PKC inhibition markedly enhances Ca 2+ signaling and phosphatidylserine exposure downstream of protease-activated receptor-1 but not protease-activated receptor-4 in human platelets

Journal of Thrombosis and Haemostasis

Volumn 9, Issue 8, 2011, Pages 1599-1607

  Harper, Matthew T ^a   Poole, Alastair W ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Bisindolylmaleimide; Calcium entry; Plasma membrane calcium ATPase; Platelets; Protein kinases; Thrombin

Indexed keywords

BISINDOLYLMALEIMIDE; CALCIUM; LIPOCORTIN 5; MANGANESE; PHOSPHATIDYLSERINE; PROCOAGULANT; PROTEIN KINASE C; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 4; THROMBIN;

ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE; CONTROLLED STUDY; ENZYME INHIBITION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE FUNCTION; THROMBOGENESIS;

ANNEXIN A5; BLOOD PLATELETS; CALCIUM SIGNALING; DOSE-RESPONSE RELATIONSHIP, DRUG; FLOW CYTOMETRY; HUMANS; INDOLES; MALEIMIDES; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PHOSPHATIDYLSERINES; PLASMA MEMBRANE CALCIUM-TRANSPORTING ATPASES; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; RECEPTOR, PAR-1; RECEPTORS, THROMBIN; THROMBIN; TIME FACTORS;

EID: 80051585023     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2011.04393.x     Document Type: Article

References (42)

1. Harper MT, Poole AW. Diverse functions of protein kinase C isoforms in platelet activation and thrombus formation. J Thromb Haemost 2010; 8: 454-62.
2. Jackson SP, Nesbitt WS, Kulkarni S. Signaling events underlying thrombus formation. J Thromb Haemost 2003; 1: 1602-12.
3. Stefanini L, Bergmeier W. CalDAG-GEFI and platelet activation. Platelets 2010; 21: 239-43.
4. Strehl A, Munnix IC, Kuijpers MJ, van der Meijden PE, Cosemans JM, Feijge MA, Nieswandt B, Heemskerk JW. Dual role of platelet protein kinase C in thrombus formation: stimulation of pro-aggregatory and suppression of procoagulant activity in platelets. J Biol Chem 2007; 282: 7046-55.
5. Quinton TM, Kim S, Dangelmaier C, Dorsam RT, Jin J, Daniel JL, Kunapuli SP. Protein kinase C- and calcium-regulated pathways independently synergize with Gi pathways in agonist-induced fibrinogen receptor activation. Biochem J 2002; 368: 535-43.
6. Toullec D, Pianetti P, Coste H, Bellevergue P, Grand-Perret T, Ajakane M, Baudet V, Boissin P, Boursier E, Loriolle F, Duhamel L, Charon D, Kirilovsky J. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem 1991; 266: 15771-81.
7. King WG, Rittenhouse SE. Inhibition of protein kinase C by staurosporine promotes elevated accumulations of inositol trisphosphates and tetrakisphosphate in human platelets exposed to thrombin. J Biol Chem 1989; 264: 6070-4.
8. Varga-Szabo D, Pleines I, Nieswandt B. Cell adhesion mechanisms in platelets. Arterioscler Thromb Vasc Biol 2008; 28: 403-12.
9. Monroe DM, Hoffmann M. What does it take to make the perfect clot? Arterioscler Thromb Vasc Biol 2006; 26: 41-84.
10. Kuijpers MJ, Munnix IC, Cosemans JM, Vlijmen BV, Reutelingsperger CP, Egbrink MO, Heemskerk JW. Key role of platelet procoagulant activity in tissue factor-and collagen-dependent thrombus formation in arterioles and venules in vivo differential sensitivity to thrombin inhibition. Microcirculation 2008; 15: 269-82.
11. Williamson P, Bevers EM, Smeets EF, Comfurius P, Schlegel RA, Zwaal RF. Continuous analysis of the mechanism of activated transbilayer lipid movement in platelets. Biochemistry 1995; 34: 10448-85.
12. Rydel TJ, Yin M, Padmanabhan KP, Blankenship DT, Cardin AD, Correa PE, Fenton JW 2nd, Tulinsky A. Crystallographic structure of human gamma-thrombin. J Biol Chem 1994; 269: 22000-6.
13. Soslau G, Goldenberg SJ, Class R, Jameson B. Differential activation and inhibition of human platelet thrombin receptors by structurally distinct alpha-, beta- and gamma-thrombin. Platelets 2004; 15: 155-66.
14. Varga-Szabo D, Braun A, Nieswandt B. Calcium signaling in platelets. J Thromb Haemost 2009; 7: 1057-66.
15. Connolly TM, Lawing WJ Jr, Majerus PW. Protein kinase C phosphorylates human platelet inositol trisphosphate 5'-phosphomonoesterase, increasing the phosphatase activity. Cell 1986; 46: 951-8.
16. Oberdisse E, Nolan RD, Lapetina EG. Thrombin and phorbol ester stimulate inositol 1, 3, 4, 5-tetrakisphosphate 3-phosphomonoesterase in human platelets. J Biol Chem 1990; 265: 726-30.
17. 2+ efflux from fura-2-loaded platelets activated by thrombin or phorbol myristate acetate. FEBS Lett 1987; 210: 132-6.
18. Rink TJ, Sage SO. Stimulated calcium efflux from fura-2-loaded human platelets. J Physiol 1987; 393: 513-24.
19. Gilio K, Harper MT, Cosemans JM, Konopatskaya O, Munnix ICPL, Leitges M, Liu Q, Molkentin JD, Heemskerk JW, Poole AW. Functional divergence of platelet protein kinase C (PKC) isoforms in thrombus formation on collagen. J Biol Chem 2010; 285: 23410-9.
20. Rauch UOJ, Fuster V, Badimon JJ, Fayad Z, Chesebro JH. Thrombus formation on atherosclerotic plaques: pathogenesis and clinical consequences. Ann Intern Med 2001; 134: 224-38.
21. Soltoff SP. Rottlerin: an inappropriate and ineffective inhibitor of PKCdelta. Trends Pharmacol Sci 2007; 28: 453-8.
22. Coughlin SR. Protease-activated receptors in hemostasis, thrombosis and vascular biology. J Thromb Haemost 2005; 3: 1800-14.
23. 12 receptor activation. J Biol Chem 2006; 281: 26665-74.
24. Adam F, Verbeuren TJ, Fauchère JL, Guillin MC, Jandrot-Perrus M. Thrombin-induced platelet PAR4 activation: role of glycoprotein Ib and ADP. J Thromb Haemost 2003; 1: 798-804.
25. 12/phosphatidylinositol 3-kinase pathway in maintaining thrombin-induced platelet aggregation. Br J Pharmacol 2010; 161: 643-58.
26. Getz TM, Mayanglambam A, Daniel JL, Kunapuli SP. Go6976 abrogates GPVI-mediated platelet functional responses in human platelets through inhibition of Syk. J Thromb Haemost 2011; 9: 608-10.
27. Arora P, Ricks TK, Trejo J. Protease-activated receptor signaling, endocytic sorting and dysregulation in cancer. J Cell Sci 2007; 120: 921-8.
28. Shapiro MJ, Weiss EJ, Faruqi TR, Coughlin SR. Protease-activated receptors 1 and 4 are shut off with distinct kinetics after activation by thrombin. J Biol Chem 2000; 275: 25216-21.
29. Yoshida K, Nachmias VT. Phorbol ester stimulates calcium sequestration in saponized human platelets. J Biol Chem 1987; 262: 16048-54.
30. 2+-ATPase pump: stimulation by phorbol ester, inhibition by calphostin C. Biochim Biophys Acta 1992; 1107: 213-22.
31. 2+ pump in cultured vascular smooth muscle cells. J Biol Chem 1989; 264: 4844-9.
32. Balasubramanyam M, Gardner JP. Protein kinase C modulates cytosolic free calcium by stimulating calcium pump activity in Jurkat T cells. Cell Calcium 1995; 18: 526-41.
33. 2+ pump isoform 4b by phosphorylation of an inhibitory region downstream of the calmodulin-binding domain. J Biol Chem 1996; 271: 32461-7.
34. 1 ion channel in platelet function. Platelets 2010; 21: 153-66.
35. Parekh AB, Putney JW Jr. Store-operated calcium channels. Phyiol Rev 2005; 85: 757-810.
36. Harper MT, Molkentin JD, Poole AW. Protein kinase C alpha enhances sodium-calcium exchange during store-operated calcium entry in mouse platelets. Cell Calcium 2010; 48: 333-40.
37. src activation in human platelets: evidence for the involvement of this pathway in store-mediated calcium entry. J Biol Chem 2004; 279: 1665-75.
38. 2+ entry in human platelets. J Thromb Haemost 2006; 4: 2695-703.
39. Hassock SR, Zhu MX, Trost C, Flockerzi V, Authi KS. Expression and role of TRPC proteins in human platelets: evidence that TRPC6 forms the store-independent calcium entry channel. Blood 2002; 100: 2801-11.
40. Rosado JA, Sage SO. Protein kinase C activates non-capacitative calcium entry in human platelets. J Physiol 2000; 529: 159-69.
41. Harper MT, Sage SO. Src family tyrosine kinases activate thrombin-induced non-capacitative cation entry in human platelets. Platelets 2010; 21: 1604-13.
42. 2+ entry and phosphatidylserine exposure downstream of glycoprotein VI in platelets. J Biol Chem 2010; 285: 19865-73.