Early intraplatelet signaling enhances the release of human platelet PAR-1 and -4 amino-terminal peptides in response to thrombin

Biochemistry

Volumn 48, Issue 7, 2009, Pages 1562-1572

  Ofosu, Frederick A ^a,b   Dewar, Lori ^b   Song, Yingqi ^a   Cedrone, Aisha C ^a   Hortelano, Gonzalo ^a,b   Craven, Sharon J ^b  

^a MCMASTER UNIVERSITY   (Canada)

^b CANADIAN BLOOD SERVICES   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EXTRACELLULAR DOMAINS; FORSKOLIN; PHOSPHORYLATION REACTIONS; PLATELET AGGREGATIONS; PLATELET RESPONSE; SIGNALING PATHWAYS; SOYBEAN TRYPSIN INHIBITORS;

AMINATION; AMINES; BLOOD SUBSTITUTES; PEPTIDES; SIGNALING;

PLATELETS;

ADENOSINE TRIPHOSPHATE; FORSKOLIN; PROTEINASE; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 4; THROMBIN; PROTEASE-ACTIVATED RECEPTOR 4; THROMBIN RECEPTOR;

AMINO TERMINAL SEQUENCE; ARTICLE; CATALYST; ENZYME ACTIVITY; HUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; THROMBOCYTE AGGREGATION; THROMBOCYTE RELEASE REACTION; BIOCATALYSIS; CHEMISTRY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; METABOLISM; SIGNAL TRANSDUCTION; THROMBOCYTE;

BIOCATALYSIS; BLOOD PLATELETS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; PHOSPHORYLATION; RECEPTOR, PAR-1; RECEPTORS, THROMBIN; SIGNAL TRANSDUCTION; THROMBIN;

GLYCINE MAX;

EID: 61749084117     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801399c     Document Type: Article

References (69)

1. Ofosu, F. A., Freedman, J., Dewar, L., Song, Y., and Fenton, J. W. (1998) A trypsin-like platelet protease propagates protease-activated receptor-1 cleavage and platelet activation. Biochem. J. 336 (Part 2), 283-285.
2. Ofosu, F. A., Dewar, L., Craven, S. J., Song, Y., Cedrone, A., Freedman, J., and Fenton, J. W. (2008) Coordinate activation of human platelet protease-activated receptor-1 and -4 in response to subnanomolar alpha-thrombin. J. Biol. Chem. 283, 26886-26893.
3. Feeney, R. E., Means, G. E., and Bigler, J. C. (1969) Inhibition of human trypsin, plasmin, and thrombin by naturally occurring inhibitors of proteolytic enzymes. J. Biol. Chem. 244, 1957-1960.
4. Bernatowicz, M. S., Klimas, C. E., Hartl, K. S., Peluso, M., Allegretto, N. J., and Seiler, S. M. (1996) Development of potent thrombin receptor antagonist peptides. J. Med. Chem. 39, 4879-4887.
5. Wu, C. C., Hwang, T. L., Liao, C. H., Kuo, S. C., Lee, F. Y., Lee, C. Y., and Teng, C. M. (2002) Selective inhibition of proteaseactivated receptor 4-dependent platelet activation by YD-3. Thromb. Haemostasis 87, 1026-1033.
6. Day, J. R., Punjabi, P. P., Randi, A. M., Haskard, D. O., Landis, R. C., and Taylor, K. M. (2004) Clinical inhibition of the seventransmembrane thrombin receptor (PAR1) by intravenous aprotinin during cardiothoracic surgery. Circulation 110, 2597-2600.
7. Poullis, M., Manning, R., Laffan, M., Haskard, D. O., Taylor, K. M., and Landis, R. C. (2000) The antithrombotic effect of aprotinin: actions mediated via the proteaseactivated receptor 1. J. Thorac. Cardiovasc. Surg. 120, 370-378.
8. Bilodeau, M. L., and Hamm, H. E. (2007) Regulation of proteaseactivated receptor (PAR) 1 and PAR4 signaling in human platelets by compartmentalized cyclic nucleotide actions. J. Pharmacol. Exp. Ther. 322, 778-788.
9. Laurenza, A., Sutkowski, E. M., and Seamon, K. B. (1989) Forskolin: a specific stimulator of adenylyl cyclase or a diterpene with multiple sites of action? Trends Pharmacol. Sci. 10, 442-447.
10. Seamon, K. B., and Daly, J. W. (1981) Forskolin: a unique diterpene activator of cyclic AMP-generating systems. J. Cyclic Nucleotide Res. 7, 201-224.
11. Feijge, M. A., Ansink, K., Vanschoonbeek, K., and Heemskerk, J. W. (2004) Control of platelet activation by cyclic AMP turnover and cyclic nucleotide phosphodiesterase type-3. Biochem. Pharmacol. 67, 1559-1567.
12. Bit, R. A., Davis, P. D., Elliott, L. H., Harris, W., Hill, C. H., Keech, E., Kumar, H., Lawton, G., Maw, A., Nixon, J. S., et al. (1993) Inhibitors of protein kinase C. 3. Potent and highly selective bisindolylmaleimides by conformational restriction. J. Med. Chem. 36, 21-29.
13. Davis, P. D., Elliott, L. H., Harris, W., Hill, C. H., Hurst, S. A., Keech, E., Kumar, M. K., Lawton, G., Nixon, J. S., and Wilkinson, S. E. (1992) Inhibitors of protein kinase C. 2. Substituted bisindolylmaleimides with improved potency and selectivity. J. Med. Chem. 35, 994-1001.
14. Bleasdale, J. E., Thakur, N. R., Gremban, R. S., Bundy, G. L., Fitzpatrick, F. A., Smith, R. J., and Bunting, S. (1990) Selective inhibition of receptor-coupled phospholipase C-dependent processes in human platelets and polymorphonuclear neutrophils. J. Pharmacol. Exp. Ther. 255, 756-768.
15. Lockhart, L. K., and McNicol, A. (1999) The phospholipase C inhibitor U73122 inhibits phorbol ester-induced platelet activation. J. Pharmacol. Exp. Ther. 289, 721-728.
16. Vlahos, C. J., Matter, W. F., Hui, K. Y., and Brown, R. F. (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-mor-pholinyl)-8- phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248.
17. Yano, H., Agatsuma, T., Nakanishi, S., Saitoh, Y., Fukui, Y., Nonomura, Y., and Matsuda, Y. (1995) Biochemical and pharmacological studies with KT7692 and LY294002 on the role of phosphatidylinositol 3-kinase in Fc epsilon RI-mediated signal transduction. Biochem. J. 312 (Part 1), 145-150.
18. Liu, L., Freedman, J., Hornstein, A., Fenton, J. W., II, Song, Y., and Ofosu, F. A. (1997) Binding of thrombin to the G-protein-linked receptor, and not to glycoprotein Ib, precedes thrombinmediated platelet activation. J. Biol. Chem. 272, 1997-2004.
19. Faruqi, T. R., Weiss, E. J., Shapiro, M. J., Huang, W., and Coughlin, S. R. (2000) Structure-function analysis of proteaseactivated receptor 4 tethered ligand peptides. Determinants of specificity and utility in assays of receptor function. J. Biol. Chem. 275, 19728-19734.
20. Fenton, J. W., II, Fasco, M. J., and Stackrow, A. B. (1977) Human thrombins. Production, evaluation, and properties of alphathrombin. J. Biol. Chem. 252, 3587-3598.
21. Mustard, J. F., Perry, D. W., Ardlie, N. G., and Packham, M. A. (1972) Preparation of suspensions of washed platelets from humans. Br. J. Haematol. 22, 193-204.
22. Liu, L., Freedman, J., Hornstein, A., Fenton, J. W., II, and Ofosu, F. A. (1994) Thrombin binding to platelets and their activation in plasma. Br. J. Haematol. 88, 592-600.
23. Niewiarowski, S., and Holt, J. C. (1985) Platelet alpha-Granule Proteins: Biochemical and Pathological Aspects, Academic Press, Orlando, FL.
24. 2+ Indicators, in Cellular Calcium. A Practical Approach (McCormack, J. G., and Cobbold, P. H., Eds.) Oxford Press, New York.
25. Brass, L. F., Vassallo, R. R., Jr., Belmonte, E., Ahuja, M., Cichowski, K., and Hoxie, J. A. (1992) Structure and function of the human platelet thrombin receptor. Studies using monoclonal antibodies directed against a defined domain within the receptor N terminus. J. Biol. Chem. 267, 13795-13798.
26. Hollenberg, M. D., Saifeddine, M., Sandhu, S., Houle, S., and Vergnolle, N. (2004) Proteinase-activated receptor-4: evaluation of tethered ligand-derived peptides as probes for receptor function and as inflammatory agonists in vivo. Br. J. Pharmacol. 143, 443-454.
27. Strande, J. L., Hsu, A., Su, J., Fu, X., Gross, G. J., and Baker, J. E. (2008) Inhibiting protease-activated receptor 4 limits myocardial ischemia/reperfusion injury in rat hearts by unmasking adenosine signaling. J. Pharmacol. Exp. Ther. 324, 1045-1054.
28. 2+ entry by protein kinase C beta. J. Biol. Chem. 270, 23887-23890.
29. Brass, L. F., Pizarro, S., Ahuja, M., Belmonte, E., Blanchard, N., Stadel, J. M., and Hoxie, J. A. (1994) Changes in the structure and function of the human thrombin receptor during receptor activation, internalization, and recycling. J. Biol. Chem. 269, 2943-2952.
30. Coughlin, S. R. (2005) Protease-activated receptors in hemostasis, thrombosis and vascular biology. J. Thromb. Haemostasis 3, 1800-1814.
31. Woulfe, D. S. (2005) Platelet G protein-coupled receptors in hemostasis and thrombosis. J. Thromb. Haemostasis 3, 2193-2200.
32. Vassallo, R. R., Kieber-Emmons, T., Cichowski, K., and Brass, L. F. (1992) Structure-function relationships in the activation of platelet thrombin receptors by receptor-derived peptides. J. Biol. Chem. 267, 6081-6085.
33. Vu, T. K., Wheaton, V. I., Hung, D. T., Charo, I., and Coughlin, S. R. (1991) Domains specifying thrombin-receptor interaction. Nature 353, 674-677.
34. 2+ mobilization. FEBS Lett. 288, 123-128.
35. Boire, A., Covic, L., Agarwal, A., Jacques, S., Sherifi, S., and Kuliopulos, A. (2005) PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 120, 303-313.
36. Sambrano, G. R., Huang, W., Faruqi, T., Mahrus, S., Craik, C., and Coughlin, S. R. (2000) Cathepsin G activates protease-activated receptor-4 in human platelets. J. Biol. Chem. 275, 6819-6823.
37. Hung, D. T., Wong, Y. H., Vu, T. K., and Coughlin, S. R. (1992) The cloned platelet thrombin receptor couples to at least two distinct effectors to stimulate phosphoinositide hydrolysis and inhibit adenylyl cyclase. J. Biol. Chem. 267, 20831-20834.
38. Quinton, T. M., Murugappan, S., Kim, S., Jin, J., and Kunapuli, S. P. (2004) Different G protein-coupled signaling pathways are involved in alpha granule release from human platelets. J. Thromb. Haemostasis 2, 978-984.
39. Yang, J., Wu, J., Jiang, H., Mortensen, R., Austin, S., Manning, D. R., Woulfe, D., and Brass, L. F. (2002) Signaling through Gi family members in platelets. Redundancy and specificity in the regulation of adenylyl cyclase and other effectors. J. Biol. Chem. 277, 46035-46042.
40. Abrams, C. S. (2005) Intracellular signaling in platelets. Curr. Opin. Hematol. 12, 401-405.
41. Ryningen, A., Olav Jensen, B., and Holmsen, H. (1998) Elevation of cyclic AMP decreases phosphoinositide turnover and inhibits thrombin-induced secretion in human platelets. Biochim. Biophys. Acta 1394, 235-248.
42. Gachet, C. (2006) Regulation of platelet functions by P2 receptors. Annu. Rev. Pharmacol. Toxicol. 46, 277-300.
43. Sun, D. S., Lo, S. J., Tsai, W. J., Lin, C. H., Yu, M. S., Chen, Y. F., and Chang, H. H. (2005) PI3-kinase is essential for ADP-stimulated integrin alpha(IIb)beta3-mediated platelet calcium oscillation, implications for P2Y receptor pathways in integrin alpha(I-Ib)beta3-initiated signaling cross-talks. J. Biomed. Sci. 12, 937-948.
44. Mahaut-Smith, M. P., Tolhurst, G., and Evans, R. J. (2004) Emerging roles for P2X1 receptors in platelet activation. Platelets 15, 131-144.
45. Erhardt, J. A., Toomey, J. R., Douglas, S. A., and Johns, D. G. (2006) P2X1 stimulation promotes thrombin receptor-mediated platelet aggregation. J. Thromb. Haemostasis 4, 882-890.
46. Rolf, M. G., Brearley, C. A., and Mahaut-Smith, M. P. (2001) Platelet shape change evoked by selective activation of P2X1 purinoceptors with alpha,beta-methylene ATP. Thromb. Haemostasis 85, 303-308.
47. Gachet, C. (2008) P2 receptors, platelet function and pharmacological implications. Thromb. Haemostasis 99, 466-472.
48. Fung, C. Y., Cendana, C., Farndale, R. W., and Mahaut-Smith, M. P. (2007) Primary and secondary agonists can use P2X(1) receptors as a major pathway to increase intracellular Ca(2+) in the human platelet. J. Thromb. Haemostasis 5, 910-917.
49. Clapham, D. E., and Neer, E. J. (1997) G protein beta gamma subunits. Annu. Rev. Pharmacol. Toxicol. 37, 167-203.
50. Grenegard, M., Vretenbrant-Oberg, K., Nylander, M., Desilets, S., Lindstrom, E. G., Larsson, A., Ramstrom, I., Ramstrom, S., and Lindahl, T. L. (2008) The ATP-gated P2X1 receptor plays a pivotal role in activation of aspirin-treated platelets by thrombin and epinephrine. J. Biol. Chem. 283, 18493-18504.
51. Jackson, S. P., Yap, C. L., and Anderson, K. E. (2004) Phosphoinositide 3-kinases and the regulation of platelet function. Biochem. Soc. Trans. 32, 387-392.
52. Seiler, S. M., Goldenberg, H. J., Michel, I. M., Hunt, J. T., and Zavoico, G. B. (1991) Multiple pathways of thrombin-induced platelet activation differentiated by desensitization and a thrombin exosite inhibitor. Biochem. Biophys. Res. Commun. 181, 636-643.
53. Vu, T. K., Hung, D. T., Wheaton, V. I., and Coughlin, S. R. (1991) Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64, 1057-1068.
54. Jakobs, K. H., and Aktories, K. (1988) Stimulation of high-affinity GTPase by trypsin and trypsin-like proteinases in membranes of human platelets. Biochem. J. 249, 639-643.
55. Jakobs, K. H., and Grandt, R. (1988) Thrombin-like inhibitory action of trypsin and trypsin-like proteases on human platelet adenylate cyclase. Eur. J. Biochem. 172, 255-260.
56. Grandt, R., Aktories, K., and Jakobs, K. H. (1986) Evidence for two GTPases activated by thrombin in membranes of human platelets. Biochem. J. 237, 669-674.
57. Aktories, K., and Jakobs, K. H. (1984) Ni-mediated inhibition of human platelet adenylate cyclase by thrombin. Eur. J. Biochem. 145, 333-338.
58. Houslay, M. D., Bojanic, D., Gawler, D., O'Hagan, S., and Wilson, A. (1986) Thrombin, unlike vasopressin, appears to stimulate two distinct guanine nucleotide regulatory proteins in human platelets. Biochem. J. 238, 109-113.
59. Leger, A. J., Jacques, S. L., Badar, J., Kaneider, N. C., Derian, C. K., Andrade-Gordon, P., Covic, L., and Kuliopulos, A. (2006) Blocking the protease-activated receptor 1-4 heterodimer in platelet-mediated thrombosis. Circulation 113, 1244-1254.
60. Furman, M. I., Nurden, P., Berndt, M. C., Nurden, A. T., Benoit, S. E., Barnard, M. R., Ofosu, F. A., and Michelson, A. D. (2000) The cleaved peptide of PAR1 results in a redistribution of the platelet surface GPIb-IX-V complex to the surface-connected canalicular system. Thromb. Haemostasis 84, 897-903.
61. Xu, W. F., Andersen, H., Whitmore, T. E., Presnell, S. R., Yee, D. P., Ching, A., Gilbert, T., Davie, E. W., and Foster, D. C. (1998) Cloning and characterization of human protease-activated receptor 4. Proc. Natl. Acad. Sci. U.S.A. 95, 6642-6646.
62. Feng, W. M., Bao, Y., Fei, M. Y., Chen, Q. Q., Yang, Q., and Dai, C. (2003) Platelet activation and the protective effect of aprotinin in hepatolithiasis patients. Hepatobiliary Pancreat. Dis. Int. 2, 602-604.
63. Landis, R. C., Haskard, D. O., and Taylor, K. M. (2001) New antiinflammatory and platelet-preserving effects of aprotinin. Ann. Thorac. Surg. 72, S1808-1813.
64. Choi, W. S., Jeon, O. H., Kim, H. H., and Kim, D. S. (2008) MMP-2 regulates human platelet activation by interacting with integrin alphaIIbbeta3. J. Thromb. Haemostasis 6, 517-523.
65. Sawicki, G., Salas, E., Murat, J., Miszta-Lane, H., and Radomski, M. W. (1997) Release of gelatinase A during platelet activation mediates aggregation. Nature 386, 616-619.
66. 2+ responses and platelet aggregation by the P2Y12 receptor antagonists AR-C69931MX and clopidogrel is enhanced by prostaglandin E1. Cqell Calcium 35, 39-46.
67. Rosado, J. A., Porras, T., Conde, M., and Sage, S. O. (2001) Cyclic nucleotides modulate store-mediated calcium entry through the activation of protein-tyrosine phosphatases and altered actin polymerization in human platelets. J. Biol. Chem. 276, 15666-15675.
68. Davie, E. W. (2003) A brief historical review of the waterfall/ cascade of blood coagulation. J. Biol. Chem. 278, 50819-50832.
69. Piccini, A., Carta, S., Tassi, S., Lasiglie, D., Fossati, G., and Rubartelli, A. (2008) ATP is released by monocytes stimulated with pathogen-sensing receptor ligands and induces IL-1beta and IL-18 secretion in an autocrine way. Proc. Natl. Acad. Sci. U.S.A. 105, 8067-8072.