The role of monocytes in thrombotic disorders

Eduard Shantsila; Gregory Y. H. Lip

doi:10.1160/TH09-01-0023

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2009; 102(05): 916-924
DOI: 10.1160/TH09-01-0023

Review Article

Schattauer GmbH

The role of monocytes in thrombotic disorders

Insights from tissue factor, monocyte-platelet aggregates and novel mechanisms

Eduard Shantsila

¹Haemostasis, Thrombosis and Vascular Biology Unit, University of Birmingham Centre for Cardiovascular Science, City Hospital, Birmingham, UK

,

Gregory Y. H. Lip

¹Haemostasis, Thrombosis and Vascular Biology Unit, University of Birmingham Centre for Cardiovascular Science, City Hospital, Birmingham, UK

› Author Affiliations

Abstract

Summary

Although, the main physiological role of monocytes is attributed to innate immunity (that is, phagocytosis) and the development of tissue macrophages and dendritic cells, the pathophysiological role of these goes far behind these (simplistic) limits. Indeed, monocytes constitute a major source of blood tissue factor, a key element of the extrinsic coagulation cascade. Monocytes actively bind to platelets, thus forming very prothrombotic monocyte-platelet aggregates. Additionally, these cells link inflammation and the procoagulant state observed in various prothrombotic conditions. However, monocytes are also crucial for successful thrombus recanalisation. In this article, we review the available data on potential mechanisms that link monocytes with thrombosis-related processes.

Keywords

Monocytes - thrombosis - tissue factor - monocyte-platelet aggregates

Full Text

References

References
1 Fox KA, Cokkinos DV, Deckers J. et al. The ENACT study: a pan-European survey of acute coronary syndromes. European Network for Acute Coronary Treatment. Eur Heart J 2000; 21: 1440-1449.
2 Hasdai D, Behar S, Wallentin L. et al. A prospective survey of the characteristics, treatments and outcomes of patients with acute coronary syndromes in Europe and the Mediterranean basin. The Euro Heart Survey of Acute Coronary Syndromes (Euro Heart Survey ACS). Eur Heart J 2002; 15: 1190-1201.
3 Cohen AT, Agnelli G, Anderson FA. et al. Venous thromboembolism (VTE) in Europe. The number of VTE events and associated morbidity and mortality. Thromb Haemost 2007; 98: 756-764.
4 Heit J, Cohen A, Anderson FJ. Estimated annual number of incident and recurrent, non-fatal and fatal venous thromboembolism (VTE) events in the US. Blood 2005; 106: 267A Abst 910..
5 Wiviott SD, Braunwald E, McCabe CH. et al. Prasugrel versus clopidogrel in patients with acute coronary syndromes. N Engl J Med 2007; 357: 2001-2015.
6 Wiiger MT, Prydz H. The changing faces of tissue factor biology. A personal tribute to the understanding of the „extrinsic coagulation activation”. Thromb Haemost 2007; 98: 38-42.
7 Edgington TS. Surfing tissue factor. From the predicted to the discovery and elucidation of unanticipated functions and biology of potential significance. Thromb Haemost 2007; 98: 36-37.
8 Carmeliet P, Mackman N, Moons L. et al. Role of tissue factor in embryonic blood vessel development. Nature 1996; 383: 73-75.
9 Cermak J, Key NS, Bach RR. et al. C-reactive protein induces human peripheral blood monocytes to synthesize tissue factor. Blood 1993; 82: 513-520.
10 van der Logt CP, Dirven RJ, Reitsma PH. et al. Expression of tissue factor and tissue factor pathway inhibitor in monocytes in response to bacterial lipopolysaccharide and phorbolester. Blood Coagul Fibrinolysis 1994; 05: 211-220.
11 Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest 2003; 111: 1805-1812.
12 Filep JG. Perplexity of monocyte responses to C-reactive protein (CRP). Thromb Haemost 2008; 99: 461-462.
13 Hanriot D, Bello G, Ropars A. et al. C-reactive protein induces pro-and anti-inflammatory effects, including activation of the liver X receptor alpha, on human monocytes. Thromb Haemost 2008; 99: 558-569.
14 Reinhardt C. New locations of intravascular tissue factor: indications. Hamostaseologie 2007; 27: 55-58.
15 van der Logt CP, Reitsma PH, Bertina RM. Alternative splicing is responsible for the presence of two tissue factor mRNA species in LPS stimulated human monocytes. Thromb Haemost 1992; 67: 272-276.
16 Sovershaev MA, Egorina EM, Gruber FX. et al. High tissue factor-expressing human monocytes carry low surface CD36: application to intersubject variability. J Thromb Haemost 2007; 05: 2453-2460.
17 McGilvray ID, Tsai V, Marshall JC. et al. Monocyte adhesion and transmigration induce tissue factor expression: role of the mitogen-activated protein kinases. Shock 2002; 18: 51-57.
18 Panes O, Matus V, Sáez CG. et al. Human platelets synthesize and express functional tissue factor. Blood 2007; 109: 5242-5250.
19 Scholz T, Temmler U, Krause S. et al. Transfer of tissue factor from platelets to monocytes: role of platelet-derived microvesicles and CD62P. Thromb Haemost 2002; 88: 1033-1038.
20 Puccetti L, Bruni F, Bova G. et al. Role of platelets in tissue factor expression by monocytes in normal and hypercholesterolemic subjects. In vitro effect of cerivastatin. Int J Clin Lab Res 2000; 30: 147-156.
21 Ichikawa K, Yoshinari M, Iwase M. et al. Advanced glycosylation end products induced tissue factor expression in human monocyte-like U937 cells and increased tissue factor expression in monocytes from diabetic patients. Atherosclerosis 1998; 136: 281-287.
22 Cai H, Song C, Endoh I. et al. Serum amyloid A induces monocyte tissue factor. J Immunol 2007; 178: 1852-1860.
23 Vaidyula VR, Boden G, Rao AK. Platelet and monocyte activation by hyperglycemia and hyperinsulinemia in healthy subjects. Platelets 2006; 17: 577-585.
24 Gerrits AJ, Koekman CA, Yildirim C. et al. Insulin inhibits tissue factor expression in monocytes. J Thromb Haemost 2009; 07: 198-205.
25 He M, He X, Xie Q. et al. Angiotensin II induces the expression of tissue factor and its mechanism in human monocytes. Thromb Res 2006; 117: 579-590.
26 Taubman MB, Marmur JD, Rosenfield CL. 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.
27 Napoleone E, Di Santo A, Camera M. et al. Angiotensin-converting enzyme inhibitors downregulate tissue factor synthesis in monocytes. Circ Res 2000; 86: 139-143.
28 Soejima H, Ogawa H, Yasue H. et al. Angiotensinconverting enzyme inhibition reduces monocyte chemoattractant protein-1 and tissue factor levels in patients with myocardial infarction. J Am Coll Cardiol 1999; 34: 983-988.
29 Koh KK, Chung WJ, Ahn JY. 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.
30 Hölschermann H, Terhalle HM, Zakel U. et al. Monocyte tissue factor expression is enhanced in women who smoke and use oral contraceptives. Thromb Haemost 1999; 82: 1614-1620.
31 Khajuria A, Houston DS. Induction of monocyte tissue factor expression by homocysteine: a possible mechanism for thrombosis. Blood 2000; 96: 966-972.
32 Lambert MP, Sachais BS, Kowalska MA. Chemokines and thrombogenicity. Thromb Haemost 2007; 97: 722-729.
33 Braunersreuther V, Mach F, Steffens S. The specific role of chemokines in atherosclerosis. Thromb Haemost 2007; 97: 714-721.
34 Muhlfelder TW, Teodorescu V, Rand J. et al. Human atheromatous plaque extracts induce tissue factor activity (TFa) in monocytes and also express constitutive TFa. Thromb Haemost 1999; 81: 146-150.
35 Scholz H, Sandberg W, Damås JK. et al. Enhanced plasma levels of LIGHT in unstable angina: possible pathogenic role in foam cell formation and thrombosis. Circulation 2005; 112: 2121-2129.
36 Kim HK, Song KS, Park YS. et al. Changes of plasma tissue factor and tissue factor pathway inhibitor antigen levels and induction of tissue factor expression on the monocytes in coronary artery disease. Cardiology 2000; 93: 31-36.
37 Mach F, Schönbeck U, Bonnefoy JY. et al. Activation of monocyte/macrophage functions related to acute atheroma complication by ligation of CD40: induction of collagenase, stromelysin, and tissue factor. Circulation 1997; 96: 396-399.
38 Kälsch T, Nguyen XD, Elmas E. et al. Coagulation activation and expression of CD40 ligand on platelets upon in vitro lipopolysaccharide-challenge in patients with unstable angina. Int J Cardiol 2006; 111: 217-223.
39 Agraou B, Corseaux D, McFadden EP. et al. Effects of coronary angioplasty on monocyte tissue factor response in patients with stable or unstable angina. Thromb Res 1997; 88: 237-243.
40 Palmerini T, Coller BS, Cervi V. et al. Monocytederived tissue factor contributes to stent thrombosis in an in vitro system. J Am Coll Cardiol 2004; 44: 1570-1577.
41 Ollivier V, Hammal S, Ameziane N. et al. Modulation of tissue factor expression by rapamycin and FK-506 in lipopolysaccharide-stimulated human mononuclear cells and serum-stimulated aortic smooth muscle cells. Thromb Haemost 2005; 94: 46-52.
42 Vieira LM, Dusse LM, Fernandes AP. et al. Monocytes and plasma tissue factor levels in normal individuals and patients with deep venous thrombosis of the lower limbs: potential diagnostic tools?. Thromb Res 2007; 119: 157-165.
43 Hölschermann H, Haberbosch W, Terhalle HM. et al. Increased monocyte tissue factor activity in women following cerebral venous thrombosis. J Neurol 2003; 250: 631-632.
44 Ollivier V, Sheibani A, Chollet-Martin S. et al. Monocyte procoagulant activity and membrane-associated D dimer after knee replacement surgery. Thromb Res 1989; 55: 179-185.
45 Pouplard C, Iochmann S, Renard B. et al. Induction of monocyte tissue factor expression by antibodies to heparin-platelet factor 4 complexes developed in heparin-induced thrombocytopenia. Blood 2001; 97: 3300-3302.
46 Kornberg A, Rahimi-Levene N, Yona R. et al. Enhanced generation of monocyte tissue factor and increased plasma prothrombin fragment1+2 levels in patients with polycythemia vera: mechanism of activation of blood coagulation. Am J Hematol 1997; 56: 5-11.
47 Arellano-Rodrigo E, Alvarez-Larrán A, Reverter JC. et al. Increased platelet and leukocyte activation as contributing mechanisms for thrombosis in essential thrombocythemia and correlation with the JAK2 mutational status. Haematologica 2006; 91: 169-175.
48 López-Pedrera C, Buendía P, Cuadrado MJ. et al. Antiphospholipid antibodies from patients with the antiphospholipid syndrome induce monocyte tissue factor expression through the simultaneous activation of NF-kappaB/Rel proteins via the p38 mitogen-activated protein kinase pathway, and of the MEK-1/ERK pathway. Arthritis Rheum 2006; 54: 301-311.
49 Wolberg AS, Roubey RA. Mechanisms of autoantibody-induced monocyte tissue factor expression. Thromb Res 2004; 114: 391-396.
50 Yasuda S, Bohgaki M, Atsumi T. et al. Pathogenesis of antiphospholipid antibodies: impairment of fibrinolysis and monocyte activation via the p38 mitogenactivated protein kinase pathway. Immunobiology 2005; 210: 775-780.
51 Cuadrado MJ, López-Pedrera C, Khamashta MA. et al. Thrombosis in primary antiphospholipid syndrome: a pivotal role for monocyte tissue factor expression. Arthritis Rheum 1997; 40: 834-841.
52 Dobado-Berrios PM, López-Pedrera C, Velasco F. et al. Increased levels of tissue factor mRNA in mononuclear blood cells of patients with primary antiphospholipid syndrome. Thromb Haemost 1999; 82: 1578-1582.
53 Dobado-Berrios PM, López-Pedrera C, Velasco F. et al. The role of tissue factor in the antiphospholipid syndrome. Arthritis Rheum 2001; 44: 2467-2476.
54 Reverter JC, Tàssies D, Font J. et al. Hypercoagulable state in patients with antiphospholipid syndrome is related to high induced tissue factor expression on monocytes and to low free protein s. Arterioscler Thromb Vasc Biol 1996; 16: 1319-1326.
55 Visvanathan S, Geczy CL, Harmer JA. et al. Monocyte tissue factor induction by activation of beta 2-glycoprotein-I-specific T lymphocytes is associated with thrombosis and fetal loss in patients with antiphospholipid antibodies. J Immunol 2000; 165: 2258-2262.
56 Zhou H, Ling S, Yu Y. et al. Involvement of annexin A2 in anti-beta2GPI/beta2GPI-induced tissue factor expression on monocytes. Cell Res 2007; 17: 737-739.
57 López-Pedrera C, Buendía P, Barbarroja N. et al. Antiphospholipid-mediated thrombosis: interplay between anticardiolipin antibodies and vascular cells. Clin Appl Thromb Hemost 2006; 12: 41-45.
58 Harding SA, Din JN, Sarma J. et al. Flow cytometric analysis of circulating platelet-monocyte aggregates in whole blood: methodological considerations. Thromb Haemost 2007; 98: 451-456.
59 Esposito CJ, Popescu WM, Rinder HM. et al. Increased leukocyte-platelet adhesion in patients with graft occlusion after peripheral vascular surgery. Thromb Haemost 2003; 90: 1128-1134.
60 Kageyama K, Nakajima Y, Shibasaki M. et al. Increased platelet, leukocyte, and endothelial cell activity are associated with increased coagulability in patients after total knee arthroplasty. J Thromb Haemost 2007; 05: 738-745.
61 Rinder HM, Bonan JL, Rinder CS. et al. Dynamics of leukocyte-platelet adhesion in whole blood. Blood 1991; 78: 1730-1737.
62 Keating FK, Dauerman HL, Whitaker DA. et al. Increased expression of platelet P-selectin and formation of platelet-leukocyte aggregates in blood from patients treated with unfractionated heparin plus eptifibatide compared with bivalirudin. Thromb Res 2006; 118: 361-369.
63 Hayward R, Campbell B, Shin YK. et al. Recombinant soluble P-selectin glycoprotein ligand-1 protects against myocardial ischemic reperfusion injury in cats. Cardiovasc Res 1999; 41: 65-76.
64 Oberle V, Fischer A, Setzer F. et al. Thrombus formation without platelets under inflammatory condition: an in vitro study. Platelets 2007; 18: 143-149.
65 Sarma J, Laan CA, Alam S. et al. Increased platelet binding to circulating monocytes in acute coronary syndromes. Circulation 2002; 105: 2166-2171.
66 Kisucka J, Chauhan AK, Zhao BQ. et al. Elevated levels of soluble P-selectin in mice alter blood-brain barrier function, exacerbate stroke, and promote atherosclerosis. Blood 2009; 113: 6015-6022.
67 Woollard KJ, Suhartoyo A, Harris EE. et al. Pathophysiological levels of soluble P-selectin mediate adhesion of leukocytes to the endothelium through Mac-1 activation. Circ Res 2008; 103: 1128-1138.
68 Silverstein RL, Asch AS, Nachman RL. Glycoprotein IV mediates thrombospondin-dependent plateletmonocyte and platelet-U937 cell adhesion. J Clin Invest 1989; 84: 546-552.
69 Michelson AD, Barnard MR, Hechtman HB. et al. In vivo tracking of platelets: circulating degranulated platelets rapidly lose surface P-selectin but continue to circulate and function. Proc Natl Acad Sci USA 1996; 93: 11877-11882.
70 Poole JC. Phagocytosis of platelets by monocytes in organizing arterial thrombi. An electron microscopical study. Q J Exp Physiol Cogn Med Sci 1966; 51: 54-59.
71 Elstad MR, La Pine TR, Cowley FS. et al. P-selectin regulates platelet-activating factor synthesis and phagocytosis by monocytes. J Immunol 1995; 155: 2109-2122.
72 Dole VS, Bergmeier W, Patten IS. et al. PSGL-1 regulates platelet P-selectin-mediated endothelial activation and shedding of P-selectin from activated platelets. Thromb Haemost 2007; 98: 806-812.
73 Simon DI, Ezratty AM, Francis SA. et al. Fibrin(ogen) is internalized and degraded by activated human monocytoid cells via Mac-1 (CD11b/CD18): a nonplasmin fibrinolytic pathway. Blood 1993; 82: 2414-2422.
74 Kirchhofer D, Riederer MA, Baumgartner HR. Specific accumulation of circulating monocytes and polymorphonuclear leukocytes on platelet thrombi in a vascular injury model. Blood 1997; 89: 1270-1278.
75 Braun OO, Johnell M, Varenhorst C. et al. Greater reduction of platelet activation markers and plateletmonocyte aggregates by prasugrel compared to clopidogrel in stable coronary artery disease. Thromb Haemost 2008; 100: 626-633.
76 Kaplar M, Kappelmayer J, Veszpremi A. et al. The possible association of in vivo leukocyte-platelet heterophilic aggregate formation and the development of diabetic angiopathy. Platelets 2001; 12: 419-422.
77 Danenberg HD, Kantak N, Grad E. et al. C-reactive protein promotes monocyte-platelet aggregation: an additional link to the inflammatory-thrombotic intricacy. Eur J Haematol 2007; 78: 246-252.
78 Konieczkowski M, Skrinska VA. Increased synthesis of thromboxane A(2) and expression of procoagulant activity by monocytes in response to arachidonic acid in diabetes mellitus. Prostaglandins Leukot Essent Fatty Acids 2001; 65: 133-138.
79 Goubareva I, Gkaliagkousi E, Shah A. et al. Age decreases nitric oxide synthesis and responsiveness in human platelets and increases formation of monocyteplatelet aggregates. Cardiovasc Res 2007; 75: 793-802.
80 Furman MI, Benoit SE, Barnard MR. et al. Increased platelet reactivity and circulating monocyteplatelet aggregates in patients with stable coronary artery disease. J Am Coll Cardiol 1998; 31: 352-358.
81 Brambilla M, Camera M, Colnago D. et al. Tissue factor in patients with acute coronary syndromes: expression in platelets, leukocytes, and platelet-leukocyte aggregates. Arterioscler Thromb Vasc Biol 2008; 28: 947-953.
82 Furman MI, Barnard MR, Krueger LA. et al. Circulating monocyte-platelet aggregates are an early marker of acute myocardial infarction. J Am Coll Cardiol 2001; 38: 1002-1006.
83 May AE, Neumann FJ, Gawaz M. et al. Reduction of monocyte-platelet interaction and monocyte activation in patients receiving antiplatelet therapy after coronary stent implantation. Eur Heart J 1997; 18: 1913-1920.
84 Zhao L, Bath PM, May J. et al. P-selectin, tissue factor and CD40 ligand expression on platelet-leucocyte conjugates in the presence of a GPIIb/IIIa antagonist. Platelets 2003; 14: 473-480.
85 Braun OO, Johnell M, Varenhorst C. et al. Greater reduction of platelet activation markers and plateletmonocyte aggregates by prasugrel compared to clopidogrel in stable coronary artery disease. Thromb Haemost 2008; 100: 626-633.
86 van Gils JM, da Costa Martins PA, Mol A. et al. Transendothelial migration drives dissociation of plateletmonocyte complexes. Thromb Haemost 2008; 100: 271-279.
87 Bharadwaj D, Stein MP, Volzer M. et al. The major receptor for C-reactive protein on leukocytes is fcgamma receptor II. J Exp Med 1999; 190: 585-590.
88 Crowell RE, Du Clos TW. et al. C-reactive protein receptors on the human monocytic cell line U-937. Evidence for additional binding to Fc gamma RI. J Immunol 1991; 147: 3445-3451.
89 Stumpf C, Lehner C, Eskafi S. et al. Enhanced levels of CD154 (CD40 ligand) on platelets in patients with chronic heart failure. Eur J Heart Fail 2003; 05: 629-637.
90 Penn MS, Topol EJ. Tissue factor, the emerging link between inflammation, thrombosis, and vascular remodeling. Circ Res 2001; 89: 1-2.
91 Pepys MB, Hirschfield GM. C-reactive protein and atherothrombosis. Ital Heart J 2001; 02: 196-199.
92 Libby P, Simon DI. Inflammation and thrombosis: the clot thickens. Circulation 2001; 103: 1718-1720.
93 Yeh ET, Anderson HV, Pasceri V. et al. C-reactive protein: linking inflammation to cardiovascular complications. Circulation 2001; 104: 974-975.
94 Le Guyader A, Davis-Gorman G, Copeland JG. et al. A flow cytometric method for determining the binding of coagulation factor X to monocytes in whole human blood. J Immunol Methods 2004; 292: 207-215.
95 Kappelmayer J, Kunapuli SP, Wyshock EG. et al. Characterization of monocyte-associated factor V. Thromb Haemost 1993; 70: 273-280.
96 Freeburn JC, Wallace JM, Strain JJ. et al. Monocyte tissue factor-like activity in post myocardial infarction patients. Br J Haematol 1998; 102: 605-608.
97 Satta N, Freyssinet JM, Toti F. The significance of human monocyte thrombomodulin during membrane vesiculation and after stimulation by lipopolysaccharide. Br J Haematol 1997; 96: 534-542.
98 Modarai B, Burnand KG, Humphries J. et al. The role of neovascularisation in the resolution of venous thrombus. Thromb Haemost 2005; 93: 801-809.
99 Davies MJ, Ballantine SJ, Robertson WB. et al. The ultrastructure of organising experimental mural thrombi in the pig aorta. J Pathol 1975; 117: 75-81.
100 McGuinness CL, Humphries J, Waltham M. et al. Recruitment of labelled monocytes by experimental venous thrombi. Thromb Haemost 2001; 85: 1018-1024.
101 Burnand KG, Gaffney PJ, McGuinness CL. et al. The role of the monocyte in the generation and dissolution of arterial and venous thrombi. Cardiovasc Surg 1998; 06: 119-125.
102 Wakefield TW, Linn MJ, Henke PK. et al. Neovascularization during venous thrombosis organization: A preliminary study. J Vasc Surg 1999; 30: 885-893.
103 Humphries J, McGuinness CL, Smith A. et al. Monocyte chemotactic protein-1 (MCP-1) accelerates the organization and resolution of venous thrombi. J Vasc Surg 1999; 30: 894-899.
104 Henke PK, Pearce CG, Moaveni DM. et al. Targeted deletion of CCR2 impairs deep vein thombosis resolution in a mouse model. J Immunol 2006; 177: 3388-3397.
105 Moldovan NI, Asahara T. Role of blood mononuclear cells in recanalization and vascularization of thrombi: past, present, and future. Trends Cardiovasc Med 2003; 13: 265-269.
106 Soo KS, Northeast AD, Happerfield LC. et al. Tissue plasminogen activator production by monocytes in venous thrombolysis. Pathol 1996; 178: 190-194.
107 Lundgren CH, Sawa H, Sobel BE. et al. Modulation of expression of monocyte/macrophage plasminogen activator activity and its implications for attenuation of vasculopathy. Circulation 1994; 90: 1927-1934.
108 Kung SK, Lau HK. Modulation of the plasminogen activation system in murine macrophages. Biochim Biophys Acta 1993; 1176: 113-122.
109 Kuraoka S, Campeau JD, Rodgers KE. et al. Effects of interleukin-1 (IL-1) on postsurgical macrophage secretion of protease and protease inhibitor activities. J Surg Res 1992; 52: 71-78.
110 Northeast ADR, Soo KS, Beaubrow LG. et al. The tissue plasminogen activator and urokinase response in vivo during natural resolution of venous thrombosis. J Vasc Surg 1995; 22: 573-579.
111 Singh I, Burnand KG, Collins M. et al. Failure of thrombus to resolve in urokinase-type plasminogen activator gene knockout mice. Circulation 2003; 107: 869-875.
112 Wakefield TW, Linn MJ, Henke PK. et al. Neovascularization during venous thrombosis organization: A preliminary study. J Vasc Surg 1999; 30: 885-893.
113 Waltham M, Burnand K, Collins M. et al. Vascular endothelial growth factor and basic fibroblast growth factor are found in resolving thrombi. J Vasc Surg 2000; 32: 988-996.
114 Henke PK, Varga A, De S, Deatrick CB. et al. Deep vein thrombosis resolution is modulated by monocyte CXCR2-mediated activity in a mouse model. Arterioscler Thromb Vasc Biol 2004; 24: 1130-1137.
115 Murdoch C, Tazzyman S, Webster S. et al. Expression of Tie-2 by human monocytes and their responses to angiopoietin-2. J Immunol 2007; 178: 7405-7411.
116 Shantsila E, Watson T, Lip GY. Endothelial progenitor cells in cardiovascular disorders. J Am Coll Cardiol 2007; 49: 741-752.
117 Castellote JC, Grau E, Linde MA. et al. Detection of both type 1 and type 2 plasminogen activator inhibitors in human monocytes. Thromb Haemost 1990; 63: 67-71.
118 Paffen E, Vos HL, Bertina RM. C-reactive protein does not directly induce tissue factor in human monocytes. Arterioscler Thromb Vasc Biol 2004; 24: 975-981.
119 Poitevin S, Cochery-Nouvellon E, Dupont A. et al. Monocyte IL-10 produced in response to lipopolysaccharide modulates thrombin generation by inhibiting tissue factor expression and release of active tissue factor-bound microparticles. Thromb Haemost 2007; 97: 598-607.
120 Ernofsson M, Tenno T, Siegbahn A. Inhibition of tissue factor surface expression in human peripheral blood monocytes exposed to cytokines. Br J Haematol 1996; 95: 249-257.
121 Herbert JM, Corseaux D, Lale A. et al. Hypoxia primes endotoxin-induced tissue factor expression in human monocytes and endothelial cells by a PAF-dependent mechanism. J Cell Physiol 1996; 169: 290-299.
122 Lawson CA, Yan SD, Yan SF. et al. Monocytes and tissue factor promote thrombosis in a murine model of oxygen deprivation. J Clin Invest 1997; 99: 1729-1738.
123 Scholz H, Sandberg W, Damås JK. et al. Enhanced plasma levels of LIGHT in unstable angina: possible pathogenic role in foam cell formation and thrombosis. Circulation 2005; 112: 2121-2129.
124 Corseaux D, Meurice T, Six I. et al. Basic fibroblast growth factor increases tissue factor expression in circulating monocytes and in vascular wall. Circulation 2000; 101: 2000-2006.
125 Casani L, Segales E, Vilahur G. et al. Moderate daily intake of red wine inhibits mural thrombosis and monocyte tissue factor expression in an experimental porcine model. Circulation 2004; 110: 460-465.
126 Napoleone E, di Santo A, Peri G. et al. The long pentraxin PTX3 up-regulates tissue factor in activated monocytes: another link between inflammation and clotting activation. J Leukoc Biol 2004; 76: 203-209.