Role of phosphoinositide 3-kinase β in platelet aggregation and thromboxane A2 generation mediated by Gi signalling pathways

Biochemical Journal

Volumn 429, Issue 2, 2010, Pages 369-377

  Garcia, Analia ^a   Kim, Soochong ^a   Bhavaraju, Kamala ^a   Schoenwaelder, Simone M ^b   Kunapuli, Satya P ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MONASH UNIVERSITY   (Australia)

Author keywords

ADP; Akt; Extracellular signal regulated kinase (ERK); Phosphoinositide 3 kinase (PI3K); Platelet; Thromboxane A2 (TXA2)

Indexed keywords

AKT; AKT PHOSPHORYLATION; EXTRACELLULAR SIGNAL-REGULATED KINASE; FUNCTIONAL RESPONSE; INHIBITORY EFFECT; ISOFORMS; MEDIATED SIGNALLING; PHOSPHOINOSITIDE 3-KINASE; PHOSPHOINOSITIDES; PLATELET AGGREGATION; PLATELET RESPONSE; RECEPTOR STIMULATION; SELECTIVE INHIBITORS; SIGNALLING PATHWAYS;

BLOOD SUBSTITUTES; PHOSPHORYLATION;

PLATELETS;

ADENOSINE DIPHOSPHATE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE BETA; PHOSPHATIDYLINOSITOL 3 KINASE DELTA; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PHOSPHOTRANSFERASE; PHOSPHOTRANSFERASE INHIBITOR; PHOSPHOTRANSFERASE INHIBITOR TGX 221; THROMBOXANE A2; UNCLASSIFIED DRUG; WORTMANNIN; 9 (1 ANILINOETHYL) 7 METHYL 2 MORPHOLINOPYRIDO[1,2 A]PYRIMIDIN 4 ONE; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; ISOENZYME; MORPHOLINE DERIVATIVE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE INHIBITOR; PURINERGIC P2 RECEPTOR; PURINERGIC P2Y1 RECEPTOR; PYRIMIDINONE DERIVATIVE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; THROMBOCYTE AGGREGATION; ANIMAL; BLOOD; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; IN VITRO STUDY; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; THROMBOCYTE;

MUS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADENOSINE DIPHOSPHATE; ANIMALS; BLOOD PLATELETS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HUMANS; ISOENZYMES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MORPHOLINES; PLATELET AGGREGATION; PROTEIN KINASE INHIBITORS; PYRIMIDINONES; RECEPTORS, PURINERGIC P2; SIGNAL TRANSDUCTION; THROMBOXANE A2;

EID: 77954710233     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100166     Document Type: Article

References (42)

1. Packham, M. A. (1994) Role of platelets in thrombosis and hemostasis. Can. J. Physiol. Pharmacol. 72, 278-284
2. Brass, L. F., Manning, D. R., Cichowski, K. and Abrams, C. S. (1997) Signaling through G proteins in platelets: to the integrins and beyond. Thromb. Haemostasis 78, 581-589 (Pubitemid 27289308)
3. Brass, L. F. (1999) More pieces of the platelet activation puzzle slide into place. J. Clin. Invest. 104, 1663-1665
4. Kunapuli, S. P., Dorsam, R. T., Kim, S. and Quinton, T. M. (2003) Platelet purinergic receptors. Curr. Opin. Pharmacol. 3, 175-180
5. Daniel, J. L., Dangelmaier, C., Jin, J., Ashby, B., Smith, J. B. and Kunapuli, S. P. (1998) Molecular basis for ADP-induced platelet activation I: evidence for three distinct ADP receptors on platelets. J. Biol. Chem. 273, 2024-2029
6. Jin, J., Daniel, J. L. and Kunapuli, S. P. (1998) Molecular basis for ADP-induced platelet activation. II. The P2Y1 receptor mediates ADP-induced intracellular calcium mobilization and shape change in platelets. J. Biol. Chem. 273, 2030-2034
7. Jin, J. and Kunapuli, S. P. (1998) Co-activation of two different G protein-coupled receptors is essential for ADP-induced platelet aggregation. Proc. Natl. Acad. Sci. U.S.A. 95, 8070-8074
8. Abrams, C. S., Zhang, J., Downes, C. P., Tang, X., Zhao, W. and Rittenhouse, S. E. (1996) Phosphopleckstrin inhibits Gβγ -activable platelet phosphatidylinositol-4,5-bisphosphate 3-kinase. J. Biol. Chem. 271, 25192-25197
9. i signaling pathways. J. Biol. Chem. 279, 4186-4195
10. Lova, P., Paganini, S., Sinigaglia, F., Balduini, C. and Torti, M. (2002) A Gi-dependent pathway is required for activation of the small GTPase Rap1B in human platelets. J. Biol. Chem. 277, 12009-12015
11. Woulfe, D., Jiang, H., Mortensen, R., Yang, J. and Brass, L. F. (2002) Activation of Rap1b by Gi family members in platelets. J. Biol. Chem. 277, 23382-23390
12. Weiss, H. J. and Rogers, J. (1972) Thrombocytopathia due to abnormalities in platelet release reaction: studies on six unrelated patients. Blood 39, 187-196
13. Quinton, T. M., Kim, S., Dangelmaier, C., Dorsam, R. T., Jin, J., Daniel, J. L. and Kunapuli, S. P. (2002) Protein kinase C- and calcium-regulated pathways independently synergize with Gi pathways in agonist-induced fibrinogen receptor activation. Biochem. J. 368, 535-543
14. Foukas, L. C. and Shepherd, P. R. (2004) Phosphoinositide 3-kinase: the protein kinase that time forgot. Biochem. Soc. Trans. 32, 330-331
15. Koyasu, S. (2003) The role of PI3K in immune cells. Nat. Immunol. 4, 313-319
16. Camps, M., Ruckle, T., Ji, H., Ardissone, V., Rintelen, F., Shaw, J., Ferrandi, C., Chabert, C., Gillieron, C., Francon, B. et al. (2005) Blockade of PI3Kγ suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat. Med. 11, 936-943
17. Condliffe, A. M., Davidson, K., Anderson, K. E., Ellson, C. D., Crabbe, T., Okkenhaug, K., Vanhaesebroeck, B., Turner, M., Webb, L., Wymann, M. P. et al. (2005) Sequential activation of class IB and class IA PI3K is important for the primed respiratory burst of human but not murine neutrophils. Blood 106, 1432-1440
18. Hayakawa, M., Kaizawa, H., Moritomo, H., Koizumi, T., Ohishi, T., Okada, M., Ohta, M., Tsukamoto, S., Parker, P., Workman, P. and Waterfield, M. (2006) Synthesis and biological evaluation of 4-morpholino-2-phenylquinazolines and related derivatives as novel PI3 kinase p110α inhibitors. Bioorg. Med. Chem. 14, 6847-6858
19. Hers, I. (2007) Insulin-like growth factor-1 potentiates platelet activation via the IRS/PI3Kα pathway. Blood 110, 4243-4252
20. Jackson, S. P., Schoenwaelder, S. M., Goncalves, I., Nesbitt, W. S., Yap, C. L., Wright, C. E., Kenche, V., Anderson, K. E., Dopheide, S. M., Yuan, Y. et al. (2005) PI3K p110β: a new target for antithrombotic therapy. Nat. Med. 11, 507-514
21. Kim, S., Garcia, A., Jackson, S. P. and Kunapuli, S. P. (2007) Insulin-like growth factor-1 regulates platelet activation through PI3-Kα isoform. Blood 110, 4206-4213
22. Knight, Z. A., Gonzalez, B., Feldman, M. E., Zunder, E. R., Goldenberg, D. D., Williams, O., Loewith, R., Stokoe, D., Balla, A., Toth, B. et al. (2006) A pharmacological map of the PI3-K family defines a role for p110α in insulin signaling. Cell 125, 733-747
23. Sadhu, C., Masinovsky, B., Dick, K., Sowell, C. G. and Staunton, D. E. (2003) Essential role of phosphoinositide 3-kinase δ in neutrophil directional movement. J. Immunol. 170, 2647-2654
24. Gilio, K., Munnix, I. C., Mangin, P., Cosemans, J. M., Feijge, M. A., van der Meijden, P. E., Olieslagers, S., Chrzanowska-Wodnicka, M. B., Lillian, R., Schoenwaelder, S. et al. (2009) Non-redundant roles of phosphoinositide 3-kinase isoforms α and β in glycoprotein VI-induced platelet signaling and thrombus formation. J. Biol. Chem. 284, 33750-33762
25. Kim, S., Mangin, P., Dangelmaier, C., Lillian, R., Jackson, S. P., Daniel, J. L. and Kunapuli, S. P. (2009) Role of phosphoinositide 3-kinase β in glycoprotein VI-mediated Akt activation in platelets. J. Biol. Chem. 284, 33763-33772
26. Kauffenstein, G., Bergmeier, W., Eckly, A., Ohlmann, P., Leon, C., Cazenave, J. P., Nieswandt, B. and Gachet, C. (2001) The P2Y12 receptor induces platelet aggregation through weak activation of the αIIbβ3 integrin: a phosphoinositide 3-kinase-dependent mechanism. FEBS Lett. 505, 281-290
27. Schoenwaelder, S. M., Ono, A., Sturgeon, S., Chan, S. M., Mangin, P., Maxwell, M. J., Turnbull, S., Mulchandani, M., Anderson, K., Kauffenstein, G. et al. (2007) Identification of a unique co-operative phosphoinositide 3-kinase signaling mechanism regulating integrin αIIbβ3 adhesive function in platelets. J. Biol. Chem. 282, 28648-28658
28. Canobbio, I., Stefanini, L., Cipolla, L., Ciraolo, E., Gruppi, C., Balduini, C., Hirsch, E. and Torti, M. (2009) Genetic evidence for a predominant role of PI3Kβ catalytic activity in ITAM- and integrin-mediated signaling in platelets. Blood 114, 2193-2196
29. Dorsam, R. T., Kim, S., Murugappan, S., Rachoor, S., Shankar, H., Jin, J. and Kunapuli, S. P. (2005) Differential requirements for calcium and Src family kinases in platelet GPIIb/IIIa activation and thromboxane generation downstream of different G-protein pathways. Blood 105, 2749-2756
30. Garcia, A., Shankar, H., Murugappan, S., Kim, S. and Kunapuli, S. P. (2007) Regulation and functional consequences of ADP receptor-mediated ERK2 activation in platelets. Biochem. J. 404, 299-308
31. Trumel, C., Payrastre, B., Plantavid, M., Hechler, B., Viala, C., Presek, P., Martinson, E. A., Cazenave, J. P., Chap, H. and Gachet, C. (1999) A key role of adenosine diphosphate in the irreversible platelet aggregation induced by the PAR1-activating peptide through the late activation of phosphoinositide 3-kinase. Blood 94, 4156-4165
32. 2+ mobilization and procoagulant activity. FEBS J. 275, 371-385
33. Woulfe, D., Jiang, H., Morgans, A., Monks, R., Birnbaum, M. and Brass, L. F. (2004) Defects in secretion, aggregation and thrombus formation in platelets from mice lacking Akt2. J. Clin. Invest. 113, 441-450
34. Hirsch, E., Bosco, O., Tropel, P., Laffargue, M., Calvez, R., Altruda, F., Wymann, M. and Montrucchio, G. (2001) Resistance to thromboembolism in PI3Kγ -deficient mice. FASEB J. 15, 2019-2021
35. Lova, P., Paganini, S., Hirsch, E., Barberis, L., Wymann, M., Sinigaglia, F., Balduini, C. and Torti, M. (2003) A selective role for phosphatidylinositol 3,4,5-trisphosphate in the Gi-dependent activation of platelet Rap1b. J. Biol. Chem. 278, 131-138
36. Schoenwaelder, S. M., Ono, A., Nesbitt, W. S., Lim, J., Jarman, K. and Jackson, S. P. (2010) Phosphoinositide 3-kinase p110β regulates integrin αIIbβ3 avidity and the cellular transmission of contractile forces. J. Biol. Chem. 285, 2886-2896
37. Guillermet-Guibert, J., Bjorklof, K., Salpekar, A., Gonella, C., Ramadani, F., Bilancio, A., Meek, S., Smith, A. J., Okkenhaug, K. and Vanhaesebroeck, B. (2008) The p110β isoform of phosphoinositide 3-kinase signals downstream of G protein-coupled receptors and is functionally redundant with p110γ . Proc. Natl. Acad. Sci. U.S.A. 105, 8292-8297
38. Martin, V., Guillermet-Guibert, J., Chicanne, G., Cabou, C., Jandrot-Perrus, M., Plantavid, M., Vanhaesebroeck, B., Payrastre, B. and Gratacap, M. P. (2010) Deletion of the p110β isoform of phosphoinositide 3-kinase in platelets reveals its central role in Akt activation and thrombus formation in vitroand in vivo. Blood 115, 2008-2013
39. 12 receptor signalling play a crucial role in thrombin-induced ERK2 activation in human platelets. Thromb. Haemostasis 92, 114-123
40. 12 receptor-mediated potentiation of thrombin-induced thromboxane A2 generation in platelets occurs through regulation of Erk1/2 activation. J. Thromb. Haemostasis 4, 638-647
41. Daniel, J. L., Dangelmaier, C., Jin, J., Kim, Y. B. and Kunapuli, S. P. (1999) Role of intracellular signaling events in ADP-induced platelet aggregation. Thromb. Haemostasis 82, 1322-1326 (Pubitemid 29473801)
42. Chen, J., De, S., Damron, D. S., Chen, W. S., Hay, N. and Byzova, T. V. (2004) Impaired platelet responses to thrombin and collagen in AKT-1-deficient mice. Blood 104, 1703-1710