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Published in: BMC Cardiovascular Disorders 1/2015

Open Access 01-12-2015 | Review

Endothelial cell control of thrombosis

Authors: Jonathan W. Yau, Hwee Teoh, Subodh Verma

Published in: BMC Cardiovascular Disorders | Issue 1/2015

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Abstract

Hemostasis encompasses a set of tightly regulated processes that govern blood clotting, platelet activation, and vascular repair. Upon vascular injury, the hemostatic system initiates a series of vascular events and activates extravascular receptors that act in concert to seal off the damage. Blood clotting is subsequently attenuated by a plethora of inhibitors that prevent excessive clot formation and eventual thrombosis. The endothelium which resides at the interface between the blood and surrounding tissues, serves an integral role in the hemostatic system. Depending on specific tissue needs and local stresses, endothelial cells are capable of evoking either antithrombotic or prothrombotic events. Healthy endothelial cells express antiplatelet and anticoagulant agents that prevent platelet aggregation and fibrin formation, respectively. In the face of endothelial dysfunction, endothelial cells trigger fibrin formation, as well as platelet adhesion and aggregation. Finally, endothelial cells release pro-fibrinolytic agents that initiate fibrinolysis to degrade the clot. Taken together, a functional endothelium is essential to maintain hemostasis and prevent thrombosis. Thus, a greater understanding into the role of the endothelium can provide new avenues for exploration and novel therapies for the management of thromboembolisms.
Literature
1.
go back to reference Wolinsky H. A proposal linking clearance of circulating lipoproteins to tissue metabolic activity as a basis for understanding atherogenesis. Circ Res. 1980;47:301–11.PubMed Wolinsky H. A proposal linking clearance of circulating lipoproteins to tissue metabolic activity as a basis for understanding atherogenesis. Circ Res. 1980;47:301–11.PubMed
4.
go back to reference Aird WC. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res. 2007;100:158–73.PubMed Aird WC. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res. 2007;100:158–73.PubMed
5.
go back to reference Monahan-Earley R, Dvorak AM, Aird WC. Evolutionary origins of the blood vascular system and endothelium. J Thromb Haemost. 2013;11 Suppl 1:46–66.PubMed Monahan-Earley R, Dvorak AM, Aird WC. Evolutionary origins of the blood vascular system and endothelium. J Thromb Haemost. 2013;11 Suppl 1:46–66.PubMed
6.
go back to reference Balda MS, Matter K. Tight junctions. J Cell Sci. 1998;111(Pt 5):541–7.PubMed Balda MS, Matter K. Tight junctions. J Cell Sci. 1998;111(Pt 5):541–7.PubMed
7.
go back to reference Cotran RS, Pober JS. Cytokine-endothelial interactions in inflammation, immunity, and vascular injury. J Am Soc Nephrol. 1990;1:225–35.PubMed Cotran RS, Pober JS. Cytokine-endothelial interactions in inflammation, immunity, and vascular injury. J Am Soc Nephrol. 1990;1:225–35.PubMed
8.
go back to reference Ebnet K, Vestweber D. Molecular mechanisms that control leukocyte extravasation: the selectins and the chemokines. Histochem Cell Biol. 1999;112:1–23.PubMed Ebnet K, Vestweber D. Molecular mechanisms that control leukocyte extravasation: the selectins and the chemokines. Histochem Cell Biol. 1999;112:1–23.PubMed
9.
go back to reference Pearson JD. Endothelial cell function and thrombosis. Baillieres Best Pract Res Clin Haematol. 1999;12:329–41.PubMed Pearson JD. Endothelial cell function and thrombosis. Baillieres Best Pract Res Clin Haematol. 1999;12:329–41.PubMed
10.
go back to reference van Hinsbergh VW. Endothelium--role in regulation of coagulation and inflammation. Semin Immunopathol. 2012;34:93–106.PubMed van Hinsbergh VW. Endothelium--role in regulation of coagulation and inflammation. Semin Immunopathol. 2012;34:93–106.PubMed
11.
go back to reference Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP, et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood. 1998;91:3527–61.PubMed Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP, et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood. 1998;91:3527–61.PubMed
12.
go back to reference Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol. 2007;7:803–15.PubMed Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol. 2007;7:803–15.PubMed
13.
go back to reference Lin Z, Kumar A, SenBanerjee S, Staniszewski K, Parmar K, Vaughan DE, et al. Kruppel-like factor 2 (KLF2) regulates endothelial thrombotic function. Circ Res. 2005;96:e48–57.PubMed Lin Z, Kumar A, SenBanerjee S, Staniszewski K, Parmar K, Vaughan DE, et al. Kruppel-like factor 2 (KLF2) regulates endothelial thrombotic function. Circ Res. 2005;96:e48–57.PubMed
14.
go back to reference Zhou G, Hamik A, Nayak L, Tian H, Shi H, Lu Y, et al. Endothelial Kruppel-like factor 4 protects against atherothrombosis in mice. J Clin Invest. 2012;122:4727–31.PubMedPubMedCentral Zhou G, Hamik A, Nayak L, Tian H, Shi H, Lu Y, et al. Endothelial Kruppel-like factor 4 protects against atherothrombosis in mice. J Clin Invest. 2012;122:4727–31.PubMedPubMedCentral
15.
go back to reference Chi JT, Chang HY, Haraldsen G, Jahnsen FL, Troyanskaya OG, Chang DS, et al. Endothelial cell diversity revealed by global expression profiling. Proc Natl Acad Sci U S A. 2003;100:10623–8.PubMedPubMedCentral Chi JT, Chang HY, Haraldsen G, Jahnsen FL, Troyanskaya OG, Chang DS, et al. Endothelial cell diversity revealed by global expression profiling. Proc Natl Acad Sci U S A. 2003;100:10623–8.PubMedPubMedCentral
16.
go back to reference Laszik Z, Mitro A, Taylor Jr FB, Ferrell G, Esmon CT. Human protein C receptor is present primarily on endothelium of large blood vessels: implications for the control of the protein C pathway. Circulation. 1997;96:3633–40.PubMed Laszik Z, Mitro A, Taylor Jr FB, Ferrell G, Esmon CT. Human protein C receptor is present primarily on endothelium of large blood vessels: implications for the control of the protein C pathway. Circulation. 1997;96:3633–40.PubMed
17.
go back to reference Aird WC. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res. 2007;100:174–90.PubMed Aird WC. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res. 2007;100:174–90.PubMed
18.
go back to reference Versteeg HH, Heemskerk JW, Levi M, Reitsma PH. New fundamentals in hemostasis. Physiol Rev. 2013;93:327–58.PubMed Versteeg HH, Heemskerk JW, Levi M, Reitsma PH. New fundamentals in hemostasis. Physiol Rev. 2013;93:327–58.PubMed
19.
go back to reference Davis SF, Yeung AC, Meredith IT, Charbonneau F, Ganz P, Selwyn AP, et al. Early endothelial dysfunction predicts the development of transplant coronary artery disease at 1 year posttransplant. Circulation. 1996;93:457–62.PubMed Davis SF, Yeung AC, Meredith IT, Charbonneau F, Ganz P, Selwyn AP, et al. Early endothelial dysfunction predicts the development of transplant coronary artery disease at 1 year posttransplant. Circulation. 1996;93:457–62.PubMed
20.
go back to reference MacFarlane RG. An enzyme cascade in the blood clotting mechanism, and its function as a biochemical amplifier. Nature. 1964;202:498–9.PubMed MacFarlane RG. An enzyme cascade in the blood clotting mechanism, and its function as a biochemical amplifier. Nature. 1964;202:498–9.PubMed
21.
go back to reference Bode MF, Mackman N. Protective and pathological roles of tissue factor in the heart. Hamostaseologie. 2014;35. Bode MF, Mackman N. Protective and pathological roles of tissue factor in the heart. Hamostaseologie. 2014;35.
22.
go back to reference Drake TA, Morrissey JH, Edgington TS. Selective cellular expression of tissue factor in human tissues. Implications for disorders of hemostasis and thrombosis. Am J Pathol. 1989;134:1087–97.PubMedPubMedCentral Drake TA, Morrissey JH, Edgington TS. Selective cellular expression of tissue factor in human tissues. Implications for disorders of hemostasis and thrombosis. Am J Pathol. 1989;134:1087–97.PubMedPubMedCentral
23.
go back to reference Owens III AP, Mackman N. Role of tissue factor in atherothrombosis. Curr Atheroscler Rep. 2012;14:394–401.PubMed Owens III AP, Mackman N. Role of tissue factor in atherothrombosis. Curr Atheroscler Rep. 2012;14:394–401.PubMed
24.
go back to reference Borissoff JI, Spronk HM, ten Cate H. The hemostatic system as a modulator of atherosclerosis. N Engl J Med. 2011;364:1746–60.PubMed Borissoff JI, Spronk HM, ten Cate H. The hemostatic system as a modulator of atherosclerosis. N Engl J Med. 2011;364:1746–60.PubMed
25.
go back to reference Marmur JD, Thiruvikraman SV, Fyfe BS, Guha A, Sharma SK, Ambrose JA, et al. Identification of active tissue factor in human coronary atheroma. Circulation. 1996;94:1226–32.PubMed Marmur JD, Thiruvikraman SV, Fyfe BS, Guha A, Sharma SK, Ambrose JA, et al. Identification of active tissue factor in human coronary atheroma. Circulation. 1996;94:1226–32.PubMed
26.
go back to reference Tremoli E, Camera M, Toschi V, Colli S. Tissue factor in atherosclerosis. Atherosclerosis. 1999;144:273–83.PubMed Tremoli E, Camera M, Toschi V, Colli S. Tissue factor in atherosclerosis. Atherosclerosis. 1999;144:273–83.PubMed
27.
go back to reference Parry GC, Mackman N. Transcriptional regulation of tissue factor expression in human endothelial cells. Arterioscler Thromb Vasc Biol. 1995;15:612–21.PubMed Parry GC, Mackman N. Transcriptional regulation of tissue factor expression in human endothelial cells. Arterioscler Thromb Vasc Biol. 1995;15:612–21.PubMed
28.
go back to reference Colucci M, Balconi G, Lorenzet R, Pietra A, Locati D, Donati MB, et al. Cultured human endothelial cells generate tissue factor in response to endotoxin. J Clin Invest. 1983;71:1893–6.PubMedPubMedCentral Colucci M, Balconi G, Lorenzet R, Pietra A, Locati D, Donati MB, et al. Cultured human endothelial cells generate tissue factor in response to endotoxin. J Clin Invest. 1983;71:1893–6.PubMedPubMedCentral
29.
go back to reference Bevilacqua MP, Pober JS, Majeau GR, Fiers W, Cotran RS, Gimbrone Jr MA. Recombinant tumor necrosis factor induces procoagulant activity in cultured human vascular endothelium: characterization and comparison with the actions of interleukin 1. Proc Natl Acad Sci U S A. 1986;83:4533–7.PubMedPubMedCentral Bevilacqua MP, Pober JS, Majeau GR, Fiers W, Cotran RS, Gimbrone Jr MA. Recombinant tumor necrosis factor induces procoagulant activity in cultured human vascular endothelium: characterization and comparison with the actions of interleukin 1. Proc Natl Acad Sci U S A. 1986;83:4533–7.PubMedPubMedCentral
30.
go back to reference Houston P, Dickson MC, Ludbrook V, White B, Schwachtgen JL, McVey JH, et al. Fluid shear stress induction of the tissue factor promoter in vitro and in vivo is mediated by Egr-1. Arterioscler Thromb Vasc Biol. 1999;19:281–9.PubMed Houston P, Dickson MC, Ludbrook V, White B, Schwachtgen JL, McVey JH, et al. Fluid shear stress induction of the tissue factor promoter in vitro and in vivo is mediated by Egr-1. Arterioscler Thromb Vasc Biol. 1999;19:281–9.PubMed
31.
go back to reference Mechtcheriakova D, Schabbauer G, Lucerna M, Clauss M, De Martin R, Binder BR, et al. Specificity, diversity, and convergence in VEGF and TNF-alpha signaling events leading to tissue factor up-regulation via EGR-1 in endothelial cells. FASEB J. 2001;15:230–42.PubMed Mechtcheriakova D, Schabbauer G, Lucerna M, Clauss M, De Martin R, Binder BR, et al. Specificity, diversity, and convergence in VEGF and TNF-alpha signaling events leading to tissue factor up-regulation via EGR-1 in endothelial cells. FASEB J. 2001;15:230–42.PubMed
32.
go back to reference Bochkov VN, Mechtcheriakova D, Lucerna M, Huber J, Malli R, Graier WF, et al. Oxidized phospholipids stimulate tissue factor expression in human endothelial cells via activation of ERK/EGR-1 and Ca(++)/NFAT. Blood. 2002;99:199–206.PubMed Bochkov VN, Mechtcheriakova D, Lucerna M, Huber J, Malli R, Graier WF, et al. Oxidized phospholipids stimulate tissue factor expression in human endothelial cells via activation of ERK/EGR-1 and Ca(++)/NFAT. Blood. 2002;99:199–206.PubMed
33.
go back to reference Zhou L, Stordeur P, de Lavareille A, Thielemans K, Capel P, Goldman M, et al. CD40 engagement on endothelial cells promotes tissue factor-dependent procoagulant activity. Thromb Haemost. 1998;79:1025–8.PubMed Zhou L, Stordeur P, de Lavareille A, Thielemans K, Capel P, Goldman M, et al. CD40 engagement on endothelial cells promotes tissue factor-dependent procoagulant activity. Thromb Haemost. 1998;79:1025–8.PubMed
34.
go back to reference Miller DL, Yaron R, Yellin MJ. CD40L-CD40 interactions regulate endothelial cell surface tissue factor and thrombomodulin expression. J Leukoc Biol. 1998;63:373–9.PubMed Miller DL, Yaron R, Yellin MJ. CD40L-CD40 interactions regulate endothelial cell surface tissue factor and thrombomodulin expression. J Leukoc Biol. 1998;63:373–9.PubMed
35.
go back to reference Slupsky JR, Kalbas M, Willuweit A, Henn V, Kroczek RA, Muller-Berghaus G. Activated platelets induce tissue factor expression on human umbilical vein endothelial cells by ligation of CD40. Thromb Haemost. 1998;80:1008–14.PubMed Slupsky JR, Kalbas M, Willuweit A, Henn V, Kroczek RA, Muller-Berghaus G. Activated platelets induce tissue factor expression on human umbilical vein endothelial cells by ligation of CD40. Thromb Haemost. 1998;80:1008–14.PubMed
36.
go back to reference Bavendiek U, Libby P, Kilbride M, Reynolds R, Mackman N, Schonbeck U. Induction of tissue factor expression in human endothelial cells by CD40 ligand is mediated via activator protein 1, nuclear factor kappa B, and Egr-1. J Biol Chem. 2002;277:25032–9.PubMed Bavendiek U, Libby P, Kilbride M, Reynolds R, Mackman N, Schonbeck U. Induction of tissue factor expression in human endothelial cells by CD40 ligand is mediated via activator protein 1, nuclear factor kappa B, and Egr-1. J Biol Chem. 2002;277:25032–9.PubMed
37.
go back to reference Vega-Ostertag M, Casper K, Swerlick R, Ferrara D, Harris EN, Pierangeli SS. Involvement of p38 MAPK in the up-regulation of tissue factor on endothelial cells by antiphospholipid antibodies. Arthritis Rheum. 2005;52:1545–54.PubMed Vega-Ostertag M, Casper K, Swerlick R, Ferrara D, Harris EN, Pierangeli SS. Involvement of p38 MAPK in the up-regulation of tissue factor on endothelial cells by antiphospholipid antibodies. Arthritis Rheum. 2005;52:1545–54.PubMed
38.
go back to reference Del Turco S, Basta G, Lazzerini G, Chancharme L, Lerond L, De Caterina R. Involvement of the TP receptor in TNF-alpha-induced endothelial tissue factor expression. Vascul Pharmacol. 2014;62:49–56.PubMed Del Turco S, Basta G, Lazzerini G, Chancharme L, Lerond L, De Caterina R. Involvement of the TP receptor in TNF-alpha-induced endothelial tissue factor expression. Vascul Pharmacol. 2014;62:49–56.PubMed
39.
go back to reference Szotowski B, Antoniak S, Poller W, Schultheiss HP, Rauch U. Procoagulant soluble tissue factor is released from endothelial cells in response to inflammatory cytokines. Circ Res. 2005;96:1233–9.PubMed Szotowski B, Antoniak S, Poller W, Schultheiss HP, Rauch U. Procoagulant soluble tissue factor is released from endothelial cells in response to inflammatory cytokines. Circ Res. 2005;96:1233–9.PubMed
40.
go back to reference Bode M, Mackman N. Regulation of tissue factor gene expression in monocytes and endothelial cells: thromboxane A2 as a new player. Vascul Pharmacol. 2014;62:57–62.PubMedPubMedCentral Bode M, Mackman N. Regulation of tissue factor gene expression in monocytes and endothelial cells: thromboxane A2 as a new player. Vascul Pharmacol. 2014;62:57–62.PubMedPubMedCentral
41.
go back to reference Semeraro N, Triggiani R, Montemurro P, Cavallo LG, Colucci M. Enhanced endothelial tissue factor but normal thrombomodulin in endotoxin-treated rabbits. Thromb Res. 1993;71:479–86.PubMed Semeraro N, Triggiani R, Montemurro P, Cavallo LG, Colucci M. Enhanced endothelial tissue factor but normal thrombomodulin in endotoxin-treated rabbits. Thromb Res. 1993;71:479–86.PubMed
42.
go back to reference Song D, Ye X, Xu H, Liu SF. Activation of endothelial intrinsic NF-{kappa}B pathway impairs protein C anticoagulation mechanism and promotes coagulation in endotoxemic mice. Blood. 2009;114:2521–9.PubMedPubMedCentral Song D, Ye X, Xu H, Liu SF. Activation of endothelial intrinsic NF-{kappa}B pathway impairs protein C anticoagulation mechanism and promotes coagulation in endotoxemic mice. Blood. 2009;114:2521–9.PubMedPubMedCentral
43.
go back to reference Erlich J, Fearns C, Mathison J, Ulevitch RJ, Mackman N. Lipopolysaccharide induction of tissue factor expression in rabbits. Infect Immun. 1999;67:2540–6.PubMedPubMedCentral Erlich J, Fearns C, Mathison J, Ulevitch RJ, Mackman N. Lipopolysaccharide induction of tissue factor expression in rabbits. Infect Immun. 1999;67:2540–6.PubMedPubMedCentral
44.
go back to reference Pawlinski R, Pedersen B, Kehrle B, Aird WC, Frank RD, Guha M, et al. Regulation of tissue factor and inflammatory mediators by Egr-1 in a mouse endotoxemia model. Blood. 2003;101:3940–7.PubMed Pawlinski R, Pedersen B, Kehrle B, Aird WC, Frank RD, Guha M, et al. Regulation of tissue factor and inflammatory mediators by Egr-1 in a mouse endotoxemia model. Blood. 2003;101:3940–7.PubMed
45.
go back to reference Chen VM, Hogg PJ. Encryption and decryption of tissue factor. J Thromb Haemost. 2013;11 Suppl 1:277–84.PubMed Chen VM, Hogg PJ. Encryption and decryption of tissue factor. J Thromb Haemost. 2013;11 Suppl 1:277–84.PubMed
46.
go back to reference Sparkenbaugh EM, Chantrathammachart P, Mickelson J, van Ryn J, Hebbel RP, Monroe DM, et al. Differential contribution of FXa and thrombin to vascular inflammation in a mouse model of sickle cell disease. Blood. 2014;123:1747–56.PubMedPubMedCentral Sparkenbaugh EM, Chantrathammachart P, Mickelson J, van Ryn J, Hebbel RP, Monroe DM, et al. Differential contribution of FXa and thrombin to vascular inflammation in a mouse model of sickle cell disease. Blood. 2014;123:1747–56.PubMedPubMedCentral
47.
go back to reference Arderiu G, Pena E, Badimon L. Angiogenic microvascular endothelial cells release microparticles rich in tissue factor that promotes postischemic collateral vessel formation. Arterioscler Thromb Vasc Biol. 2015;35:348–57.PubMed Arderiu G, Pena E, Badimon L. Angiogenic microvascular endothelial cells release microparticles rich in tissue factor that promotes postischemic collateral vessel formation. Arterioscler Thromb Vasc Biol. 2015;35:348–57.PubMed
48.
go back to reference Schousboe I. Binding of activated Factor XII to endothelial cells affects its inactivation by the C1-esterase inhibitor. Eur J Biochem. 2003;270:111–8.PubMed Schousboe I. Binding of activated Factor XII to endothelial cells affects its inactivation by the C1-esterase inhibitor. Eur J Biochem. 2003;270:111–8.PubMed
49.
go back to reference Webster WP, Zukoski CF, Hutchin P, Reddick RL, Mandel SR, Penick GD. Plasma factor VIII synthesis and control as revealed by canine organ transplantation. Am J Physiol. 1971;220:1147–54.PubMed Webster WP, Zukoski CF, Hutchin P, Reddick RL, Mandel SR, Penick GD. Plasma factor VIII synthesis and control as revealed by canine organ transplantation. Am J Physiol. 1971;220:1147–54.PubMed
50.
go back to reference Do H, Healey JF, Waller EK, Lollar P. Expression of factor VIII by murine liver sinusoidal endothelial cells. J Biol Chem. 1999;274:19587–92.PubMed Do H, Healey JF, Waller EK, Lollar P. Expression of factor VIII by murine liver sinusoidal endothelial cells. J Biol Chem. 1999;274:19587–92.PubMed
51.
go back to reference Norman JC, Covelli VH, Sise HS. Transplantation of the spleen: experimental cure of hemophilia. Surgery. 1968;64:1–14.PubMed Norman JC, Covelli VH, Sise HS. Transplantation of the spleen: experimental cure of hemophilia. Surgery. 1968;64:1–14.PubMed
52.
go back to reference Veltkamp JJ, Asfaou E, van de Torren K, van der Does JA, van Tilburg NH, Pauwels EK. Extrahepatic factor VIII synthesis. Lung transplants in hemophilic dogs. Transplantation. 1974;18:56–62.PubMed Veltkamp JJ, Asfaou E, van de Torren K, van der Does JA, van Tilburg NH, Pauwels EK. Extrahepatic factor VIII synthesis. Lung transplants in hemophilic dogs. Transplantation. 1974;18:56–62.PubMed
53.
go back to reference Fahs SA, Hille MT, Shi Q, Weiler H, Montgomery RR. A conditional knockout mouse model reveals endothelial cells as the principal and possibly exclusive source of plasma factor VIII. Blood. 2014;123:3706–13.PubMedPubMedCentral Fahs SA, Hille MT, Shi Q, Weiler H, Montgomery RR. A conditional knockout mouse model reveals endothelial cells as the principal and possibly exclusive source of plasma factor VIII. Blood. 2014;123:3706–13.PubMedPubMedCentral
54.
go back to reference Everett LA, Cleuren AC, Khoriaty RN, Ginsburg D. Murine coagulation factor VIII is synthesized in endothelial cells. Blood. 2014;123:3697–705.PubMedPubMedCentral Everett LA, Cleuren AC, Khoriaty RN, Ginsburg D. Murine coagulation factor VIII is synthesized in endothelial cells. Blood. 2014;123:3697–705.PubMedPubMedCentral
55.
go back to reference Wagner DD, Marder VJ. Biosynthesis of von Willebrand protein by human endothelial cells: processing steps and their intracellular localization. J Cell Biol. 1984;99:2123–30.PubMed Wagner DD, Marder VJ. Biosynthesis of von Willebrand protein by human endothelial cells: processing steps and their intracellular localization. J Cell Biol. 1984;99:2123–30.PubMed
56.
go back to reference Dubois C, Panicot-Dubois L, Gainor JF, Furie BC, Furie B. Thrombin-initiated platelet activation in vivo is vWF independent during thrombus formation in a laser injury model. J Clin Invest. 2007;117:953–60.PubMedPubMedCentral Dubois C, Panicot-Dubois L, Gainor JF, Furie BC, Furie B. Thrombin-initiated platelet activation in vivo is vWF independent during thrombus formation in a laser injury model. J Clin Invest. 2007;117:953–60.PubMedPubMedCentral
57.
go back to reference Vlot AJ, Koppelman SJ, van den Berg MH, Bouma BN, Sixma JJ. The affinity and stoichiometry of binding of human factor VIII to von Willebrand factor. Blood. 1995;85:3150–7.PubMed Vlot AJ, Koppelman SJ, van den Berg MH, Bouma BN, Sixma JJ. The affinity and stoichiometry of binding of human factor VIII to von Willebrand factor. Blood. 1995;85:3150–7.PubMed
58.
go back to reference Denis C, Methia N, Frenette PS, Rayburn H, Ullman-Cullere M, Hynes RO, et al. A mouse model of severe von Willebrand disease: defects in hemostasis and thrombosis. Proc Natl Acad Sci U S A. 1998;95:9524–9.PubMedPubMedCentral Denis C, Methia N, Frenette PS, Rayburn H, Ullman-Cullere M, Hynes RO, et al. A mouse model of severe von Willebrand disease: defects in hemostasis and thrombosis. Proc Natl Acad Sci U S A. 1998;95:9524–9.PubMedPubMedCentral
59.
go back to reference Sadler JE, Budde U, Eikenboom JC, Favaloro EJ, Hill FG, Holmberg L, et al. Update on the pathophysiology and classification of von Willebrand disease: a report of the Subcommittee on von Willebrand factor. J Thromb Haemost. 2006;4:2103–14.PubMed Sadler JE, Budde U, Eikenboom JC, Favaloro EJ, Hill FG, Holmberg L, et al. Update on the pathophysiology and classification of von Willebrand disease: a report of the Subcommittee on von Willebrand factor. J Thromb Haemost. 2006;4:2103–14.PubMed
60.
go back to reference Giblin JP, Hewlett LJ, Hannah MJ. Basal secretion of von Willebrand factor from human endothelial cells. Blood. 2008;112:957–64.PubMed Giblin JP, Hewlett LJ, Hannah MJ. Basal secretion of von Willebrand factor from human endothelial cells. Blood. 2008;112:957–64.PubMed
61.
go back to reference Johnsen J, Lopez JA. VWF secretion: what’s in a name? Blood. 2008;112:926–7.PubMed Johnsen J, Lopez JA. VWF secretion: what’s in a name? Blood. 2008;112:926–7.PubMed
62.
go back to reference Levine JD, Harlan JM, Harker LA, Joseph ML, Counts RB. Thrombin-mediated release of factor VIII antigen from human umbilical vein endothelial cells in culture. Blood. 1982;60:531–4.PubMed Levine JD, Harlan JM, Harker LA, Joseph ML, Counts RB. Thrombin-mediated release of factor VIII antigen from human umbilical vein endothelial cells in culture. Blood. 1982;60:531–4.PubMed
63.
go back to reference Rusu L, Andreeva A, Visintine DJ, Kim K, Vogel SM, Stojanovic-Terpo A, et al. G protein-dependent basal and evoked endothelial cell vWF secretion. Blood. 2014;123:442–50.PubMedPubMedCentral Rusu L, Andreeva A, Visintine DJ, Kim K, Vogel SM, Stojanovic-Terpo A, et al. G protein-dependent basal and evoked endothelial cell vWF secretion. Blood. 2014;123:442–50.PubMedPubMedCentral
64.
go back to reference Torisu T, Torisu K, Lee IH, Liu J, Malide D, Combs CA, et al. Autophagy regulates endothelial cell processing, maturation and secretion of von Willebrand factor. Nat Med. 2013;19:1281–7.PubMedPubMedCentral Torisu T, Torisu K, Lee IH, Liu J, Malide D, Combs CA, et al. Autophagy regulates endothelial cell processing, maturation and secretion of von Willebrand factor. Nat Med. 2013;19:1281–7.PubMedPubMedCentral
65.
go back to reference Dmitrieva NI, Burg MB. Secretion of von Willebrand factor by endothelial cells links sodium to hypercoagulability and thrombosis. Proc Natl Acad Sci U S A. 2014;111:6485–90.PubMedPubMedCentral Dmitrieva NI, Burg MB. Secretion of von Willebrand factor by endothelial cells links sodium to hypercoagulability and thrombosis. Proc Natl Acad Sci U S A. 2014;111:6485–90.PubMedPubMedCentral
66.
go back to reference Watson SP. Platelet activation by extracellular matrix proteins in haemostasis and thrombosis. Curr Pharm Des. 2009;15:1358–72.PubMed Watson SP. Platelet activation by extracellular matrix proteins in haemostasis and thrombosis. Curr Pharm Des. 2009;15:1358–72.PubMed
67.
go back to reference Schmidt VA, Nierman WC, Maglott DR, Cupit LD, Moskowitz KA, Wainer JA, et al. The human proteinase-activated receptor-3 (PAR-3) gene. Identification within a Par gene cluster and characterization in vascular endothelial cells and platelets. J Biol Chem. 1998;273:15061–8.PubMed Schmidt VA, Nierman WC, Maglott DR, Cupit LD, Moskowitz KA, Wainer JA, et al. The human proteinase-activated receptor-3 (PAR-3) gene. Identification within a Par gene cluster and characterization in vascular endothelial cells and platelets. J Biol Chem. 1998;273:15061–8.PubMed
68.
go back to reference O’Brien PJ, Prevost N, Molino M, Hollinger MK, Woolkalis MJ, Woulfe DS, et al. Thrombin responses in human endothelial cells. Contributions from receptors other than PAR1 include the transactivation of PAR2 by thrombin-cleaved PAR1. J Biol Chem. 2000;275:13502–9.PubMed O’Brien PJ, Prevost N, Molino M, Hollinger MK, Woolkalis MJ, Woulfe DS, et al. Thrombin responses in human endothelial cells. Contributions from receptors other than PAR1 include the transactivation of PAR2 by thrombin-cleaved PAR1. J Biol Chem. 2000;275:13502–9.PubMed
69.
go back to reference Adams MN, Ramachandran R, Yau MK, Suen JY, Fairlie DP, Hollenberg MD, et al. Structure, function and pathophysiology of protease activated receptors. Pharmacol Ther. 2011;130:248–82.PubMed Adams MN, Ramachandran R, Yau MK, Suen JY, Fairlie DP, Hollenberg MD, et al. Structure, function and pathophysiology of protease activated receptors. Pharmacol Ther. 2011;130:248–82.PubMed
70.
go back to reference Coughlin SR. Thrombin signalling and protease-activated receptors. Nature. 2000;407:258–64.PubMed Coughlin SR. Thrombin signalling and protease-activated receptors. Nature. 2000;407:258–64.PubMed
71.
go back to reference Coughlin SR. Protease-activated receptors in hemostasis, thrombosis and vascular biology. J Thromb Haemost. 2005;3:1800–14.PubMed Coughlin SR. Protease-activated receptors in hemostasis, thrombosis and vascular biology. J Thromb Haemost. 2005;3:1800–14.PubMed
72.
go back to reference Esmon CT, Esmon NL. The link between vascular features and thrombosis. Annu Rev Physiol. 2011;73:503–14.PubMed Esmon CT, Esmon NL. The link between vascular features and thrombosis. Annu Rev Physiol. 2011;73:503–14.PubMed
73.
74.
go back to reference Sandset PM, Abildgaard U, Larsen ML. Heparin induces release of extrinsic coagulation pathway inhibitor (EPI). Thromb Res. 1988;50:803–13.PubMed Sandset PM, Abildgaard U, Larsen ML. Heparin induces release of extrinsic coagulation pathway inhibitor (EPI). Thromb Res. 1988;50:803–13.PubMed
75.
go back to reference Hansen JB, Svensson B, Olsen R, Ezban M, Osterud B, Paulssen RH. Heparin induces synthesis and secretion of tissue factor pathway inhibitor from endothelial cells in vitro. Thromb Haemost. 2000;83:937–43.PubMed Hansen JB, Svensson B, Olsen R, Ezban M, Osterud B, Paulssen RH. Heparin induces synthesis and secretion of tissue factor pathway inhibitor from endothelial cells in vitro. Thromb Haemost. 2000;83:937–43.PubMed
76.
go back to reference Lupu C, Poulsen E, Roquefeuil S, Westmuckett AD, Kakkar VV, Lupu F. Cellular effects of heparin on the production and release of tissue factor pathway inhibitor in human endothelial cells in culture. Arterioscler Thromb Vasc Biol. 1999;19:2251–62.PubMed Lupu C, Poulsen E, Roquefeuil S, Westmuckett AD, Kakkar VV, Lupu F. Cellular effects of heparin on the production and release of tissue factor pathway inhibitor in human endothelial cells in culture. Arterioscler Thromb Vasc Biol. 1999;19:2251–62.PubMed
77.
go back to reference Wood JP, Ellery PE, Maroney SA, Mast AE. Protein S is a cofactor for platelet and endothelial tissue factor pathway inhibitor-alpha but not for cell surface-associated tissue factor pathway inhibitor. Arterioscler Thromb Vasc Biol. 2014;34:169–76.PubMed Wood JP, Ellery PE, Maroney SA, Mast AE. Protein S is a cofactor for platelet and endothelial tissue factor pathway inhibitor-alpha but not for cell surface-associated tissue factor pathway inhibitor. Arterioscler Thromb Vasc Biol. 2014;34:169–76.PubMed
78.
go back to reference Huang ZF, Higuchi D, Lasky N, Broze Jr GJ. Tissue factor pathway inhibitor gene disruption produces intrauterine lethality in mice. Blood. 1997;90:944–51.PubMed Huang ZF, Higuchi D, Lasky N, Broze Jr GJ. Tissue factor pathway inhibitor gene disruption produces intrauterine lethality in mice. Blood. 1997;90:944–51.PubMed
79.
go back to reference White TA, Johnson T, Zarzhevsky N, Tom C, Delacroix S, Holroyd EW, et al. Endothelial-derived tissue factor pathway inhibitor regulates arterial thrombosis but is not required for development or hemostasis. Blood. 2010;116:1787–94.PubMedPubMedCentral White TA, Johnson T, Zarzhevsky N, Tom C, Delacroix S, Holroyd EW, et al. Endothelial-derived tissue factor pathway inhibitor regulates arterial thrombosis but is not required for development or hemostasis. Blood. 2010;116:1787–94.PubMedPubMedCentral
80.
go back to reference Dahm A, Van Hylckama Vlieg A, Bendz B, Rosendaal F, Bertina RM, Sandset PM. Low levels of tissue factor pathway inhibitor (TFPI) increase the risk of venous thrombosis. Blood. 2003;101:4387–92.PubMed Dahm A, Van Hylckama Vlieg A, Bendz B, Rosendaal F, Bertina RM, Sandset PM. Low levels of tissue factor pathway inhibitor (TFPI) increase the risk of venous thrombosis. Blood. 2003;101:4387–92.PubMed
81.
go back to reference Morange PE, Simon C, Alessi MC, Luc G, Arveiler D, Ferrieres J, et al. Endothelial cell markers and the risk of coronary heart disease: the Prospective Epidemiological Study of Myocardial Infarction (PRIME) study. Circulation. 2004;109:1343–8.PubMed Morange PE, Simon C, Alessi MC, Luc G, Arveiler D, Ferrieres J, et al. Endothelial cell markers and the risk of coronary heart disease: the Prospective Epidemiological Study of Myocardial Infarction (PRIME) study. Circulation. 2004;109:1343–8.PubMed
82.
go back to reference Martin FA, McLoughlin A, Rochfort KD, Davenport C, Murphy RP, Cummins PM. Regulation of thrombomodulin expression and release in human aortic endothelial cells by cyclic strain. PLoS One. 2014;9:e108254.PubMedPubMedCentral Martin FA, McLoughlin A, Rochfort KD, Davenport C, Murphy RP, Cummins PM. Regulation of thrombomodulin expression and release in human aortic endothelial cells by cyclic strain. PLoS One. 2014;9:e108254.PubMedPubMedCentral
83.
go back to reference Anastasiou G, Gialeraki A, Merkouri E, Politou M, Travlou A. Thrombomodulin as a regulator of the anticoagulant pathway: implication in the development of thrombosis. Blood Coagul Fibrinolysis. 2012;23:1–10.PubMed Anastasiou G, Gialeraki A, Merkouri E, Politou M, Travlou A. Thrombomodulin as a regulator of the anticoagulant pathway: implication in the development of thrombosis. Blood Coagul Fibrinolysis. 2012;23:1–10.PubMed
84.
go back to reference Griffin JH, Zlokovic BV, Mosnier LO. Protein C anticoagulant and cytoprotective pathways. Int J Hematol. 2012;95:333–45.PubMedPubMedCentral Griffin JH, Zlokovic BV, Mosnier LO. Protein C anticoagulant and cytoprotective pathways. Int J Hematol. 2012;95:333–45.PubMedPubMedCentral
85.
go back to reference Owen WG, Esmon CT. Functional properties of an endothelial cell cofactor for thrombin-catalyzed activation of protein C. J Biol Chem. 1981;256:5532–5.PubMed Owen WG, Esmon CT. Functional properties of an endothelial cell cofactor for thrombin-catalyzed activation of protein C. J Biol Chem. 1981;256:5532–5.PubMed
86.
go back to reference Fukudome K, Esmon CT. Identification, cloning, and regulation of a novel endothelial cell protein C/activated protein C receptor. J Biol Chem. 1994;269:26486–91.PubMed Fukudome K, Esmon CT. Identification, cloning, and regulation of a novel endothelial cell protein C/activated protein C receptor. J Biol Chem. 1994;269:26486–91.PubMed
87.
go back to reference Stearns-Kurosawa DJ, Kurosawa S, Mollica JS, Ferrell GL, Esmon CT. The endothelial cell protein C receptor augments protein C activation by the thrombin-thrombomodulin complex. Proc Natl Acad Sci U S A. 1996;93:10212–6.PubMedPubMedCentral Stearns-Kurosawa DJ, Kurosawa S, Mollica JS, Ferrell GL, Esmon CT. The endothelial cell protein C receptor augments protein C activation by the thrombin-thrombomodulin complex. Proc Natl Acad Sci U S A. 1996;93:10212–6.PubMedPubMedCentral
88.
go back to reference Fukudome K, Kurosawa S, Stearns-Kurosawa DJ, He X, Rezaie AR, Esmon CT. The endothelial cell protein C receptor. Cell surface expression and direct ligand binding by the soluble receptor. J Biol Chem. 1996;271:17491–8.PubMed Fukudome K, Kurosawa S, Stearns-Kurosawa DJ, He X, Rezaie AR, Esmon CT. The endothelial cell protein C receptor. Cell surface expression and direct ligand binding by the soluble receptor. J Biol Chem. 1996;271:17491–8.PubMed
89.
go back to reference Gu JM, Crawley JT, Ferrell G, Zhang F, Li W, Esmon NL, et al. Disruption of the endothelial cell protein C receptor gene in mice causes placental thrombosis and early embryonic lethality. J Biol Chem. 2002;277:43335–43.PubMed Gu JM, Crawley JT, Ferrell G, Zhang F, Li W, Esmon NL, et al. Disruption of the endothelial cell protein C receptor gene in mice causes placental thrombosis and early embryonic lethality. J Biol Chem. 2002;277:43335–43.PubMed
90.
go back to reference Collen D, Lijnen HR. The tissue-type plasminogen activator story. Arterioscler Thromb Vasc Biol. 2009;29:1151–5.PubMed Collen D, Lijnen HR. The tissue-type plasminogen activator story. Arterioscler Thromb Vasc Biol. 2009;29:1151–5.PubMed
91.
go back to reference Rijken DC, Lijnen HR. New insights into the molecular mechanisms of the fibrinolytic system. J Thromb Haemost. 2009;7:4–13.PubMed Rijken DC, Lijnen HR. New insights into the molecular mechanisms of the fibrinolytic system. J Thromb Haemost. 2009;7:4–13.PubMed
92.
go back to reference Huber D, Cramer EM, Kaufmann JE, Meda P, Masse JM, Kruithof EK, et al. Tissue-type plasminogen activator (t-PA) is stored in Weibel-Palade bodies in human endothelial cells both in vitro and in vivo. Blood. 2002;99:3637–45.PubMed Huber D, Cramer EM, Kaufmann JE, Meda P, Masse JM, Kruithof EK, et al. Tissue-type plasminogen activator (t-PA) is stored in Weibel-Palade bodies in human endothelial cells both in vitro and in vivo. Blood. 2002;99:3637–45.PubMed
93.
go back to reference Emeis JJ, Eijnden-Schrauwen Y, van den Hoogen CM, de Priester W, Westmuckett A, Lupu F. An endothelial storage granule for tissue-type plasminogen activator. J Cell Biol. 1997;139:245–56.PubMedPubMedCentral Emeis JJ, Eijnden-Schrauwen Y, van den Hoogen CM, de Priester W, Westmuckett A, Lupu F. An endothelial storage granule for tissue-type plasminogen activator. J Cell Biol. 1997;139:245–56.PubMedPubMedCentral
94.
go back to reference Carmeliet P, Schoonjans L, Kieckens L, Ream B, Degen J, Bronson R, et al. Physiological consequences of loss of plasminogen activator gene function in mice. Nature. 1994;368:419–24.PubMed Carmeliet P, Schoonjans L, Kieckens L, Ream B, Degen J, Bronson R, et al. Physiological consequences of loss of plasminogen activator gene function in mice. Nature. 1994;368:419–24.PubMed
95.
go back to reference Lijnen HR, Moons L, Beelen V, Carmelie P, Collen D. Biological effects of combined inactivation of plasminogen activator and plasminogen activator inhibitor-1 gene function in mice. Thromb Haemost. 1995;74:1126–31.PubMed Lijnen HR, Moons L, Beelen V, Carmelie P, Collen D. Biological effects of combined inactivation of plasminogen activator and plasminogen activator inhibitor-1 gene function in mice. Thromb Haemost. 1995;74:1126–31.PubMed
96.
go back to reference Giles AR, Nesheim ME, Herring SW, Hoogendoorn H, Stump DC, Heldebrant CM. The fibrinolytic potential of the normal primate following the generation of thrombin in vivo. Thromb Haemost. 1990;63:476–81.PubMed Giles AR, Nesheim ME, Herring SW, Hoogendoorn H, Stump DC, Heldebrant CM. The fibrinolytic potential of the normal primate following the generation of thrombin in vivo. Thromb Haemost. 1990;63:476–81.PubMed
97.
go back to reference Chung DW, Fujikawa K. Processing of von Willebrand factor by ADAMTS-13. Biochemistry. 2002;41:11065–70.PubMed Chung DW, Fujikawa K. Processing of von Willebrand factor by ADAMTS-13. Biochemistry. 2002;41:11065–70.PubMed
98.
go back to reference Turner N, Nolasco L, Tao Z, Dong JF, Moake J. Human endothelial cells synthesize and release ADAMTS-13. J Thromb Haemost. 2006;4:1396–404.PubMed Turner N, Nolasco L, Tao Z, Dong JF, Moake J. Human endothelial cells synthesize and release ADAMTS-13. J Thromb Haemost. 2006;4:1396–404.PubMed
99.
go back to reference Moake JL. Thrombotic microangiopathies. N Engl J Med. 2002;347:589–600.PubMed Moake JL. Thrombotic microangiopathies. N Engl J Med. 2002;347:589–600.PubMed
100.
go back to reference Petraglia AL, Marky AH, Walker C, Thiyagarajan M, Zlokovic BV. Activated protein C is neuroprotective and mediates new blood vessel formation and neurogenesis after controlled cortical impact. Neurosurgery. 2010;66:165–71.PubMedPubMedCentral Petraglia AL, Marky AH, Walker C, Thiyagarajan M, Zlokovic BV. Activated protein C is neuroprotective and mediates new blood vessel formation and neurogenesis after controlled cortical impact. Neurosurgery. 2010;66:165–71.PubMedPubMedCentral
101.
go back to reference Ribes JA, Ni F, Wagner DD, Francis CW. Mediation of fibrin-induced release of von Willebrand factor from cultured endothelial cells by the fibrin beta chain. J Clin Invest. 1989;84:435–42.PubMedPubMedCentral Ribes JA, Ni F, Wagner DD, Francis CW. Mediation of fibrin-induced release of von Willebrand factor from cultured endothelial cells by the fibrin beta chain. J Clin Invest. 1989;84:435–42.PubMedPubMedCentral
102.
go back to reference Shaikh FM, Callanan A, Kavanagh EG, Burke PE, Grace PA, McGloughlin TM. Fibrin: a natural biodegradable scaffold in vascular tissue engineering. Cells Tissues Organs. 2008;188:333–46.PubMed Shaikh FM, Callanan A, Kavanagh EG, Burke PE, Grace PA, McGloughlin TM. Fibrin: a natural biodegradable scaffold in vascular tissue engineering. Cells Tissues Organs. 2008;188:333–46.PubMed
103.
go back to reference Wijelath ES, Murray J, Rahman S, Patel Y, Ishida A, Strand K, et al. Novel vascular endothelial growth factor binding domains of fibronectin enhance vascular endothelial growth factor biological activity. Circ Res. 2002;91:25–31.PubMed Wijelath ES, Murray J, Rahman S, Patel Y, Ishida A, Strand K, et al. Novel vascular endothelial growth factor binding domains of fibronectin enhance vascular endothelial growth factor biological activity. Circ Res. 2002;91:25–31.PubMed
104.
go back to reference Italiano Jr JE, Richardson JL, Patel-Hett S, Battinelli E, Zaslavsky A, Short S, et al. Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood. 2008;111:1227–33.PubMedPubMedCentral Italiano Jr JE, Richardson JL, Patel-Hett S, Battinelli E, Zaslavsky A, Short S, et al. Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood. 2008;111:1227–33.PubMedPubMedCentral
105.
go back to reference Ruf W, Disse J, Carneiro-Lobo TC, Yokota N, Schaffner F. Tissue factor and cell signalling in cancer progression and thrombosis. J Thromb Haemost. 2011;9 Suppl 1:306–15.PubMedPubMedCentral Ruf W, Disse J, Carneiro-Lobo TC, Yokota N, Schaffner F. Tissue factor and cell signalling in cancer progression and thrombosis. J Thromb Haemost. 2011;9 Suppl 1:306–15.PubMedPubMedCentral
106.
go back to reference Belting M, Ahamed J, Ruf W. Signaling of the tissue factor coagulation pathway in angiogenesis and cancer. Arterioscler Thromb Vasc Biol. 2005;25:1545–50.PubMed Belting M, Ahamed J, Ruf W. Signaling of the tissue factor coagulation pathway in angiogenesis and cancer. Arterioscler Thromb Vasc Biol. 2005;25:1545–50.PubMed
107.
go back to reference Folkman J. Tumor angiogenesis and tissue factor. Nat Med. 1996;2:167–8.PubMed Folkman J. Tumor angiogenesis and tissue factor. Nat Med. 1996;2:167–8.PubMed
108.
go back to reference Giannarelli C, Alique M, Rodriguez DT, Yang DK, Jeong D, Calcagno C, et al. Alternatively spliced tissue factor promotes plaque angiogenesis through the activation of hypoxia-inducible factor-1alpha and vascular endothelial growth factor signaling. Circulation. 2014;130:1274–86.PubMedPubMedCentral Giannarelli C, Alique M, Rodriguez DT, Yang DK, Jeong D, Calcagno C, et al. Alternatively spliced tissue factor promotes plaque angiogenesis through the activation of hypoxia-inducible factor-1alpha and vascular endothelial growth factor signaling. Circulation. 2014;130:1274–86.PubMedPubMedCentral
109.
go back to reference Hobbs JE, Zakarija A, Cundiff DL, Doll JA, Hymen E, Cornwell M, et al. Alternatively spliced human tissue factor promotes tumor growth and angiogenesis in a pancreatic cancer tumor model. Thromb Res. 2007;120 Suppl 2:S13–21.PubMed Hobbs JE, Zakarija A, Cundiff DL, Doll JA, Hymen E, Cornwell M, et al. Alternatively spliced human tissue factor promotes tumor growth and angiogenesis in a pancreatic cancer tumor model. Thromb Res. 2007;120 Suppl 2:S13–21.PubMed
110.
go back to reference van den Berg YW, van den Hengel LG, Myers HR, Ayachi O, Jordanova E, Ruf W, et al. Alternatively spliced tissue factor induces angiogenesis through integrin ligation. Proc Natl Acad Sci U S A. 2009;106:19497–502.PubMedPubMedCentral van den Berg YW, van den Hengel LG, Myers HR, Ayachi O, Jordanova E, Ruf W, et al. Alternatively spliced tissue factor induces angiogenesis through integrin ligation. Proc Natl Acad Sci U S A. 2009;106:19497–502.PubMedPubMedCentral
111.
go back to reference Sandset PM, Warn-Cramer BJ, Rao LV, Maki SL, Rapaport SI. Depletion of extrinsic pathway inhibitor (EPI) sensitizes rabbits to disseminated intravascular coagulation induced with tissue factor: evidence supporting a physiologic role for EPI as a natural anticoagulant. Proc Natl Acad Sci U S A. 1991;88:708–12.PubMedPubMedCentral Sandset PM, Warn-Cramer BJ, Rao LV, Maki SL, Rapaport SI. Depletion of extrinsic pathway inhibitor (EPI) sensitizes rabbits to disseminated intravascular coagulation induced with tissue factor: evidence supporting a physiologic role for EPI as a natural anticoagulant. Proc Natl Acad Sci U S A. 1991;88:708–12.PubMedPubMedCentral
112.
go back to reference Sandset PM, Warn-Cramer BJ, Maki SL, Rapaport SI. Immunodepletion of extrinsic pathway inhibitor sensitizes rabbits to endotoxin-induced intravascular coagulation and the generalized Shwartzman reaction. Blood. 1991;78:1496–502.PubMed Sandset PM, Warn-Cramer BJ, Maki SL, Rapaport SI. Immunodepletion of extrinsic pathway inhibitor sensitizes rabbits to endotoxin-induced intravascular coagulation and the generalized Shwartzman reaction. Blood. 1991;78:1496–502.PubMed
Metadata
Title
Endothelial cell control of thrombosis
Authors
Jonathan W. Yau
Hwee Teoh
Subodh Verma
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Cardiovascular Disorders / Issue 1/2015
Electronic ISSN: 1471-2261
DOI
https://doi.org/10.1186/s12872-015-0124-z

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