Intrinsic pathway of coagulation and arterial thrombosis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 27, Issue 12, 2007, Pages 2507-2513

  Gailani, David ^a   Renné, Thomas ^b  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Arterial thrombosis; Coagulation; Intrinsic pathways

Indexed keywords

BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 12; PROTEINASE;

ARTERY INJURY; ARTERY THROMBOSIS; BLOOD CLOTTING; BRAIN ISCHEMIA; HEART INFARCTION; HEMOSTASIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; REPERFUSION INJURY; REVIEW; THROMBOCYTE ACTIVATION; THROMBOGENESIS;

ANIMALS; ANTICOAGULANTS; BLOOD COAGULATION; DISEASE MODELS, ANIMAL; FACTOR XI; FACTOR XI DEFICIENCY; FACTOR XII; FACTOR XII DEFICIENCY; FIBRIN; HEMOSTASIS; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MICE; MICE, KNOCKOUT; PROTEASE INHIBITORS; REPERFUSION INJURY; THROMBOEMBOLISM; THROMBOSIS;

EID: 36349012420     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.107.155952     Document Type: Review

References (88)

1. Jiang Y, Doolittle RF. The evolution of vertebrate blood coagulation as viewed from a comparison of puffer fish and sea squirt genomes. Proc Natl Acad Sci U S A. 2003;100:7527-7532.
2. Davidson CJ, Hirt RP, Lal K, Snell P, Elgar G, Tuddenham EGD, McVey JH. Molecular evolution of the vertebrate blood coagulation network. Thrombo Haemost. 2003;89:420-428.
3. Rosenberg RD, Aird WC. Vascular-bed-specific hemostasis and hypercoagulable states. N Engl J Med. 1999;340:1555-1564.
4. Mann KG. Biochemistry and physiology of blood Coagulation. Thomb Haemost. 1999;82:165-174.
5. Furie B, Furie B. Molecular and cellular biology of blood coagulation. N Engl J Med. 1992;326:800-806.
6. Dahlback B. Blood coagulation. Lancet. 2000;355:1627-1632.
7. Davie EW. Kulman JD. An overview of the structure and function of thrombin. Semin Thromb Hemost. 2006;Suppl 1:3-15.
8. Macfarlane RG. Haemostasis: introduction. Br Med Bull. 1977;33:183-185.
9. Woodward M, Rumley A, Welsh P, MacMahon S, Lowe G. A comparison of the association between seven hemostatic or inflammatory variables and coronary artery disease. J Thromb Haemost. 2007;5:1795-1800.
10. Levine MN, Raskob G, Landefeld S, Kearon C. Hemorrhagic complications of anticoagulant treatment. Chest. 2001;119:108S-121S.
11. Weitz JI, Bates SM. New anticoagulants. J Thromb Haemost. 2005;3:1843-1853.
12. Schulman S, Ogren M. New concepts in optimal management of anticoagulant therapy for extended treatment of venous thromboembolism. Thromb Haemost. 2006;96:258-266.
13. Colman RW. Are hemostasis and thrombosis two sides of the same coin? J Exp Med. 2006;203:493-495.
14. Renné T, Pozgajova M, Gruner S, Schuh K, Pauer HU, Burfeind P, Gailani D, Nieswandt B. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med. 2005;202:271-281.
15. Wang X, Cheng Q, Xu L, Feuerstein GZ, Hsu MY, Smith PL, Seiffert DA, Schumacher WA, Ogletree ML, Gailani D. Effects of factor IX or factor XI deficiency on ferric chloride-induced carotid artery occlusion in mice. J Thromb Haemost. 2005;3:695-702.
16. Macfarlane RG. An enzyme cascade in the blood clotting mechanism, and its function as a biochemical amplifier. Nature. 1964;202:498-499.
17. Davie EW, Ratnoff OD. Waterfall Sequence for Intrinsic Blood Clotting. Science. 1964;145:1310-1312.
18. Mackman N. Role of tissue factor in hemostasis, thrombosis, and vascular development. Arterioscler Thromb Vasc Biol. 2004;24:1015-1022.
19. Morrissey JH. Tissue factor: a key molecule in hemostatic and nonhemostatic systems. Int J Hematol. 2004;79:103-108.
20. Gailani D, Broze G. Factor XI and the contact system. In: Scriver C, Beaudet A, Sly W, Valle D, Childs B, Kinzler K, Vogelstein B, eds. Metabolic and Molecular Basis of Inherited Disease. New York: McGraw-Hill. 2001.
21. Gailani D, Renné T. The intrinsic pathway of coagulation: a target for treating thromboembolic disease? J Thromb Haemost. 2007;5:1106-1112.
22. Renné T, Gailani D. The role of factor XII in hemostasis and thrombosis: Clinical Implications. Expert Rev Cardiovasc Therapy. 2007;5:733-741.
23. Lozier JN, Kessler CM. Clinical aspects and therapy of hemophilia, in Hoffman R, Benz E, Shattil S, Furie B, Cohen H, Silberstein L, McGlave P (eds). Hematology: Basic Principles and Practice, 4th ed. New York: Churchill Livingstone. 2005;p 2047.
24. Salomon O, Steinberg DM, Seligshon U. Variable bleeding manifestations characterize different types of surgery in patients with severe factor XI deficiency enabling parsimonious use of replacement therapy. Haemophilia. 2006;12:490-493.
25. Lammle B, Wuillemin W, Huber I, Krauskopf M, Zurcher C, Plugshaupt R, Furlan M. Thrombo-embolism and bleeding tendency in congenital factor XII deficiency: A study of 74 subjects from 14 Swiss families. Thromb Haemost. 1991;65:117-121.
26. Kaplan AP. Intrinsic coagulation, thrombosis, and bleeding. Blood. 1996;87:2090.
27. Rapaport SI, Rao LV. The tissue factor pathway: how it has become a "prima ballerina". Thromb Haemost. 1995;74:7-17.
28. Osterud B, Rapaport SI. Activation of factor IX by the reaction product of tissue factor and factor VII: additional pathway for initiating blood coagulation. Proc Natl Acad Sci U S A. 1977;74:5260-5264.
29. Naito K, Fujikawa K. Activation of human blood coagulation factor XI independent of factor XII. Factor XI is activated by thrombin and factor XIa in the presence of negatively charged surfaces. J Biol Chem. 1991;266:7353-7358.
30. Gailani D, Broze GJ, Jr. Factor XI activation in a revised model of blood coagulation. Science. 1991;253:909-912.
31. von dem Borne P, Meijers J, Bouma BN. Feedback activation of factor XI by thrombin in plasma results in additional formation of thrombin that protects fibrin clots from fibrinolysis. Blood. 1995;86:3035-3042.
32. Broze G, Girard T, Novotny W. Regulation of coagulation by a multivalent Kunitz-type inhibitor. Biochemistry. 1990;29:7539-7546.
33. Koster T, Blann AD, Breit E, Vandenbroucke JP, Rosendall FR. Role of clotting factor VIII in effect of von Willebrand factor on occurrence of deep-vein thrombosis. Lancet. 1995;345:152-155.
34. Van Hylckama Vlieg A, van der Linden IK, Bertina RM, Rosendaal FR. High levels of factor IX increase risk of venous thrombosis. Blood. 2000;95:3678-3682.
35. Meijers J, Tekelenburg W, Bouma B, Bertina R, Rosendaal F. High levels of coagulation factor XI as a risk factor for venous thrombosis. N Engl J Med. 2000;342:696-701. New 29.
36. Martinelli I. von Willebrand factor and factor VIII as risk factors for arterial and venous thrombosis. Sem Hematol. 2005;42:49-55.
37. Girolami A, Scandellari R, Zanon E, Sartori R, Girolami B. Non-catheter associated venous thrombosis in hemophilia A and B. A critical review of all reported cases. J Thromb Thrombolysis. 2006;21:279-284.
38. Girolami A, Ruzzon E, Tezza F, Scandellarti R, Vettore S, Girolami B. Arterial and venous thrombosis in rare congenital bleeding disorders: a critical review. Haemophilia. 2006;12:345-351.
39. Briggs N, Harman C, Dash CH. A decade of experience with factor XI concentrate. Hemophilia. 1996;2:s14.
40. Sramek A, Reiber JH, Gerrits WB, Rosendaal FR. Decreased coagulability has no clinically relevant effect on atherogenesis: observations in individuals with a hereditary bleeding tendency. Circulation. 2001;104:762-767.
41. Sramek A, Bucciarelli P, Federici AB, Mannucci PM, De Rosa V, Castaman G, Morfini M, Mazzucconi MG, Rocino A, Schiavoni M, Scaraggi FA, Reiber JH, Rosendaal FR. Patients with type 3 severe von Willebrand disease are not protected against atherosclerosis: results from a multicenter study in 47 patients. Circulation. 2004;109:740-744.
42. Shpilberg O, Rabi I, Schiller K, Walden R, Harats D, Tyrrell KS, Coller B, Seligsohn U. Patients with Glanzmann thrombasthenia lacking platelet glycoprotein alpha(IIb)beta(3) (GPIIb/IIIa) and alpha(v)beta(3) receptors are not protected from atherosclerosis. Circulation. 2002;105:1044-1048.
43. Bilora F, Zanon E, Petrobelli F, Cavraro M, Prandoni P, Pagnan A, Girolami A. Does hemophilia protect against atherosclerosis? A case-control study. Clin Appl Thromb Hemost. 2006;12:193-198.
44. Khallou-Laschet J, Caligiuri G, Tupin E, Gaston AT, Poirier B, Groyer E, Urbain D, Maisnier-Patin S, Sarkar R, Kaveri SV, Lacroix-Desmazes S, Nicoletti A. Role of the intrinsic coagulation pathway in atherogenesis assessed in hemophilic apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol. 2005;25:123-126.
45. Rosendaal FR, Briet E, Stibbe J, van Herpen G, Leuven JA, Hofman A, Vandenbroucke JP. Haemophilia protects against ischaemic heart disease: a study of risk factors. Br J Haematol. 1990;75:525-530.
46. Triemstra M, Rosendaal FR, Smit C, Van der Ploeg HM, Briet E. Mortality in patients with hemophilia. Changes in a Dutch population from 1986 to 1992 and 1973 to 1986. Ann Intern Med. 1995;123:823-827.
47. Girolami A, Randi ML, Ruzzon E, Zanon E, Girolami B. Myocardial infarction, other arterial thrombosis and invasive coronary procedures in Haemophilia B: a critical evaluation of case reports. J Thromb Thrombolysis. 2005;20:43-46.
48. Girolami A, Ruzzon E, Fabris C, Varvarikis R, Sartori R, Girolami B. Myocardial infarction and other arterial occlusions in hemophilia A patients. A cardiological evaluation of all 42 cases reported in the literature. Acta Haematol. 2006;116:120-125.
49. Salomon O, Steinberg D, Dardik R, Rosenberg N, Zivelin A, Tamarin I, Ravid B, Berliner S, Seligsohn. Inherited factor XI deficiency confers no protection against acute myocardial infarction. J Thromb Haemost. 2003;1:658-661.
50. Doggen CJ, Rosendaal FR, Meijers JC. Levels of intrinsic coagulation factors and the risk of myocardial infarction among men: Opposite and synergistic effects of factors XI and XII. Blood. 2006;108:4045-4051.
51. Yang DT, Flanders MM, Kim H, Rodgers GM. Elevated factor XI activity levels are associated with an increased odds ratio for cerebrovascular events. Am J Clin Pathol. 2006;126:411-415.
52. Gruber A, Hanson SR. Factor XI-dependence of surface- and tissue factor-initiated thrombus propagation in primates. Blood. 2003;102:953-955.
53. Yamashita A, Nishihira K, Kitazawa T, Yoshihashi K, Soeda T, Esaki K, Imamura T, Hattori K, Asada Y. Factor XI contributes to thrombus propagation on injured neointima of the rabbit iliac artery. J Thromb Haemost. 2006;4:1496-1501.
54. Salomon O, Steinberg DM, Koren-Morag N, Seligson U. Decreased incidence of ischemic stroke in patients with severe factor XI deficiency suggests that the deficiency confers protection. J Thromb Haemost. 2007;5 Supplement 2:P-M-203.
55. Ratnoff OD. A quarter century with Mr. Hageman. Thromb Haemost. 1980;43:95-98.
56. Girolami A, Randi ML, Gavasso S, Lombardi AM, Spiezia F. The occasional venous thromboses seen in patients with severe (homozygous) FXII deficiency are probably due to associated risk factors: a study of prevalence in 21 patients and review of the literature. J Thromb Thrombolysis. 2004;17:139-143.
57. Zeerleder S, Schloesser M, Redondo M, Wuillemin WA, Engel W, Furlan M, Lammle B. Reevaluation of the incidence of thromboembolic complications in congenital factor XII deficiency-a study on 73 subjects from 14 Swiss families. Thromb Haemost. 1999;82:1240-1246.
58. Koster T, Rosendaal FR, Briet E, Vandenbroucke JP. John Hageman's factor and deep-vein thrombosis: Leiden thrombophilia Study. Br J Haematol. 1994;87:422-424.
59. Endler G, Marsik C, Jilma B, Schickbauer T, Mannhalter C. Evidence of a U-shaped association between FXII activity and overall survival. J Thromb Haemost. 2007;5:1143-1148.
60. Zito F, Drummond F, Bujac SR, Esnouf MP, Morrissey JH, Humphries SE, Miller GJ. Epidemiological and genetic associations of activated factor XII concentration with factor VII activity, fibrinopeptide A concentration, and risk of coronary heart disease in men. Circulation. 2000;102:2058-2062.
61. Grundt H, Nilsen DW, Hetland O, Valente E, Fagertun HE. Activated factor 12 (FXIIa) predicts recurrent coronary events after an acute myocardial infarction. Am Heart J. 2004;147:260-266.
62. Govers-Riemslag JW, Smid M, Cooper JA, Bauer KA, Rosenberg RD, Hack CE, Hamulyak K, Spronk HM, Miller GJ, Ten Cate H. The plasma kallikrein-kinin system and risk of cardiovascular disease in men. J Thromb Haemost. 2007;5:1896-1903.
63. Jones DW, Gallimore MJ, MacKie IJ, Harris SL, Winter M. Reduced factor XII levels in patients with the antiphospholipid syndrome are associated with antibodies to factor XII. Br J Haematol. 2000;110:721-726.
64. Jones DW, Nichols PJ, Donohoe S, Gallimore MJ, Winter M. Antibodies to factor XII are distinct from antibodies to prothrombin in patients with the anti-phospholipid syndrome. Thromb Haemost. 2002;87:426-430.
65. Bi L, Lawler AM, Antonarakis SE, High KA, Gearhart JD, Kazazian HH Jr. Targeted disruption of the mouse factor VIII gene produces a model of haemophilia A. Nat Genet. 1995;10:119-121.
66. Lin HF, Maeda N, Smithies O, Straight DL, Stafford DW. A coagulation factor IX-deficient mouse model for human hemophilia B. Blood. 1997;90:3962-3966.58.
67. Gailani D, Lasky NM, Broze GJ, Jr. A murine model of factor XI deficiency. Blood Coagul Fibrinolysis. 1997;8:134-144.
68. Pauer HU, Renné T, Hemmerlein B, Legler T, Fritzlar S, Adham I, Muller-Esterl W, Emons G, Sancken U, Engel W, Burfeind P. Targeted deletion of murine coagulation factor XII gene-a model for contact phase activation in vivo. Thromb Haemost. 2004;92:503-508.
69. Emeis JJ, Jirouskova M, Muchitsch EM, Shet AS, Smyth SS, Johnson GJA. Guide to murine coagulation factor structure, function, assays, and genetic alterations. J Thromb Haemost. 2007;5:670-679.
70. Bi L, Sarkar R, Naas T, Lawler AM, Pain J, Shumaker SL, Bedian V, Kazazian HH. Further characterization of factor VIII-deficient mice created by gene targeting: RNA and protein studies. Blood. 1996;88:3446-3450.
71. Muchitsch EM, Turecek PL, Zimmermann K, Pichler L, Auer W, Richter G, Gritsch H, Schwarz HP. Phenotypic expression of murine hemophilia. Thromb Haemost. 1999;82:1371-1373.
72. Asakai R, Chung DW, Davie EW, Seligsohn U. Factor XI deficiency in Ashkenazi Jews in Israel. N Engl J Med. 1991;325:153-158.
73. Furie B, Furie BC. Thrombus formation in vivo. J Clin Invest. 2005;115:3355-3362.65.
74. Baird TR, Gailani D, Furie B, Furie B. Factor XI deficient mice have reduced platelet accumulation and fibrin deposition after laser injury. Blood. 2004;104:66a.
75. Kleinschnitz C, Stoll G, Bendszus M, Schuh K, Pauer HU, Burfeind P, Renné C, Gailani D, Nieswandt B, Renne T. Targeting coagulation factor XII provides protection from pathological thrombosis in cerebral ischemia without interfering with hemostasis. J Exp Med. 2006;203:513-518.
76. Choudhri TF, Hoh BL, Prestigiacomo CJ, Huang J, Kim LJ, Schmidt AM, Kisiel W, Connolly ES, Jr., Pinsky DJ. Targeted inhibition of intrinsic coagulation limits cerebral injury in stroke without increasing intracerebral hemorrhage. J Exp Med. 1999;190:91-9968.
77. Radcliffe R, Bagdasarian A, Colman R, Nemerson Y. Activation of bovine factor VII by Hageman factor fragments. Blood. 1977;50:611-617.
78. Ghebrehiwet B, Randazzo BP, Dunn JT, Silverberg M, Kaplan AP. Mechanisms of activation of the classical pathway of complement by Hageman factor fragment. J Clin Invest. 1983;71:1450-1456.
79. Ichinose A, Fujikawa K, Suyama T. The activation of pro-urokinase by plasma kallikrein and its inactivation by thrombin. J Biol Chem. 1986;261:3486-3489.
80. Renné T, Schuh K, Muller-Esterl W. Local bradykinin formation is controlled by glycosaminoglycans. J Immunol. 2005;175:3377-3385.
81. Groger M, Lebesgue D, Pruneau D, Relton J, Kim SW, Nussberger J, Plesnila N. Release of bradykinin and expression of kinin B2 receptors in the brain: role for cell death and brain edema formation after focal cerebral ischemia in mice. J Cereb Blood Flow Metab. 2005;25:978-989.
82. Xia CF, Smith RS, Jr., Shen B, Yang ZR, Borlongan CV, Chao L, Chao J. Postischemic brain injury is exacerbated in mice lacking the kinin B2 receptor. Hypertension. 2006;47:752-761.
83. Shariat-Madar Z, Mahdi F, Warnock M, Homeister JW, Srikanth S, Krijanovski Y, Murphey LJ, Jaffa AA, Schmaier AH. Bradykinin B2 receptor knockout mice are protected from thrombosis by increased nitric oxide and prostacyclin. Blood. 2006;108:192-199.
84. Thompson RE, Mandle R Jr., Kaplan AP. Association of factor XI and high molecular weight kininogen in human plasma. J Clin Invest. 1977;60:1376-1380.
85. Sainz IM, Pixley RA, Colman RW. Fifty years of research on the plasma kallikrein-kinin system: from protein structure and function to cell biology and in-vivo pathophysiology. Thromb Haemost. 2007;98:77-83.
86. Cheng Q, Zhao Y, Lawson WE, Polosukhin VV, Johnson JE, Blackwell TS, Gailani D. The effects of intrinsic pathway protease deficiencies on plasminogen-deficient mice. Blood. 2005;106:3055-3057.
87. Santamaria A, Mateo J, Tirado I, Oliver A, Belvis R, Marti-Fabregas J, Felices R, Soria JM, Souto JC, Fontcuberta J. Homozygosity of the T allele of the 46 C->T polymorphism in the F12 gene is a risk factor for ischemic stroke in the Spanish population. Stroke. 2004;35:1795-1799.
88. Wang X, Smith PL, Hsu M-Y, Gailani D, Schumacher WA, Ogletree ML, and Seiffert DA. Effects of factor XI deficiency on ferric chloride-induced vena cava thrombosis in mice. J Thromb Haemost. 2006;4:1982-1988.