Platelet PI3Kβ and GSK3 regulate thrombus stability at a high shear rate

Blood

Volumn 125, Issue 5, 2015, Pages 881-888

  Laurent, Pierre Alexandre ^a   Séverin, Sonia ^a   Hechler, Béatrice ^b   Vanhaesebroeck, Bart ^c   Payrastre, Bernard ^a,d,e   Gratacap, Marie Pierre ^a  

^a INSERM   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d TOULOUSE UNIVERSITY HOSPITAL   (France)

^e Université de Toulouse   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE BETA; PROTEIN KINASE B; PROTEIN P110; PROTEIN P110 BETA; UNCLASSIFIED DRUG; 1-PHOSPHATIDYLINOSITOL 3-KINASE P110 SUBUNIT, MOUSE; 2-(1-(7-METHYL-2-MORPHOLIN-4-YL-4-OXO-4H-PYRIDO(1,2-A)PYRIMIDIN-9-YL)ETHYLAMINO)BENZOIC ACID; 6 [[2 [[4 (2,4 DICHLOROPHENYL) 5 (4 METHYL 1H IMIDAZOL 2 YL) 2 PYRIMIDINYL]AMINO]ETHYL]AMINO]NICOTINONITRILE; ANTHRANILIC ACID DERIVATIVE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PYRIDINE DERIVATIVE; PYRIMIDINE DERIVATIVE; PYRIMIDINONE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY THROMBOSIS; ARTICLE; BLOOD CLOT RETRACTION; BLOOD CLOTTING; CELL LINEAGE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EX VIVO STUDY; GENE DELETION; IN VIVO STUDY; MEGAKARYOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SHEAR RATE; ANIMAL; ANTAGONISTS AND INHIBITORS; DEFICIENCY; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; PATHOLOGY; PHOSPHORYLATION; THROMBOCYTE; THROMBOCYTE AGGREGATION; THROMBOSIS; TRANSGENIC MOUSE;

ANIMALS; BLOOD PLATELETS; CLASS I PHOSPHATIDYLINOSITOL 3-KINASES; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, TRANSGENIC; ORTHO-AMINOBENZOATES; PHOSPHORYLATION; PLATELET AGGREGATION; PROTO-ONCOGENE PROTEINS C-AKT; PYRIDINES; PYRIMIDINES; PYRIMIDINONES; STRESS, MECHANICAL; THROMBOSIS;

EID: 84921724552     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-07-588335     Document Type: Article

References (42)

1. Siddiqui TI, Kumar K S A, Dikshit DK. Platelets and atherothrombosis: causes, targets and treatments for thrombosis. Curr Med Chem. 2013;20(22):2779-2797.
2. Michelson AD. Antiplatelet therapies for the treatment of cardiovascular disease. Nat Rev Drug Discov. 2010;9(2):154-169.
3. Vanhaesebroeck B, Guillermet-Guibert J, Graupera M, Bilanges B. The emerging mechanisms of isoform-specific PI3K signalling. Nat Rev Mol Cell Biol. 2010;11(5):329-341.
4. Carlton JG, Cullen PJ. Coincidence detection in phosphoinositide signaling. Trends Cell Biol. 2005;15(10):540-547.
5. Lemmon MA. Pleckstrin homology (PH) domains and phosphoinositides. Biochem Soc Symp. 2007;(74):81-93.
6. Canobbio I, Stefanini L, Cipolla L, et al. Genetic evidence for a predominant role of PI3Kbeta catalytic activity in ITAM- and integrin-mediated signaling in platelets. Blood. 2009;114(10):2193-2196.
7. Cosemans JM, Munnix IC, Wetzker R, Heller R, Jackson SP, Heemskerk JW. Continuous signaling via PI3K isoforms beta and gamma is required for platelet ADP receptor function in dynamic thrombus stabilization. Blood. 2006;108(9):3045-3052.
8. Kim S, Mangin P, Dangelmaier C, et al. Role of phosphoinositide 3-kinase beta in glycoprotein VI-mediated Akt activation in platelets. J Biol Chem. 2009;284(49):33763-33772.
9. Jackson SP, Schoenwaelder SM. PI 3-Kinase p110β regulation of platelet integrin α(IIb)β3. Curr Top Microbiol Immunol. 2010;346:203-224.
10. Martin V, Guillermet-Guibert J, Chicanne G, et al. Deletion of the p110beta isoform of phosphoinositide 3-kinase in platelets reveals its central role in Akt activation and thrombus formation in vitro and in vivo. Blood. 2010;115(10):2008-2013.
11. Schoenwaelder SM, Ono A, Nesbitt WS, Lim J, Jarman K, Jackson SP. Phosphoinositide 3-kinase p110 beta regulates integrin alpha IIb beta 3 avidity and the cellular transmission of contractile forces. J Biol Chem. 2010;285(4):2886-2896.
12. Jackson SP, Schoenwaelder SM, Goncalves I, et al. PI 3-kinase p110beta: a new target for antithrombotic therapy. Nat Med. 2005;11(5):507-514.
13. Nylander S, Kull B, Björkman JA, et al. Human target validation of phosphoinositide 3-kinase (PI3K)β: effects on platelets and insulin sensitivity, using AZD6482 a novel PI3Kβ inhibitor. J Thromb Haemost. 2012;10(10):2127-2136.
14. Tiedt R, Schomber T, Hao-Shen H, Skoda RC. Pf4-Cre transgenic mice allow the generation of lineage-restricted gene knockouts for studying megakaryocyte and platelet function in vivo. Blood. 2007;109(4):1503-1506.
15. Cosemans JM, Angelillo-Scherrer A, Mattheij NJ, Heemskerk JW. The effects of arterial flow on platelet activation, thrombus growth, and stabilization. Cardiovasc Res. 2013;99(2):342-352.
16. Kroll MH, Hellums JD, McIntire LV, Schafer AI, Moake JL. Platelets and shear stress. Blood. 1996;88(5):1525-1541.
17. Peterson DM, Stathopoulos NA, Giorgio TD, Hellums JD, Moake JL. Shear-induced platelet aggregation requires von Willebrand factor and platelet membrane glycoproteins Ib and IIb-IIIa. Blood. 1987;69(2):625-628.
18. Jackson SP, Nesbitt WS, Westein E. Dynamics of platelet thrombus formation. J Thromb Haemost. 2009;7(Suppl 1):17-20.
19. O'Brien KA, Stojanovic-Terpo A, Hay N, Du X. An important role for Akt3 in platelet activation and thrombosis. Blood. 2011;118(15):4215-4223.
20. Li D, August S, Woulfe DS. GSK3beta is a negative regulator of platelet function and thrombosis. Blood. 2008;111(7):3522-3530.
21. Moore SF, van den Bosch MT, Hunter RW, Sakamoto K, Poole AW, Hers I. Dual regulation of glycogen synthase kinase 3 (GSK3)α/β by protein kinase C (PKC)α and Akt promotes thrombin-mediated integrin αIIbβ3 activation and granule secretion in platelets. J Biol Chem. 2013;288(6):3918-3928.
22. Hechler B, Nonne C, Eckly A, et al. Arterial thrombosis: relevance of a model with two levels of severity assessed by histologic, ultrastructural and functional characterization. J Thromb Haemost. 2010;8(1):173-184.
23. Nesbitt WS, Mangin P, Salem HH, Jackson SP. The impact of blood rheology on the molecular and cellular events underlying arterial thrombosis. J Mol Med (Berl). 2006;84(12):989-995.
24. Nesbitt WS, Westein E, Tovar-Lopez FJ, et al. A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med. 2009;15(6):665-673.
25. Ni H, Denis CV, Subbarao S, et al. Persistence of platelet thrombus formation in arterioles of mice lacking both von Willebrand factor and fibrinogen. J Clin Invest. 2000;106(3):385-392.
26. Welsh JD, Stalker TJ, Voronov R, et al. A systems approach to hemostasis: 1. The interdependence of thrombus architecture and agonist movements in the gaps between platelets. Blood. 2014;124(11):1808-1815.
27. Stalker TJ, Welsh JD, Tomaiuolo M, et al. A systems approach to hemostasis: 3. Thrombus consolidation regulates intrathrombus solute transport and local thrombin activity. Blood. 2014;124(11):1824-1831.
28. Tomaiuolo M, Stalker TJ, Welsh JD, Diamond SL, Sinno T, Brass LF. A systems approach to hemostasis: 2. Computational analysis of molecular transport in the thrombus microenvironment. Blood. 2014;124(11):1816-1823.
29. Gachet C. Regulation of platelet functions by P2 receptors. Annu Rev Pharmacol Toxicol. 2006;46:277-300.
30. Stalker TJ, Traxler EA, Wu J, et al. Hierarchical organization in the hemostatic response and its relationship to the platelet-signaling network. Blood. 2013;121(10):1875-1885.
31. Canobbio I, Cipolla L, Consonni A, et al. Impaired thrombin-induced platelet activation and thrombus formation in mice lacking the Ca(2+)-dependent tyrosine kinase Pyk2. Blood. 2013;121(4):648-657.
32. Niu H, Chen X, Gruppo RA, et al. Integrin αIIb-mediated PI3K/Akt activation in platelets. PLoS ONE. 2012;7(10):e47356.
33. O'Brien KA, Gartner TK, Hay N, Du X. ADP-stimulated activation of Akt during integrin outside-in signaling promotes platelet spreading by inhibiting glycogen synthase kinase-3β. Arterioscler Thromb Vasc Biol. 2012;32(9):2232-2240.
34. Barry FA, Gibbins JM. Protein kinase B is regulated in platelets by the collagen receptor glycoprotein VI. J Biol Chem. 2002;277(15):12874-12878.
35. Woulfe DS. Akt signaling in platelets and thrombosis. Expert Rev Hematol. 2010;3(1):81-91.
36. Chen J, De S, Damron DS, Chen WS, Hay N, Byzova TV. Impaired platelet responses to thrombin and collagen in AKT-1-deficient mice. Blood. 2004;104(6):1703-1710.
37. Woulfe D, Jiang H, Morgans A, Monks R, Birnbaum M, Brass LF. Defects in secretion, aggregation, and thrombus formation in platelets from mice lacking Akt2. J Clin Invest. 2004;113(3):441-450.
38. Chen X, Zhang Y, Wang Y, et al. PDK1 regulates platelet activation and arterial thrombosis. Blood. 2013;121(18):3718-3726.
39. Kirk RI, Sanderson MR, Lerea KM. Threonine phosphorylation of the beta 3 integrin cytoplasmic tail, at a site recognized by PDK1 and Akt/PKB in vitro, regulates Shc binding. J Biol Chem. 2000;275(40):30901-30906.
40. Barry FA, Graham GJ, Fry MJ, Gibbins JM. Regulation of glycogen synthase kinase 3 in human platelets: a possible role in platelet function? FEBS Lett. 2003;553(1-2):173-178.
41. Bianchi M, De Lucchini S, Marin O, Turner DL, Hanks SK, Villa-Moruzzi E. Regulation of FAK Ser-722 phosphorylation and kinase activity by GSK3 and PP1 during cell spreading and migration. Biochem J. 2005;391(Pt 2):359-370.
42. Hitchcock IS, Fox NE, Prévost N, Sear K, Shattil SJ, Kaushansky K. Roles of focal adhesion kinase (FAK) in megakaryopoiesis and platelet function: studies using a megakaryocyte lineage specific FAK knockout. Blood. 2008;111(2):596-604.