Acute and persistent platelet and coagulant activities in atherothrombosis

Journal of Thrombosis and Haemostasis

Volumn 13, Issue S1, 2015, Pages S272-S280

  Mastenbroek, T G ^a   van Geffen, J P ^a   Heemskerk, J W M ^a   Cosemans, J M E M ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Atherosclerotic plaque; Blood coagulation; Mouse; Platelets; Rupture; Thrombosis

Indexed keywords

ACETYLSALICYLIC ACID; BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 12; BLOOD CLOTTING FACTOR 12A; CELL PROTEIN; CHEMOKINE RECEPTOR CCR2; CLOPIDOGREL; COLLAGEN TYPE 1; COLLAGEN TYPE 3; GLYCOPROTEIN VI; LEPTIN RECEPTOR; LIPOPROTEIN LIPASE RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROSTAGLANDIN E RECEPTOR 3; PURINERGIC P2Y1 RECEPTOR; THROMBOPLASTIN; TISSUE FACTOR PATHWAY INHIBITOR; UNCLASSIFIED DRUG; APOLIPOPROTEIN E; COLLAGEN;

ARTIFICIAL EMBOLISM; BLOOD CLOTTING; CELL INTERACTION; EXPERIMENTAL ANIMAL; FIBRINOLYSIS; HEMOSTASIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; THROMBOCYTE FUNCTION; THROMBOSIS; ANIMAL; ARTERY; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD; DEFICIENCY; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; RUPTURE; THROMBOCYTE;

ANIMALS; APOLIPOPROTEINS E; ARTERIES; ATHEROSCLEROSIS; BLOOD COAGULATION; BLOOD PLATELETS; COLLAGEN; DISEASE MODELS, ANIMAL; FIBRINOLYSIS; HUMANS; MICE, KNOCKOUT; PLAQUE, ATHEROSCLEROTIC; PLASMINOGEN ACTIVATOR INHIBITOR 1; PLATELET ACTIVATION; RUPTURE, SPONTANEOUS; SIGNAL TRANSDUCTION; THROMBOSIS;

EID: 84931307415     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12972     Document Type: Review

References (62)

1. Jackson SP. Arterial thrombosis: insidious, unpredictable and deadly. Nat Med 2011; 17: 1423-36.
2. Versteeg HH, Heemskerk JW, Levi M, Reitsma PH. New fundamentals in hemostasis. Physiol Rev 2013; 93: 327-58.
3. Heemskerk JW, Mattheij N, Cosemans JM. Platelet-based coagulation: different populations, different functions. J Thromb Haemost 2013; 11: 2-11.
4. Bentzon JF, Otsuka F, Virmani R, Falk E. Mechanisms of plaque formation and rupture. Circ Res 2014; 114: 1852-66.
5. Rittersma SZ, van der Wal AC, Koch KT, Piek JJ, Henriques JP, Mulder KJ, Ploegmakers JP, Meesterman M, de Winter RJ. Plaque instability frequently occurs days or weeks before occlusive coronary thrombosis: a pathological thrombectomy study in primary percutaneous coronary intervention. Circulation 2005; 111: 1160-5.
6. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Kissela BM, Kittner SJ, Lackland DT, et al. Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 2013; 127: e6-245.
7. Cullen P, Baetta R, Bellosta S, Bernini F, Chinetti G, Cignarella A, von Eckardstein A, Exley A, Goddard M, Hofker M, Hurt-Camejo E, Kanters E, Kovanen P, Lorkowski S, McPheat W, Pentikainen M, Rauterberg J, Ritchie A, Staels B, Weitkamp B, et al. Rupture of the atherosclerotic plaque: does a good animal model exist? Arterioscler Thromb Vasc Biol 2003; 23: 535-42.
8. Reddick RL, Zhang SH, Maeda N. Aortic atherosclerotic plaque injury in apolipoprotein E deficient mice. Atherosclerosis 1998; 140: 297-305.
9. Kuijpers MJ, Gilio K, Reitsma S, Nergiz-Ünal R, Prinzen L, Heeneman S, Lutgens E, van Zandvoort MA, Nieswandt B, Egbrink MG, Heemskerk JW. Complementary roles of platelets and coagulation in thrombus formation on plaques acutely ruptured by targeted ultrasound treatment: a novel intravital model. J Thromb Haemost 2009; 7: 152-61.
10. Hechler B, Gachet C. Comparison of two murine models of thrombosis induced by atherosclerotic plaque injury. Thromb Haemost 2011; 105: S3-12.
11. Eitzman DT, Westrick RJ, Xu Z, Tyson J, Ginsburg D. Hyperlipidemia promotes thrombosis after injury to atherosclerotic vessels in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2000; 20: 1831-4.
12. King SM, McNamee RA, Houng AK, Patel R, Brands M, Reed GL. Platelet dense-granule secretion plays a critical role in thrombosis and subsequent vascular remodeling in atherosclerotic mice. Circulation 2009; 120: 785-91.
13. Jiang P, Xue D, Zhang Y, Ye L, Liu Y, Makale M, Kesari S, Edgington TS, Liu C. The extrinsic coagulation cascade and tissue factor pathway inhibitor in macrophages: a potential therapeutic opportunity for atherosclerotic thrombosis. Thromb Res 2014; 133: 657-66.
14. Westrick RJ, Winn ME, Eitzman DT. Murine models of vascular thrombosis (Eitzman series). Arterioscler Thromb Vasc Biol 2007; 27: 2079-93.
15. Kretz CA, Vaezzadeh N, Gross PL. Tissue factor and thrombosis models. Arterioscler Thromb Vasc Biol 2010; 30: 900-8.
16. van Kruchten R, Cosemans JM, Heemskerk JW. Measurement of whole blood thrombus formation using parallel-plate flow chambers: a practical guide. Platelets 2012; 23: 229-42.
17. Nieswandt B, Pleines I, Bender M. Platelet adhesion and activation mechanisms in arterial thrombosis and ischaemic stroke. J Thromb Haemost 2011; 9 (Suppl. 1): 92-104.
18. Cosemans JM, Kuijpers MJ, Lecut C, Loubele ST, Heeneman S, Jandrot-Perrus M, Heemskerk JW. Contribution of platelet glycoprotein VI to the thrombogenic effect of collagens in fibrous atherosclerotic lesions. Atherosclerosis 2005; 181: 19-27.
19. Penz S, Reininger AJ, Brandl R, Goyal P, Rabie T, Bernlochner I, Rother E, Goetz C, Engelmann B, Smethurst PA, Ouwehand WH, Farndale R, Nieswandt B, Siess W. Human atheromatous plaques stimulate thrombus formation by activating platelet glycoprotein VI. FASEB J 2005; 19: 898-909.
20. Reininger AJ, Bernlochner I, Penz SM, Ravanat C, Smethurst P, Farndale RW, Gachet C, Brandl R, Siess W. A 2-step mechanism of arterial thrombus formation induced by human atherosclerotic plaques. J Am Coll Cardiol 2010; 55: 1147-58.
21. van Zanten GH, de Graaf S, Slootweg PJ, Heijnen HF, Connolly TM, de Groot PG, Sixma JJ. Increased platelet deposition on atherosclerotic coronary arteries. J Clin Invest 1994; 93: 615-32.
22. Penz SM, Reininger AJ, Toth O, Deckmyn H, Brandl R, Siess W. Glycoprotein Ibalpha inhibition and ADP receptor antagonists, but not aspirin, reduce platelet thrombus formation in flowing blood exposed to atherosclerotic plaques. Thromb Haemost 2007; 97: 435-43.
23. 12 receptors in shear-dependent thrombus formation on ruptured plaques. PLoS ONE 2010; 5: e10130.
24. Schulz C, Konrad I, Sauer S, Orschiedt L, Koellnberger M, Lorenz R, Walter U, Massberg S. Effect of chronic treatment with acetylsalicylic acid and clopidogrel on atheroprogression and atherothrombosis in ApoE-deficient mice in vivo. Thromb Haemost 2008; 99: 190-5.
25. van Geffen JP, Kleinegris MC, Verdoold R, Baaten CC, Cosemans JM, Clemetson KJ, Ten Cate H, Roest M, de Laat B, Heemskerk JW. Normal platelet activation profile in patients with peripheral arterial disease on aspirin. Thromb Res 2015; 135: 513-20.
26. 2 exacerbates arterial thrombosis and atherothrombosis through platelet EP3 receptors. J Exp Med 2007; 204: 311-20.
27. 2 with DG-041 decreases thrombosis without impairing haemostatic competence. Cardiovasc Res 2014; 101: 482-91.
28. 2 in human atherosclerotic plaque on platelet EP3 and EP4 receptor activation and platelet function in whole blood. J Thromb Thrombolysis 2011; 32: 158-66.
29. Fernandez-Ortiz A, Badimon JJ, Falk E, Fuster V, Meyer B, Mailhac A, Weng D, Shah PK, Badimon L. Characterization of the relative thrombogenicity of atherosclerotic plaque components: implications for consequences of plaque rupture. J Am Coll Cardiol 1994; 23: 1562-9.
30. Badimon JJ, Lettino M, Toschi V, Fuster V, Berrozpe M, Chesebro JH, Badimon L. Local inhibition of tissue factor reduces the thrombogenicity of disrupted human atherosclerotic plaques: effects of tissue factor pathway inhibitor on plaque thrombogenicity under flow conditions. Circulation 1999; 99: 1780-7.
31. Kuijpers MJ, van der Meijden PE, Feijge MA, Mattheij NJ, May F, Govers-Riemslag J, Meijers JC, Heemskerk JW, Renne T, Cosemans JM. Factor XII regulates the pathological process of thrombus formation on ruptured plaques. Arterioscler Thromb Vasc Biol 2014; 34: 1674-80.
32. Westrick RJ, Bodary PF, Xu Z, Shen YC, Broze GJ, Eitzman DT. Deficiency of tissue factor pathway inhibitor promotes atherosclerosis and thrombosis in mice. Circulation 2001; 103: 3044-6.
33. van der Meijden PE, Munnix IC, Auger JM, Govers-Riemslag JW, Cosemans JM, Kuijpers MJ, Spronk HM, Watson SP, Renne T, Heemskerk JW. Dual role of collagen in factor XII-dependent thrombus formation. Blood 2009; 114: 881-90.
34. van Montfoort ML, Kuijpers MJ, Knaup VL, Bhanot S, Monia BP, Roelofs JJ, Heemskerk JW, Meijers JC. Factor XI regulates pathological thrombus formation on acutely ruptured atherosclerotic plaques. Arterioscler Thromb Vasc Biol 2014; 34: 1668-73.
35. Hagedorn I, Schmidbauer S, Pleines I, Kleinschnitz C, Kronthaler U, Stoll G, Dickneite G, Nieswandt B. Factor XIIa inhibitor recombinant human albumin Infestin-4 abolishes occlusive arterial thrombus formation without affecting bleeding. Circulation 2010; 121: 1510-7.
36. Cheng Q, Tucker EI, Pine MS, Sisler I, Matafonov A, Sun MF, White-Adams TC, Smith SA, Hanson SR, McCarty OJ, Renne T, Gruber A, Gailani D. A role for factor XIIa-mediated factor XI activation in thrombus formation in vivo. Blood 2010; 116: 3981-9.
37. Büller HR, Bethune C, Bhanot S, Gailani D, Monia BP, Raskob GE, Segers A, Verhamme P, Weitz JI; Investigators F-AT. Factor XI antisense oligonucleotide for prevention of venous thrombosis. N Engl J Med 2015; 372: 232-40.
38. Alame G, Mangin PH, Freund M, Riehl N, Magnenat S, Petitou M, Hechler B, Gachet C. EP217609, a neutralisable dual-action FIIa/FXa anticoagulant, with antithrombotic effects in arterial thrombosis. Thromb Haemost 2015; 113: 385-95.
39. Cosemans JM, Mattheij NJ, Angelillo-Scherrer A, Heemskerk JW. The effects of arterial flow on platelet activation, thrombus growth and stabilization. Cardiovasc Res 2013; 99: 342-52.
40. Eitzman DT, Westrick RJ, Xu Z, Tyson J, Ginsburg D. Plasminogen activator inhibitor-1 deficiency protects against atherosclerosis progression in the mouse carotid artery. Blood 2000; 96: 4212-5.
41. Luttun A, Lupu F, Storkebaum E, Hoylaerts MF, Moons L, Crawley J, Bono F, Poole AR, Tipping P, Herbert JM, Collen D, Carmeliet P. Lack of plasminogen activator inhibitor-1 promotes growth and abnormal matrix remodeling of advanced atherosclerotic plaques in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2002; 22: 499-505.
42. Schäfer K, Muller K, Hecke A, Mounier E, Goebel J, Loskutoff DJ, Konstantinides S. Enhanced thrombosis in atherosclerosis-prone mice is associated with increased arterial expression of plasminogen activator inhibitor-1. Arterioscler Thromb Vasc Biol 2003; 23: 2097-103.
43. Xian X, Ding Y, Zhang L, Wang Y, McNutt MA, Ross C, Hayden MR, Deng X, Liu G. Enhanced atherothrombotic formation after oxidative injury by FeCl3 to the common carotid artery in severe combined hyperlipidemic mice. Biochem Biophys Res Commun 2009; 385: 563-9.
44. Bodary PF, Gu S, Shen Y, Hasty AH, Buckler JM, Eitzman DT. Recombinant leptin promotes atherosclerosis and thrombosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2005; 25: e119-22.
45. van der Donckt C, van Herck JL, Schrijvers DM, Vanhoutte G, Verhoye M, Blockx I, van der Linden A, Bauters D, Lijnen HR, Sluimer JC, Roth L, van Hove CE, Fransen P, Knaapen MW, Hervent AS, de Keulenaer GW, Bult H, Martinet W, Herman AG, De Meyer GR. Elastin fragmentation in atherosclerotic mice leads to intraplaque neovascularization, plaque rupture, myocardial infarction, stroke, and sudden death. Eur Heart J 2014; 36: 1049-58.
46. Gough PJ, Gomez IG, Wille PT, Raines EW. Macrophage expression of active MMP-9 induces acute plaque disruption in apoE-deficient mice. J Clin Invest 2006; 116: 59-69.
47. -/- mice after adenovirus-mediated transfer of p53. Circulation 2002; 105: 2064-70.
48. -/- mice. Circulation 2007; 116: 2444-52.
49. Projahn D, Koenen RR. Platelets: key players in vascular inflammation. J Leukoc Biol 2012; 92: 1167-75.
50. Schober A, Zernecke A, Liehn EA, von Hundelshausen P, Knarren S, Kuziel WA, Weber C. Crucial role of the CCL2/CCR2 axis in neointimal hyperplasia after arterial injury in hyperlipidemic mice involves early monocyte recruitment and CCL2 presentation on platelets. Circ Res 2004; 95: 1125-33.
51. Burkhart JM, Gambaryan S, Watson SP, Jurk K, Walter U, Sickmann A, Heemskerk JW, Zahedi RP. What can proteomics tell us about platelets? Circ Res 2014; 114: 1204-19.
52. Schulz C, Massberg S. Platelets in atherosclerosis and thrombosis. Handb Exp Pharmacol 2012; 210: 111-33.
53. Ramadan R, Dhawan SS, Syed H, Pohlel FK, Binongo JN, Ghazzal ZB, Quyyumi AA. Effects of clopidogrel therapy on oxidative stress, inflammation, vascular function, and progenitor cells in stable coronary artery disease. J Cardiovasc Pharmacol 2014; 63: 369-74.
54. Blann AD, Kuzniatsova N, Lip GY. Vascular and platelet responses to aspirin in patients with coronary artery disease. Eur J Clin Invest 2013; 43: 91-9.
55. Borissoff JI, Otten JJ, Heeneman S, Leenders P, van Oerle R, Soehnlein O, Loubele ST, Hamulyak K, Hackeng TM, Daemen MJ, Degen JL, Weiler H, Esmon CT, van Ryn J, Biessen EA, Spronk HM, ten Cate H. Genetic and pharmacological modifications of thrombin formation in apolipoprotein e-deficient mice determine atherosclerosis severity and atherothrombosis onset in a neutrophil-dependent manner. PLoS ONE 2013; 8: e55784.
56. Kalz J, ten Cate H, Spronk HM. Thrombin generation and atherosclerosis. J Thromb Thrombolysis 2014; 37: 45-55.
57. Tilley RE, Pedersen B, Pawlinski R, Sato Y, Erlich JH, Shen Y, Day S, Huang Y, Eitzman DT, Boisvert WA, Curtiss LK, Fay WP, Mackman N. Atherosclerosis in mice is not affected by a reduction in tissue factor expression. Arterioscler Thromb Vasc Biol 2006; 26: 555-62.
58. Gibson CM, Chakrabarti AK, Mega J, Bode C, Bassand JP, Verheugt FW, Bhatt DL, Goto S, Cohen M, Mohanavelu S, Burton P, Stone G, Braunwald E; Investigators A-AT. Reduction of stent thrombosis in patients with acute coronary syndromes treated with rivaroxaban in ATLAS-ACS 2 TIMI 51. J Am Coll Cardiol 2013; 62: 286-90.
59. Thacker SG, Zhao W, Smith CK, Luo W, Wang H, Vivekanandan-Giri A, Rabquer BJ, Koch AE, Pennathur S, Davidson A, Eitzman DT, Kaplan MJ. Type I interferons modulate vascular function, repair, thrombosis, and plaque progression in murine models of lupus and atherosclerosis. Arthritis Rheum 2012; 64: 2975-85.
60. 2A receptor antagonists on human platelet activation in blood exposed to physiologic stimuli and atherosclerotic plaque. J Thromb Haemost 2011; 9: 2112-5.
61. Palazon CP, Alfon J, Gaffney P, Berrozpe M, Royo T, Badimon L. Effects of reducing LDL and increasing HDL with gemfibrozil in experimental coronary lesion development and thrombotic risk. Atherosclerosis 1998; 136: 333-45.
62. Suades R, Padro T, Vilahur G, Badimon L. Circulating and platelet-derived microparticles in human blood enhance thrombosis on atherosclerotic plaques. Thromb Haemost 2012; 108: 1208-19.