Toll-Like Receptor 9 Signaling Regulates Tissue Factor and Tissue Factor Pathway Inhibitor Expression in Human Endothelial Cells and Coagulation in Mice

Critical Care Medicine

Volumn 43, Issue 6, 2015, Pages e179-e189

  El Kebir, Driss ^a   Damlaj, Anas ^a   Makhezer, Nesrine ^a   Filep, János G ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

bacterial DNA; coagulation; endothelial cell; nuclear factor B; tissue factor; Toll like receptor 9

Indexed keywords

BACTERIAL DNA; CLODRONIC ACID; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; OLIGONUCLEOTIDE; SMALL INTERFERING RNA; THROMBIN ANTITHROMBIN COMPLEX; THROMBOPLASTIN; TISSUE FACTOR PATHWAY INHIBITOR; TOLL LIKE RECEPTOR 9; LIPOPROTEIN; LIPOPROTEIN-ASSOCIATED COAGULATION INHIBITOR; TLR9 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLEEDING TIME; BLOOD CLOTTING; CELL CULTURE; CONTROLLED STUDY; CORONARY ARTERY; ENDOTHELIUM CELL; FEMALE; GENE DELETION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MONOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; TELOMERE; WILD TYPE; ANIMAL; CORONARY BLOOD VESSEL; DRUG EFFECTS; GENE EXPRESSION; METABOLISM; PHYSIOLOGY; TISSUE CULTURE TECHNIQUE;

ANIMALS; BLOOD COAGULATION; CORONARY VESSELS; DNA, BACTERIAL; ENDOTHELIAL CELLS; GENE EXPRESSION; HUMANS; LIPOPROTEINS; MICE; NF-KAPPA B; RNA, MESSENGER; RNA, SMALL INTERFERING; THROMBOPLASTIN; TISSUE CULTURE TECHNIQUES; TOLL-LIKE RECEPTOR 9;

EID: 84937556786     PISSN: 00903493     EISSN: 15300293     Source Type: Journal    
DOI: 10.1097/CCM.0000000000001005     Document Type: Article

References (54)

1. Krieg AM, Yi AK, Matson S, et al: CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 1995; 374:546-549
2. Schwartz DA, Quinn TJ, Thorne PS, et al: CpG motifs in bacterial DNA cause infammation in the lower respiratory tract. J Clin Invest 1997; 100:68-73
3. Krieg AM: CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 2002; 20:709-760
4. Zhang Q, Raoof M, Chen Y, et al: Circulating mitochondrial DAMPs cause infammatory responses to injury. Nature 2010; 464:104-107
5. Lehtiniemi J, Karhunen PJ, Goebeler S, et al: Identification of different bacterial DNAs in human coronary arteries. Eur J Clin Invest 2005; 35:13-16
6. Ratanarat R, Cazzavillan S, Ricci Z, et al: Usefulness of a molecular strategy for the detection of bacterial DNA in patients with severe sepsis undergoing continuous renal replacement therapy. Blood Purif 2007; 25:106-111
7. Hemmi H, Takeuchi O, Kawai T, et al: A Toll-like receptor recognizes bacterial DNA. Nature 2000; 408:740-745
8. Akira S, Uematsu S, Takeuchi O: Pathogen recognition and innate immunity. Cell 2006; 124:783-801
9. El Kebir D, József L, Pan W, et al: Bacterial DNA activates endothelial cells and promotes neutrophil adherence through TLR9 signaling. J Immunol 2009; 182:4386-4394
10. Fitzner N, Clauberg S, Essmann F, et al: Human skin endothelial cells can express all 10 TLR genes and respond to respective ligands. Clin Vaccine Immunol 2008; 15:138-146
11. Pegu A, Qin S, Fallert Junecko BA, et al: Human lymphatic endothelial cells express multiple functional TLRs. J Immunol 2008; 180:3399-3405
12. Edfieldt K, Swedenborg J, Hansson GK, et al: Expression of toll-like receptors in human atherosclerotic lesions: A possible pathway for plaque activation. Circulation 2002; 105:1158-1161
13. Steffel J, Lüscher TF, Tanner FC: Tissue factor in cardiovascular diseases: Molecular mechanisms and clinical implications. Circulation 2006; 113:722-731
14. van der Poll T: Tissue factor as an initiator of coagulation and infammation in the lung. Crit Care 2008; 12(Suppl 6):S3
15. Drake TA, Morrissey JH, Edgington TS: Selective cellular expression of tissue factor in human tissues. Implications for disorders of hemo-stasis and thrombosis. Am J Pathol 1989; 134:1087-1097
16. Colucci M, Balconi G, Lorenzet R, et al: Cultured human endothelial cells generate tissue factor in response to endotoxin. J Clin Invest 1983; 71:1893-1896
17. Parry GC, Mackman N: Transcriptional regulation of tissue factor expression in human endothelial cells. Arterioscler Thromb Vasc Biol 1995; 15:612-621
18. Marmur JD, Thiruvikraman SV, Fyfe BS, et al: Identification of active tissue factor in human coronary atheroma. Circulation 1996; 94:1226-1232
19. van Till JW, Levi M, Bresser P, et al: Early procoagulant shift in the bronchoalveolar compartment of patients with secondary peritonitis. J Infect Dis 2006; 194:1331-1339
20. Tang H, Ivanciu L, Popescu N, et al: Sepsis-induced coagulation in the baboon lung is associated with decreased tissue factor pathway inhibitor. Am J Pathol 2007; 171:1066-1077
21. Ott I, Miyagi Y, Miyazaki K, et al: Reversible regulation of tissue factor-induced coagulation by glycosyl phosphatidylinositol-anchored tissue factor pathway inhibitor. Arterioscler Thromb Vasc Biol 2000; 20:874-882
22. Crawley JT, Lane DA: The haemostatic role of tissue factor pathway inhibitor. Arterioscler Thromb Vasc Biol 2008; 28:233-242
23. Pawlinski R, Pedersen B, Schabbauer G, et al: Role of tissue factor and protease-activated receptors in a mouse model of endotoxemia. Blood 2004; 103:1342-1347
24. Pawlinski R, Wang JG, Owens AP 3rd, et al: Hematopoietic and non-hematopoietic cell tissue factor activates the coagulation cascade in endotoxemic mice. Blood 2010; 116:806-814
25. Badimon JJ, Lettino M, Toschi V, et al: Local inhibition of tissue factor reduces the thrombogenicity of disrupted human atherosclerotic plaques: Effects of tissue factor pathway inhibitor on plaque thrombogenicity under flow conditions. Circulation 1999; 99:1780-1787
26. Roqué M, Reis ED, Fuster V, et al: Inhibition of tissue factor reduces thrombus formation and intimal hyperplasia after porcine coronary angioplasty. J Am Coll Cardiol 2000; 36:2303-2310
27. Nishida T, Ueno H, Atsuchi N, et al: Adenovirus-mediated local expression of human tissue factor pathway inhibitor eliminates shear stress-induced recurrent thrombosis in the injured carotid artery of the rabbit. Circ Res 1999; 84:1446-1452
28. Creasey AA, Chang AC, Feigen L, et al: Tissue factor pathway inhibitor reduces mortality from Escherichia coli septic shock. J Clin Invest 1993; 91:2850-2860
29. Gursel I, Gursel M, Yamada H, et al: Repetitive elements in mammalian telomeres suppress bacterial DNA-induced immune activation. J Immunol 2003; 171:1393-1400
30. Bogdanov VY, Cimmino G, Tardos JG, et al: Assessment of plasma tissue factor activity in patients presenting with coronary artery disease: Limitations of a commercial assay. J Thromb Haemost 2009; 7:894-897
31. Lund J, Sato A, Akira S, et al: Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J Exp Med 2003; 198:513-520
32. Kirchhofer D, Moran P, Bullens S, et al: A monoclonal antibody that inhibits mouse tissue factor function. J Thromb Haemost 2005; 3:1098-1099
33. Sunderkötter C, Nikolic T, Dillon MJ, et al: Subpopulations of mouse blood monocytes differ in maturation stage and infammatory response. J Immunol 2004; 172:4410-4417
34. Schwarz M, Meade G, Stoll P, et al: Conformation-specific blockade of the integrin GPIIb/IIIa: A novel antiplatelet strategy that selectively targets activated platelets. Circ Res 2006; 99:25-33
35. Wang MY, Ji SR, Bai CJ, et al: A redox switch in C-reactive protein modulates activation of endothelial cells. FASEB J 2011; 25:3186-3196
36. Stacey KJ, Young GR, Clark F, et al: The molecular basis for the lack of immunostimulatory activity of vertebrate DNA. J Immunol 2003; 170:3614-3620
37. Wu SQ, Aird WC: Thrombin, TNF-alpha, and LPS exert overlapping but nonidentical effects on gene expression in endothelial cells and vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 2005; 289:H873-H885
38. Steffel J, Hermann M, Greutert H, et al: Celecoxib decreases endothelial tissue factor expression through inhibition of c-Jun terminal NH2 kinase phosphorylation. Circulation 2005; 111:1685-1689
39. Cirillo P, Golino P, Calabrò P, et al: C-reactive protein induces tissue factor expression and promotes smooth muscle and endothelial cell proliferation. Cardiovasc Res 2005; 68:47-55
40. Zhao Y, Zhou S, Heng CK: Impact of serum amyloid A on tissue factor and tissue factor pathway inhibitor expression and activity in endothelial cells. Arterioscler Thromb Vasc Biol 2007; 27:1645-1650
41. Shimokawa T, Yamamoto K, Kojima T, et al: Down-regulation of murine tissue factor pathway inhibitor mRNA by endotoxin and tumor necrosis factor-alpha in vitro and in vivo. Thromb Res 2000; 100:211-221
42. Szotowski B, Antoniak S, Poller W, et al: Procoagulant soluble tissue factor is released from endothelial cells in response to infammatory cytokines. Circ Res 2005; 96:1233-1239
43. Brandtzaeg P, Sandset PM, Joø GB, et al: The quantitative association of plasma endotoxin, antithrombin, protein C, extrinsic pathway inhibitor and fbrinopeptide A in systemic meningococcal disease. Thromb Res 1989; 55:459-470
44. Akira S, Takeda K: Toll-like receptor signalling. Nat Rev Immunol 2004; 4:499-511
45. Kim JS, Park DW, Lee HK, et al: Early growth response-1 is involved in foam cell formation and is upregulated by the TLR9-MyD88-ERK1/2 pathway. Biochem Biophys Res Commun 2009; 390:196-200
46. Takaoka A, Wang Z, Choi MK, et al: DAI (DLM-1/ZBP1) is a cyto-solic DNA sensor and an activator of innate immune response. Nature 2007; 448:501-505
47. Hornung V, Latz E: Intracellular DNA recognition. Nat Rev Immunol 2010; 10:123-130
48. Ye X, Ding J, Zhou X, et al: Divergent roles of endothelial NF-kappaB in multiple organ injury and bacterial clearance in mouse models of sepsis. J Exp Med 2008; 205:1303-1315
49. Song D, Ye X, Xu H, et al: Activation of endothelial intrinsic NF-{kappa} B pathway impairs protein C anticoagulation mechanism and promotes coagulation in endotoxemic mice. Blood 2009; 114:2521-2529
50. Chantrathammachart P, Mackman N, Sparkenbaugh E, et al: Tissue factor promotes activation of coagulation and infammation in a mouse model of sickle cell disease. Blood 2012; 120:636-646
51. Knuefermann P, Baumgarten G, Koch A, et al: CpG oligonucleotide activates Toll-like receptor 9 and causes lung infammation in vivo. Respir Res 2007; 8:72
52. Itagaki K, Adibnia Y, Sun S, et al: Bacterial DNA induces pulmonary damage via TLR-9 through cross-talk with neutrophils. Shock 2011; 36:548-552
53. József L, Khreiss T, Filep JG: CpG motifs in bacterial DNA delay apop-tosis of neutrophil granulocytes. FASEB J 2004; 18:1776-1778
54. Henke PK, Mitsuya M, Luke CE, et al: Toll-like receptor 9 signaling is critical for early experimental deep vein thrombosis resolution. Arterioscler Thromb Vasc Biol 2011; 31:43-49