The focal adhesion kinase Pyk2 links Ca2+ signalling to Src family kinase activation and protein tyrosine phosphorylation in thrombin-stimulated platelets

Biochemical Journal

Volumn 469, Issue 2, 2015, Pages 199-210

  Canobbio, Ilaria ^a   Cipolla, Lina ^a   Guidetti, Gianni F ^a   Manganaro, Daria ^a   Visconte, Caterina ^a   Kim, Soochong ^b,c   Okigaki, Mitsuhiko ^d   Falasca, Marco ^e   Kunapuli, Satya P ^b   Torti, Mauro ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Chungbuk National University   (South Korea)

^d KYOTO PREFECTURAL UNIVERSITY   (Japan)

^e CURTIN UNIVERSITY   (Australia)

Author keywords

Calcium; G protein coupled receptor (GPCR); Platelets; Protein phosphorylation; Signal transduction; Thrombin; Tyrosine kinase

Indexed keywords

CALCIMYCIN; FOCAL ADHESION KINASE 2; PROTEIN KINASE FYN; PROTEIN KINASE LYN; PROTEIN TYROSINE KINASE; THROMBIN; FYN PROTEIN, HUMAN; FYN PROTEIN, MOUSE; HEMOSTATIC AGENT; LYN PROTEIN-TYROSINE KINASE; PTK2B PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CHELATION; CONTROLLED STUDY; HUMAN; IMMUNOPRECIPITATION; KNOCKOUT MOUSE; MOUSE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; THROMBOCYTE; THROMBOCYTE AGGREGATION; ANIMAL; CYTOLOGY; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; THROMBOCYTE ACTIVATION;

MURINAE; MUS;

ANIMALS; BLOOD PLATELETS; CALCIUM SIGNALING; ENZYME ACTIVATION; FOCAL ADHESION KINASE 2; HEMOSTATICS; HUMANS; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; PLATELET ACTIVATION; PROTO-ONCOGENE PROTEINS C-FYN; SRC-FAMILY KINASES; THROMBIN;

EID: 84937054160     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20150048     Document Type: Article

References (42)

1. Jackson, S.P. (2007) The growing complexity of platelet aggregation. Blood 109, 5087-5095 CrossRef PubMed
2. Ferrell, Jr, J.E. and Martin, G.S. (1988) Platelet tyrosine-specific protein phosphorylation is regulated by thrombin. Mol. Cell. Biol. 8, 3603-3610 PubMed
3. Golden, A. and Brugge, J.S. (1989) Thrombin treatment induces rapid changes in tyrosine phosphorylation in platelets. Proc. Natl. Acad. Sci. U.S.A. 86, 901-905 CrossRef PubMed
4. Komatsu, N., Adamson, J.W., Yamamoto, K., Altschuler, D., Torti, M., Marzocchini, R. and Lapetina, E.G. (1992) Erythropoietin rapidly induces tyrosine phosphorylation in the human erythropoietin-dependent cell line, UT-7. Blood 80, 53-59 PubMed
5. Golden, A., Nemeth, S.P. and Brugge, J.S. (1986) Blood platelets express high levels of the pp60c-Src-specific tyrosine kinase activity. Proc. Natl. Acad. Sci. U.S.A. 83, 852-856 CrossRef PubMed
6. Huang, M.M., Bolen, J.B., Barnwell, J.W., Shattil, S.J. and Brugge, J.S. (1991) Membrane glycoprotein IV (CD36) is physically associated with the Fyn, Lyn, and Yes protein-tyrosine kinases in human platelets. Proc. Natl. Acad. Sci. U.S.A. 88, 7844-7848 CrossRef PubMed
7. Pestina, T.I., Stenberg, P.E., Druker, B.J., Steward, S.A., Hutson, N.K., Barrie, R.J. and Jackson, C.W. (1997) Identification of the Src family kinases, Lck and Fgr in platelets. Their tyrosine phosphorylation status and subcellular distribution compared with other Src family members. Arterioscler. Thromb. Vasc. Biol. 17, 3278-3285 CrossRef PubMed
8. Senis, Y.A., Mazharian, A. and Mori, J. (2014) Src family kinases: at the forefront of platelet activation. Blood 124, 2013-2024 CrossRef PubMed
9. Suzuki-Inoue, K., Tulasne, D., Shen, Y., Bori-Sanz, T., Inoue, O., Jung, S.M., Moroi, M., Andrews, R.K., Berndt, M.C. and Watson, S.P. (2002) Association of Fyn and Lyn with the proline-rich domain of glycoprotein VI regulates intracellular signaling. J. Biol. Chem. 277, 21561-21566 CrossRef PubMed
10. Arias-Salgado, E.G., Lizano, S., Sarkar, S., Brugge, J.S., Ginsberg, M.H. and Shattil, S.J. (2003) Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proc. Natl. Acad. Sci. U.S.A. 100, 13298-13302 CrossRef PubMed
11. Reddy, K.B., Smith, D.M. and Plow, E.F. (2008) Analysis of Fyn function in hemostasis andαIIbß3-integrin signaling. J. Cell. Sci. 121, 1641-1648 CrossRef PubMed
12. Yin, H., Liu, J., Li, Z., Berndt, M.C., Lowell, C.A. and Du, X. (2008) Src family tyrosine kinase Lyn mediates VWF/GPIb-IX-induced platelet activation via the cGMP signaling pathway. Blood 112, 1139-1146 CrossRef PubMed
13. Briddon, S.J. and Watson, S.P. (1999) Evidence for the involvement of p59fyn and p53/56lyn in collagen receptor signalling in human platelets. Biochem. J. 338, 203-209
14. 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 CrossRef PubMed
15. Cho, M.J., Pestina, T.I., Steward, S.A., Lowell, C.A., Jackson, C.W. and 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 γ-thrombin. Blood 99, 2442-2447 CrossRef PubMed
16. Li, Z., Zhang, G., Liu, J., Stojanovic, A., Ruan, C., Lowell, C.A. and Du, X. (2010) An important role of the SRC family kinase Lyn in stimulating platelet granule secretion. J. Biol. Chem. 285, 12559-12570 CrossRef PubMed
17. Xiang, B., Zhang, G., Stefanini, L., Bergmeier, W., Gartner, T.K., Whiteheart, S.W. and Li, Z. (2012) The Src family kinases and protein kinase C synergize to mediate Gq-dependent platelet activation. J. Biol. Chem. 287, 41277-41287 CrossRef PubMed
18. Kim, S. and Kunapuli, S.P. (2011) Negative regulation of Gq-mediated pathways in platelets by G12/13 pathways through Fyn kinase. J. Biol. Chem. 286, 24170-24179 CrossRef PubMed
19. Ma, Y.C., Huang, J., Ali, S., Lowry, W. and Huang, X.Y. (2000) Src tyrosine kinase is a novel direct effector of G proteins. Cell 102, 635-646 CrossRef PubMed
20. Torti, M., Crouch, M.F. and Lapetina, E.G. (1992) Epinephrine induces association of pp60src with Gi alpha in human platelets. Biochem. Biophys. Res. Commun. 186, 440-447 CrossRef PubMed
21. Xiang, B., Zhang, G., Liu, J., Morris, A.J., Smyth, S.S., Gartner, T.K. and Li, Z. (2010) A Gi-independent mechanism mediating Akt phosphorylation in platelets. J. Thromb. Haemost. 8, 2032-2041 CrossRef PubMed
22. Avraham, S., London, R., Fu, Y., Ota, S., Hiregowdara, D., Li, J., Jiang, S., Pasztor, L.M., White, R.A., Groopman, J.E. and Avraham, H. (1995) Identification and characterization of a novel related adhesion focal tyrosine kinase (RAFTK) from megakaryocytes and brain. J. Biol Chem. 270, 27742-27751 CrossRef PubMed
23. Avraham, H., Park, S.Y., Schinkmann, K. and Avraham, S. (2000) RAFTK/Pyk2-mediated cellular signalling. Cell Signal. 12, 123-133 CrossRef PubMed
24. Raja, S., Avraham, S. and Avraham, H. (1997) Tyrosine phosphorylation of the novel protein-tyrosine kinase RAFTK during an early phase of platelet activation by an integrin glycoprotein IIb-IIIa-independent mechanism. J. Biol. Chem. 272, 10941-10947 CrossRef PubMed
25. Canobbio, I., Lova, P., Sinigaglia, F., Balduini, C. and Torti, M. (2002) Proline-rich tyrosine kinase 2 and focal adhesion kinase are involved in different phases of platelet activation by vWF. Thromb. Haemost. 87, 509-517 PubMed
26. Ohmori, T., Yatomi, Y., Asazuma, N., Satoh, K. and Ozaki, Y. (2000) Involvement of proline-rich tyrosine kinase 2 in platelet activation. Tyrosine phosphorylation mostly dependent on αIIbß3 integrin and protein kinase C, translocation to the cytoskeleton and association with Shc through Grb2. Biochem. J. 347, 561-569 CrossRef PubMed
27. Consonni, A., Cipolla, L., Guidetti, G., Canobbio, I., Ciraolo, E., Hirsch, E., Falasca, M., Okigaki, M., Balduini, C. and Torti, M. (2012) Role and regulation of phosphatidylinositol 3-kinase β in platelet integrin α2β1 signaling. Blood 119, 847-856 CrossRef PubMed
28. Cipolla, L., Consonni, A., Guidetti, G., Canobbio, I., Okigaki, M., Falasca, M., Ciraolo, E., Hirsch, E., Balduini, C. and Torti, M. (2013) The proline-rich tyrosine kinase Pyk2 regulates platelet integrin αIIbß3 outside-in signaling. J. Thromb. Haemost. 11, 345-356 CrossRef PubMed
29. 2+ -dependent tyrosine kinase Pyk2. Blood 121, 648-657 CrossRef PubMed
30. Kim, S., Cipolla, L., Guidetti, G., Okigaki, M., Jin, J., Torti, M. and Kunapuli, S.P. (2013) Distinct role of Pyk2 in mediating thromboxane generation downstream of both G12/13 and integrin αIIbß3 in platelets. J. Biol. Chem. 288, 18194-18203 CrossRef PubMed
31. Matsui, A., Okigaki, M., Amano, K., Adachi, Y., Jin, D., Takai, S., Yamashita, T., Kawashima, S., Kurihara, T., Miyazaki, M. et al. (2007) Central role of calcium-dependent tyrosine kinase PYK2 in endothelial nitric oxide synthase-mediated angiogenic response and vascular function. Circulation 116, 1041-1051 CrossRef PubMed
32. 2+ dependent activation of platelet Rap1b GTPase. Biochem. J. 453, 115-123 CrossRef PubMed
33. Guidetti, G.F., Lova, P., Bernardi, B., Campus, F., Baldanzi, G., Graziani, A., Balduini, C. and Torti, M. (2008) The Gi-coupled P2Y12 receptor regulates diacylglycerol-mediated signaling in human platelets. J. Biol. Chem. 283, 28795-28805 CrossRef PubMed
34. Canobbio, I., Stefanini, L., Guidetti, G.F., Balduini, C. and Torti, M. (2006) A new role for Fcγ RIIA in the potentiation of human platelet activation induced by weak stimulation. Cell. Signal. 18, 861-870 CrossRef PubMed
35. Qian, D., Lev, S., van Oers, N.S., Dikic, I., Schlessinger, J. and Weiss, A. (1997) Tyrosine phosphorylation of Pyk2 is selectively regulated by Fyn during TCR signaling. J. Exp. Med. 185, 1253-1259 CrossRef PubMed
36. 2+ entry in human platelets through the reorganization of the actin cytoskeleton. Biochem. J. 351, 429-437 CrossRef PubMed
37. 2+/calmodulin to FERM F2 alpha2 helix and thus forming its dimer. Biochem. J. 410, 513-523 CrossRef PubMed
38. Chapman, N.M. and Houtman, J.C. (2014) Functions of the FAK family kinases in T cells: beyond actin cytoskeletal rearrangement. Immunol. Res. 59, 23-34 CrossRef PubMed
39. Ohmori, T., Yatomi, Y., Asazuma, N., Satoh, K. and Ozaki, Y. (1999) Suppression of protein kinase C is associated with inhibition of PYK2 tyrosine phosphorylation and enhancement of PYK2 interaction with Src in thrombin-activated platelets. Thromb. Res. 93, 291-298 CrossRef PubMed
40. 2+ -induced regulation of ion channel and MAP kinase functions. Nature 376, 737-745 CrossRef PubMed
41. Quek, L.S., Pasquet, J.M., Hers, I., Cornall, R., Knight, G., Barnes, M., Hibbs, M.L., Dunn, A.R., Lowell, C.A. and Watson, S.P. (2000) Fyn and Lyn phosphorylate the Fc receptor gamma chain downstream of glycoprotein VI in murine platelets, and Lyn regulates a novel feedback pathway. Blood 96, 4246-4253 PubMed
42. Pollock, W.K., Rink, T.J. and Irvine, R.F. (1986) Liberation of [3H]arachidonic acid and changes in cytosolic free calcium in fura-2-loaded human platelets stimulated by ionomycin and collagen. Biochem. J. 235, 869-877 PubMed