Tissue factor, protease activated receptors and pathologic heart remodelling

Silvio Antoniak; Erica Sparkenbaugh; Rafal Pawlinski

doi:10.1160/th14-03-0243

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2014; 112(05): 893-900
DOI: 10.1160/th14-03-0243

Theme Issue Article

Schattauer GmbH

Tissue factor, protease activated receptors and pathologic heart remodelling

Authors

Silvio Antoniak

¹Division of Hematology and Oncology, Department of Medicine, McAllister Heart Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
Erica Sparkenbaugh

¹Division of Hematology and Oncology, Department of Medicine, McAllister Heart Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA
Rafal Pawlinski

¹Division of Hematology and Oncology, Department of Medicine, McAllister Heart Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA

Abstract

Summary

Tissue factor is the primary initiator of coagulation cascade and plays an essential role in haemostasis and thrombosis. In addition, tissue factor and coagulation proteases contribute to many cellular responses via activation of protease activated receptors. The heart is an organ with high levels of constitutive tissue factor expression. This review focuses on the role of tissue factor, coagulation proteases and protease activated receptors in heart haemostasis and the pathological heart remodelling associated with myocardial infarction, viral myocarditis and hypertension.

Full Text

References

References
1 Williams JC, Mackman N. Tissue factor in health and disease. Front Biosci 2012; 4: 358-372.
2 Pawlinski R, Mackman N. Cellular sources of tissue factor in endotoxemia and sepsis. Thromb Res 2010; 125 (Suppl. 01) S70-73. Epub 2010/02/27.
3 Coughlin SR. Thrombin signalling and protease-activated receptors. Nature 2000; 407: 258-264.
4 Riewald M. et al. Gene induction by coagulation factor Xa is mediated by activation of protease-activated receptor 1. Blood 2001; 97: 3109-3116.
5 Riewald M. et al. Activation of endothelial cell protease activated receptor 1 by the protein C pathway. Science 2002; 296: 1880-1882.
6 Camerer E. et al. Genetic evidence that protease-activated receptors mediate factor Xa signalling in endothelial cells. J Biol Chem 2002; 277: 16081-16087.
7 Boire A. et al. PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 2005; 120: 303-313.
8 Austin KM. et al. Matrix metalloproteases and PAR1 activation. Blood 2013; 121: 431-439.
9 Jaffre F. et al. Beta-adrenergic receptor stimulation transactivates protease-activated receptor 1 via matrix metalloproteinase 13 in cardiac cells. Circulation 2012; 125: 2993-3003.
10 Camerer E. et al. Tissue factor- and factor X-dependent activation of protease-activated receptor 2 by factor VIIa. Proc Natl Acad Sci USA 2000; 97: 5255-5260.
11 Rao LV, Pendurthi UR. Tissue factor-factor VIIa signalling. Arterioscler Thromb Vasc Biol 2005; 25: 47-56.
12 Brown RD. et al. The cardiac fibroblast: therapeutic target in myocardial remodelling and failure. Ann Rev Pharmacol Toxicol 2005; 45: 657-687.
13 Chien KR, Olson EN. Converging pathways and principles in heart development and disease: CV@CSH. Cell 2002; 110: 153-162.
14 Jessup M, Brozena S. Heart failure. N Engl J Med 2003; 348: 2007-2018.
15 Steinberg SF. The cardiovascular actions of protease-activated receptors. Mol Pharmacol 2005; 67: 2-11.
16 Mackman N. Role of tissue factor in haemostasis, thrombosis, and vascular development. Arterioscler Thromb Vasc Biol 2004; 24: 1015-1022.
17 Pawlinski R. et al. Tissue factor deficiency causes cardiac fibrosis and left ventricular dysfunction. Proc Natl Acad Sci USA 2002; 99: 15333-15338.
18 Parry GC. et al. Low levels of tissue factor are compatible with development and haemostasis in mice. J Clin Invest 1998; 101: 560-569.
19 Xu H. et al. Severe deficiency of coagulation Factor VII results in spontaneous cardiac fibrosis in mice. J Pathol 2009; 217: 362-371.
20 Pawlinski R. et al. Role of cardiac myocyte tissue factor in heart haemostasis. J Thromb Haemost 2007; 5: 1693-1700.
21 Luther T. et al. Tissue factor expression during human and mouse development. Am J Pathol 1996; 149: 101-113.
22 Luther T, Mackman N. Tissue factor in the heart. Multiple roles in haemostasis, thrombosis, and inflammation. Trends Cardiovasc Med 2001; 11: 307-312.
23 Szotowski B. et al. Alterations in myocardial tissue factor expression and cellular localization in dilated cardiomyopathy. J Am Coll Cardiol 2005; 45: 1081-1089.
24 Luther T. et al. Functional implications of tissue factor localization to cell-cell contacts in myocardium. J Pathol 2000; 192: 121-130.
25 Rauch U. Tissue factor and cardiomyocytes. Thromb Res 2012; 129 (Suppl. 02) S41-43.
26 Pena E. et al. Subcellular localization of tissue factor and human coronary artery smooth muscle cell migration. J Thromb Haemost 2012; 10: 2373-2382.
27 Ott I. et al. A role for tissue factor in cell adhesion and migration mediated by interaction with actin-binding protein 280. J Cell Biol 1998; 140: 1241-1253.
28 Versteeg HH. et al. Factor VIIa/tissue factor-induced signalling via activation of Src-like kinases, phosphatidylinositol 3-kinase, and Rac. J Biol Chem 2000; 275: 28750-28756.
29 Versteeg HH. et al. Inhibition of tissue factor signalling suppresses tumor growth. Blood 2008; 111: 190-199.
30 White HD, Chew DP. Acute myocardial infarction. Lancet 2008; 372: 570-584.
31 Braunwald E, Kloner RA. Myocardial reperfusion: a double-edged sword?. J Clin Invest 1985; 76: 1713-1719.
32 Golino P. et al. Effects of tissue factor induced by oxygen free radicals on coronary flow during reperfusion. Nat Med 1996; 2: 35-40.
33 Erlich JH. et al. Inhibition of the tissue factor-thrombin pathway limits infarct size after myocardial ischaemia-reperfusion injury by reducing inflammation. Am J Pathol 2000; 157: 1849-1862.
34 Golino P. et al. Recombinant human, active site-blocked factor VIIa reduces infarct size and no-reflow phenomenon in rabbits. Am J Physiol Heart Circul Physiol 2000; 278: H1507-1516.
35 Loubele ST. et al. Active site inhibited factor VIIa attenuates myocardial ischaemia/reperfusion injury in mice. J Thromb Haemost 2009; 7: 290-298.
36 Yeh CH. et al. Potent cardioprotection from ischaemia-reperfusion injury by a two-domain fusion protein comprising annexin V and Kunitz protease inhibitor. J Thromb Haemost 2013; 11: 1454-1463.
37 Macchi L. et al. The synthetic pentasaccharide fondaparinux attenuates myocardial ischaemia-reperfusion injury in rats via STAT-3. Shock 2014; 41: 166-171.
38 Pawlinski R. et al. Protease-activated receptor-1 contributes to cardiac remodelling and hypertrophy. Circulation 2007; 116: 2298-2306.
39 Petzelbauer P. et al. The fibrin-derived peptide Bbeta15–42 protects the myocardium against ischaemia-reperfusion injury. Nature Med 2005; 11: 298-304.
40 Zacharowski K. et al. Fibrin(ogen) and its fragments in the pathophysiology and treatment of myocardial infarction. J Mol Med 2006; 84: 469-477.
41 Strande JL. et al. SCH 79797, a selective PAR1 antagonist, limits myocardial ischaemia/reperfusion injury in rat hearts. Basic Res Cardiol 2007; 102: 350-358.
42 Di Serio C. et al. Protease-activated receptor 1-selective antagonist SCH79797 inhibits cell proliferation and induces apoptosis by a protease-activated receptor 1-independent mechanism. Basic Clin Pharmacol Toxicol 2007; 101: 63-69.
43 Strande JL. Letter by Strande regarding article “Protease-activated receptor-1 contributes to cardiac remodelling and hypertrophy”. Circulation 2008; 117: e495 author reply e496.
44 Glembotski CC. et al. Myocardial alpha-thrombin receptor activation induces hypertrophy and increases atrial natriuretic factor gene expression. J Biol Chem 1993; 268: 20646-20652.
45 Sabri A. et al. Signalling properties and functions of two distinct cardiomyocyte protease-activated receptors. Circulation Res 2000; 86: 1054-1061.
46 Loubele ST. et al. Activated protein C protects against myocardial ischaemia/ reperfusion injury via inhibition of apoptosis and inflammation. Arterioscl Thromb Vasc Biol 2009; 29: 1087-1092.
47 Antoniak S. et al. Protease-activated receptor 2 deficiency reduces cardiac ischaemia/reperfusion injury. Arterioscler Thromb Vasc Biol 2010; 30: 2136-2142.
48 Antoniak S. et al. Protease activated receptor-2 contributes to heart failure. PLoS One 2013; 8: e81733.
49 Bhattacharya K. et al. Mast cell deficient W/Wv mice have lower serum IL-6 and less cardiac tissue necrosis than their normal littermates following myocardial ischaemia-reperfusion. Intern J Immunopathol Pharmacol 2007; 20: 69-74.
50 Somasundaram P. et al. Mast cell tryptase may modulate endothelial cell pheno-type in healing myocardial infarcts. J Pathol 2005; 205: 102-111.
51 Napoli C. et al. Protease-activated receptor-2 modulates myocardial ischaemiareperfusion injury in the rat heart. Proc Natl Acad Sci USA 2000; 97: 3678-3683.
52 Jiang R. et al. PAR-2 activation at the time of reperfusion salvages myocardium via an ERK1/2 pathway in in vivo rat hearts. Am J Physiol Heart Circ Physiol 2007; 293: H2845-2852.
53 McLean PG. et al. Protease-activated receptor-2 activation causes EDHF-like coronary vasodilation: selective preservation in ischaemia/reperfusion injury: involvement of lipoxygenase products, VR1 receptors, and C-fibers. Circ Res 2002; 90: 465-472.
54 Seqqat R. et al. Protease activated receptor-4 regulates post-infarction ventricular remodelling and cardiac function. Circulation 2007; 116 Suppl 45.
55 Strande JL. et al. Inhibiting protease-activated receptor 4 limits myocardial ischaemia/reperfusion injury in rat hearts by unmasking adenosine signalling. J Pharmacol Exp Ther 2008; 324: 1045-1054.
56 Antoniak S. et al. Protease-activated receptors and myocardial infarction. IUBMB life 2011; 63: 383-389.
57 Rajagopal S. et al. Teaching old receptors new tricks: biasing seven-transmembrane receptors. Nature Rev Drug Discov 2010; 9: 373-386.
58 Ramachandran R. et al. Agonist-biased signalling via proteinase activated receptor-2: differential activation of calcium and mitogen-activated protein kinase pathways. Mol Pharmacol 2009; 76: 791-801.
59 Betts RJ. et al. Inhibitory influence of the hexapeptidic sequence SLIGRL on influenza A virus infection in mice. J Pharmacol Exp Therap 2012; 343: 725-735.
60 Shauer A. et al. Acute viral myocarditis: current concepts in diagnosis and treatment. Israel Med Assoc J 2013; 15: 180-185.
61 Antoniak S, Mackman N. Coagulation, protease-activated receptors, and viral myocarditis. J Cardiovasc Translat Res 2014; 7: 203-211.
62 Antoniak S, Mackman N. Multiple roles of the coagulation protease cascade during virus infection. Blood 2014; 123: 2605-2613.
63 Tomioka N. et al. Mural thrombi in mice with acute viral myocarditis. Japan Circulation J 1985; 49: 1277-1279.
64 Antoniak S. et al. Viral myocarditis and coagulopathy: increased tissue factor expression and plasma thrombogenicity. J Mol Cell Cardiol 2008; 45: 118-126.
65 Antoniak S. et al. Regulation of cardiomyocyte full-length tissue factor expression and microparticle release under inflammatory conditions in vitro. J Thromb Haemost 2009; 7: 871-878.
66 Sutherland MR. et al. Thrombin enhances herpes simplex virus infection of cells involving protease-activated receptor 1. J Thromb Haemost 2007; 5: 1055-1061.
67 Antoniak S. et al. PAR-1 contributes to the innate immune response during viral infection. J Clin Invest 2013; 123: 1310-1322.
68 Weithauser A. et al. Protease-activated receptor 2 regulates the Innate Immune Response to Viral Infection in a CVB3-induced Myocarditis. J Am Coll Cardiol 2013; 62: 1737-1745.
69 Mehta PK, Griendling KK. Angiotensin II cell signalling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 2007; 292: C82-97.
70 Marchesi C. et al. Role of the renin-angiotensin system in vascular inflammation. Trends Pharmacol Sci 2008; 29: 367-374.
71 Varughese GI, Lip GY. Is hypertension a prothrombotic state?. Curr Hyperten Rep 2005; 7: 168-173.
72 Taubman MB. et al. Agonist-mediated tissue factor expression in cultured vascular smooth muscle cells. Role of Ca2+ mobilization and protein kinase C activation. J Clin Invest 1993; 91: 547-552.
73 Sugano T. et al. Adrenomedullin inhibits angiotensin II-induced expression of tissue factor and plasminogen activator inhibitor-1 in cultured rat aortic endothelial cells. Arterioscler Thromb Vasc Biol 2001; 21: 1078-1083.
74 Napoleone E. et al. Angiotensin-converting enzyme inhibitors downregulate tissue factor synthesis in monocytes. Circ Res 2000; 86: 139-143.
75 Muller DN. et al. Angiotensin II (AT(1)) receptor blockade reduces vascular tissue factor in angiotensin II-induced cardiac vasculopathy. Am J Pathol 2000; 157: 111-122.
76 Koh KK. et al. Angiotensin II type 1 receptor blockers reduce tissue factor activity and plasminogen activator inhibitor type-1 antigen in hypertensive patients: a randomized, double-blind, placebo-controlled study. Atherosclerosis 2004; 177: 155-160.
77 Matej R. et al. Radiation-induced production of PAR-1 and TGF-beta 1 mRNA in lung of C57Bl6 and C3H murine strains and influence of pharmacoprophylaxis by ACE inhibitors. Pathol Res Pract 2007; 203: 107-114.
78 McGuire JJ. et al. Blood pressures, heart rate and locomotor activity during salt loading and angiotensin II infusion in protease-activated receptor 2 (PAR2) knockout mice. BMC Physiol 2008; 8: 20.
79 Hughes KH. et al. Effects of chronic in-vivo treatments with protease-activated receptor 2 agonist on endothelium function and blood pressures in mice. Canad J Physiol Pharmacol 2013; 91: 295-305.
80 Chia E. et al. Protection of protease-activated receptor 2 mediated vasodilatation against angiotensin II-induced vascular dysfunction in mice. BMC Pharmacol 2011; 11: 10.
81 Pinelli A. et al. Myocardial infarction non-invasively induced in rabbits by administering isoproterenol and vasopressin: protective effects exerted by verapamil. Fundament Clin Pharmacol 2004; 18: 657-667.
82 Sato S. et al. Ion transport regulated by protease-activated receptor 2 in human airway Calu-3 epithelia. Br J Pharmacol 2005; 146: 397-407.
83 Levick SP. et al. Cardiac mast cells mediate left ventricular fibrosis in the hyper-tensive rat heart. Hypertension 2009; 53: 1041-1047.
84 Miura S. et al. Inhibition of matrix metalloproteinases prevents cardiac hyper-trophy induced by beta-adrenergic stimulation in rats. J Cardiovasc Pharmacol 2003; 42: 174-181.
85 Bakouboula B. et al. Procoagulant membrane microparticles correlate with the severity of pulmonary arterial hypertension. Am J Resp Crit Care Med 2008; 177: 536-543.
86 Berger G. et al. Coagulation and anticoagulation in pulmonary arterial hyper-tension. Israel Med Assoc J 2009; 11: 376-379.
87 Altman R. et al. Coagulation and fibrinolytic parameters in patients with pulmonary hypertension. Clin Cardiol 1996; 19: 549-554.
88 White RJ. et al. Plexiform-like lesions and increased tissue factor expression in a rat model of severe pulmonary arterial hypertension. American journal of physiology Lung Cell Mol Physiol 2007; 293: L583-590.
89 White RJ. et al. Tissue factor is induced in a rodent model of severe pulmonary hypertension characterized by neointimal lesions typical of human disease. Chest 2005; 128 (Suppl. 06) 612S-613S.
90 Bauer EM. et al. Complement C3 deficiency attenuates chronic hypoxia-induced pulmonary hypertension in mice. PloS one 2011; 6: e28578.
91 Delbeck M. et al. A role for coagulation factor Xa in experimental pulmonary arterial hypertension. Cardiovasc Res 2011; 92: 159-168.
92 Humbert M. et al. Cellular and molecular pathobiology of pulmonary arterial hypertension. J Am Coll Cardiol 2004; 43 (Suppl. 12) S 13S-24S.
93 Mandegar M. et al. Cellular and molecular mechanisms of pulmonary vascular remodelling: role in the development of pulmonary hypertension. Microvasc Res 2004; 68: 75-103.
94 White TA. et al. Tissue factor pathway inhibitor overexpression inhibits hypoxia-induced pulmonary hypertension. Am J Resp Cell Mol Biol 2010; 43: 35-45.
95 Delbeck M. et al. A role for coagulation factor Xa in experimental pulmonary arterial hypertension. Cardiovasc Res 2011; 92: 159-168.
96 Kwapiszewska G. et al. PAR-2 inhibition reverses experimental pulmonary hypertension. Circulation Res 2012; 110: 1179-1191.
97 Farber HW, Loscalzo J. Pulmonary arterial hypertension. N Engl J Med 2004; 351: 1655-1665.
98 Nickel KF. et al. Thrombin has biphasic effects on the nitric oxide-cGMP pathway in endothelial cells and contributes to experimental pulmonary hypertension. PloS one 2013; 8: e63504.
99 Maki J. et al. Involvement of reactive oxygen species in thrombin-induced pulmonary vasoconstriction. Am J Respir Crit Care Med 2010; 182: 1435-1444.
100 Maki J. et al. Thrombin activation of proteinase-activated receptor 1 potentiates the myofilament Ca2+ sensitivity and induces vasoconstriction in porcine pulmonary arteries. Br J Pharmacol 2010; 159: 919-927.