Protease-activated receptor (PAR) 1 and PAR4 differentially regulate factor V expression from human platelets

Molecular Pharmacology

Volumn 83, Issue 4, 2013, Pages 781-792

  Duvernay, Matthew ^a   Young, Summer ^a   Gailani, David ^a,b   Schoenecker, Jonathan ^a,b   Hamm, Heidi ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 5; MYOSIN LIGHT CHAIN; PROCOAGULANT; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 4; RHO KINASE;

ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; PLATELET MICROPARTICLE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; THROMBOCYTE; THROMBOCYTE MEMBRANE; WESTERN BLOTTING;

BLOOD PLATELETS; FACTOR V; GENE EXPRESSION REGULATION; HUMANS; RECEPTOR, PAR-1; RECEPTORS, THROMBIN; THROMBIN;

EID: 84875410453     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.083477     Document Type: Article

References (59)

1. Alberio L, Safa O, Clemetson KJ, Esmon CT, and Dale GL (2000) Surface expression and functional characterization of alpha-granule factor V in human platelets: effects of ionophore A23187, thrombin, collagen, and convulxin. Blood 95:1694-1702.
2. Bilodeau ML and Hamm HE (2007) Regulation of protease-activated receptor (PAR) 1 and PAR4 signaling in human platelets by compartmentalized cyclic nucleotide actions. J Pharmacol Exp Ther 322:778-788.
3. Cohen Z, Gonzales RF, Davis-Gorman GF, Copeland JG, and McDonagh PF (2002) Thrombin activity and platelet microparticle formation are increased in type 2 diabetic platelets: a potential correlation with caspase activation. Thromb Res 107:217-221.
4. Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, and Olson MF (2001) Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat Cell Biol 3:339-345.
5. Connor DE, Exner T, Ma DD, and Joseph JE (2010) The majority of circulating platelet-derived microparticles fail to bind annexin V, lack phospholipid-dependent procoagulant activity and demonstrate greater expression of glycoprotein Ib. Thromb Haemost 103:1044-1052.
6. Coughlin SR (2000) Thrombin signalling and protease-activated receptors. Nature 407:258-264.
7. Covic L, Gresser AL, and Kuliopulos A (2000) Biphasic kinetics of activation and signaling for PAR1 and PAR4 thrombin receptors in platelets. Biochemistry 39: 5458-5467.
8. De Smedt E, Al Dieri R, Spronk HM, Hamulyak K, ten Cate H, and Hemker HC (2008) The technique of measuring thrombin generation with fluorogenic substrates: 1. Necessity of adequate calibration. Thromb Haemost 100:343-349.
9. Diamandis M, Veljkovic DK, Maurer-Spurej E, Rivard GE, and Hayward CP (2008) Quebec platelet disorder: features, pathogenesis and treatment. Blood Coagul Fibrinolysis 19:109-119.
10. Diamant M, Nieuwland R, Pablo RF, Sturk A, Smit JW, and Radder JK (2002) Elevated numbers of tissue-factor exposing microparticles correlate with components of the metabolic syndrome in uncomplicated type 2 diabetes mellitus. Circulation 106:2442-2447.
11. Diehl P, Nagy F, Sossong V, Helbing T, Beyersdorf F, Olschewski M, Bode C, and Moser M (2008) Increased levels of circulating microparticles in patients with severe aortic valve stenosis. Thromb Haemost 99:711-719.
12. Duckers C, Simioni P, Spiezia L, Radu C, Dabrilli P, Gavasso S, Rosing J, and Castoldi E (2010) Residual platelet factor V ensures thrombin generation in patients with severe congenital factor V deficiency and mild bleeding symptoms. Blood 115:879-886.
13. Fälker K, Haglund L, Gunnarsson P, Nylander M, Lindahl TL, and Grenegård M (2011) Protease-activated receptor 1 (PAR1) signalling desensitization is counteracted via PAR4 signalling in human platelets. Biochem J 436:469-480.
14. Faruqi TR,Weiss EJ, ShapiroMJ, Huang W, and Coughlin SR (2000) Structure-function analysis of protease-activated receptor 4 tethered ligand peptides. Determinants of specificity and utility in assays of receptor function. J Biol Chem 275:19728-19734.
15. Flaumenhaft R, Dilks JR, Richardson J, Alden E, Patel-Hett SR, Battinelli E, Klement GL, Sola-Visner M, and Italiano JE, Jr (2009) Megakaryocyte-derived microparticles: direct visualization and distinction from platelet-derived microparticles. Blood 113:1112-1121.
16. Flaumenhaft R, Mairuhu AT, and Italiano JE (2010) Platelet- and megakaryocytederived microparticles. Semin Thromb Hemost 36:881-887.
17. Gabbeta J, Yang X, Kowalska MA, Sun L, Dhanasekaran N, and Rao AK (1997) Platelet signal transduction defect with Galpha subunit dysfunction and diminished Galphaq in a patient with abnormal platelet responses. Proc Natl Acad Sci USA 94:8750-8755.
18. Getz TM, Dangelmaier CA, Jin J, Daniel JL, and Kunapuli SP (2010) Differential phosphorylation of myosin light chain (Thr)18 and (Ser)19 and functional implications in platelets. J Thromb Haemost 8:2283-2293.
19. Gilbert GE, Sims PJ, Wiedmer T, Furie B, Furie BC, and Shattil SJ (1991) Plateletderived microparticles express high affinity receptors for factor VIII. J Biol Chem 266:17261-17268.
20. Grigg AP, Dauer R, and Thurlow PJ (1989) Bleeding due to an acquired inhibitor of platelet associated factor V. Aust N Z J Med 19:310-314.
21. Hammes SR and Coughlin SR (1999) Protease-activated receptor-1 can mediate responses to SFLLRN in thrombin-desensitized cells: evidence for a novel mechanism for preventing or terminating signaling by PAR1's tethered ligand. Biochemistry 38:2486-2493.
22. Harper MT and Poole AW (2011) PKC inhibition markedly enhances Ca2+ signaling and phosphatidylserine exposure downstream of protease-activated receptor-1 but not protease-activated receptor-4 in human platelets. J Thromb Haemost 9:1599-1607.
23. Hemker HC, Giesen P, Al Dieri R, Regnault V, de Smedt E, Wagenvoord R, Lecompte T, and Béguin S (2003) Calibrated automated thrombin generation measurement in clotting plasma. Pathophysiol Haemost Thromb 33:4-15.
24. Hoffman M, Monroe DM, and Roberts HR (1992a) Coagulation factor IXa binding to activated platelets and platelet-derived microparticles: a flow cytometric study. Thromb Haemost 68:74-78.
25. Hoffman M, Monroe DM, and Roberts HR (1992b) A rapid method to isolate platelets from human blood by density gradient centrifugation. Am J Clin Pathol 98: 531-533.
26. Holinstat M, Preininger AM, Milne SB, Hudson WJ, Brown HA, and Hamm HE (2009) Irreversible platelet activation requires protease-activated receptor 1-mediated signaling to phosphatidylinositol phosphates. Mol Pharmacol 76: 301-313.
27. Holinstat M, Voss B, Bilodeau ML, and Hamm HE (2007) Protease-activated receptors differentially regulate human platelet activation through a phosphatidic acid-dependent pathway. Mol Pharmacol 71:686-694.
28. Holinstat M, Voss B, Bilodeau ML, McLaughlin JN, Cleator J, and Hamm HE (2006) PAR4, but not PAR1, signals human platelet aggregation via Ca2+ mobilization and synergistic P2Y12 receptor activation. J Biol Chem 281:26665-26674.
29. Italiano JE, Jr, Mairuhu AT, and Flaumenhaft R (2010) Clinical relevance of microparticles from platelets and megakaryocytes. Curr Opin Hematol 17:578-584.
30. Jin J, Mao Y, Thomas D, Kim S, Daniel JL, and Kunapuli SP (2009) RhoA downstream of G(q) and G(12/13) pathways regulates protease-activated receptormediated dense granule release in platelets. Biochem Pharmacol 77:835-844.
31. Koga H, Sugiyama S, Kugiyama K, Fukushima H, Watanabe K, Sakamoto T, Yoshimura M, Jinnouchi H, and Ogawa H (2006) Elevated levels of remnant lipoproteins are associated with plasma platelet microparticles in patients with type-2 diabetes mellitus without obstructive coronary artery disease. Eur Heart J 27:817-823.
32. Liu LW, Vu TK, Esmon CT, and Coughlin SR (1991) The region of the thrombin receptor resembling hirudin binds to thrombin and alters enzyme specificity. J Biol Chem 266:16977-16980.
33. Ma L, Perini R, McKnight W, Dicay M, Klein A, Hollenberg MD, and Wallace JL (2005) Proteinase-activated receptors 1 and 4 counter-regulate endostatin and VEGF release from human platelets. Proc Natl Acad Sci USA 102:216-220.
34. Mallat Z, Benamer H, Hugel B, Benessiano J, Steg PG, Freyssinet JM, and Tedgui A (2000) Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation 101:841-843.
35. Moers A, Nieswandt B, Massberg S, Wettschureck N, Grüner S, Konrad I, Schulte V, Aktas B, Gratacap MP, and Simon MI et al. (2003) G13 is an essential mediator of platelet activation in hemostasis and thrombosis. Nat Med 9:1418-1422.
36. Monković DD and Tracy PB (1990) Functional characterization of human platelet-released factor V and its activation by factor Xa and thrombin. J Biol Chem 265: 17132-17140.
37. Monroe DM, Hoffman M, and Roberts HR (2002) Platelets and thrombin generation. Arterioscler Thromb Vasc Biol 22:1381-1389.
38. Nesheim ME, Nichols WL, Cole TL, Houston JG, Schenk RB, Mann KG, and Bowie EJ (1986) Isolation and study of an acquired inhibitor of human coagulation factor V. J Clin Invest 77:405-415.
39. Nomura S, Suzuki M, Katsura K, Xie GL, Miyazaki Y, Miyake T, Kido H, Kagawa H, and Fukuhara S (1995) Platelet-derived microparticles may influence the development of atherosclerosis in diabetes mellitus. Atherosclerosis 116:235-240.
40. O'Connell DJ, Rozenvayn N, and Flaumenhaft R (2005) Phosphatidylinositol 4,5-bisphosphate regulates activation-induced platelet microparticle formation. Biochemistry 44:6361-6370.
41. Offermanns S, Toombs CF, Hu YH, and Simon MI (1997) Defective platelet activation in G alpha(q)-deficient mice. Nature 389:183-186.
42. Ofosu FA, Dewar L, Craven SJ, Song Y, Cedrone A, Freedman J, and Fenton JW, 2nd (2008) Coordinate activation of human platelet protease-activated receptor-1 and -4 in response to subnanomolar alpha-thrombin. J Biol Chem 283:26886-26893.
43. Pleines I, Hagedorn I, Gupta S, May F, Chakarova L, van Hengel J, Offermanns S, Krohne G, Kleinschnitz C, and Brakebusch C et al. (2012) Megakaryocyte-specific RhoA deficiency causes macrothrombocytopenia and defective platelet activation in hemostasis and thrombosis. Blood 119:1054-1063.
44. Preston RA, Jy W, Jimenez JJ, Mauro LM, Horstman LL, Valle M, Aime G, and Ahn YS (2003) Effects of severe hypertension on endothelial and platelet microparticles. Hypertension 41:211-217.
45. Sims PJ, Faioni EM, Wiedmer T, and Shattil SJ (1988) Complement proteins C5b-9 cause release of membrane vesicles from the platelet surface that are enriched in the membrane receptor for coagulation factor Va and express prothrombinase activity. J Biol Chem 263:18205-18212.
46. Sims PJ, Wiedmer T, Esmon CT, Weiss HJ, and Shattil SJ (1989) Assembly of the platelet prothrombinase complex is linked to vesiculation of the platelet plasma membrane. Studies in Scott syndrome: an isolated defect in platelet procoagulant activity. J Biol Chem 264:17049-17057.
47. Tan KT and Lip GY (2005) The potential role of platelet microparticles in atherosclerosis. Thromb Haemost 94:488-492.
48. Tan KT, Tayebjee MH, Lim HS, and Lip GY (2005) Clinically apparent atherosclerotic disease in diabetes is associated with an increase in platelet microparticle levels. Diabet Med 22:1657-1662.
49. Tracy PB, Giles AR, Mann KG, Eide LL, Hoogendoorn H, and Rivard GE (1984) Factor V (Quebec): a bleeding diathesis associated with a qualitative platelet Factor V deficiency. J Clin Invest 74:1221-1228.
50. Tricoci P, Huang Z, Held C, Moliterno DJ, Armstrong PW, Van De Werf F, White HD, Aylward PE, Wallentin L, and Chen E et al. (2012) Thrombin-receptor antagonist vorapaxar in acute coronary syndromes. N Engl J Med 366:20-33.
51. van der Zee PM, Biró E, Ko Y, de Winter RJ, Hack CE, Sturk A, and Nieuwland R (2006) P-selectin- and CD63-exposing platelet microparticles reflect platelet activation in peripheral arterial disease and myocardial infarction. Clin Chem 52:657-664.
52. Voss B, McLaughlin JN, Holinstat M, Zent R, and Hamm HE (2007) PAR1, but not PAR4, activates human platelets through a Gi/o/phosphoinositide-3 kinase signaling axis. Mol Pharmacol 71:1399-1406.
53. Vretenbrant K, Ramström S, Bjerke M, and Lindahl TL (2007) Platelet activation via PAR4 is involved in the initiation of thrombin generation and in clot elasticity development. Thromb Haemost 97:417-424.
54. Vu TK, Wheaton VI, Hung DT, Charo I, and Coughlin SR (1991) Domains specifying thrombin-receptor interaction. Nature 353:674-677.
55. Walker TR and Watson SP (1993) Synergy between Ca2+ and protein kinase C is the major factor in determining the level of secretion from human platelets. Biochem J 289: 277-282.
56. Weiss HJ and Lages B (1997) Platelet prothrombinase activity and intracellular calcium responses in patients with storage pool deficiency, glycoprotein IIb-IIIa deficiency, or impaired platelet coagulant activity-a comparison with Scott syndrome. Blood 89:1599-1611.
57. Weiss HJ, Lages B, Zheng S, and Hayward CP (2001) Platelet factor V New York: a defect in factor V distinct from that in factor V Quebec resulting in impaired prothrombinase generation. Am J Hematol 66:130-139.
58. Xu WF, Andersen H, Whitmore TE, Presnell SR, Yee DP, Ching A, Gilbert T, Davie EW, and Foster DC (1998) Cloning and characterization of human proteaseactivated receptor 4. Proc Natl Acad Sci USA 95:6642-6646.
59. Zeiger F, Stephan S, Hoheisel G, Pfeiffer D, Ruehlmann C, and Koksch M (2000) PSelectin expression, platelet aggregates, and platelet-derived microparticle formation are increased in peripheral arterial disease. Blood Coagul Fibrinolysis 11:723-728.