The control of blood platelets by cAMP signalling

Biochemical Society Transactions

Volumn 42, Issue 2, 2014, Pages 289-294

  Raslan, Zaher ^a   Naseem, Khalid M ^a  

^a UNIVERSITY OF HULL   (United Kingdom)

Author keywords

A kinase anchoring protein (AKAP); cAMP; Compartmentalization; Phosphodiesterase (PDE); Platelet; Protein kinase A (PKA)

Indexed keywords

ADENOSINE DIPHOSPHATE; CYCLIC AMP; MEMBRANE PROTEIN; NITRIC OXIDE; SCLEROPROTEIN; THROMBIN; THROMBOCYTE RECEPTOR; THROMBOXANE A2;

ACTIN POLYMERIZATION; CALCIUM MOBILIZATION; CELL TYPE; CELLULAR DISTRIBUTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SHORT SURVEY; THROMBOCYTE; THROMBOCYTE FUNCTION; ANIMAL; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION;

ANIMALS; BLOOD PLATELETS; CYCLIC AMP; HUMANS; PHOSPHORYLATION; PLATELET ACTIVATION; SIGNAL TRANSDUCTION;

EID: 84896996761     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20130278     Document Type: Short Survey

References (45)

1. Jackson, S.P. (2013) The growing complexity of platelet aggregation. Blood 109, 5087-5095
2. Schwarz, U.R., Walter, U. and Eigenthaler, M. (2001) Taming platelets with cyclic nucleotides. Biochem. Pharmacol. 62, 1153-1161 (Pubitemid 33055619)
3. Sadana, R. and Dessauer, C.W. (2009) Physiological roles for G protein-regulated adenylyl cyclase isoforms: insights from knockout and overexpression studies. Neurosignals 17, 5-22
4. Simonds, W.F., Goldsmith, P.K., Codina, J., Unson, C.G. and Spiegel, A.M. (1989) Gi2 mediates α2-adrenergic inhibition of adenylyl cyclase in platelet membranes: in situ identification with Gα C-terminal antibodies. Proc. Natl. Acad. Sci. U.S.A. 86, 7809-7813
5. Rowley, J.W., Oler, A.J., Tolley, N.D., Hunter, B.N., Low, E.N., Nix, D.A., Yost, C.C., Zimmerman, G.A. and Weyrich, A.S. (2011) Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes. Blood 118, e101-e111
6. Burkhart, J.M., Vaudel, M., Gambaryan, S., Radau, S., Walter, U., Martens, L., Sickmann, A. and Zahedi, R.P. (2012) The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood 120, e73-e82
7. Taskén, K. and Aandahl, E.M. (2004) Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol. Rev. 84, 137-167 (Pubitemid 38049878)
8. Haslam, R.J., Dickinson, N.T. and Jang, E.K. (1999) Cyclic nucleotides and phosphodiesterases in platelets. Thromb. Haemost. 82, 412-423
9. Hunter, R.W., Mackintosh, C. and Hers, I. (2009) Protein kinase C-mediated phosphorylation and activation of PDE3A regulate cAMP levels in human platelets. J. Biol. Chem. 284, 12339-12348
10. Gorman, R.R., Bunting, S. and Miller, O.V. (1977) Modulation of human platelet adenylate cyclase by prostacyclin (PGX). Prostaglandins 13, 377-388 (Pubitemid 8076557)
11. Sim, D.S., Merrill-Skoloff, G., Furie, B.C., Furie, B. and Flaumenhaft, R. (2004) Initial accumulation of platelets during arterial thrombus formation in vivo is inhibited by elevation of basal cAMP levels. Blood 103, 2127-2134 (Pubitemid 38326229)
12. Bodnar, R.J., Xi, X., Li, Z., Berndt, M.C. and Du, X. (2002) Regulation of glycoprotein Ib-IX-von Willebrand factor interaction by cAMP-dependent protein kinase-mediated phosphorylation at Ser166 of glycoprotein Ibß. J. Biol. Chem. 277, 47080-47087 (Pubitemid 36159216)
13. Ichinohe, T., Takayama, H., Ezumi, Y., Yanagi, S., Yamamura, H. and Okuma, M. (1995) Cyclic AMP-insensitive activation of c-Src and Syk protein-tyrosine kinases through platelet membrane glycoprotein VI. J. Biol. Chem. 270, 28029-28036
14. Takayama, H., Hosaka, Y., Nakayama, K., Shirakawa, K., Naitoh, K., Matsusue, T., Shinozaki, M., Honda, M., Yatagai, Y., Kawahara, T. et al. (2008) A novel antiplatelet antibody therapy that induces cAMP-dependent endocytosis of the GPVI/Fc receptor γ-chain complex. J. Clin. Invest. 118, 1785-1795 (Pubitemid 351632381)
15. Loyau, S., Dumont, B., Ollivier, V., Boulaftali, Y., Feldman, L., Ajzenberg, N. and Jandrot-Perrus, M. (2012) Platelet glycoprotein VI dimerization, an active process inducing receptor competence, is an indicator of platelet reactivity. Arterioscler. Thromb. Vasc. Biol. 32, 778-785
16. Reid, H.M. and Kinsella, B.T. (2003) The α, but not the β, isoform of the human thromboxane A2 receptor is a target for nitric oxide-mediated desensitization: independent modulation of Tpα signaling by nitric oxide and prostacyclin. J. Biol. Chem. 278, 51190-51202
17. Manganello, J.M., Huang, J.-S., Kozasa, T., Voyno-Yasenetskaya, T.A. and Le Breton, G.C. (2003) Protein kinase A-mediated phosphorylation of the Gα13 switch I region alters the Gαβγ 13-G protein-coupled receptor complex and inhibits Rho activation. J. Biol. Chem. 278, 124-130
18. Aslan, J.E. and McCarty, O.J.T. (2013) Rho GTPases in platelet function. J. Thromb. Haemost. 11, 35-46
19. Chrzanowska-Wodnicka, M., Smyth, S.S., Schoenwaelder, S.M., Fischer, T.H. and White, G.C. (2005) Rap1b is required for normal platelet function and hemostasis in mice. J. Clin. Invest. 115, 680-687 (Pubitemid 40322242)
20. Schultess, J., Danielewski, O. and Smolenski, A.P. (2005) Rap1GAP2 is a new GTPase-activating protein of Rap1 expressed in human platelets. Blood 105, 3185-3192
21. Subramanian, H., Zahedi, R.P., Sickmann, A., Walter, U. and Gambaryan, S. (2013) Phosphorylation of CalDAG-GEFI by protein kinase A prevents Rap1b activation. J. Thromb. Haemost. 11, 1574-1582
22. Guidetti, G.F., Manganaro, D., Consonni, A., Canobbio, I., Balduini, C. and Torti, M. (2013) Phosphorylation of the guanine-nucleotide-exchange factor CalDAG-GEFI by protein kinase A regulates Ca2+-dependent activation of platelet Rap1b GTPase. Biochem. J. 453, 115-123
23. Lapetina, E.G., Lacal, J.C., Reep, B.R. and Molina y Vedia, L. (1989) A ras-related protein is phosphorylated and translocated by agonists that increase cAMP levels in human platelets. Proc. Natl. Acad. Sci. U.S.A. 86, 3131-3134 (Pubitemid 19129572)
24. Klages, B., Brandt, U., Simon, M.I., Schultz, G. and 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
25. Aburima, A., Wraith, K.S., Raslan, Z., Law, R., Magwenzi, S. and Naseem, K.M. (2013) cAMP signaling regulates platelet myosin light chain (MLC) phosphorylation and shape change through targeting the RhoA-Rho kinase-MLC phosphatase signaling pathway. Blood 122, 3533-3545
26. Gegenbauer, K., Elia, G., Blanco-Fernandez, A. and Smolenski, A. (2012) Regulator of G-protein signaling 18 integrates activating and inhibitory signaling in platelets. Blood 119, 3799-3807
27. Hartwig, J.H., Barkalow, K., Azim, A. and Italiano, J. (1999) The elegant platelet: signals controlling actin assembly. Thromb. Haemost. 82, 392-398
28. Beck, F., Geiger, J., Gambaryan, S., Veit, J., Vaudel, M., Nollau, P., Kohlbacher, O., Martens, L., Walter, U., Sickmann, A. and Zahedi, R.P. (2013) Time-resolved characterization of cAMP/PKA-dependent signaling reveals that platelet inhibition is a concerted process involving multiple signaling pathways. Blood, doi:10.1182/blood-2013-07-512384
29. Butt, E., Abel, K., Krieger, M., Palm, D., Hoppe, V., Hoppe, J. and Walter, U. (1994) cAMP- and cGMP-dependent protein kinase phosphorylation sites of the focal adhesion vasodilator-stimulated phosphoprotein (VASP) in vitro and in intact human platelets. J. Biol. Chem. 269, 14509-14517 (Pubitemid 24194005)
30. Butt, E., Immler, D., Meyer, H.E., Kotlyarov, A., Laass, K. and Gaestel, M. (2000) Heat shock protein 27 is a substrate of cGMP-dependent protein kinase in intact human platelets: phosphorylation-induced actin polymerization caused by Hsp27 mutants. J. Biol. Chem. 276, 7108-7113
31. Hettasch, J.M. and Sellers, J.R. (1991) Caldesmon phosphorylation in intact human platelets by cAMP-dependent protein kinase and protein kinase C. J. Biol. Chem. 266, 11876-11881 (Pubitemid 21907031)
32. Butt, E., Gambaryan, S., Göttfert, N., Galler, A., Marcus, K. and Meyer, H.E. (2003) Actin binding of human LIM and SH3 protein is regulated by cGMP- and cAMP-dependent protein kinase phosphorylation on serine 146. J. Biol. Chem. 278, 15601-15607 (Pubitemid 36799669)
33. Chen, M. and Stracher, A. (1989) In situ phosphorylation of platelet actin-binding protein by cAMP-dependent protein kinase stabilizes it against proteolysis by calpain. J. Biol. Chem. 264, 14282-14289 (Pubitemid 19214256)
34. Varga-Szabo, D., Braun, A. and Nieswandt, B. (2009) Calcium signaling in platelets. J. Thromb. Haemost. 7, 1057-1066
35. Geiger, J., Nolte, C. and Walter, U. (1994) Regulation of calcium mobilization and entry in human platelets by endothelium-derived factors. Am. J. Physiol. 267, C236-C244
36. el-Daher, S.S., Eigenthaler, M., Walter, U., Furuichi, T., Miyawaki, A., Mikoshiba, K., Kakkar, V.V. and Authi, K.S. (1996) Distribution and activation of cAMP- and cGMP-dependent protein kinases in highly purified human platelet plasma and intracellular membranes. Thromb. Haemost. 76, 1063-1071
37. Quinton, T.M. and Dean, W.L. (1992) Cyclic AMP-dependent phosphorylation of the inositol-1,4,5-trisphosphate receptor inhibits Ca2+ release from platelet membranes. Biochem. Biophys. Res. Commun. 184, 893-899
38. Hassock, S.R., Zhu, M.X., Trost, C., Flockerzi, V. and Authi, K.S. (2002) Expression and role of TRPC proteins in human platelets: evidence that TRPC6 forms the store-independent calcium entry channel. Blood 100, 2801-2811
39. Fung, C.Y.E., Jones, S., Ntrakwah, A., Naseem, K.M., Farndale, R.W. and Mahaut-Smith, M.P. (2012) Platelet Ca2+ responses coupled to glycoprotein VI and Toll-like receptors persist in the presence of endothelial-derived inhibitors: roles for secondary activation of P2X1 receptors and release from intracellular Ca2+ stores. Blood 119, 3613-3621
40. Hayes, J.S., Brunton, L.L. and Mayer, S.E. (1980) Selective activation of particulate cAMP-dependent protein kinase by isoproterenol and prostaglandin E1. J. Biol. Chem. 255, 5113-5119 (Pubitemid 10015830)
41. Carnegie, G.K., Means, C.K. and Scott, J.D. (2009) A-kinase anchoring proteins: from protein complexes to physiology and disease. IUBMB Life 61, 394-406
42. Di Benedetto, G., Zoccarato, A., Lissandron, V., Terrin, A., Li, X., Houslay, M.D., Baillie, G.S. and Zaccolo, M. (2008) Protein kinase A type I and type II define distinct intracellular signaling compartments. Circ. Res. 103, 836-844
43. Manns, J.M., Brenna, K.J., Colman, R.W. and Sheth, S.B. (2002) Differential regulation of human platelet responses by cGMP inhibited and stimulated cAMP phosphodiesterases. Thromb. Haemost. 87, 873-879 (Pubitemid 34516617)
44. Margarucci, L., Roest, M., Preisinger, C., Bleijerveld, O.B., van Holten, T.C., Heck, A.J.R. and Scholten, A. (2011) Collagen stimulation of platelets induces a rapid spatial response of cAMP and cGMP signaling scaffolds. Mol. Biosyst. 7, 2311-2319
45. Burgers, P.P., Ma, Y., Margarucci, L., Mackey, M., van der Heyden, M.A.G., Ellisman, M., Scholten, A., Taylor, S.S. and Heck, A.J.R. (2012) A small novel A-kinase anchoring protein (AKAP) that localizes specifically protein kinase A-regulatory subunit I (PKA-RI) to the plasma membrane. J. Biol. Chem. 287, 43789-43797