C-reactive protein induces expression of tissue factor and plasminogen activator inhibitor-1 and promotes fibrin accumulation in vein grafts

Journal of Thrombosis and Haemostasis

Volumn 12, Issue 10, 2014, Pages 1667-1677

  Ji, Y ^a   Fish, P M ^a   Strawn, T L ^a   Lohman, A W ^a   Wu, J ^a   Szalai, A J ^b   Fay, W P ^a,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Alabama at Birmingham   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

C reactive protein; Plasminogen activator inhibitor 1; Thrombosis; Tissue factor; Vascular graft occlusion

Indexed keywords

C REACTIVE PROTEIN; FIBRIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; THROMBOPLASTIN; CHLORIDE; FERRIC CHLORIDE; FERRIC ION; RECOMBINANT PROTEIN; SERPINE1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOACCUMULATION; CELL INVASION; CELL STIMULATION; CONTROLLED STUDY; FIBRIN DEPOSITION; FIBRIN FORMATION; GENE EXPRESSION; HUMAN; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE MIGRATION; MALE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; POSTOPERATIVE THROMBOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENE; VASCULAR ENDOTHELIUM; VEIN GRAFT; VEIN THROMBOSIS; WILD TYPE; ANIMAL; BLOOD; C57BL MOUSE; CELL MOTION; CHEMISTRY; CORONARY ARTERY BYPASS GRAFT; MACROPHAGE; METABOLISM; TRANSGENIC MOUSE; TRANSPLANTATION; VEIN;

ANIMALS; C-REACTIVE PROTEIN; CELL MOVEMENT; CHLORIDES; CORONARY ARTERY BYPASS; FERRIC COMPOUNDS; FIBRIN; HUMANS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PLASMINOGEN ACTIVATOR INHIBITOR 1; RECOMBINANT PROTEINS; THROMBOPLASTIN; TRANSGENES; VEINS; VENOUS THROMBOSIS;

EID: 84907881557     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12680     Document Type: Article

References (36)

1. Motwani JG, Topol EJ. Aortocoronary saphenous vein graft disease: pathogenesis, predisposition, and prevention. Circulation 1998; 97: 916-31.
2. Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest 2003; 111: 1805-12.
3. Aouifi A, Piriou V, Blanc P, Bouvier H, Bastien O, Chiari P, Rousson R, Evans R, Lehot JJ. Effect of cardiopulmonary bypass on serum procalcitonin and C-reactive protein concentrations. Br J Anaesth 1999; 83: 602-7.
4. Hedman A, Larsson PT, Alam M, Wallen NH, Nordlander R, Samad BA. CRP, IL-6 and endothelin-1 levels in patients undergoing coronary artery bypass grafting. Do preoperative inflammatory parameters predict early graft occlusion and late cardiovascular events? Int J Cardiol 2007; 120: 108-14.
5. Balciunas M, Bagdonaite L, Samalavicius R, Griskevicius L, Vuylsteke A. Pre-operative high sensitive C-reactive protein predicts cardiovascular events after coronary artery bypass grafting surgery: a prospective observational study. Ann Card Anaesth 2009; 12: 127-32.
6. Jabs WJ, Theissing E, Nitschke M, Bechtel JFM, Duchrow M, Mohamed S, Jahrbeck B, Sievers HH, Steinhoff J, Bartels C. Local generation of C-reactive protein in diseased coronary artery venous bypass grafts and normal vascular tissue. Circulation 2003; 108: 1428-31.
7. Gulkarov I, Pintucci G, Bohmann K, Saunders PC, Sullivan RF, Ferrari G, Mignatti P, Galloway AC. Mechanisms of C-reactive protein up-regulation in arterialized vein grafts. Surgery 2006; 139: 254-62.
8. Chen Y, Wang J, Yao Y, Yuan W, Kong M, Lin Y, Geng D, Nie R. CRP regulates the expression and activity of tissue factor as well as tissue factor pathway inhibitor via NF-kappaB and ERK 1/2 MAPK pathway. FEBS Lett 2009; 583: 2811-18.
9. Cirillo P, Golino P, Calabro P, Cali G, Ragni M, De Rosa S, Cimmino G, Pacileo M, De Palma R, Forte L, Corigliano FG, Angri V, Spagnuolo R, Nitsch L, Chiariello M. C-reactive protein induces tissue factor expression and promotes smooth muscle and endothelial cell proliferation. Cardiovasc Res 2005; 68: 47-55.
10. Wu J, Stevenson MJ, Brown JM, Grunz EA, Strawn TL, Fay WP. C-reactive protein enhances tissue factor expression by vascular smooth muscle cells. Mechanisms and in vivo significance. Arterioscler Thromb Vasc Biol 2008; 28: 698-704.
11. Devaraj S, Xu DY, Jialal I. C-reactive protein increases plasminogen activator inhibitor-1 expression and activity in human aortic endothelial cells. Circulation 2003; 107: 398-404.
12. Chen C, Nan B, Lin P, Yao Q. C-reactive protein increases plasminogen activator inhibitor-1 expression in human endothelial cells. Thromb Res 2008; 122: 125-33.
13. Ciliberto G, Arcone R, Wagner EF, Rüther U. Inducible and tissue-specific expression of human C-reactive protein in transgenic mice. EMBO J 1987; 6: 4017-22.
14. Szalai AJ, van Ginkel FW, Dalrymple SA, Murray R, McGhee JR, Volanakis JE. Testosterone and IL-6 requirements for human C-reactive protein gene expression in transgenic mice. J Immunol 1998; 160: 5294-9.
15. Zou Y, Dietrich H, Hu Y, Metzler B, Wick G, Xu Q. Mouse model of venous bypass graft arteriosclerosis. Am J Pathol 1998; 153: 1301-10.
16. Ji Y, Strawn TL, Grunz EA, Stevenson MJ, Lohman AW, Lawrence DA, Fay WP. Multifaceted role of plasminogen activator inhibitor-1 in regulating early remodeling of vein bypass grafts. Arterioscler Thromb Vasc Biol 2011; 31: 1781-7.
17. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-delta delta CT method. Methods 2001; 25: 402-8.
18. Reinhardt C, von Brühl ML, Manukyan D, Grahl L, Lorenz M, Altmann B, Dlugai S, Hess S, Konrad I, Orschiedt L, Mackman N, Ruddock L, Massberg S, Engelmann B. Protein disulfide isomerase acts as an injury response signal that enhances fibrin generation via tissue factor activation. J Clin Invest 2008; 118: 1110-22.
19. Fay WP, Parker AC, Ansari MN, Zheng X, Ginsburg D. Vitronectin inhibits the thrombotic response to arterial injury in mice. Blood 1999; 93: 1825-30.
20. Zahedi K, Tebo JM, Siripont J, Klimo GF, Mortensen RF. Binding of human C-reactive protein to mouse macrophages is mediated by distinct receptors. J Immunol 1989; 142: 2384-92.
21. Bisoendial RJ, Kastelein JJP, Levels JHM, Zwaginga JJ, van den Bogaard B, Reitsma PH, Meijers JCM, Hartman D, Levi M, Stroes ESG. Activation of inflammation and coagulation after infusion of C-reactive protein in humans. Circ Res 2005; 96: 714-16.
22. Stark VK, Warner TF, Hoch JR. An ultrastructural study of progressive intimal hyperplasia in rat vein grafts. J Vasc Surg 1997; 26: 94-103.
23. Hoch JR, Stark VK, van Rooijen N, Kim JL, Nutt MP, Warner TF. Macrophage depletion alters vein graft intimal hyperplasia. Surgery 1999; 126: 428-37.
24. Stein MP, Mold C, Du Clos TW. C-reactive protein binding to murine leukocytes requires Fc gamma receptors. J Immunol 2000; 164: 1514-20.
25. Xing D, Hage FG, Chen YF, McCrory MA, Feng W, Skibinski GA, Majid-Hassan E, Oparil S, Szalai AJ. Exaggerated neointima formation in human C-reactive protein transgenic mice is IgG Fc receptor type I (FcgammaRI)-dependent. Am J Pathol 2008; 172: 22-30.
26. Hage FG, Oparil S, Xing D, Chen YF, McCrory MA, Szalai AJ. C-reactive protein-mediated vascular injury requires complement. Arterioscler Thromb Vasc Biol 2010; 30: 1189-95.
27. Ho KJ, Owens CD, Longo T, Sui XX, Ifantides C, Conte MS. C-reactive protein and vein graft disease: evidence for a direct effect on smooth muscle cell phenotype via modulation of PDGF receptor-beta. Am J Physiol Heart Circ Physiol 2008; 295: H1132-40.
28. Wilson AM, Swan JD, Ding H, Zhang Y, Whitbourn RJ, Gurry J, Yii M, Wilson AC, Hill M, Triggle C, Best JD, Jenkins AJ. Widespread vascular production of C-reactive protein (CRP) and a relationship between serum CRP, plaque CRP and intimal hypertrophy. Atherosclerosis 2007; 191: 175-81.
29. Nakagomi A, Freedman SB, Geczy CL. Interferon-γ and lipopolysaccharide potentiate monocyte tissue factor induction by C-reactive protein: relationship with age, sex, and hormone replacement treatment. Circulation 2000; 101: 1785-91.
30. Devaraj S, Dasu MR, Singh U, Rao LV, Jialal I. C-reactive protein stimulates superoxide anion release and tissue factor activity in vivo. Atherosclerosis 2009; 203: 67-74.
31. Kockx M, Cambier B, Bortier H, Meyer G, Cauwelaert P. The modulation of smooth muscle cell phenotype is an early event in human aorto-coronary saphenous vein grafts. Virchows Arch A Pathol Anat Histopathol 1992; 420: 155-62.
32. Danenberg HD, Kantak N, Grad E, Swaminathan RV, Lotan C, Edelman ER. C-reactive protein promotes monocyte-platelet aggregation: an additional link to the inflammatory-thrombotic intricacy. Eur J Haematol 2007; 78: 246-52.
33. Yaron G, Brill A, Dashevsky O, Yosef-Levi IM, Grad E, Danenberg HD, Varon D. C-reactive protein promotes platelet adhesion to endothelial cells: a potential pathway in atherothrombosis. Br J Haematol 2006; 134: 426-31.
34. Devaraj S, Kumaresan PR, Jialal I. C-reactive protein induces release of both endothelial microparticles and circulating endothelial cells in vitro and in vivo: further evidence of endothelial dysfunction. Clin Chem 2011; 57: 1757-61.
35. Danenberg HD, Szalai AJ, Swaminathan RV, Peng L, Chen Z, Seifert P, Fay WP, Simon DI, Edelman ER. Increased thrombosis after arterial injury in human C-reactive protein-transgenic mice. Circulation 2003; 108: 512-15.
36. Dubois C, Panicot-Dubois L, Merrill-Skoloff G, Furie B, Furie BC. Glycoprotein VI-dependent and -independent pathways of thrombus formation in vivo. Blood 2006; 107: 3902-6.