The impact of the fibrinolytic system on the risk of venous and arterial thrombosis

Seminars in Thrombosis and Hemostasis

Volumn 35, Issue 5, 2009, Pages 468-477

  Meltzer, Mirjam E ^a,b   Doggen, Carine J M ^b   De Groot, Philip G ^a   Rosendaal, Frits R ^b   Lisman, Ton ^a,c  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Arterial thrombosis; Fibrinolysis; Venous thrombosis

Indexed keywords

ALPHA 2 ANTIPLASMIN; ANTIFIBRINOLYTIC AGENT; FIBROLASE; PLASMINOGEN; PLASMINOGEN ACTIVATOR INHIBITOR 1; THROMBIN; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR; TISSUE PLASMINOGEN ACTIVATOR; UROKINASE;

ARTERY DISEASE; ARTERY THROMBOSIS; ATHEROSCLEROSIS; BLOOD CLOTTING TIME; DISEASE ASSOCIATION; DISEASE COURSE; ENZYME ACTIVITY; FIBRINOLYSIS; HUMAN; INFLAMMATION; METABOLIC SYNDROME X; PLEIOTROPY; PRIORITY JOURNAL; REVIEW; RISK FACTOR; VEIN THROMBOSIS;

ALPHA-2-ANTIPLASMIN; FIBRINOLYSIN; FIBRINOLYSIS; HUMANS; PLASMINOGEN; PLASMINOGEN ACTIVATOR INHIBITOR 1; RISK; TATA-BINDING PROTEIN ASSOCIATED FACTORS; THROMBOSIS; TISSUE PLASMINOGEN ACTIVATOR; TRANSCRIPTION FACTOR TFIID; VENOUS THROMBOSIS;

EID: 70449431788     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0029-1234142     Document Type: Review

References (98)

1. Rosendaal F R. Clotting and myocardial infarction: a cycle of insights. J Thromb Haemost 2003 1 (4) 640-642
2. Lisman T, de Groot P G., Meijers J CM, Rosendaal F R. Reduced plasma fibrinolytic potential is a risk factor for venous thrombosis. Blood 2005 105 (3) 1102-1105
3. Meltzer M E., Doggen C JM, de Groot P G., Rosendaal F R., Lisman T. Reduced plasma fibrinolytic capacity as a potential risk factor for a first myocardial infarction in young men. Br J Haematol 2009 145 (1) 121-127
4. Meltzer M E., Lisman T, Doggen C JM, de Groot P G., Rosendaal F R. Synergistic effects of hypofibrinolysis and genetic and acquired risk factors on the risk of a first venous thrombosis. PLoS Med 2008 5 (5) e97
5. Lijnen H R. Plasmin and matrix metalloproteinases in vascular remodeling. Thromb Haemost 2001 86 (1) 324-333
6. Kooistra T, Schrauwen Y, Arts J, Emeis J J. Regulation of endothelial cell t-PA synthesis and release. Int J Hematol 1994 59 (4) 233-255
7. Hoylaerts M, Rijken D C., Lijnen H R., Collen D. Kinetics of the activation of plasminogen by human tissue plasminogen activator. Role of fibrin. J Biol Chem 1982 257 (6) 2912-2919
8. Chmielewska J, Rånby M, Wiman B. Kinetics of the inhibition of plasminogen activators by the plasminogen-activator inhibitor. Evidence for second-site interactions. Biochem J 1988 251 (2) 327-332
9. Chmielewska J, Rånby M, Wiman B. Evidence for a rapid inhibitor to tissue plasminogen activator in plasma. Thromb Res 1983 31 427-436
10. Rijken D C., Lijnen H R. New insights into the molecular mechanisms of the fibrinolytic system. J Thromb Haemost 2009 7 (1) 4-13
11. Collen D. Identification and some properties of a new fast-reacting plasmin inhibitor in human plasma. Eur J Biochem 1976 69 (1) 209-216
12. Rákóczi I, Wiman B, Collen D. On the biological significance of the specific interaction between fibrin, plasminogen and antiplasmin. Biochim Biophys Acta 1978 540 (2) 295-300
13. Sakata Y, Aoki N. Significance of cross-linking of alpha 2-plasmin inhibitor to fibrin in inhibition of fibrinolysis and in hemostasis. J Clin Invest 1982 69 (3) 536-542
14. Mosnier L O., Bouma B N. Regulation of fibrinolysis by thrombin activatable fibrinolysis inhibitor, an unstable carboxypeptidase B that unites the pathways of coagulation and fibrinolysis. Arterioscler Thromb Vasc Biol 2006 26 (11) 2445-2453
15. Prins M H., Hirsh J. A critical review of the evidence supporting a relationship between impaired fibrinolytic activity and venous thromboembolism. Arch Intern Med 1991 151 (9) 1721-1731
16. Lisman T, Leebeek F WG, Mosnier L O. et al. Thrombin-activatable fibrinolysis inhibitor deficiency in cirrhosis is not associated with increased plasma fibrinolysis. Gastroenterology 2001 121 (1) 131-139
17. Guimaräes A H., de Bruijne E L., Lisman T et al. Hypofibrinolysis as risk factor for arterial thrombosis at young age. Br J Haematol 2009 145 (1) 115-120
18. Meade T W., Ruddock V, Stirling Y, Chakrabarti R, Miller G J. Fibrinolytic activity, clotting factors, and long-term incidence of ischaemic heart disease in the Northwick Park Heart Study. Lancet 1993 342 (8879) 1076-1079
19. Meade T W., Cooper J A., Chakrabarti R, Miller G J., Stirling Y, Howarth D J. Fibrinolytic activity and clotting factors in ischaemic heart disease in women. BMJ 1996 312 (7046) 1581
20. Zorio E, Castelló R, Falcó C et al. Thrombin-activatable fibrinolysis inhibitor in young patients with myocardial infarction and its relationship with the fibrinolytic function and the protein C system. Br J Haematol 2003 122 (6) 958-965
21. Juhan-Vague I, Pyke S D., Alessi M C., Jespersen J, Haverkate F, Thompson S G. Fibrinolytic factors and the risk of myocardial infarction or sudden death in patients with angina pectoris. ECAT Study Group. European Concerted Action on Thrombosis and Disabilities. Circulation 1996 94 (9) 2057-2063
22. Cortellaro M, Cofrancesco E, Boschetti C et al, The PLAT Group. Increased fibrin turnover and high PAI-1 activity as predictors of ischemic events in atherosclerotic patients. A case-control study. Arterioscler Thromb 1993 13 (10) 1412-1417
23. Doggen C JM, Rosendaal F R., Meijers J CM. Levels of intrinsic coagulation factors and the risk of myocardial infarction among men: opposite and synergistic effects of factors XI and XII. Blood 2006 108 (13) 4045-4051
24. Segev A, Ellis M H., Segev F et al. High prevalence of thrombophilia among young patients with myocardial infarction and few conventional risk factors. Int J Cardiol 2005 98 (3) 421-424
25. Mignatti P, Robbins E, Rifkin D B. Tumor invasion through the human amniotic membrane: requirement for a proteinase cascade. Cell 1986 47 (4) 487-498
26. Lijnen H R. Matrix metalloproteinases and cellular fibrinolytic activity. Biochemistry (Mosc) 2002 67 (1) 92-98
27. Shah P K., Galis Z S. Matrix metalloproteinase hypothesis of plaque rupture: players keep piling up but questions remain. Circulation 2001 104 (16) 1878-1880
28. Carmeliet P, Moons L, Ploplis V, Plow E, Collen D. Impaired arterial neointima formation in mice with disruption of the plasminogen gene. J Clin Invest 1997 99 (2) 200-208 (Pubitemid 27053462)
29. Xiao Q, Danton M J., Witte D P. et al. Plasminogen deficiency accelerates vessel wall disease in mice predisposed to atherosclerosis. Proc Natl Acad Sci U S A 1997 94 (19) 10335-10340
30. Matsushima K, Taguchi M, Kovacs E J., Young H A., Oppenheim J J. Intracellular localization of human monocyte associated interleukin 1 (IL 1) activity and release of biologically active IL 1 from monocytes by trypsin and plasmin. J Immunol 1986 136 (8) 2883-2891
31. Lyons R M., Gentry L E., Purchio A F., Moses H L. Mechanism of activation of latent recombinant transforming growth factor beta 1 by plasmin. J Cell Biol 1990 110 (4) 1361-1367
32. Degen J L., Bugge T H., Goguen J D. Fibrin and fibrinolysis in infection and host defense. J Thromb Haemost 2007 5 (Suppl 1) 24-31
33. Epstein S E. The multiple mechanisms by which infection may contribute to atherosclerosis development and course. Circ Res 2002 90 (1) 2-4
34. Favier R, Aoki N, de Moerloose P. Congenital alpha(2)-plasmin inhibitor deficiencies: a review. Br J Haematol 2001 114 (1) 4-10
35. Brandt J T. Plasminogen and tissue-type plasminogen activator deficiency as risk factors for thromboembolic disease. Arch Pathol Lab Med 2002 126 (11) 1376-1381
36. Okamoto A, Sakata T, Mannami T et al. Population-based distribution of plasminogen activity and estimated prevalence and relevance to thrombotic diseases of plasminogen deficiency in the Japanese: the Suita Study. J Thromb Haemost 2003 1 (11) 2397-2403
37. Hamsten A, Blombäck M, Wiman B et al. Haemostatic function in myocardial infarction. Br Heart J 1986 55 (1) 58-66
38. Folsom A R., Aleksic N, Park E, Salomaa V, Juneja H, Wu K K. Prospective study of fibrinolytic factors and incident coronary heart disease: the Atherosclerosis Risk in Communities (ARIC) Study. Arterioscler Thromb Vasc Biol 2001 21 (4) 611-617 (Pubitemid 32323396)
39. Jenkins G R., Seiffert D, Parmer R J., Miles L A. Regulation of plasminogen gene expression by interleukin-6. Blood 1997 89 (7) 2394-2403
40. Alessi M C., Poggi M, Juhan-Vague I. Plasminogen activator inhibitor-1, adipose tissue and insulin resistance. Curr Opin Lipidol 2007 18 (3) 240-245
41. Samad F, Pandey M, Bell P A., Loskutoff D J. Insulin continues to induce plasminogen activator inhibitor 1 gene expression in insulin-resistant mice and adipocytes. Mol Med 2000 6 (8) 680-692
42. Peraldi P, Spiegelman B M. Studies of the mechanism of inhibition of insulin signaling by tumor necrosis factor-alpha. J Endocrinol 1997 155 (2) 219-220 (Pubitemid 27475814)
43. Samad F, Yamamoto K, Loskutoff D J. Distribution and regulation of plasminogen activator inhibitor-1 in murine adipose tissue in vivo. Induction by tumor necrosis factor-alpha and lipopolysaccharide. J Clin Invest 1996 97 (1) 37-46
44. Sakamoto T, Woodcock-Mitchell J, Marutsuka K, Mitchell J J., Sobel B E., Fujii S. TNF-alpha and insulin, alone and synergistically, induce plasminogen activator inhibitor-1 expression in adipocytes. Am J Physiol 1999 276 (6 Pt 1) C1391-C1397
45. Festa A, DAgostino R Jr, Tracy R P., Haffner S M., Insulin Resistance Atherosclerosis Study. Elevated levels of acute-phase proteins and plasminogen activator inhibitor-1 predict the development of type 2 diabetes: the insulin resistance atherosclerosis study. Diabetes 2002 51 (4) 1131-1137
46. Morange P E., Alessi M C., Verdier M, Casanova D, Magalon G, Juhan-Vague I. PAI-1 produced ex vivo by human adipose tissue is relevant to PAI-1 blood level. Arterioscler Thromb Vasc Biol 1999 19 (5) 1361-1365
47. De Taeye B M., Novitskaya T, Gleaves L, Covington J W., Vaughan D E. Bone marrow plasminogen activator inhibitor-1 influences the development of obesity. J Biol Chem 2006 281 (43) 32796-32805
48. Schäfer K, Fujisawa K, Konstantinides S, Loskutoff D J. Disruption of the plasminogen activator inhibitor 1 gene reduces the adiposity and improves the metabolic profile of genetically obese and diabetic ob/ob mice. FASEB J 2001 15 (10) 1840-1842
49. Skurk T, Lee Y M., Hauner H. Angiotensin II and its metabolites stimulate PAI-1 protein release from human adipocytes in primary culture. Hypertension 2001 37 (5) 1336-1340
50. Birgel M, Gottschling-Zeller H, Röhrig K, Hauner H. Role of cytokines in the regulation of plasminogen activator inhibitor-1 expression and secretion in newly differentiated subcutaneous human adipocytes. Arterioscler Thromb Vasc Biol 2000 20 (6) 1682-1687
51. Felmeden D C., Lip G Y. The renin-angiotensin-aldosterone system and fibrinolysis. J Renin Angiotensin Aldosterone Syst 2000 1 (3) 240-244
52. Schneiderman J, Sawdey M S., Keeton M R. et al. Increased type 1 plasminogen activator inhibitor gene expression in atherosclerotic human arteries. Proc Natl Acad Sci U S A 1992 89 (15) 6998-7002
53. Lupu F, Bergonzelli G E., Heim D A. et al. Localization and production of plasminogen activator inhibitor-1 in human healthy and atherosclerotic arteries. Arterioscler Thromb 1993 13 (7) 1090-1100
54. Sjöland H, Eitzman D T., Gordon D, Westrick R, Nabel E G., Ginsburg D. Atherosclerosis progression in LDL receptor-deficient and apolipoprotein E-deficient mice is independent of genetic alterations in plasminogen activator inhibitor-1. Arterioscler Thromb Vasc Biol 2000 20 (3) 846-852
55. Eitzman D T., Westrick R J., Xu Z, Tyson J, Ginsburg D. Plasminogen activator inhibitor-1 deficiency protects against atherosclerosis progression in the mouse carotid artery. Blood 2000 96 (13) 4212-4215
56. Luttun A, Lupu F, Storkebaum E et al. Lack of plasminogen activator inhibitor-1 promotes growth and abnormal matrix remodeling of advanced atherosclerotic plaques in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2002 22 (3) 499-505
57. Kienast J, Padró T, Steins M et al. Relation of urokinase-type plasminogen activator expression to presence and severity of atherosclerotic lesions in human coronary arteries. Thromb Haemost 1998 79 (3) 579-586
58. Degryse B, Sier C F., Resnati M, Conese M, Blasi F. PAI-1 inhibits urokinase-induced chemotaxis by internalizing the urokinase receptor. FEBS Lett 2001 505 (2) 249-254
59. Meltzer M E., Doggen C JM, de Groot P G., Rosendaal F R., Lisman T. Fibrinolysis and the risk of venous and arterial thrombosis. Curr Opin Hematol 2007 14 (3) 242-248
60. Grimaudo V, Hauert J, Bachmann F, Kruithof E K. Diurnal variation of the fibrinolytic system. Thromb Haemost 1988 59 (3) 495-499
61. Mannucci P M., Bernardinelli L, Foco L et al. Tissue plasminogen activator antigen is strongly associated with myocardial infarction in young women. J Thromb Haemost 2005 3 (2) 280-286
62. Thögersen A M., Jansson J H., Boman K et al. High plasminogen activator inhibitor and tissue plasminogen activator levels in plasma precede a first acute myocardial infarction in both men and women: evidence for the fibrinolytic system as an independent primary risk factor. Circulation 1998 98 (21) 2241-2247
63. Scarabin P Y., Aillaud M F., Amouyel P et al, Prospective Epidemiological Study of Myocardial Infarction. Associations of fibrinogen, factor VII and PAI-1 with baseline findings among 10,500 male participants in a prospective study of myocardial infarctionthe PRIME Study. Thromb Haemost 1998 80 (5) 749-756
64. Lundblad D, Dinesen B, Rautio A, Røder M E., Eliasson M. Low level of tissue plasminogen activator activity in non-diabetic patients with a first myocardial infarction. J Intern Med 2005 258 (1) 13-20
65. Smith A, Patterson C, Yarnell J, Rumley A, Ben-Shlomo Y, Lowe G. Which hemostatic markers add to the predictive value of conventional risk factors for coronary heart disease and ischemic stroke? The Caerphilly Study. Circulation 2005 112 (20) 3080-3087
66. Verheugt F W., ten Cate J W., Sturk A et al. Tissue plasminogen activator activity and inhibition in acute myocardial infarction and angiographically normal coronary arteries. Am J Cardiol 1987 59 (12) 1075-1079
67. Båvenholm P, de Faire U, Landou C et al. Progression of coronary artery disease in young male post-infarction patients is linked to disturbances of carbohydrate and lipoprotein metabolism and to impaired fibrinolytic function. Eur Heart J 1998 19 (3) 402-410
68. Juhan-Vague I, Morange P E., Frere C et al, HIFMECH Study Group. The plasminogen activator inhibitor-1 -675 4G/5G genotype influences the risk of myocardial infarction associated with elevated plasma proinsulin and insulin concentrations in men from Europe: the HIFMECH study. J Thromb Haemost 2003 1 (11) 2322-2329
69. Munkvad S, Gram J, Jespersen J. A depression of active tissue plasminogen activator in plasma characterizes patients with unstable angina pectoris who develop myocardial infarction. Eur Heart J 1990 11 (6) 525-528
70. Robinson S D., Ludlam C A., Boon N A., Newby D E. Endothelial fibrinolytic capacity predicts future adverse cardiovascular events in patients with coronary heart disease. Arterioscler Thromb Vasc Biol 2007 27 (7) 1651-1656
71. Jansson J H., Nilsson T K., Olofsson B O. Tissue plasminogen activator and other risk factors as predictors of cardiovascular events in patients with severe angina pectoris. Eur Heart J 1991 12 (2) 157-161
72. Cushman M, Lemaitre R N., Kuller L H. et al. Fibrinolytic activation markers predict myocardial infarction in the elderly. The Cardiovascular Health Study. Arterioscler Thromb Vasc Biol 1999 19 (3) 493-498
73. Itakura H, Sobel B E., Boothroyd D et al, Atherosclerotic Disease, Vascular Function and Genetic Epidemiology Advance (ADVANCE) Study. Do plasma biomarkers of coagulation and fibrinolysis differ between patients who have experienced an acute myocardial infarction versus stable exertional angina? Am Heart J 2007 154 (6) 1059-1064
74. Ridker P M., Vaughan D E., Stampfer M J. et al. Baseline fibrinolytic state and the risk of future venous thrombosis. A prospective study of endogenous tissue-type plasminogen activator and plasminogen activator inhibitor. Circulation 1992 85 (5) 1822-1827
75. Ladenvall P, Johansson L, Jansson J H. et al. Tissue-type plasminogen activator -7,351C/T enhancer polymorphism is associated with a first myocardial infarction. Thromb Haemost 2002 87 (1) 105-109
76. Tzoulaki I, Murray G D., Lee A J., Rumley A, Lowe G D., Fowkes F G. Relative value of inflammatory, hemostatic, and rheological factors for incident myocardial infarction and stroke: the Edinburgh Artery Study. Circulation 2007 115 (16) 2119-2127
77. van der Bom J G., de Knijff P, Haverkate F et al. Tissue plasminogen activator and risk of myocardial infarction. The Rotterdam Study. Circulation 1997 95 (12) 2623-2627
78. Lowe G D., Danesh J, Lewington S et al. Tissue plasminogen activator antigen and coronary heart disease. Prospective study and meta-analysis. Eur Heart J 2004 25 (3) 252-259
79. Gram J, Bladbjerg E M., Møller L, Sjøl A, Jespersen J. Tissue-type plasminogen activator and C-reactive protein in acute coronary heart disease. A nested case-control study. J Intern Med 2000 247 (2) 205-212
80. Pineda J, Marin F, Marco P et al. Premature coronary artery disease in young (age <45) subjects: Interactions of lipid profile, thrombophilic and haemostatic markers. Int J Cardiol 2008 July 12 (Epub ahead of print)
81. MacCallum P K., Cooper J A., Howarth D J., Meade T W., Miller G J. Sex differences in the determinants of fibrinolytic activity. Thromb Haemost 1998 79 (3) 587-590
82. Crowther M A., Roberts J, Roberts R et al. Fibrinolytic variables in patients with recurrent venous thrombosis: a prospective cohort study. Thromb Haemost 2001 85 (3) 390-394
83. Bajzar L, Manuel R, Nesheim M E. Purification and characterization of TAFI, a thrombin-activatable fibrinolysis inhibitor. J Biol Chem 1995 270 (24) 14477-14484
84. Boffa M B., Koschinsky M L. Curiouser and curiouser: recent advances in measurement of thrombin-activatable fibrinolysis inhibitor (TAFI) and in understanding its molecular genetics, gene regulation, and biological roles. Clin Biochem 2007 40 (7) 431-442
85. Campbell W D., Lazoura E, Okada N, Okada H. Inactivation of C3a and C5a octapeptides by carboxypeptidase R and carboxypeptidase N. Microbiol Immunol 2002 46 (2) 131-134
86. Myles T, Nishimura T, Yun T H. et al. Thrombin activatable fibrinolysis inhibitor, a potential regulator of vascular inflammation. J Biol Chem 2003 278 (51) 51059-51067
87. Swaisgood C M., Schmitt D, Eaton D, Plow E F. In vivo regulation of plasminogen function by plasma carboxypeptidase B. J Clin Invest 2002 110 (9) 1275-1282
88. Asai S, Sato T, Tada T et al. Absence of procarboxypeptidase R induces complement-mediated lethal inflammation in lipopolysaccharide-primed mice. J Immunol 2004 173 (7) 4669-4674
89. Sato T, Miwa T, Akatsu H et al. Pro-carboxypeptidase R is an acute phase protein in the mouse, whereas carboxypeptidase N is not. J Immunol 2000 165 (2) 1053-1058
90. te Velde E A., Wagenaar G T., Reijerkerk A et al. Impaired healing of cutaneous wounds and colonic anastomoses in mice lacking thrombin-activatable fibrinolysis inhibitor. J Thromb Haemost 2003 1 (10) 2087-2096
91. van Tilburg N H., Rosendaal F R., Bertina R M. Thrombin activatable fibrinolysis inhibitor and the risk for deep vein thrombosis. Blood 2000 95 (9) 2855-2859
92. Eichinger S, Schönauer V, Weltermann A et al. Thrombin-activatable fibrinolysis inhibitor and the risk for recurrent venous thromboembolism. Blood 2004 103 (10) 3773-3776 (Pubitemid 38596294)
93. Libourel E J., Bank I, Meinardi J R. et al. Co-segregation of thrombophilic disorders in factor V Leiden carriers; the contributions of factor VIII, factor XI, thrombin activatable fibrinolysis inhibitor and lipoprotein(a) to the absolute risk of venous thromboembolism. Haematologica 2002 87 (10) 1068-1073
94. Silveira A, Schatteman K, Goossens F et al. Plasma procarboxypeptidase U in men with symptomatic coronary artery disease. Thromb Haemost 2000 84 (3) 364-368
95. Santamaría A, Martínez-Rubio A, Borrell M, Mateo J, Ortín R, Fontcuberta J. Risk of acute coronary artery disease associated with functional thrombin activatable fibrinolysis inhibitor plasma level. Haematologica 2004 89 (7) 880-881
96. Schroeder V, Wilmer M, Buehler B, Kohler H P. TAFI activity in coronary artery disease: a contribution to the current discussion on TAFI assays. Thromb Haemost 2006 96 (2) 236-237
97. Morange P E., Tregouet D A., Frere C et al, The Prime Study Group. TAFI gene haplotypes, TAFI plasma levels and future risk of coronary heart disease: the PRIME Study. J Thromb Haemost 2005 3 (7) 1503-1510
98. Meltzer M E., Doggen C J., de Groot P G., Meijers J C., Rosendaal F R., Lisman T. Low thrombin activatable fibrinolysis inhibitor activity levels are associated with an increased risk of a first myocardial infarction in men. Haematologica 2009 94 (6) 811-818