phospholipase C-beta 2 isozyme in human platelets with impaired function. Blood, 88, 1684 1691.
63. Leon, C., Eckly, A., Hechler, B., Aleil, B., Freund, M., Ravanat, C., Jourdain, M., Nonne, C., Weber, J. Tiedt, R. (2007) Megakaryocyte-restricted MYH9 inactivation dramatically affects hemostasis while preserving platelet aggregation and secretion. Blood, 110, 3183 3191.
64. Léon, C., Hechler, B., Freund, M., Eckly, A., Vial, C., Ohlmann, P., Dierich, A., LeMeur, M., Cazenave, J. Gachet, C. (1999) Defective platelet aggregation and increased resistance to thrombosis in purinergic P2Y1 receptor-null mice. Journal of Clinical Investigation, 104, 1731 1737.
65. Lian, L., Wang, Y., Draznin, J., Eslin, D., Bennett, J., Poncz, M., Wu, D. Abrams, C. (2005) The relative role of PLCß and PI3Kγ in platelet activation. Blood, 106, 110 117.
66. Liu, Z., Doan, Q., Blumenthal, P. Dubois, R. (2007) A systematic review evaluating health-related quality of life, work impairment, and health-care costs and utilization in abnormal uterine bleeding. Value in Health, 10, 183 194.
67. Malinin, N., Zhang, L., Choi, J., Ciocea, A., Razorenova, O., Ma, Y., Podrez, E., Tosi, M., Lennon, D. Caplan, A. (2009) A point mutation in KINDLIN3 ablates activation of three integrin subfamilies in humans. Nature Medicine, 15, 313 318.
68. Mangin, P., Nonne, C., Eckly, A., Ohlmann, P., Freund, M., Nieswandt, B., Cazenave, J., Gachet, C. Lanza, F. (2003) A PLCγ2-independent platelet collagen aggregation requiring functional association of GPVI and integrin a2ß1. FEBS Letters, 542, 53 59.
69. Mangin, P., Yap, C., Nonne, C., Sturgeon, S., Goncalves, I., Yuan, Y., Schoenwaelder, S., Wright, C., Lanza, F. Jackson, S. (2006) Thrombin overcomes the thrombosis defect associated with platelet GPVI/FcR gamma deficiency. Blood, 107, 4346 4353.
70. Massberg, S., Gawaz, M., Gruner, S., Schulte, V., Konrad, I., Zohlnhofer, D., Heinzmann, U. Nieswandt, B. (2003) A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. Journal of Experimental Medicine, 197, 41 49.
71. Matijevic-Aleksic, N., McPhedran, P. Wu, K.K. (1996) Bleeding disorder due to platelet prostaglandin H synthase-1 (PGHS-1) deficiency. British Journal of Haematology, 92, 212 217.
72. Maurer-Spurej, E., Kahr, W.H., Carter, C.J., Pittendreigh, C., Cameron, M. Cyr, T.D. (2008) The value of proteomics for the diagnosis of a platelet-related bleeding disorder. Platelets, 19, 342 351.
73. Miller, J. Castella, A. (1982) Platelet-type von Willebrand's disease: characterization of a new bleeding disorder. Blood, 60, 790 794.
74. Moebius, J., Zahedi, R.P., Lewandrowski, U., Berger, C., Walter, U. Sickmann, A. (2005) The human platelet membrane proteome reveals several new potential membrane proteins. Molecular and Cellular Proteomics, 4, 1754 1761.
75. Moroi, M., Jung, S., Okuma, M. Shinmyozu, K. (1989) A patient with platelets deficient in glycoprotein VI that lack both collagen-induced aggregation and adhesion. Journal of Clinical Investigation, 84, 1440 1445.
76. Moser, M., Nieswandt, B., Ussar, S., Pozgajova, M. Fässler, R. (2008) Kindlin-3 is essential for integrin activation and platelet aggregation. Nature Medicine, 14, 325 330.
77. Moser, M., Bauer, M., Schmid, S., Ruppert, R., Schmidt, S., Sixt, M., Wang, H.V., Sperandio, M. Fässler, R. (2009) Kindlin-3 is required for ß2 integrin-mediated leukocyte adhesion to endothelial cells. Nature Medicine, 15, 300 305.
78. Nazarian, R., Falcon-Perez, J.M. Dell'Angelica, E.C. (2003) Biogenesis of lysosome-related organelles complex 3 (BLOC-3): a complex containing the Hermansky-Pudlak syndrome (HPS) proteins HPS1 and HPS4. Proceedings of the National Academy of Sciences of the United States of America, 100, 8770 8775.
79. Nieswandt, B., Brakebusch, C., Bergmeier, W., Schulte, V., Bouvard, D., Mokhtari-Nejad, R., Lindhout, T., Heemskerk, J.W.M., Zirngibl, H. Fässler, R. (2001) Glycoprotein VI but not alpha 2 beta 1 integrin is essential for platelet interaction with collagen. The EMBO Journal, 20, 2120 2130.
80. Nieswandt, B., Aktas, B., Moers, A. Sachs, U. (2005) Platelets in atherothrombosis: lessons from mouse models. Journal of Thrombosis and Haemostasis, 3, 1725 1736.
81. Nieswandt, B., Moser, M., Pleines, I., Varga-Szabo, D., Monkley, S., Critchley, D. Fassler, R. (2007) Loss of talin1 in platelets abrogates integrin activation, platelet aggregation, and thrombus formation in vitro and in vivo. Journal of Experimental Medicine, 204, 3113 3118.
82. Nonne, C., Lenain, N., Hechler, B., Mangin, P., Cazenave, J., Gachet, C. Lanza, F. (2005) Importance of platelet phospholipase Cγ2 signaling in arterial thrombosis as a function of lesion severity. Arteriosclerosis, Thrombosis, and Vascular Biology, 25, 1293 1298.
83. Nonne, C., Hechler, B., Cazenave, J., Gachet, C. Lanza, F. (2008) Reassessment of in vivo thrombus formation in glycoprotein V deficient mice backcrossed on a C57Bl/6 strain. Journal of Thrombosis and Haemostasis, 6, 210 212.
84. Noris, P., Guidetti, G.F., Conti, V., Ceresa, I.F., Di Pumpo, M., Pecci, A., Torti, M., Savoia, A. Balduini, C.L. (2006) Autosomal dominant thrombocytopenias with reduced expression of glycoprotein Ia. Thrombosis and Haemostasis, 95, 483 489.
85. Nurden, A. (2006) Glanzmann thrombasthenia. Orphanet Journal of Rare Diseases, 1 : 10.
86. Nurden, A. Caen, J. (1975) Specific roles for platelet surface glycoproteins in platelet function. Nature, 255, 720 722.
87. Nurden, A. Nurden, P. (2007) The gray platelet syndrome: clinical spectrum of the disease. Blood Reviews, 21, 21 36.
88. Nurden, P. Nurden, A. (2008) Congenital disorders associated with platelet dysfunction. Thrombosis and Haemostasis, 99, 253 263.
89. Nurden, P., Jandrot-Perrus, M., Combrie, R., Winckler, J., Arocas, V., Lecut, C., Pasquet, J., Kunicki, T. Nurden, A. (2004) Severe deficiency of glycoprotein VI in a patient with gray platelet syndrome. Blood, 104, 107 114.
90. Offermanns, S., Toombs, C.F., Hu, Y.H. Simon, M.I. (1997) Defective platelet activation in G alpha(q)-deficient mice. Nature (London), 389, 183 186.
91. Oh, J., Bailin, T., Fukai, K., Feng, G., Ho, L., Mao, J., Frenk, E., Tamura, N. Spritz, R. (1996) Positional cloning of a gene for Hermansky-Pudlak syndrome, a disorder of cytoplasmic organelles. Nature Genetics, 14, 300 306.
92. Othman, M., Notley, C., Lavender, F., White, H., Byrne, C., Lillicrap, D. O'Shaughnessy, D. (2005) Identification and functional characterization of a novel 27-bp deletion in the macroglycopeptide-coding region of the GPIb alpha gene resulting in platelet-type von Willebrand disease. Blood, 105, 4330 4336.
93. Philipp, C., Dilley, A., Miller, C., Evatt, B., Baranwal, A., Schwartz, R., Bachmann, G. Saidi, P. (2003) Platelet functional defects in women with unexplained menorrhagia. Journal of Thrombosis and Haemostasis, 1, 477 484.
94. Poole, A., Gibbins, J.M., Turner, M., van Vugt, M.J., van de Winkel, J.G.J., Saito, T., Tybulewicz, V.L.J. Watson, S.P. (1997) The Fc receptor gamma-chain and the tyrosine kinase Syk are essential for activation of mouse platelets by collagen. The EMBO Journal, 16, 2333 2341.
95. Quiroga, T., Goycoolea, M., Panes, O., Aranda, E., Martinez, C., Belmont, S., Munoz, B., Zuniga, P., Pereira, J. Mezzano, D. (2007) High prevalence of bleeders of unknown cause among patients with inherited mucocutaneous bleeding. A prospective study of 280 patients and 299 controls. Haematologica, 92, 357 365.
96. Ramakrishnan, V., Reeves, P.S., DeGuzman, F., Deshpande, U., Ministri-Madrid, K., DuBridge, R.B. Phillips, D.R. (1999) Increased thrombin responsiveness in platelets from mice lacking glycoprotein V. Proceedings of the National Academy of Sciences of the United States of America, 96, 13336 13341.
97. Reddy, K., Smith, D. Plow, E. (2008) Analysis of Fyn function in hemostasis and alpha IIb beta 3-integrin signaling. Journal of Cell Science, 121, 1641 1648.
98. Roux, D.T.L., Roullot, V., Poujol, C., Kortulewski, T., Nurden, P. Marguerie, G. (2000) Thrombasthenic mice generated by replacement of the integrin alpha IIb gene: demonstration that transcriptional activation of this megakaryocytic locus precedes lineage commitment. Blood, 96, 1399 1408.
99. Ruggeri, Z. (2009) Platelet adhesion under flow. Microcirculation, 16, 58 83.
100. Ryo, R., Yoshida, A., Sugano, W., Yasunaga, M., Nakayama, K., Saigo, K., Adachi, M., Yamaguchi, N. Okuma, M. (1992) Deficiency of P62, a putative collagen receptor, in platelets from a patient with defective collagen-induced platelet aggregation. American Journal of Hematology, 39, 25 31.
101. Sachs, U.J. Nieswandt, B. (2007) In vivo thrombus formation in murine models. Circulation Research, 100, 979 991.
102. Sambrano, G.R., Weiss, E.J., Zheng, Y.W., Huang, W. Coughlin, S.R. (2001) Role of thrombin signalling in platelets in haemostasis and thrombosis. Nature, 413, 74 78.
103. Savoia, A., Balduini, C., Savino, M., Noris, P., Del Vecchio, M., Perrotta, S., Belletti, S., Poggi, V. Iolascon, A. (2001) Autosomal dominant macrothrombocytopenia in Italy is most frequently a type of heterozygous Bernard-Soulier syndrome. Blood, 97, 1330 1335.
104. Schade, A., Arya, M., Gao, S., Diz-Kucukkaya, R., Anvari, B., McIntire, L., Lopez, J. Dong, J. (2003) Cytoplasmic truncation of glycoprotein Ib [alpha] weakens its interaction with von Willebrand factor and impairs cell adhesion. Biochemistry, 42, 2245 2251.
105. Seri, M., Cusano, R., Gangarossa, S., Caridi, G., Bordo, D., Lo Nigro, C., Ghiggeri, G., Ravazzolo, R., Savino, M. Del Vecchio, M. (2000) Mutations in MYH9 result in the May-Hegglin anomaly, and Fechtner and Sebastian syndromes. The May-Heggllin/Fechtner Syndrome consortium. Nature Genetics, 26, 103 105.
106. Siegel, D., Ashton, G., Penagos, H., Lee, J., Feiler, H., Wilhelmsen, K., South, A., Smith, F., Prescott, A. Wessagowit, V. (2003) Loss of kindlin-1, a human homolog of the Caenorhabditis elegans actin-extracellular-matrix linker protein UNC-112, causes Kindler syndrome. American Journal of Human Genetics, 73, 174 187.
107. Smyth, S.S., Reis, E.D., Vaananen, H., Zhang, W. Coller, B.S. (2001) Variable protection of beta 3-integrin-deficient mice from thrombosis initiated by different mechanisms. Blood, 98, 1055 1062.
108. Snapper, S.B., Rosen, F.S., Mizoguchi, E., Cohen, P., Khan, W., Liu, C.H., Hagemann, T.L., Kwan, S.P., Ferrini, R., Davidson, L., Bhan, A.K. Alt, F.W. (1998) Wiskott-Aldrich syndrome protein-deficient mice reveal a role for WASP in T but not B cell activation. Immunity, 9, 81 91.
109. Spritz, R. (1998) Genetic defects in Chediak-Higashi syndrome and the beige mouse. Journal of Clinical Immunology, 18, 97 105.
110. Sugiyama, T., Okuma, M., Ushikubi, F., Sensaki, S., Kanaji, K. Uchino, H. (1987) A novel platelet aggregating factor found in a patient with defective collagen-induced platelet aggregation and autoimmune thrombocytopenia. Blood, 69, 1712 1720.
111. Suzuki-Inoue, K., Inoue, O., Frampton, J. Watson, S.P. (2003) Murine GPVI stimulates weak integrin activation in PLC gamma 2-/-platelets: involvement of PLC amma 1 and PI3-kinase. Blood, 102, 1367 1373.
112. Symons, M., Derry, J., Karlak, B., Jiang, S., Lemahieu, V., McCormick, F., Francke, U. Abo, A. (1996) Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization. Cell, 84, 723 734.
113. Tadokoro, S., Shattil, S.J., Eto, K., Tai, V., Liddington, R.C., de Pereda, J.M., Ginsberg, M.H. Calderwood, D.A. (2003) Talin binding to integrin ß tails: a final common step in integrin activation. Science, 302, 103 106.
114. Takahashi, H. Moroi, M. (2001) Antibody against platelet membrane glycoprotein VI in a patient with systemic lupus erythematosus. American Journal of Hematology, 67, 262 267.
115. Thomas, D.W., Mannon, R.B., Mannon, P.J., Latour, A., Oliver, J.A., Hoffman, M., Smithies, O., Koller, B.H. Coffman, T.M. (1998) Coagulation defects and altered hemodynamic responses in mice lacking receptors for thromboxane A2. Journal of Clinical Investigation, 102, 1994 2001.
116. Tolmachova, T., Åbrink, M., Futter, C., Authi, K. Seabra, M. (2007) Rab27b regulates number and secretion of platelet dense granules. Proceedings of the National Academy of Sciences of the United States of America, 104, 5872 5877.
117. Tsakiris, D., Scudder, L., Hodivala-Dilke, K., Hynes, R. Coller, B. (1999) Hemostasis in the mouse (Mus musculus): a review. Thrombosis and Haemostasis, 81, 177 188.
118. Tsuji, M., Ezumi, Y., Arai, M. Takayama, H. (1997) A novel association of Fc receptor γ-chain with glycoprotein VI and their co-expression as a collagen receptor in human platelets. Journal of Biological Chemistry, 272, 23528 23531.
119. Tubman, V.N., Levine, J.E., Campagna, D.R., Monahan-Earley, R., Dvorak, A.M., Neufeld, E.J. Fleming, M.D. (2007) X-linked gray platelet syndrome due to a GATA1 Arg216Gln mutation. Blood, 109, 3297 3299.
120. Ussar, S., Wang, H., Linder, S., Fässler, R. Moser, M. (2006) The kindlins: subcellular localization and expression during murine development. Experimental Cell Research, 312, 3142 3151.
121. Varga-Szabo, D., Pleines, I. Nieswandt, B. (2008a) Cell adhesion mechanisms in platelets. Arteriosclerosis, Thrombosis, and Vascular Biology, 28, 403 412.
122. Varga-Szabo, D., Braun, A., Kleinschnitz, C., Bender, M., Pleines, I., Pham, M., Renne, T., Stoll, G. Nieswandt, B. (2008b) The calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. Journal of Experimental Medicine, 205, 1583 1591.
123. Vettore, S., Scandellari, R., Moro, S., Lombardi, A.M., Scapin, M., Randi, M.L. Fabris, F. (2008) Novel point mutation in a leucine-rich repeat of the GPIbalpha chain of the platelet von Willebrand factor receptor, GPIb/IX/V, resulting in an inherited dominant form of Bernard-Soulier syndrome affecting two unrelated families: the N41H variant. Haematologica, 93, 1743 1747.
124. Wang, D., Feng, J., Wen, R., Marine, J.C., Sangster, M.Y., Parganas, E., Hoffmeyer, A., Jackson, C.W., Cleveland, J.L. Murray, P.J. (2000) Phospholipase Cγ2 is essential in the functions of B Cell and several Fc receptors. Immunity, 13, 25 35.
125. Ware, J., Russell, S. Ruggeri, Z. (2000) Generation and rescue of a murine model of platelet dysfunction: the Bernard-Soulier syndrome. Proceedings of the National Academy of Sciences of the United States of America, 97, 2803 2808.
126. Weiss, H. (1994) Scott syndrome: a disorder of platelet coagulant activity. Seminars in Hematology, 31, 312 319.
127. Weiss, H., Turitto, V. Baumgartner, H. (1978) Effect of shear rate on platelet interaction with subendothelium in citrated and native blood. I. Shear rate - dependent decrease of adhesion in von Willebrand's disease and the Bernard-Soulier syndrome. The Journal of Laboratory and Clinical Medicine, 92, 750 764.
128. Weiss, E.J., Hamilton, J.R., Lease, K.E. Coughlin, S.R. (2002) Protection against thrombosis in mice lacking PAR3. Blood, 100, 3240 3244.
129. Williamson, D., Pikovski, I., Cranmer, S., Mangin, P., Mistry, N., Domagala, T., Chehab, S., Lanza, F., Salem, H. Jackson, S. (2002) Interaction between platelet glycoprotein Ibα and filamin-1 is essential for glycoprotein Ib/IX receptor anchorage at high shear. Journal of Biological Chemistry, 277, 2151 2159.
130. Yu, I. (2004) TXAS-deleted mice exhibit normal thrombopoiesis, defective hemostasis, and resistance to arachidonate-induced death. Blood, 104, 135 142.