Coagulation factor and protease pathways in thrombosis and cardiovascular disease

Hugo ten Cate; Tilman M. Hackeng; Pablo García de Frutos

doi:10.1160/TH17-02-0079

Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 2017; 117(07): 1265-1271
DOI: 10.1160/TH17-02-0079

60th Anniversary

Schattauer GmbH

Coagulation factor and protease pathways in thrombosis and cardiovascular disease

Hugo ten Cate

¹Department of Internal Medicine, Cardiovascular Research Institute Maastricht (CARIM), Maastricht, the Netherlands

³Thrombosis Expert Center, Maastricht University Medical Center (MUMC+), Maastricht, the Netherlands

,

Tilman M. Hackeng

²Department of Biochemistry, Cardiovascular Research Institute Maastricht (CARIM), Maastricht, the Netherlands

,

Pablo García de Frutos

⁴Department of Cell Death and Proliferation, IIBB-CSIC and IDIBAPS, Barcelona, Spain

› Institutsangaben

Abstract

Summary

The biochemical characterisation of the proteolytic pathways that constitute blood coagulation was one of the most relevant achievements in biomedical research during the second half of the 20th century. Understanding these pathways was of crucial importance for improving global health through application in haemostasis and thrombosis pathologies. Immediately after the cloning of the genes corresponding to these proteins, mutations were discovered in them that were associated with imbalances in haemostasis. Later, the importance of coagulation pathways in other pathological processes was demonstrated, such as in atherosclerosis and inflammation, both essential processes involved in vascular disease. In the present review we evaluate the concepts that have allowed us to reach the integrated vision on coagulation that we have today. The thrombo-inflammation model encompassing these aspects includes a pivotal role for the proteases of the coagulation pathway as well as the regulatory proteins thereof. These concepts illustrate the importance of the coagulation cascade in cardiovascular pathology, not only in thrombotic processes, but also in atherosclerotic processes and in the response to ischaemia-reperfusion injury, making it a central mechanism in cardiovascular disease.

Keywords

Atherothrombosis - coagulation factors - coagulation inhibitors - proteases - protein C/S pathway - thrombosis - TFPI - vitamin K-dependent factors

Volltext

Referenzen

References
1 Versteeg HH. et al. New fundamentals in hemostasis. Physiol Rev 2013; 93: 327-358.
2 Kanthou C, Benzakour O. Cellular effects and signalling pathways activated by the anti-coagulant factor, protein S, in vascular cells protein S cellular effects. Adv Exp Med Biol 2000; 476: 155-166.
3 Wood JP. et al. Biology of tissue factor pathway inhibitor. Blood 2014; 123: 2934-2943.
4 Fomin ME. et al. Progress and challenges in the development of a cell-based therapy for hemophilia A. J Thromb Haemost 2014; 12: 1954-1965.
5 ten Cate H. et al. The activation of factor X and prothrombin by recombinant factor VIIa in vivo is mediated by tissue factor. J Clin Invest 1993; 92: 1207-1212.
6 Crawley JTB. et al. The central role of thrombin in hemostasis. J Thromb Haemost 2007; 5 (Suppl. 01) 95-101.
7 van Dieijen G. et al. Assembly of the intrinsic factor X activating complex--interactions between factor IXa, factor VIIIa and phospholipid. Thromb Haemost 1985; 53: 396-400.
8 Ahmad SS, Walsh PN. Platelet membrane-mediated coagulation protease complex assembly. Trends Cardiovasc Med 1994; 4: 271-278.
9 Mann KG. et al. Assembly of the prothrombinase complex. Biophys J 1982; 37: 106-107.
10 Bevers EM. et al. Generation of prothrombin-converting activity and the exposure of phosphatidylserine at the outer surface of platelets. Eur J Biochem 1982; 122: 429-436.
11 Rosing J. et al. The role of activated human platelets in prothrombin and factor X activation. Blood 1985; 65: 319-332.
12 Gilbert GE. et al. Platelet-derived microparticles express high affinity receptors for factor VIII. J Biol Chem 1991; 266: 17261-17268.
13 Bouwens EAM. et al. Mechanisms of anticoagulant and cytoprotective actions of the protein C pathway. J Thromb Haemost 2013; 11 (Suppl. 01) 242-253.
14 Hackeng TM, Rosing J. Protein S as Cofactor for TFPI. Arterioscler Thromb Vasc Biol 2009; 29: 2015-2020.
15 van Doorn P. et al. The C-terminus of tissue factor pathway inhibitor-a inhibits factor V activation by protecting the Arg(1545) cleavage site. J Thromb Haemost 2017; 15: 140-149.
16 De Meyer SF. et al. Thromboinflammation in Stroke Brain Damage. Stroke 2016; 47: 1165-1172.
17 Borissoff JI. et al. The Hemostatic System as a Modulator of Atherosclerosis. N Engl J Med 2011; 364: 1746-1760.
18 García de Frutos P, Zöller B. Genetic aspects of thrombotic disease. Thromb Haemost 2015; 114: 883-884.
19 Morange P-E. et al. Genetics of Venous Thrombosis: update in 2015. Thromb Haemost 2015; 114: 910-919.
20 Hermida J. et al. Poor Relationship between Phenotypes of Protein S Deficiency and Mutations in the Protein S Alpha Gene. Thromb Haemost 1999; 82: 1634-1638.
21 Egeberg O. On the natural blood coagulation inhibitor system. Investigations of inhibitor factors based on antithrombin deficient blood. Thromb Diath Haemorrh 1965; 14: 473-489.
22 Davie EW. A Brief Historical Review of the Waterfall/Cascade of Blood Coagulation. J Biol Chem 2003; 278: 50819-5032.
23 Mannucci PM, Franchini M. Classic thrombophilic gene variants. Thromb Haemost 2015; 114: 885-889.
24 Simmonds RE. et al. Clarification of the risk for venous thrombosis associated with hereditary protein S deficiency by investigation of a large kindred with a characterized gene defect. Ann Intern Med 1998; 128: 8-14.
25 Koenen RR. et al. The Ser460Pro mutation in recombinant protein S Heerlen does not affect its APC-cofactor and APC-independent anticoagulant activities. Thromb Haemost 2004; 91: 1105-1114.
26 Giri TK. et al. Deficient APC-cofactor activity of protein S Heerlen in degradation of factor Va Leiden: a possible mechanism of synergism between thrombophilic risk factors. Blood 2000; 96: 523-531.
27 Segers O. et al. Influence of single nucleotide polymorphisms on thrombin generation in factor V Leiden heterozygotes. Thromb Haemost 2013; 111: 1-9.
28 Tang L. et al. PROC c.574_576del polymorphism: A common genetic risk factor for venous thrombosis in the Chinese population. J Thromb Haemost 2012; 10: 2019-2026.
29 Corral J. et al. Antithrombin Cambridge II (A384S): an underestimated genetic risk factor for venous thrombosis. Blood 2007; 109: 4258-4263.
30 Navarro S. et al. The endothelial cell protein C receptor: Its role in thrombosis. Thromb Res 2011; 128: 410-416.
31 Segers K. et al. Coagulation factor V and thrombophilia: background and mechanisms. Thromb Haemost 2007; 98: 530-542.
32 Reitsma PH, Rosendaal FR. Past and future of genetic research in thrombosis. J Thromb Haemost 2007; 5 (Suppl. 01) 264-269.
33 Rather RA, Dhawan V. Genetic markers: Potential candidates for cardiovascular disease. Int J Cardiol 2016; 220: 914-923.
34 Posma JJN. et al. Coagulation and non-coagulation effects of thrombin. J Thromb Haemost 2016; 14: 1908-1916.
35 Griffin JH. et al. Activated protein C: biased for translation. Blood 2015; 125: 2898-2907.
36 Castoldi E, Rosing J. APC resistance: biological basis and acquired influences. J Thromb Haemost 2010; 8: 445-453.
37 Rosing J. Mechanisms of OC related thrombosis. Thromb Res 2005; 81-83.
38 Raps M. et al. The effect of different hormonal contraceptives on plasma levels of free protein S and free TFPI. Thromb Haemost 2013; 109: 606-613.
39 Hackeng TM. et al. Protein S stimulates inhibition of the tissue factor pathway by tissue factor pathway inhibitor. Proc Natl Acad Sci USA 2006; 103: 3106-3111.
40 Hoke M. et al. Tissue factor pathway inhibitor and the risk of recurrent venous thromboembolism. Thromb Haemost 2005; 94: 787-790.
41 Zakai NA. et al. Total tissue factor pathway inhibitor and venous thrombosis. Thromb Haemost 2010; 104: 207-212.
42 Winckers K. et al. Impaired tissue factor pathway inhibitor function is associated with recurrent venous thromboembolism in patients with first unprovoked deep venous thrombosis. J Thromb Haemost 2012; 10: 2208-2211.
43 Borissoff JI. et al. Early Atherosclerosis Exhibits an Enhanced Procoagulant State. Circulation 2010; 122: 821-830.
44 Wilcox JN. et al. Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque. Proc Natl Acad Sci USA 1989; 86: 2839-2843.
45 Wilcox JN. et al. Extrahepatic synthesis of factor VII in human atherosclerotic vessels. Arterioscler Thromb Vasc Biol 2003; 23: 136-141.
46 Spronk HMH. et al. New Insights into Modulation of Thrombin Formation. Curr Atheroscler Rep 2013; 15: 363.
47 Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med 1999; 340: 115-126.
48 Laszik ZG. et al. Down-Regulation of Endothelial Expression of Endothelial Cell Protein C Receptor and Thrombomodulin in Coronary Atherosclerosis. Am J Pathol 2001; 159: 797-802.
49 Lentz SR. et al. Impaired anticoagulant response to infusion of thrombin in atherosclerotic monkeys associated with acquired defects in the protein C system. Arterioscler Thromb Vasc Biol 1999; 19: 1744-1750.
50 Moren X. et al. Proteomic and lipidomic analyses of paraoxonase defined high density lipoprotein particles: Association of paraoxonase with the anti-coagulant, protein S. PROTEOMICS - Clin Appl 2016; 10: 230-238.
51 Van Der Meer JHM. et al. TAM receptors, Gas6, and protein S: Roles in inflammation and hemostasis. Blood 2014; 123: 2460-2469.
52 Nyberg P. et al. Stimulation of Sky tyrosine phosphorylation by bovine protein S--domains involved in the receptor-ligand interaction. Eur J Biochem 1997; 246: 147-154.
53 Lew ED. et al. Differential TAM receptor-ligand-phospholipid interactions delimit differential TAM bioactivities. Elife 2014; 3: 1-23.
54 Hansson K, Stenflo J. Post-translational modifications in proteins involved in blood coagulation. J Thromb Haemost 2005; 3: 2633-2648.
55 Chen D. et al. Expression of Human Tissue Factor Pathway Inhibitor on Vascular Smooth Muscle Cells Inhibits Secretion of Macrophage Migration Inhibitory Factor and Attenuates Atherosclerosis in ApoE-/- Mice. Circulation 2015; 131: 1350-1360.
56 Yamashita A. et al. Thrombin generation by intimal tissue factor contributes to thrombus formation on macrophage-rich neointima but not normal intima of hyperlipidemic rabbits. Atherosclerosis 2009; 206: 418-426.
57 Hembrough TA. et al. Tissue Factor Pathway Inhibitor Inhibits Endothelial Cell Proliferation via Association with the Very Low Density Lipoprotein Receptor. J Biol Chem 2001; 276: 12241-12248.
58 Pan S. et al. Vascular-directed tissue factor pathway inhibitor overexpression regulates plasma cholesterol and reduces atherosclerotic plaque development. Circ Res 2009; 105: 713-720.
59 Winckers K. et al. The role of tissue factor pathway inhibitor in atherosclerosis and arterial thrombosis. Blood Rev 2013; 27: 119-132.
60 Seehaus S. et al. Hypercoagulability Inhibits Monocyte Transendothelial Migration Through Protease-Activated Receptor-1-, Phospholipase-C -, Phosphoinositide 3-Kinase-, and Nitric Oxide-Dependent Signaling in Monocytes and Promotes Plaque Stability. Circulation 2009; 120: 774-784.
61 Borissoff JI. et al. Genetic and Pharmacological Modifications of Thrombin Formation in Apolipoprotein E-deficient Mice Determine Atherosclerosis Severity and Atherothrombosis Onset in a Neutrophil-Dependent Manner. Reitsma PH, editor. PLoS One 2013; 8: e55784.
62 Erlich JH. et al. Inhibition of the Tissue Factor-Thrombin Pathway Limits Infarct Size after Myocardial Ischemia-Reperfusion Injury by Reducing Inflammation. Am J Pathol 2000; 157: 1849-1862.
63 Loubele STBG. et al. Active site inhibited factor VIIa attenuates myocardial ischemia/reperfusion injury in mice. J Thromb Haemost 2009; 7: 290-298.
64 Loubele STBG. et al. Activated Protein C Protects Against Myocardial Ischemia/ Reperfusion Injury via Inhibition of Apoptosis and Inflammation. Arterioscler Thromb Vasc Biol 2009; 29: 1087-1092.
65 Costa R. et al. Activated protein C modulates cardiac metabolism and augments autophagy in the ischemic heart. J Thromb Haemost 2012; 10: 1736-1744.
66 Cheng T. et al. Activated protein C blocks p53-mediated apoptosis in ischemic human brain endothelium and is neuroprotective. Nat Med 2003; 9: 338-342.
67 Dömötör E. et al. Activated protein C alters cytosolic calcium flux in human brain endothelium via binding to endothelial protein C receptor and activation of protease activated receptor-1. Blood 2003; 101: 4797-4801.
68 Guo H. et al. Activated protein C prevents neuronal apoptosis via protease activated receptors 1 and 3. Neuron 2004; 41: 563-572.
69 Guo H. et al. Neuroprotective activities of activated protein C mutant with reduced anticoagulant activity. Eur J Neurosci 2009; 29: 1119-1130.
70 Griffin JH. et al. 2016 Scientific Sessions Sol Sherry Distinguished Lecturer in Thrombosis. Arterioscler Thromb Vasc Biol 2016; 36: 2143-2151.