Glanzmann thrombasthenia: State of the art and future directions

Seminars in Thrombosis and Hemostasis

Volumn 39, Issue 6, 2013, Pages 642-655

  Nurden, Alan T ^a   Pillois, Xavier ^a,b   Wilcox, David A ^c,d  

^a Ctr Geriatrie Ctr Hosp Univ B   (France)

^b HAUT LÉVÊQUE HOSPITAL   (France)

^c BLOOD RESEARCH INSTITUTE   (United States)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

IIb 3 integrin; gene therapy; Glanzmann thrombasthenia; mutation analysis; platelet aggregation

Indexed keywords

ADENOSINE DIPHOSPHATE; BETA3 INTEGRIN; EPIDERMAL GROWTH FACTOR; VITRONECTIN RECEPTOR;

ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; BLEEDING; BLOOD CLOT RETRACTION; BLOOD TRANSFUSION; CALCIUM BINDING; CHROMOSOME; DEEP VEIN THROMBOSIS; DIFFERENTIAL DIAGNOSIS; EXTRAMEDULLARY HEMATOPOIESIS; FLOW CYTOMETRY; GENE MUTATION; GENETIC DISORDER; GLANZMANN DISEASE; HUMAN; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LIGAND BINDING; MISSENSE MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; THROMBOCYTE AGGREGATION; THROMBOCYTOPENIA; VIRAL GENE THERAPY;

BLOOD PLATELETS; GENETIC THERAPY; HEMORRHAGE; HUMANS; MUTATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; STEM CELL TRANSPLANTATION; THROMBASTHENIA; TRANSPLANTATION, AUTOLOGOUS;

EID: 84883249514     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0033-1353393     Document Type: Article

References (124)

1. George J. N., Caen J. P., Nurden A. T. Glanzmann's thrombasthenia: the spectrum of clinical disease. Blood: 1990; 75 7 1383 1395
2. Nurden A. T., Fiore M., Nurden P., Pillois X. Glanzmann thrombasthenia: a review of ITGA2B and ITGB3 defects with emphasis on variants, phenotypic variability, and mouse models. Blood: 2011; 118 23 5996 6005
3. Nurden A. T., Pillois X., Nurden P. Understanding the genetic basis of Glanzmann thrombasthenia: implications for treatment. Expert Rev Hematol: 2012; 5 5 487 503
4. Xiao T., Takagi J., Coller B. S., Wang J. H., Springer T. A. Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics. Nature: 2004; 432 7013 59 67
5. Arnaout M. A., Mahalingam B., Xiong J. P. Integrin structure, allostery, and bidirectional signalling. Annu Rev Cell Biol: 2005; 21 381 410
6. Coller B. S., Shattil S. J. The GPIIb/IIIa (integrin alphaIIbbeta3) odyssey: a technology-driven saga of a receptor with twists, turns, and even a bend. Blood: 2008; 112 8 3011 3025
7. Harrison P., Mackie I., Mumford A., et al. British Committee for Standards in Haematology Guidelines for the laboratory investigation of heritable disorders of platelet function. Br J Haematol: 2011; 155 1 30 44
8. Bolton-Maggs P. HB, Chalmers E. A., Collins P. W., et al. UKHCDO A review of inherited platelet disorders with guidelines for their management on behalf of the UKHCDO. Br J Haematol: 2006; 135 5 603 633
9. Niessner H., Clemetson K. J., Panzer S., Mueller-Eckhardt C., Santoso S., Bettelheim P. Acquired thrombasthenia due to GPIIb/IIIa-specific platelet autoantibodies. Blood: 1986; 68 2 571 576
10. Thornton M. A., Poncz M., Korostishevsky M., et al. The human platelet alphaIIb gene is not closely linked to its integrin partner beta 3. Blood: 1999; 94 6 2039 2047
11. Kunicki T. J., Williams S. A., Nugent D. J., Yeager M. Mean platelet volume and integrin alleles correlate with levels of integrins α(IIb)β(3) and α(2)β(1) in acute coronary syndrome patients and normal subjects. Arterioscler Thromb Vasc Biol: 2012; 32 1 147 152
12. Jallu V., Dusseaux M., Panzer S., et al. AlphaIIbbeta3 integrin: new allelic variants in Glanzmann thrombasthenia, effects on ITGA2B and ITGB3 mRNA splicing, expression, and structure-function. Hum Mutat: 2010; 31 3 237 246
13. Jayo A., Pabón D., Lastres P., Jiménez-Yuste V., González-Manchón C. Type II Glanzmann thrombasthenia in a compound heterozygote for the α IIb gene. A novel missense mutation in exon 27. Haematologica: 2006; 91 10 1352 1359
14. Peterson J. A., Pechauer S. M., Gitter M. L., et al. New platelet glycoprotein polymorphisms causing maternal immunization and neonatal alloimmune thrombocytopenia. Transfusion: 2012; 52 5 1117 1124
15. Newman P. J., Seligsohn U., Lyman S., Coller B. S. The molecular genetic basis of Glanzmann thrombasthenia in the Iraqi-Jewish and Arab populations in Israel. Proc Natl Acad Sci U S A: 1991; 88 8 3160 3164
16. Rosenberg N., Hauschner H., Peretz H., et al. A 13-bp deletion in α(IIb) gene is a founder mutation that predominates in Palestinian-Arab patients with Glanzmann thrombasthenia. J Thromb Haemost: 2005; 3 12 2764 2772
17. Fiore M., Pillois X., Nurden P., Nurden A. T., Austerlitz F. Founder effect and estimation of the age of the French Gypsy mutation associated with Glanzmann thrombasthenia in Manouche families. Eur J Hum Genet: 2011; 19 9 981 987
18. González-Manchón C., Arias-Salgado E. G., Butta N., et al. A novel homozygous splice junction mutation in GPIIb associated with alternative splicing, nonsense-mediated decay of GPIIb-mRNA, and type II Glanzmann's thrombasthenia. J Thromb Haemost: 2003; 1 5 1071 1078
19. Tronik-Le Roux D., Roullot V., Poujol C., Kortulewski T., Nurden P., Marguerie G. Thrombasthenic mice generated by replacement of the integrin α(IIb) gene: demonstration that transcriptional activation of this megakaryocytic locus precedes lineage commitment. Blood: 2000; 96 4 1399 1408
20. Mitchell W. B., Li J. H., French D. L., Coller B. S. alphaIIbbeta3 biogenesis is controlled by engagement of alphaIIb in the calnexin cycle via the N15-linked glycan. Blood: 2006; 107 7 2713 2719
21. Rosenberg N., Yatuv R., Sobolev V., Peretz H., Zivelin A., Seligsohn U. Major mutations in calf-1 and calf-2 domains of glycoprotein IIb in patients with Glanzmann thrombasthenia enable GPIIb/IIIa complex formation, but impair its transport from the endoplasmic reticulum to the Golgi apparatus. Blood: 2003; 101 12 4808 4815
22. 3 complex formation. J Thromb Haemost: 2004; 2 7 1167 1175
23. 3 activation. J Biol Chem: 2001; 276 42 38628 38635
24. 3 Thromb Haemost: 2007; 98 6 1257 1265
25. 3 Science: 2001; 294 5541 339 345
26. 3 in complex with an Arg-Gly-Asp ligand. Science: 2002; 296 5565 151 155
27. Kamata T., Tieu K. K., Irie A., Springer T. A., Takada Y. Amino acid residues in the α IIb subunit that are critical for ligand binding to integrin alphaIIb beta3 are clustered in the β-propeller model. J Biol Chem: 2001; 276 47 44275 44283
28. Poujol C., Nurden A. T., Nurden P. Ultrastructural analysis of the distribution of the vitronectin receptor (α v β 3) in human platelets and megakaryocytes reveals an intracellular pool and labelling of the α-granule membrane. Br J Haematol: 1997; 96 4 823 835
29. Morel-Kopp M. C., Melchior C., Chen P., et al. A naturally occurring point mutation in the β3 integrin MIDAS-like domain affects differently alphavbeta3 and alphaIIIbbeta3 receptor function. Thromb Haemost: 2001; 86 6 1425 1434
30. Nurden A. T., Ruan J., Pasquet J-M., et al. A novel 196Leu to Pro substitution in the beta3 subunit of the alphaIIbbeta3 integrin in a patient with a variant form of Glanzmann thrombasthenia. Platelets: 2002; 13 2 101 111
31. Ward C. M., Kestin A. S., Newman P. J. A Leu262Pro mutation in the integrin β(3) subunit results in an α(IIb)-β(3) complex that binds fibrin but not fibrinogen. Blood: 2000; 96 1 161 169
32. Jackson D. E., White M. M., Jennings L. K., Newman P. J. A Ser162->Leu mutation within glycoprotein (GP) IIIa (integrin β3) results in an unstable alphaIIbbeta3 complex that retains partial function in a novel form of type II Glanzmann thrombasthenia. Thromb Haemost: 1998; 80 1 42 48
33. Ambo H., Kamata T., Handa M., et al. Three novel integrin β3 subunit missense mutations (H280P, C560F, and G579S) in thrombasthenia, including one (H280P) prevalent in Japanese patients. Biochem Biophys Res Commun: 1998; 251 3 763 768
34. Tadokoro S., Tomiyama Y., Honda S., et al. Missense mutations in the β(3) subunit have a different impact on the expression and function between α(IIb)β(3) and α(v)β(3). Blood: 2002; 99 3 931 938
35. Hauschner H., Landau M., Seligsohn U., Rosenberg N. A unique interaction between alphaIIb and beta3 in the head region is essential for outside-in signaling-related functions of alphaIIbbeta3 integrin. Blood: 2010; 115 22 4542 4550
36. Basani R. B., Brown D. L., Vilaire G., Bennett J. S., Poncz M. A. A Leu117->Trp mutation within the RGD-peptide cross-linking region of beta3 results in Glanzmann thrombasthenia by preventing alphaIIb beta3 export to the platelet surface. Blood: 1997; 90 8 3082 3088
37. Newman P. J., Weyerbusch-Bottum S., Visentin G. P., Gidwitz S., White G. C. Type II Glanzmann thrombasthenia due to a destabilizing amino acid substitution in platelet membrane glycoprotein IIIa. Thromb Haemost: 1993; 69 1017 (abstr)
38. Grimaldi C. M., Chen F., Scudder L. E., Coller B. S., French D. LA. A Cys374Tyr homozygous mutation of platelet glycoprotein IIIa (beta 3) in a Chinese patient with Glanzmann's thrombasthenia. Blood: 1996; 88 5 1666 1675
39. 3 integrins in different manner. J Biol Chem: 2012; 287 8878 8891
40. 3 from endoplasmic reticulum to Golgi. J Thromb Haemost: 2005; 3 12 2773 2783
41. Poncz M., Rifat S., Coller B. S., et al. Glanzmann thrombasthenia secondary to a Gly273->Asp mutation adjacent to the first calcium-binding domain of platelet glycoprotein IIb. J Clin Invest: 1994; 93 172 179
42. Wilcox D. A., Paddock C. M., Lyman S., Gill J. C., Newman P. J. Glanzmann thrombasthenia resulting from a single amino acid substitution between the second and third calcium-binding domains of GPIIb. Role of the GPIIb amino terminus in integrin subunit association. J Clin Invest: 1995; 95 4 1553 1560
43. 3 integrin complex. J Biol Chem: 1994; 269 6 4450 4457
44. Jackson D. E., Poncz M., Holyst M. T., Newman P. J. Inherited mutations within the calcium-binding sites of the integrin αIIb subunit (platelet glycoprotein IIb). Effects of the amino acid side chain and the amino acid position on cation binding. Eur J Biochem: 1996; 240 1 280 287
45. 3 Blood: 1996; 88 1 167 173
46. 3 biogenesis. Blood: 2003; 101 6 2268 2276
47. Peretz H., Rosenberg N., Landau M., et al. Molecular diversity of Glanzmann thrombasthenia in southern India: new insights into mRNA splicing and structure-function correlations of alphaIIbbeta3 integrin (ITGA2B, ITGB3). Hum Mutat: 2006; 27 4 359 369
48. Kannan M., Ahmad F., Yadav B. K., Kumar R., Choudhry V. P., Saxena R. Molecular defects in ITGA2B and ITGB3 genes in patients with Glanzmann thrombasthenia. J Thromb Haemost: 2009; 7 11 1878 1885
49. Grimaldi C. M., Chen F., Wu C., Weiss H. J., Coller B. S., French D. L. Glycoprotein IIb Leu214Pro mutation produces Glanzmann thrombasthenia with both quantitative and qualitative abnormalities in GPIIb/IIIa. Blood: 1998; 91 5 1562 1571
50. Shen W-Z, Ding Q-L, Jin P-P., et al. A novel Pro126His β propeller mutation in integrin alphaIIb causes Glanzmann thrombasthenia by impairing progression of pro-alphaIIbbeta3 from endoplasmic reticulum to Golgi. Blood Cells Mol Dis: 2009; 42 1 44 50
51. Nurden A. T., Fiore M., Nurden P., Heilig R., Pillois X. Are bone defects in rare patients with Glanzmann's thrombasthenia associated with ITGB3 or ITGA2B mutations? Platelets: 2011; 22 7 547 551
52. McKay B. S., Annis D. S., Honda S., Christie D., Kunicki T. J. Molecular requirements for assembly and function of a minimized human integrin alphaIIbbeta3. J Biol Chem: 1996; 271 48 30544 30547
53. 3 function for soluble ligands but retains its ability for mediating cell adhesion and clot retraction: comparison with other mutations causing ligand-binding defects. Blood: 2003; 101 9 3485 3491
54. Honda S., Tomiyama Y., Shiraga M., et al. A two-amino acid insertion in the Cys146- Cys167 loop of the alphaIIb subunit is associated with a variant of Glanzmann thrombasthenia. Critical role of Asp163 in ligand binding. J Clin Invest: 1998; 102 6 1183 1192
55. 3 Blood: 2000; 95 1 180 188
56. Westrup D., Santoso S., Follert-Hagendorff K., et al. Glanzmann thrombasthenia Frankfurt I is associated with a point mutation Thr176Ile in the N-terminal region of αIIb subunit integrin. Thromb Haemost: 2004; 92 5 1040 1051
57. Mansour W., Einav Y., Hauschner H., Koren A., Seligsohn U., Rosenberg N. An αIIb mutation in patients with Glanzmann thrombasthenia located in the N-terminus of blade 1 of the β-propeller (Asn2Asp) disrupts a calcium binding site in blade 6. J Thromb Haemost: 2011; 9 1 192 200
58. Zhu J., Luo B. H., Xiao T., Zhang C., Nishida N., Springer T. A. Structure of a complete integrin ectodomain in a physiologic resting state and activation and deactivation by applied forces. Mol Cell: 2008; 32 6 849 861
59. Mitchell W. B., Li J. H., Murcia M., Valentin N., Newman P. J., Coller B. S. Mapping early conformational changes in alphaIIb and beta3 during biogenesis reveals a potential mechanism for alphaIIbbeta3 adopting its bent conformation. Blood: 2007; 109 9 3725 3732
60. Calvete J. J., Henschen A., González-Rodríguez J. Assignment of disulphide bonds in human platelet GPIIIa. A disulphide pattern for the β-subunits of the integrin family. Biochem J: 1991; 274 Pt 1 63 71
61. Kamata T., Ambo H., Puzon-McLaughlin W., et al. Critical cysteine residues for regulation of integrin alphaIIbbeta3 are clustered in the epidermal growth factor domains of the beta3 subunit. Biochem J: 2004; 378 Pt 3 1079 1082
62. 3 maturation and result in Glanzmann thrombasthenia. Thromb Haemost: 2002; 88 1 104 110
63. Ruiz C., Liu C-Y, Sun Q-H., et al. A point mutation in the cysteine-rich domain of glycoprotein (GP) IIIa results in the expression of a GPIIb-IIIa (alphaIIbbeta3) integrin receptor locked in a high-affinity state and a Glanzmann thrombasthenia-like phenotype. Blood: 2001; 98 8 2432 2441
64. 3 to bind fibrinogen continuously yet resulted in a severe bleeding syndrome and increased murine mortality. J Thromb Haemost: 2013; 11 6 1163 1171
65. Nurden A., Nurden P. Advances in our understanding of the molecular basis of disorders of platelet function. J Thromb Haemost: 2011; 9 01 76 91
66. 3 J Biol Chem: 2008; 28 19235 19244
67. Beglova N., Blacklow S. C., Takagi J., Springer T. A. Cysteine-rich module structure reveals a fulcrum for integrin rearrangement upon activation. Nat Struct Biol: 2002; 9 4 282 287
68. Wang R., Peterson J., Aster R. H., Newman P. J. Disruption of a long-range disulfide bond between residues Cys406 and Cys655 in glycoprotein IIIa does not affect the function of platelet glycoprotein IIb-IIIa. Blood: 1997; 90 4 1718 1719
69. Luo B. H., Springer T. A., Takagi J. Stabilizing the open conformation of the integrin headpiece with a glycan wedge increases affinity for ligand. Proc Natl Acad Sci U S A: 2003; 100 5 2403 2408
70. Kashiwagi H., Tomiyama Y., Tadokoro S., et al. A mutation in the extracellular cysteine-rich repeat region of the beta3 subunit activates integrins alphaIIbbeta3 and alphaVbeta3. Blood: 1999; 93 8 2559 2568
71. Donald J. E., Zhu H., Litvinov R. I., DeGrado W. F., Bennett J. S. Identification of interacting hot spots in the β3 integrin stalk using comprehensive interface design. J Biol Chem: 2010; 285 49 38658 38665
72. González-Manchón C., Butta N., Larrucea S., et al. A variant thrombasthenic phenotype associated with compound heterozygosity of integrin beta3-subunit: (Met124Val)beta3 alters the subunit dimerization rendering a decreased number of constitutive active alphaIIbbeta3 receptors. Thromb Haemost: 2004; 92 6 1377 1386
73. Loftus J. C., O'Toole T. E., Plow E. F., Glass A., Frelinger A. L. III, Ginsberg M. H. A beta3 integrin mutation abolishes ligand binding and alters divalent cation-dependent conformation. Science: 1990; 249 4971 915 918
74. 3 (platelet glycoprotein IIb-IIIa) helps define a ligand binding site. J Biol Chem: 1992; 267 6 3789 3794
75. Tozer E. C., Liddington R. C., Sutcliffe M. J., Smeeton A. H., Loftus J. C. Ligand binding to integrin alphaIIbbeta3 is dependent on a MIDAS-like domain in the beta3 subunit. J Biol Chem: 1996; 271 36 21978 21984
76. Tuckwell D. S., Humphries M. J. A structure prediction for the ligand-binding region of the integrin β subunit: evidence for the presence of a von Willebrand factor A domain. FEBS Lett: 1997; 400 3 297 303
77. Springer T. A., Zhu J., Xiao T. Structural basis for distinctive recognition of fibrinogen gammaC peptide by the platelet integrin alphaIIbbeta3. J Cell Biol: 2008; 182 4 791 800
78. Vanhoorelbeke K., De Meyer S. F., Pareyn I., et al. The novel S527F mutation in the integrin beta3 chain induces a high affinity alphaIIbbeta3 receptor by hindering adoption of the bent conformation. J Biol Chem: 2009; 284 22 14914 14920
79. 3 (glycoprotein IIb-IIIa) in a variant of Glanzmann thrombasthenia. Proc Natl Acad Sci U S A: 1992; 89 21 10169 10173
80. Wang R., Shattil S. J., Ambruso D. R., Newman P. J. Truncation of the cytoplasmic domain of β3 in a variant form of Glanzmann thrombasthenia abrogates signaling through the integrin α(IIb)β3 complex. J Clin Invest: 1997; 100 9 2393 2403
81. 3 integrin. Semin Thromb Hemost: 2011; 37 6 698 706
82. Peyruchaud O., Nurden A. T., Milet S., et al. R to Q amino acid substitution in the GFFKR sequence of the cytoplasmic domain of the integrin αIIb subunit in a patient with a Glanzmann's thrombasthenia-like syndrome. Blood: 1998; 92 11 4178 4187
83. 3 receptor affects proplatelet formation and causes congenital macrothrombocytopenia. Blood: 2011; 117 20 5479 5484
84. 3 transmembrane-cytoplasmic heterocomplex provides insight into integrin activation. Proc Natl Acad Sci U S A: 2009; 106 42 17729 17734
85. Ghevaert C., Salsmann A., Watkins N. A., et al. A nonsynonymous SNP in the ITGB3 gene disrupts the conserved membrane-proximal cytoplasmic salt bridge in the alphaIIbbeta3 integrin and cosegregates dominantly with abnormal proplatelet formation and macrothrombocytopenia. Blood: 2008; 111 7 3407 3414
86. Schaffner-Reckinger E., Salsmann A., Debili N., et al. Overexpression of the partially activated α(IIb)β3D723H integrin salt bridge mutant downregulates RhoA activity and induces microtubule-dependent proplatelet-like extensions in Chinese hamster ovary cells. J Thromb Haemost: 2009; 7 7 1207 1217
87. Gresele P., Falcinelli E., Giannini S., et al. Dominant inheritance of a novel integrin β3 mutation associated with a hereditary macrothrombocytopenia and platelet dysfunction in two Italian families. Haematologica: 2009; 94 5 663 669
88. 3 clustering and lipid microdomain coalescence, and associates with a thrombasthenia-like phenotype. Haematologica: 2010; 95 7 1158 1166
89. 3 impairs proplatelet formation in human megakaryocytes. PLoS ONE: 2012; 7 4 e34449
90. Van de Walle G. R., Schoolmeester A., Iserbyt B. F., et al. Activation of alphaIIbbeta3 is a sufficient but also an imperative prerequisite for activation of α2β1 on platelets. Blood: 2007; 109 2 595 602
91. Moser M., Nieswandt B., Ussar S., Pozgajova M., Fässler R. Kindlin-3 is essential for integrin activation and platelet aggregation. Nat Med: 2008; 14 3 325 330
92. Svensson L., Howarth K., McDowall A., et al. Leukocyte adhesion deficiency-III is caused by mutations in KINDLIN3 affecting integrin activation. Nat Med: 2009; 15 3 306 312
93. van de Vijver E., De Cuyper I. M., Gerrits A. J., et al. Defects in Glanzmann thrombasthenia and LAD-III (LAD-1/v) syndrome: the role of integrin β1 and β3 in platelet adhesion to collagen. Blood: 2012; 119 2 583 586
94. Bialkowska K., Ma Y-Q, Bledzka K., et al. The integrin co-activator Kindlin-3 is expressed and functional in a non-hematopoietic cell, the endothelial cell. J Biol Chem: 2010; 285 24 18640 18649
95. Pasvolsky R., Feigelson S. W., Kilic S. S., et al. A LAD-III syndrome is associated with defective expression of the Rap-1 activator CalDAG-GEFI in lymphocytes, neutrophils, and platelets. J Exp Med: 2007; 204 7 1571 1582
96. st EUPLAN platelet conference, Maastricht, Holland, 2012.
97. Topalov N. N., Yakimenko A. O., Canault M., et al. Two types of procoagulant platelets are formed upon physiological activation and are controlled by integrin α(IIb)β(3). Arterioscler Thromb Vasc Biol: 2012; 32 10 2475 2483
98. D'Andrea G., Margaglione M. Glansmann's Thrombasthemia Italian Team (GLATIT) Glanzmann's thrombasthenia: modulation of clinical phenotype by α2C807T gene polymorphism. Haematologica: 2003; 88 12 1378 1382
99. Kunicki T. J., Williams S. A., Nugent D. J. Genetic variants that affect platelet function. Curr Opin Hematol: 2012; 19 5 371 379
100. Gruel Y., Pacouret G., Bellucci S., Caen J. Severe proximal deep vein thrombosis in a Glanzmann thrombasthenia variant successfully treated with a low molecular weight heparin. Blood: 1997; 90 2 888 890
101. Ten Cate H., Brandjes D. PM, Smits P. HM, van Mourik J. A. The role of platelets in venous thrombosis: a patient with Glanzmann's thrombasthenia and a factor V Leiden mutation suffering from deep venous thrombosis. J Thromb Haemost: 2003; 1 2 394 395
102. Rezende S. M. Secondary prophylaxis with warfarin for recurrent thrombosis in a patient with Glanzmann thrombasthenia and F5 G1691A. Br J Haematol: 2012; 156 1 144
103. Phillips R., Richards M. Venous thrombosis in Glanzmann's thrombasthenia. Haemophilia: 2007; 13 6 758 759
104. d'Oiron R., Ménart C., Trzeciak M. C., et al. Use of recombinant factor VIIa in 3 patients with inherited type I Glanzmann's thrombasthenia undergoing invasive procedures. Thromb Haemost: 2000; 83 5 644 647
105. Nurden A., Mercié P., Zely P., Nurden P. Deep vein thrombosis, Raynaud's phenomenon and Prinzmetal angina in a patient with Glanzmann thrombasthenia. Case Rep Hematol: 2012; 2012 156290
106. Brill A., Fuchs T. A., Chauhan A. K., et al. von Willebrand factor-mediated platelet adhesion is critical for deep vein thrombosis in mouse models. Blood: 2011; 117 4 1400 1407
107. Lisman T., Adelmeijer J., Heijnen H. FG, de Groot P. G. Recombinant factor VIIa restores aggregation of alphaIIbbeta3-deficient platelets via tissue factor-independent fibrin generation. Blood: 2004; 103 5 1720 1727
108. Morgan E. A., Schneider J. G., Baroni T. E., et al. Dissection of platelet and myeloid cell defects by conditional targeting of the β3-integrin subunit. FASEB J: 2010; 24 4 1117 1127
109. Nurden A. T., Freson K., Seligsohn U. Inherited platelet disorders. Haemophilia: 2012; 18 04 154 160
110. Bellucci S., Devergie A., Gluckman E., et al. Complete correction of Glanzmann's thrombasthenia by allogeneic bone-marrow transplantation. Br J Haematol: 1985; 59 4 635 641
111. Johnson A., Goodall A. H., Downie C. J., Vellodi A., Michael D. P. Bone marrow transplantation for Glanzmann's thrombasthenia. Bone Marrow Transplant: 1994; 14 1 147 150
112. McColl M. D., Gibson B. ES. Sibling allogeneic bone marrow transplantation in a patient with type I Glanzmann's thrombasthenia. Br J Haematol: 1997; 99 1 58 80
113. Bellucci S., Damaj G., Boval B., et al. Bone marrow transplantation in severe Glanzmann's thrombasthenia with antiplatelet alloimmunization. Bone Marrow Transplant: 2000; 25 3 327 330
114. Fujimoto T-T, Kishimoto M., Ide K., et al. Glanzmann thrombasthenia with acute myeloid leukemia successfully treated by bone marrow transplantation. Int J Hematol: 2005; 81 1 77 80
115. Flood V. H., Johnson F. L., Boshkov L. K., et al. Sustained engraftment post bone marrow transplant despite anti-platelet antibodies in Glanzmann thrombasthenia. Pediatr Blood Cancer: 2005; 45 7 971 975
116. Connor P., Khair K., Liesner R., et al. Stem cell transplantation for children with Glanzmann thrombasthenia. Br J Haematol: 2008; 140 5 568 571
117. Kitko C. L., Levine J. E., Matthews D. C., Carpenter P. A. Successful unrelated donor cord blood transplantation for Glanzmann's thrombasthenia. Pediatr Transplant: 2011; 15 3 e42 e46
118. Ishaqi M. K., El-Hayek M., Gassas A., et al. Allogeneic stem cell transplantation for Glanzmann thrombasthenia. Pediatr Blood Cancer: 2009; 52 5 682 683
119. Miller W., Dunn A., Chiang K. Y. Sustained engraftment and resolution of bleeding phenotype after unrelated cord blood hematopoietic stem cell transplantation for severe glanzmann thrombasthenia. J Pediatr Hematol Oncol: 2009; 31 6 437 439
120. Wilcox D. A., Olsen J. C., Ishizawa L., Griffith M., White G. C. II. Integrin alphaIIb promoter-targeted expression of gene products in megakaryocytes derived from retrovirus-transduced human hematopoietic cells. Proc Natl Acad Sci U S A: 1999; 96 17 9654 9659
121. Wilcox D. A., Olsen J. C., Ishizawa L., et al. Megakaryocyte-targeted synthesis of the integrin β(3)-subunit results in the phenotypic correction of Glanzmann thrombasthenia. Blood: 2000; 95 12 3645 3651
122. Fang J., Hodivala-Dilke K., Johnson B. D., et al. Therapeutic expression of the platelet-specific integrin, alphaIIbbeta3, in a murine model for Glanzmann thrombasthenia. Blood: 2005; 106 8 2671 2679
123. Lipscomb D. L., Bourne C., Boudreaux M. K. Two genetic defects in alphaIIb are associated with type I Glanzmann's thrombasthenia in a Great Pyrenees dog: a 14-base insertion in exon 13 and a splicing defect of intron 13. Vet Pathol: 2000; 37 6 581 588
124. Fang J., Jensen E. S., Boudreaux M. K., et al. Platelet gene therapy improves hemostatic function for integrin alphaIIbbeta3-deficient dogs. Proc Natl Acad Sci U S A: 2011; 108 23 9583 9588