G12/13 signaling pathways substitute for integrin αIIbβ3-signaling for thromboxane generation in platelets

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Bhavaraju, Kamala ^a   Lakhani, Parth R ^a   Dorsam, Robert T ^a   Jin, Jianguo ^a   Hitchcock, Ian S ^b   Sanjay, Archana ^a   Kunapuli, Satya P ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ALPHA2BBETA3 INTEGRIN; FOCAL ADHESION KINASE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; INTEGRIN; PROTEIN KINASE P60; PROTEIN KINASE SYK; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; THROMBOXANE A2; UNCLASSIFIED DRUG; FIBRINOGEN RECEPTOR; PROTEIN TYROSINE KINASE; RHO KINASE; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; THROMBOCYTE; ANIMAL; BIOSYNTHESIS; CYTOLOGY; ENZYMOLOGY; METABOLISM;

MUS;

ADENOSINE DIPHOSPHATE; ANIMALS; BLOOD PLATELETS; ENZYME ACTIVATION; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS PP60(C-SRC); RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; THROMBOXANE A2;

EID: 79951832889     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016586     Document Type: Article

References (47)

1. Dorsam RT, Kunapuli SP, (2004) Central role of the P2Y12 receptor in platelet activation. J Clin Invest 113: 340-345.
2. Freedman JE, (2005) Molecular regulation of platelet-dependent thrombosis. Circulation 112: 2725-2734.
3. Kahner BN, Shankar H, Murugappan S, Prasad GL, Kunapuli SP, (2006) Nucleotide receptor signaling in platelets. J Thromb Haemost 4: 2317-2326.
4. Ruggeri ZM, (1997) Mechanisms initiating platelet thrombus formation. Thromb Haemost 78: 611-616.
5. Murugappan S, Shankar H, Kunapuli SP, (2004) Platelet receptors for adenine nucleotides and thromboxane A2. Semin Thromb Hemost 30: 411-418.
6. Paul BZ, Jin J, Kunapuli SP, (1999) Molecular mechanism of thromboxane A(2)-induced platelet aggregation. Essential role for p2t(ac) and alpha(2a) receptors. J Biol Chem 274: 29108-29114.
7. Lages B, Weiss HJ, (1988) Heterogeneous defects of platelet secretion and responses to weak agonists in patients with bleeding disorders. Br J Haematol 68: 53-62.
8. Brass LF, Hoxie JA, Kieber-Emmons T, Manning DR, Poncz M, et al. (1993) Agonist receptors and G proteins as mediators of platelet activation. Adv Exp Med Biol 344: 17-36.
9. Francischetti IM, Saliou B, Leduc M, Carlini CR, Hatmi M, et al. (1997) Convulxin, a potent platelet-aggregating protein from Crotalus durissus terrificus venom, specifically binds to platelets. Toxicon 35: 1217-1228.
10. Jin J, Quinton TM, Zhang J, Rittenhouse SE, Kunapuli SP, (2002) Adenosine diphosphate (ADP)-induced thromboxane A(2) generation in human platelets requires coordinated signaling through integrin alpha(IIb)beta(3) and ADP receptors. Blood 99: 193-198.
11. Offermanns S, Laugwitz KL, Spicher K, Schultz G, (1994) G proteins of the G12 family are activated via thromboxane A2 and thrombin receptors in human platelets. Proc Natl Acad Sci U S A 91: 504-508.
12. Klages B, Brandt U, Simon MI, Schultz G, Offermanns S, (1999) Activation of G12/G13 results in shape change and Rho/Rho-kinase-mediated myosin light chain phosphorylation in mouse platelets. J Cell Biol 144: 745-754.
13. Kim S, Jin J, Kunapuli SP, (2006) Relative contribution of G-protein-coupled pathways to protease-activated receptor-mediated Akt phosphorylation in platelets. Blood 107: 947-954.
14. Paul BZ, Daniel JL, Kunapuli SP, (1999) Platelet shape change is mediated by both calcium-dependent and-independent signaling pathways. Role of p160 Rho-associated coiled-coil-containing protein kinase in platelet shape change. J Biol Chem 274: 28293-28300.
15. Jin J, Mao Y, Thomas D, Kim S, Daniel JL, et al. (2009) RhoA downstream of G(q) and G(12/13) pathways regulates protease-activated receptor-mediated dense granule release in platelets. Biochem Pharmacol 77: 835-844.
16. Dorsam RT, Kim S, Jin J, Kunapuli SP, (2002) Coordinated signaling through both G12/13 and G(i) pathways is sufficient to activate GPIIb/IIIa in human platelets. J Biol Chem 277: 47588-47595.
17. Shattil SJ, Newman PJ, (2004) Integrins: dynamic scaffolds for adhesion and signaling in platelets. Blood 104: 1606-1615.
18. Flevaris P, Li Z, Zhang G, Zheng Y, Liu J, et al. (2009) Two distinct roles of mitogen-activated protein kinases in platelets and a novel Rac1-MAPK-dependent integrin outside-in retractile signaling pathway. Blood 113: 893-901.
19. Law DA, DeGuzman FR, Heiser P, Ministri-Madrid K, Killeen N, et al. (1999) Integrin cytoplasmic tyrosine motif is required for outside-in alphaIIbbeta3 signalling and platelet function. Nature 401: 808-811.
20. Jenkins AL, Nannizzi-Alaimo L, Silver D, Sellers JR, Ginsberg MH, et al. (1998) Tyrosine phosphorylation of the beta3 cytoplasmic domain mediates integrin-cytoskeletal interactions. J Biol Chem 273: 13878-13885.
21. Wonerow P, Pearce AC, Vaux DJ, Watson SP, (2003) A critical role for phospholipase Cgamma2 in alphaIIbbeta3-mediated platelet spreading. J Biol Chem 278: 37520-37529.
22. Hato T, Pampori N, Shattil SJ, (1998) Complementary roles for receptor clustering and conformational change in the adhesive and signaling functions of integrin alphaIIb beta3. J Cell Biol 141: 1685-1695.
23. Hitchcock IS, Fox NE, Prevost N, Sear K, Shattil SJ, et al. (2008) Roles of focal adhesion kinase (FAK) in megakaryopoiesis and platelet function: studies using a megakaryocyte lineage specific FAK knockout. Blood 111: 596-604.
24. Mitra SK, Hanson DA, Schlaepfer DD, (2005) Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6: 56-68.
25. Arias-Salgado EG, Haj F, Dubois C, Moran B, Kasirer-Friede A, et al. (2005) PTP-1B is an essential positive regulator of platelet integrin signaling. J Cell Biol 170: 837-845.
26. Vijayan KV, Liu Y, Li TT, Bray PF, (2004) Protein phosphatase 1 associates with the integrin alphaIIb subunit and regulates signaling. J Biol Chem 279: 33039-33042.
27. Naik UP, Patel PM, Parise LV, (1997) Identification of a novel calcium-binding protein that interacts with the integrin alphaIIb cytoplasmic domain. J Biol Chem 272: 4651-4654.
28. Buensuceso CS, Obergfell A, Soriani A, Eto K, Kiosses WB, et al. (2005) Regulation of outside-in signaling in platelets by integrin-associated protein kinase C beta. J Biol Chem 280: 644-653.
29. Prevost N, Mitsios JV, Kato H, Burke JE, Dennis EA, et al. (2009) Group IVA cytosolic phospholipase A2 (cPLA2alpha) and integrin alphaIIbbeta3 reinforce each other's functions during alphaIIbbeta3 signaling in platelets. Blood 113: 447-457.
30. Murugappa S, Kunapuli SP, (2006) The role of ADP receptors in platelet function. Front Biosci 11: 1977-1986.
31. Nieswandt B, Schulte V, Zywietz A, Gratacap MP, Offermanns S, (2002) Costimulation of Gi- and G12/G13-mediated signaling pathways induces integrin alpha IIbbeta 3 activation in platelets. J Biol Chem 277: 39493-39498.
32. Obergfell A, Eto K, Mocsai A, Buensuceso C, Moores SL, et al. (2002) Coordinate interactions of Csk, Src, and Syk kinases with [alpha]IIb[beta]3 initiate integrin signaling to the cytoskeleton. J Cell Biol 157: 265-275.
33. Sada K, Takano T, Yanagi S, Yamamura H, (2001) Structure and function of Syk protein-tyrosine kinase. J Biochem 130: 177-186.
34. Schlaepfer DD, Hauck CR, Sieg DJ, (1999) Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71: 435-478.
35. Takasaki J, Saito T, Taniguchi M, Kawasaki T, Moritani Y, et al. (2004) A novel Galphaq/11-selective inhibitor. J Biol Chem 279: 47438-47445.
36. Shi Q, Hjelmeland AB, Keir ST, Song L, Wickman S, et al. (2007) A novel low-molecular weight inhibitor of focal adhesion kinase, TAE226, inhibits glioma growth. Mol Carcinog 46: 488-496.
37. Lipinski CA, Loftus JC, Targeting Pyk2 for therapeutic intervention. Expert Opin Ther Targets 14: 95-108.
38. Malmsten C, Kindahl H, Samuelsson B, Levy-Toledano S, Tobelem G, et al. (1977) Thromboxane synthesis and the platelet release reaction in Bernard-Soulier syndrome, thrombasthenia Glanzmann and Hermansky-Pudlak syndrome. Br J Haematol 35: 511-520.
39. Stefanini L, Roden RC, Bergmeier W, (2009) CalDAG-GEFI is at the nexus of calcium-dependent platelet activation. Blood 114: 2506-2514.
40. Gong H, Shen B, Flevaris P, Chow C, Lam SC, et al. G protein subunit Galpha13 binds to integrin alphaIIbbeta3 and mediates integrin "outside-in" signaling. Science 327: 340-343.
41. Murugappan S, Shankar H, Bhamidipati S, Dorsam RT, Jin J, et al. (2005) Molecular mechanism and functional implications of thrombin-mediated tyrosine phosphorylation of PKCdelta in platelets. Blood 106: 550-557.
42. Jones ML, Shawe-Taylor AJ, Williams CM, Poole AW, (2009) Characterization of a novel focal adhesion kinase inhibitor in human platelets. Biochem Biophys Res Commun 389: 198-203.
43. Garcia A, Shankar H, Murugappan S, Kim S, Kunapuli SP, (2007) Regulation and functional consequences of ADP receptor-mediated ERK2 activation in platelets. Biochem J 404: 299-308.
44. Tiedt R, Schomber T, Hao-Shen H, Skoda RC, (2007) Pf4-Cre transgenic mice allow the generation of lineage-restricted gene knockouts for studying megakaryocyte and platelet function in vivo. Blood 109: 1503-1506.
45. Soriano P, Montgomery C, Geske R, Bradley A, (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64: 693-702.
46. Jin J, Kunapuli SP, (1998) Coactivation of two different G protein-coupled receptors is essential for ADP-induced platelet aggregation. Proc Natl Acad Sci U S A 95: 8070-8074.
47. Bhavaraju K, Kim S, Daniel JL, Kunapuli SP, (2008) Evaluation of [3-(1-methyl-1H-indol-3-yl-methylene)-2-oxo-2, 3-dihydro-1H-indole-5-sulfonamide] (OXSI-2), as a Syk-selective inhibitor in platelets. Eur J Pharmacol 580: 285-290.