Off-target effect of the Epac agonist 8-pCPT-2'-O-Me-cAMP on P2Y12 receptors in blood platelets

Biochemical and Biophysical Research Communications

Volumn 437, Issue 4, 2013, Pages 603-608

  Herfindal, Lars ^a,b   Nygaard, Gyrid ^a   Kopperud, Reidun ^a   Krakstad, Camilla ^a   Døskeland, Stein Ove ^a   Selheim, Frode ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

ADP; Blood platelets; cAMP; Epac; P2Y12 receptor; Thromboxane

Indexed keywords

8 PCPT 2' O ME CAMP; ACETYLSALICYLIC ACID; ADENOSINE DIPHOSPHATE; CYCLIC AMP DERIVATIVE; CYCLOOXYGENASE 1; G PROTEIN COUPLED RECEPTOR; PADGEM PROTEIN; PURINERGIC P2Y12 RECEPTOR; RAP1 PROTEIN; THROMBIN; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ISOLATION; COMPUTER MODEL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; FLOW CYTOMETRY; GENOTYPE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE RELEASE REACTION; THROMBOCYTE SHAPE; WESTERN BLOTTING;

(Β-PHENYL-1), N(2)-ETHENO-8-BROMOGUANOSINE-3′,5′-CYCLIC MONOPHOSPHATE; (RP)-ADENOSINE-3′,5′-CYCLIC MONOPHOSPHOROTHIOATE, RP-ISOMER; 2-METHYLTHIO-ADENOSINE DIPHOSPHATE; 2-METHYLTHIO-ADENOSINE MONOPHOSPHATE; 2MESADP; 2MESAMP; 5,6-DICHLORO-1-Β-D-RIBOFURANOSYLBENZIMIDAZOLE-3′,5′-CYCLIC MONOPHOSPHOROTHIOATE, SP-ISOMER; 8-(4-CHLOROPHENYLTHIO)-2′-O-METHYLADENOSINE-3′,5′-CYCLIC MONOPHOSPHATE; 8-(4-CHLOROPHENYLTHIO)-2′-O-METHYLADENOSINE-3′,5′-CYCLIC MONOPHOSPHOROTHIOATE, SP-ISOMER; 8-BR-PET-CGMP; 8-BROMOADENOSINEADENOSINE-3′,5′-CYCLIC MONOPHOSPHOROTHIOATE, RP-ISOMER; 8-PCPT-2′-O-ME-CAMP; ADENOSINE DIPHOSPHATE; ADP; BLOOD PLATELETS; CAMP; CAMP-ACTIVATED PROTEIN KINASE; CGMP-ACTIVATED PROTEIN KINASE; CP/CPK; CREATINE PHOSPHATE/CREATINE PHOSPHOKINASE; CYCLIC ADENOSINE MONOPHOSPHATE; EPAC; EXCHANGE FACTOR DIRECTLY ACTIVATED BY CAMP; P2Y(12) RECEPTOR; PHORBOL 12-MYRISTATE 13-ACETATE; PHOSPHATIDYL-INOSITOL-3 KINASE; PI3K; PKA; PKG; PMA; RP-8-BR-CAMPS; RP-CAMPS; SP-5, 6-DCL-CBIMPS; SP-8-PCPT-2′-O-ME-CAMPS; THROMBOXANE; THROMBOXANE RECEPTOR A(2); TXA(2);

ANIMALS; BLOOD PLATELETS; CYCLIC AMP; DOSE-RESPONSE RELATIONSHIP, DRUG; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MICE; MICE, TRANSGENIC; MODELS, MOLECULAR; P-SELECTIN; PHOSPHORYLATION; PLATELET ACTIVATION; PROTEIN TRANSPORT; RECEPTORS, PURINERGIC P2Y12; TETRADECANOYLPHORBOL ACETATE; THROMBOXANES;

EID: 84881557772     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.07.007     Document Type: Article

References (42)

1. Poppe H., Rybalkin S.D., Rehmann H., et al. Cyclic nucleotide analogs as probes of signaling pathways. Nat. Methods 2008, 5:277-278.
2. Christensen A.E., Døskeland S.O. Cyclic nucleotide analogs. Handbook of Cell Signaling 2003, Academic Press/Elsevier Science, San Diego, pp. 549-554.
3. Christensen A.E., Selheim F., de Rooij J., et al. CAMP analog mapping of Epac1 and cAMP kinase. Discriminating analogs demonstrate that Epac and cAMP kinase act synergistically to promote PC-12 cell neurite extension. J. Biol. Chem. 2003, 278:35394-35402.
4. Schwede F., Christensen A., Liauw S., et al. 8-substituted cAMP analogues reveal marked differences in adaptability, hydrogen bonding, and charge accomodation between homologous binding sites (AI/AII and BI/BII) in cAMP kinase I and II. Biochemistry 2000, 39:8803-8812.
5. Bain J., Plater L., Elliott M., et al. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 2007, 408:297-315.
6. Davies S.P., Reddy H., Caivano M., et al. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 2000, 351:95-105.
7. Bain J., McLauchlan H., Elliott M., et al. The specificities of protein kinase inhibitors: an update. Biochem. J. 2003, 371:199-204.
8. Sand C., Grandoch M., Borgermann C., et al. 8-pCPT-conjugated cyclic AMP analogs exert thromboxane receptor antagonistic properties. Thromb. Haemost. 2010, 103:662-678.
9. Pulcinelli F.M., Ashby B., Gazzaniga P.P., et al. Protein kinase C activation is not a key step in ADP-mediated exposure of fibrinogen receptors on human platelets. FEBS Lett. 1995, 364:87-90.
10. Pulcinelli F.M., Ciampa M.T., Favilla M., et al. Concomitant activation of Gi protein-coupled receptor and protein kinase C or phospholipase C is required for platelet aggregation. FEBS Lett. 1999, 460:37-40.
11. Steen V.M., Holmsen H. Current aspects on human platelet activation and responses. Eur. J. Haematol. 1987, 38:383-399.
12. Selheim F., Idsoe R., Fukami M.H., et al. Formation of PI 3-kinase products in platelets by thrombin, but not collagen, is dependent on synergistic autocrine stimulation, particularly through secreted ADP. Biochem. Biophys. Res. Commun. 1999, 263:780-785.
13. Selheim F., Froyset A.K., Strand I., et al. Adrenaline potentiates PI 3-kinase in platelets stimulated with thrombin and SFRLLN: role of secreted ADP. FEBS Lett. 2000, 485:62-66.
14. Ryningen A., Holmsen H. Thrombin per se does not induce tyrosine protein phosphorylation in human platelets as judged by western blotting, while collagen does: the significance of synergistic, autocrine stimulation. Biochem. Biophys. Res. Commun. 1998, 245:757-763.
15. Trumel C., Payrastre B., Plantavid M., et al. 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 1999, 94:4156-4165.
16. Andre P., Delaney S.M., LaRocca T., et al. P2Y12 regulates platelet adhesion/activation, thrombus growth, and thrombus stability in injured arteries. J. Clin. Invest. 2003, 112:398-406.
17. Dawood B.B., Wilde J., Watson S.P. Reference curves for aggregation and ATP secretion to aid diagnose of platelet-based bleeding disorders: effect of inhibition of ADP and thromboxane A(2) pathways. Platelets 2007, 18:329-345.
18. Jin J., Kunapuli S.P. Coactivation of two different G protein-coupled receptors is essential for ADP-induced platelet aggregation. Proc. Nat. Acad. Sci. USA 1998, 95:8070-8074.
19. Kopperud R., Rygh C.B., Karlsen T.V., et al. The Epac1 null mouse has increased micro-vascular permeability. Circ. Res. Submitted 2003.
20. Jensen B.O., Selheim F., Døskeland S.O., et al. Protein kinase A mediates inhibition of the thrombin-induced platelet shape change by nitric oxide. Blood 2004, 104:2775-2782.
21. Selheim F., Holmsen H., Vassbotn F.S. Platelet-derived growth factor inhibits platelet activation in heparinized whole blood. Thromb. Res. 1999, 95:185-196.
22. Jensen B.O., Kleppe R., Kopperud R., et al. Dipyridamole synergizes with nitric oxide to prolong inhibition of thrombin-induced platelet shape change. Platelets 2011, 22:8-19.
23. van Triest M., de Rooij J., Bos J.L. Measurement of GTP-bound Ras-like GTPases by activation-specific probes. Methods Enzymol. 2001, 333:343-348.
24. 12 nucleotide receptor. J. Comput. Aided Mol. Des. 2011, 25:329-338.
25. Lorenowicz M.J., van Gils J., de Boer M., et al. Epac1-Rap1 signaling regulates monocyte adhesion and chemotaxis. J. Leukoc. Biol. 2006, 80:1542-1552.
26. Tiwari S., Felekkis K., Moon E.Y., et al. Among circulating hematopoietic cells, B-CLL uniquely expresses functional EPAC1, but EPAC1-mediated Rap1 activation does not account for PDE4 inhibitor-induced apoptosis. Blood 2004, 103:2661-2667.
27. Offermanns S. Activation of platelet function through G protein-coupled receptors. Circ. Res. 2006, 99:1293-1304.
28. Nieswandt B., Watson S.P. Platelet-collagen interaction: is GPVI the central receptor?. Blood 2003, 102:449-461.
29. Laxman S., Riechers A., Sadilek M., et al. Hydrolysis products of cAMP analogs cause transformation of Trypanosoma brucei from slender to stumpy-like forms. Proc. Nat. Acad. Sci. USA 2006, 103:19194-19199.
30. Yoshioka A., Shirakawa R., Nishioka H., et al. Identification of protein kinase Calpha as an essential, but not sufficient, cytosolic factor for Ca2+-induced alpha- and dense-core granule secretion in platelets. J. Biol. Chem. 2001, 276:39379-39385.
31. Woulfe D.S. Platelet G protein-coupled receptors in hemostasis and thrombosis. J. Thromb. Haemost. 2005, 3:2193-2200.
32. Chrzanowska-Wodnicka M., Smyth S.S., Schoenwaelder S.M., et al. Rap1b is required for normal platelet function and hemostasis in mice. J Clin Invest 2005, 115:680-687.
33. Guidetti G.F., Torti M. The small GTPase Rap1b: a bidirectional regulator of platelet adhesion receptors. J. Signal Transduct. 2012, 2012:412089.
34. Crittenden J.R., Bergmeier W., Zhang Y., et al. CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nat. Med. 2004, 10:982-986.
35. Cifuni S.M., Wagner D.D., Bergmeier W. CalDAG-GEFI and protein kinase C represent alternative pathways leading to activation of integrin alphaIIbbeta3 in platelets. Blood 2008, 112:1696-1703.
36. Smolenski A., Bachmann C., Reinhard K., et al. Analysis and regulation of vasodilator-stimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody. J. Biol. Chem. 1998, 273:20029-20035.
37. Jacobson K.A., Deflorian F., Mishra S., et al. Pharmacochemistry of the platelet purinergic receptors. Purinergic Signal 2011, 7:305-324.
38. Jacobson K.A., Costanzi S., Deflorian F. Probing GPCR structure: adenosine and P2Y nucleotide receptors. Methods Enzymol. 2013, 520:199-217.
39. Hoffmann K., Sixel U., Di Pasquale F., et al. Involvement of basic amino acid residues in transmembrane regions 6 and 7 in agonist and antagonist recognition of the human platelet P2Y(12)-receptor. Biochem. Pharmacol. 2008, 76:1201-1213.
40. 12 receptor. J. Thromb. Haemost. 2008, 6:1908-1914.
41. Enserink J.M., Christensen A.E., de Rooij J., et al. A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat. Cell Biol. 2002, 4:901-906.
42. Paul B.Z., Jin J., Kunapuli S.P. Molecular mechanism of thromboxane A(2)-induced platelet aggregation. Essential role for p2t(ac) and alpha(2a) receptors. J. Biol. Chem. 1999, 274:29108-29114.