The Syk-kinase inhibitor R406 impairs platelet activation and monocyte tissue factor expression triggered by heparin-PF4 complex directed antibodies

Journal of Thrombosis and Haemostasis

Volumn 9, Issue 10, 2011, Pages 2067-2076

  Lhermusier, T ^a   Van Rottem, J ^a   Garcia, C ^b   Xuereb, J M ^a   Ragab, A ^a   Martin, V ^a   Gratacap, M P ^a   Sie P ^a,b   Payrastre, B ^a,b  

^a University Hospital of Toulouse   (France)

^b TOULOUSE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FOSTAMATINIB; HEPARIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C GAMMA2; PROTEIN KINASE B; PROTEIN KINASE SYK; THROMBOCYTE FACTOR 4;

ADULT; ANTICOAGULATION; ARTICLE; CLINICAL ARTICLE; DEEP VEIN THROMBOSIS; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HEPARIN INDUCED THROMBOCYTOPENIA; HUMAN; HUMAN CELL; LUNG EMBOLISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOCYTE AGGREGATION;

BASE SEQUENCE; DNA PRIMERS; HEPARIN; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MONOCYTES; OXAZINES; PLATELET ACTIVATION; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; PYRIDINES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THROMBOPLASTIN;

EID: 80053397337     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2011.04470.x     Document Type: Article

References (49)

1. Warkentin TE, Chong BH, Greinacher A. Heparin-induced thrombocytopenia: towards consensus. Thromb Haemost 1998; 79: 1-7.
2. Walenga JM, Jeske WP, Prechel MM, Bakhos M. Newer insights on the mechanism of heparin-induced thrombocytopenia. Semin Thromb Hemost 2004; 30 (Suppl. 1): 57-67.
3. Greinacher A. Heparin-induced thrombocytopenia. J Thromb Haemost 2009; 7 (Suppl. 1): 9-12.
4. Kelton JG, Warkentin TE. Heparin-induced thrombocytopenia a historical perspective. Blood 2008; 112: 2607-15.
5. Tardy-Poncet B, Piot M, Chapelle C, France G, Campos L, Garraud O, Decousus H, Mismetti P, Tardy B. Thrombin generation and heparin-induced thrombocytopenia. J Thromb Haemost 2009; 7: 1474-81.
6. Warkentin TE, Hayward CPM, Boshkov LK, Santos AV, Sheppard JA, Bode AP, Kelton JG. Sera from patients with heparin-induced thrombocytopenia generate platelet-derived microparticles with procoagulant activity: an explanation for the thrombotic complications of heparin-induced thrombocytopenia. Blood 1994; 84: 3691-9.
7. Arepally GM, Mayer IM. Antibodies from patients with heparin-induced thrombocytopenia stimulate monocytic cells to express tissue factor and secrete interleukin-8. Blood 2001; 98: 1252-4.
8. Pouplard C, Iochmann S, Renard B, Herault O, Colombat P, Amiral J, Gruel Y. Induction of monocyte tissue factor expression by antibodies to heparin-platelet factor 4 complexes developed in heparin-induced thrombocytopenia. Blood 2001; 97: 3300-2.
9. Rauova L, Hirsch JD, Greene TK, Zhai L, Hayes VM, Kowalska MA, Cines DB, Poncz M. Monocyte-bound PF4 in the pathogenesis of heparin-induced thrombocytopenia. Blood 2010; 116: 5021-31.
10. Cines DB, Tomaski A, Tannenbaum S. Immune endothelial-cell injury in heparin-associated thrombocytopenia. N Engl J Med 1987; 316: 581-9.
11. Reilly MP, Taylor SM, Hartman NK, Arepally GM, Sachais BS, Cines DB, Poncz M, McKenzie S. Heparin-induced thrombocytopenia/thrombosis in a transgenic mouse model requires human platelet factor 4 and platelet activation through FcγRIIA. Blood 2001; 98: 2442-7.
12. Kasirer-friede A, Kahn ML, Shattil SJ. Platelet integrins and immunoreceptors. Immunol Rev 2007; 218: 247-64.
13. Huang MM, Indik Z, Brass LF, Hoxie JA, Schreiber AD, Brugge JS. Activation of Fcgamma RII induces tyrosine phosphorylation of multiple proteins including FcgammaRII. J Biol Chem 1992; 267: 5467-73.
14. Chacko GW, Duchemin AM, Coggeshall KM, Osbone JM, Brandt JT, Anderson CL. Clustering of the platelet Fc gamma receptor induces noncovalent association with the tyrosine kinase p72syk. J Biol Chem 1994; 269: 32435-40.
15. Falet H, Pollitt AY, Begonja AJ, Weber SE, Duerschmied D, Wagner DD, Watson SP, Hartwig JH. A novel interaction between FlnA and Syk regulates platelet ITAM-mediated receptor signaling and function. J Exp Med 2010; 207: 1967-79.
16. Watson SP, Gibbins J. Collagen receptor signalling in platelets: extending the role of the ITAM. Immunol Today 1998; 19: 260-4.
17. Watson SP, Auger JM, McCarty OJT, Pearce AC. GPVI and integrin αIIbβ3 signaling in platelets. J Thromb Haemost 2005; 3: 1752-62.
18. Poole A, Gibbins JM, Turner M, van Vugt MJ, van de Winkel JG, Saito T, Tybulewicz VL, Watson SP. The Fc receptor gamma-chain and the tyrosine kinase Syk are essential for activation of mouse platelets by collagen. EMBO J 1997; 16: 2333-41.
19. Clark EA, Shattil SJ, Ginsberg MH, Bolen J, Brugge JS. Regulation of the protein tyrosine kinase pp72syk by platelet agonists and the integrin alphaIIb beta 3. J Biol Chem 1994; 269: 28859-64.
20. Mocsai A, Ruland J, Tybulewicz VLJ. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat Rev Immunol 2010; 10: 387-402.
21. Hughes CE, Pollitt AY, Mori J, Eble JA, Tomlinson MG, Hartwig JH, O'Callaghan CA, Fütterer K, Watson SP. CLEC-2 activates Syk through dimerization. Blood 2010; 115: 2947-55.
22. Canobbio I, Stefanini L, Gianni F, Guidetti GF, Balduini C, Torti M. A new role for FcγRIIA in the potentiation of human platelet activation induced by weak stimulation. Cell Signal 2006; 18: 861-70.
23. Obergfell A, Eto K, Mocsai A, Buensuceso C, Moores SL, Brugge JS, Lowell CA, Shattil SJ. Coordinate interactions of Csk, SRC, and Syk kinases with alphaIIbbeta 3 initiate integrin signaling to the cytoskeleton. J Cell Biol 2002; 157: 265-75.
24. Boylan B, Gao C, Rathore V, Gill JC, Newman DK, Newman PJ. Identification of FcγRIIa as the ITAM-bearing receptor mediating αIIbβ3 outside-in integrin signaling in human platelets. Blood 2008; 112: 2780-6.
25. Podolanczuk A, Lazarus AH, Crow AR, Grossbard E, Bussel JB. Of mice and men: an open-label pilot study for treatment of immune thrombocytopenic purpura by an inhibitor of Syk. Blood 2009; 113: 3154-60.
26. Riccaboni M, Bianchi I, Petrillo P. Spleen tyrosine kinases: biology, therapeutic targets and drugs. Drug Discovery Today 2010; 15: 517-30.
27. Braselmann S, Taylor V, Zhao H, Wang S, Sylvain C, Baluom M, Qu K, Herlaar E, Lau A, Young C, Wong BR, Lowell S, Sun T, Park G, Argade A, Jurcevic S, Pine P, Singh R, Grossbard EB, Payan DG, et al. R406, an orally available spleen tyrosine kinase inhibitor blocks Fc receptor signaling and reduces immune complex-mediated inflammation. J Pharmacol Exp Ther 2006; 319: 998-1008.
28. Reilly MP, Sinha U, Andre P, Taylor SM, Pak Y, DeGuzman FR, Nanda N, Pandey A, Stolla M, Bergmeier W, McKenzie SE. PRT060318, a novel Syk inhibitor, prevents heparin-induced thrombocytopenia in a transgenic mouse model. Blood 2010; 117: 2241-6.
29. Lo GK, Juhl D, Warkentin TE, Sigouin CS, Eichler P, Greinacher A. Evaluation of pretest clinical score (4 T's) for the diagnosis of heparin-induced thrombocytopenia in two clinical settings. J Thromb Haemost 2006; 4: 759-65.
30. Gratacap MP, Payrastre B, Viala C, Mauco G, Plantavid M, Chap H. Phosphatidylinositol 3, 4, 5-trisphosphate-dependent stimulation of phospholipase C-gamma2 is an early key event in FcgammaRIIA-mediated activation of human platelets. J Biol Chem 1998; 273: 24314-21.
31. Gratacap MP, Hérault JP, Viala C, Ragab A, Savi P, Herbert JM, Chap H, Plantavid M, Payrastre B. FcγRIIA requires a Gi-dependent pathway for an efficient stimulation of phosphoinositide 3-kinase, calcium mobilization and platelet aggregation. Blood 2000; 96: 3439-46.
32. Lacroix R, Robert S, Poncelet P, Kasthuri RS, Key NS, Dignat-George F on behalf of the ISTH SSC Workshop. Standardization of platelet-derived microparticle enumeration by flow cytometry with calibrated beads: results of the international society on thrombosis and haemostasis SSC collaborative workshop. J Thromb Haemost 2010; 8: 2571-4.
33. Zeller JM, Gewurz H. Enhancement of Human Peripheral Blood Monocyte Respiratory Burst Activity by Aggregated C-Reactive Protein. J Leuk Biol 1986; 40: 769-83.
34. Essayagh S, Xuereb J-M, Terrisse A-D, Tellier-Cirioni L, Pipy B, Sié P. Microparticles from apoptotic monocytes induce transient platelet recruitment and tissue factor expression by cultured human vascular endothelial cells via a redox-sensitive mechanism. Thromb Haemost 2007; 98: 831-7.
35. Ghrib F, Brisset AC, Dupouy D, Terrisse AD, Navarro C, Cadroy Y, Boneu B, Sié P. The expression of tissue factor and tissue factor pathway inhibitor in aortic smooth muscle cells is up-regulated in synthetic compared to contractile phenotype. Thromb Haemost 2002; 87: 1051-6.
36. Luther T, Flössel C, Hietschhold V, Koslowski R, Müller M. Flow cytometric analysis of tissue factor (TF) expression on stimulated monocytes-comparison to procoagulant activity of mononuclear blood cells. Blut 1990; 61: 375-8.
37. Spalton JC, Mori J, Pollittt AY, Hughes CE, Eble JA, Watson SP. The novel Syk inhibitor R406 reveals mechanistic differences in the initiation of GPVI and CLEC-2 signaling in platelets. J Thromb Haemost 2009; 7: 1192-9.
38. Ragab A, Séverin S, Gratacap M-P, Aguado E, Malissen M, Jandrot-Perrus M, Malissen B, Ragab-Thomas J, Payrastre B. Roles of the C-terminal tyrosine residues of LAT in GPVI-induced platelet activation; insights in the mechanism of PLCγ2 activation. Blood 2007; 110: 2466-74.
39. Shantsila E, Lip GYH. The role of monocytes in thrombotic disorders: insights from tissue factor, monocyte-platelet aggregates and novel mechanisms. Thromb Haemost 2009; 102: 916-24.
40. McKenzie SE, Reilly MP. Heparin-induced thrombocytopenia and other immune thrombocytopenias lessons from mouse models. Semin Thromb Hemost 2004; 30: 559-68.
41. Reilly RF. The pathophysiology of immune-mediated heparin-induced thrombocytopenia. Semin Dial 2003; 16: 54-60.
42. Reilly MP, McKenzie SE. Insights from mouse models of heparin-induced thrombocytopenia and thrombosis. Curr Opin Hematol 2002; 9: 395-400.
43. Weinblatt ME, Kavanaugh A, Burgos-Vargas R, Dikranian AH, Medrano-Ramirez G, Morales-Torres J, Murphy FT, Musser TK, Straniero N, Vicente-Gonzales AV, Grossbard E. Treatment of rheumatoid arthritis with a Syk inhibitor. Arthritis Rheum 2008; 11: 3309-18.
44. Pan XQ, Darby C, Indik ZK, Schreiber AD. Activation of three classes of nonreceptor tyrosine kinases following Fcγ receptor crosslinking in human monocytes. Clin Immunol 1999; 90: 55-64.
45. Kasper B, Brandt E, Brandau S, Petersen F. Platelet factor 4 (CXC chemokine ligand 4) differentially regulates respiratory burst, survival, and cytokine expression of human monocytes by using distinct signaling pathways. J Immunol 2007; 179: 2584-91.
46. Steffel J, Luscher TF, Tanner FC. Tissue factor in cardiovascular diseases: molecular mechanisms and clinical implications. Circulation 2006; 113: 722-31.
47. Law DA, Nannzzi-Alaimo L, Ministri K, Hughes PE, Forsyth J, Turner M, Shattil SJ, Ginsberg MH, Tybulewicz VL, Phillips DR. Genetic and pharmacological analyses of Syk function in alphaIIbbeta-3 signaling in platelets. Blood 1999; 93: 2645-52.
48. Gao C, Boylan B, Bougie D, Gill JC, Birenbaum J, Newman DK, Aster R, Newman PJ. Eptifibatide-induced thrombocytopenia and thrombosis in humans require FcγRIIa and the integrin β3 cytoplasmic domain. J Clin Invest 2009; 119: 504-11.
49. Epelman S, Nair D, Downey R, Militello M, Askari AT. Eptifibatide-induced thrombocytopenia and thrombosis. J Thrombosis Thrombolysis 2006; 22: 151-4.