Role of blood coagulation factor XI in downregulation of fibrinolysis

Current Opinion in Hematology

Volumn 7, Issue 5, 2000, Pages 266-272

  Bouma, Bonno N ^a   Meijers, Joost C M ^a,b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 12; PROCOAGULANT; THROMBIN; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR; THROMBOMODULIN;

BLEEDING; BLOOD CLOT LYSIS; BLOOD CLOTTING; FIBRIN CLOT; FIBRINOLYSIS; HEMOSTASIS; HUMAN; MOLECULAR WEIGHT; PRIORITY JOURNAL; REVIEW; RISK FACTOR; VEIN THROMBOSIS;

ANIMALS; DOWN-REGULATION; FACTOR XI; FIBRINOLYSIS; HUMANS; THROMBIN; VENOUS THROMBOSIS;

EID: 0033875539     PISSN: 10656251     EISSN: None     Source Type: Journal    
DOI: 10.1097/00062752-200009000-00002     Document Type: Review

References (58)

1. 1 Colman RW, Schmaier AH: Contact system: A vascular biology modulator with anticoagulant, profibrinolytic, antiadhesive, and proinflammatory attributes. Blood 1997, 90:3819-3843.
2. 2 Asakai R, Chung DW, Davie EW, et al.: Factor XI deficiency in Ashkenazi Jews in Israel. N Engl J Med 1991, 325:153-158.
3. 3 Berliner S, Horowitz I, Martinowitz U, et al.: Dental surgery in patients with severe factor XI deficiency without plasma replacement. Blood Coagul Fibrinol 1992, 3:465-468.
4. 4 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.
5. 5 Gailani D, Broze G: Factor XI activation in a revised model of coagulation. Science 1991, 253:909-912.
6. 6 Von dem Borne PAK, Meijers JCM, Bouma BN: Feedback activation of factor XI by thrombin results in additional formation of thrombin that protects fibrin clots from fibrinolysis. Blood 1995, 86:3035-3042.
7. 7 Baglia FA, Jameson BA, Walsh PN: Localization of the high molecular weight kininogen binding site in the heavy chain of human factor XI to amino acids phenylalanine 56 through serine 86. J Biol Chem 1990, 265:4149-4154.
8. 8 Baglia FA, Walsh PN: A binding site for thrombin in the apple 1 domain of factor XI. J Biol Chem 1996, 271:3652-3658.
9. 9 Baglia FA, Jameson BA, Walsh PN: Identification and chemical synthesis of a substrate-binding site for factor IX on coagulation factor XIa. J Biol Chem 1991, 266: 24190-24197.
10. 10 Sun MF, Zhao MM, Gailani D: Identification of amino acids in the factor XI apple 3* domain required for activation of factor IX. J Biol Chem 1999, 274:36373-36378. Using recombinant chimeric factor XI in which the individual apple domains were replaced by the corresponding domain from plasma prekallikrein, it is shown that the apple 3 domain is required for the interaction with factor IX. These data are in contrast to those described in [9], where the A2 domain was reported to be important for the interaction with factor IX. The descripancy might be explained by the use of synthetic peptides to block the interaction of factor XI with factor IX in stead of exchanging entire domains of factor XI.
11. 11 Ho DH, Badellino K, Baglia FA, et al.: A binding site for heparin in the apple 3 domain of factor XI. J Biol Chem 1998, 273:16382-16390.
12. 12 Zhao MM, Abdel-Razek T, Sun MF, et al.: Characterization of a heparin binding site in the heavy chain of factor XI. J Biol Chem 1998, 273:31153-31159.
13. 13 Ho DH, Baglia FA, Walsh PN: Factor XI binding to activated platelets is mediated by residues R 250, K 255, F 260 and Q 263 within the apple 3 domain. Biochemistry 2000, 39:316-323. This is an interesting study in which the platelet binding site on factor XI is localized in the C-terminal amino acid sequence of the apple 3 domain (Threonine 249-Valine 271)
14. 14 Baglia FA, Walsh PN: Prothrombin is a cofactor for the binding of factor XI to the platelet surface and for platelet-mediated factor XI activation by thrombin. Biochemistry 1998, 37:2271-2281.
15. 15 Meijers JCM, Mulvihill ER, Davie EW, et al.: Apple 4 in human blood coagulation factor XI mediates dimer formation. Biochemistry 1992, 31:4680-4684.
16. 16 Meijers JCM, Davie EW, Chung DW: Expression of human blood coagulation factor XI: characterization of the defect in factor XI type III deficiency. Blood 1992, 79:1435-1440.
17. 17 Asakai R, Chung DW, Ratnoff OD, et al.: Factor XI (plasma thromboplastin antecedent) deficiency in Askenazi Jews is a bleeding disorder that can result from three types of point mutations. Proc Natl Acad Sci U S A 1989, 86:7667-7671.
18. 18 Peretz H, Mulai A, Usher S, et al.: The two common mutations causing factor XI deficiency in Jews stem from distinct founders: one of ancient Middle Eastern origin and another of more recent European origin. Blood 1997, 90:2654-2659.
19. 19 Goldstein DB, Reich DE, Bradman N, et al: Age estimates of two common mutations causing factor XI deficiency: recent genetic drift is not necessary for elevated disease incidence among Ashkenazi Jews. Am J Human Genet 1999, 64: 1071-1075. The type II and type III mutations at the factor XI locus, which cause factor XI deficiency, have high frequencies in Jewish populations. The type III mutation is largely restricted to Ashkenazi Jews, but the type II mutation is observed at high frequency in both Ashkenzi and Iraqi Jews. In this interesting article the ages of the type II and type III mutations are reported. The type III mutation is shown to be of recent origin whereas the type II mutation appeared within the ancestral Jewish population before the separation of the Iraqi and Askenazi communities.
20. 20 Martincic D, Zimmerman SA, Ware RE, et al.: Identification of mutations and polymorphisms in the factor XI genes of an African American family by dideoxyfingerprinting. Blood 1998, 92:3309-3317.
21. 21 Mitchell M, Cutler J, Thompson S, et al.: Heterozygous factor XI deficiency associated with three novel mutations. Br J Haematol 1999, 107:763-765.
22. 22 Alhaq A, Mitchell M, Sethi M, et al.: Identification of a novel mutation in non-Jewish factor XI deficient kindred. Br J Haemat 1999, 104:44-49.
23. 23 Gailani D, Broze GJ: Factor XII-independent activation of factor XI in plasma: effects of sulfatides on tissue factor-induced coagulation. Blood 1993, 82:813-819.
24. 24 Oliver JA, Monroe DM, Roberts HR, et al.: Thrombin activates factor XI on activated platelets in the absence of factor XII. Arterioscler Thromb Vasc Biol 1999, 19:170-77. This interesting article describes that factor XI can be activated by thrombin on the surface of platelets independent of factor XII. Although only small amounts of factor XI are activated, the coagulation system amplifies this signal into the generation of significant amounts of thrombin. Interestingly, the authors also demonstrate the activation of factor XI by factor Xa on the platelet surface.
25. 25 Cawthern KM, van't Veer C, Lock JB, et al.: Blood coagulation in Hemophilia A and Hemophilia C. Blood 1998, 91:4581-4592.
26. 26 Minnema MC, Pajkrt D, Wuillemin WA, et al.: Activation of clotting factor XI without detectable contact activation in experimental human endotoxemia. Blood 1998, 92:3294-3301.
27. 27 Von dem Borne PAK, Mosnier LO, Tans G, et al.: Factor XI activation by meizothrombin: stimulation by phospholipid vesicles containing both phosphatidylserine and phosphatidylethanolamine. Thromb Haemost 1997, 78:838-839.
28. 28 Røjkjær R, Hasan AAK, Schmaier AH: A novel mechanism for factor XI activation on endothelial cells independent of autoactivation. α-thrombin or factor XIIa. Blood 1998, 92(Suppl 1):40.
29. 29 Von dem Borne PAK, Bajzar L, Meijers JCM, et al.: Thrombin-mediated activation of factor XI results in a thrombin-activatable fibrinolysis inhibitor dependent inhibition of fibrinolysis. J Clin Invest 1997, 99:2323-2327.
30. 30 Bajzar L, Manuel R. Nesheim ME: Purification and characterization of TAFI, a thrombin-activable fibrinolysis inhibitor. J Biol Chem 1995, 270:14477-14484.
31. 31 Tan AK, Eaton DL: Activation and characterization of procarboxypeptidase B from human plasma. Biochemistry 1995, 34:5811-5816.
32. 32 Redlitz A, Tan AK, Eaton DL, et al.: Plasma carboxypeptidases as regulators of the plasminogen system. J Clin Invest 1995, 96:2534-2538.
33. 33 Wang W, Hendriks DF, Scharpé SS: Carboxypeptidase U, a plasma carboxypeptidase with high affinity for plasminogen. J Biol Chem 1994, 269:15937-15944.
34. 34 Mosnier LO, von dem Borne PAK, Meijers JCM, et al.: Plasma TAFI levels influence the clot lysis time in healthy individuals in the presence of an intact intrinsic pathway of coagulation. Thromb Haemost 1998, 80:829-835.
35. 35 Minnema MC, Friederich PW, Levi M, et al.: Enhancement of rabbit jugular vein thrombolysis by neutralization of factor XI: in vivo evidence for a role of factor XI as an anti-fibrinolytic factor. J Clin Invest 1998, 101:10-14.
36. 36 Von dem Borne PAK, Meijers JCM, Bouma BN: Effect of heparin on the activation of factor XI by fibrin bound thrombin. Thromb Haemost 1996, 76:347-353.
37. 37 Sakharov DV, Plow EF, Rijken DC: On the mechanism of the antifibrinolytic activity of plasma carboxypeptidase B. J Biol Chem 1997, 272:14477-14482.
38. 38 Biemond BJ, Friederich PW, Levi M, et al.: Comparison of sustained antithrombotic effects of inhibitors of thrombin and factor Xa in experimental thrombosis. Circulation 1996, 93:153-160.
39. 39 Bajzar L, Morser J, Nesheim ME: TAFI, or plasma procarboxypeptidase B, couples the coagulation and fibrinolytic cascades through the thrombin-thrombomodulin complex. J Biol Chem 1996, 271:16603-16608.
40. 40 Broze GJ, Higuchi DA: Coagulation-dependent inhibition of fibrinolysis: role of carboxypeptidase-U and the premature lysis of clots from hemophilic plasma. Blood 1996, 88:3815-3823.
41. 41 Ichinose A: The physiology and biochemistry of factor XIII. In Hemostasis and Thrombosis. Edited by Bloom AL, Forbes CD, Thomas DP, et al. Edinburgh: Churchill Livingstone; 1994:531-546.
42. 42 Lenich C, Pannell R, Gurewich V: Assembly and activation of the intrinsic fibrinolytic pathway on the surface of human endothelial cells in culture. Thromb Haemost 1995, 74:698-703.
43. 43 Gurewich V, Pannell R: Inactivation of single-chain urokinase (pro-urokinase) by thrombin and thrombin-like enzymes: relevance of the findings to the interpretation of fibrin binding experiments. Blood 1987, 69:769-772.
44. 44 Lijnen HR, van Hoef B, Collen D: Activation with plasmin of two-chain urokinase-type plasminogen activator derived from single-chain urokinase-type plasminogen activator by treatment with thrombin. Eur J Biochem 1987, 169:359-364.
45. 45 Braat EAM, Los P, Rijken D: The inactivation of single-chain urokinase-type plasminogen activator by thrombin in a plasma milieu: effect of thrombomodulin. Blood Coag Fibrinol 1998, 9:419-427.
46. 46 Braat EAM, Rijken DC: The inactivation of single-chain urokinase type-plasminogen activator by thrombin may provide an additional explanation for the antifibrinolytic effect of factor XI [letter]. Thromb Haemost 1999, 81:657. In this letter to the editor, it is shown that the factor XI dependent thrombin generation that results in a downregulation of fibrinolysis in plasma is not only mediated by TAFI as suggested in ref 29 but probably also by sc-uPA. The method used in [29] was insensitive for scu-PA because high concentrations of tPA were added to the reaction mixture.
47. 47 Bouma BN, Mosnier LO, Meijers JCM, et al.: Factor XI dependent and independent activation of thrombin activatable fibrinolysis inhibitor (TAFI) in plasma associated with clot formation. Thromb hemost 1999, 82:1703-1708. In this article, it is shown that the activation of TAFI in plasma can also take place via the extrinsic pathway of coagulation. Interestingly, there is a large variation in the contribution of this pathway to the activation of TAFI in normal individuals.
48. 48 Meijers JCM, Middeldorp S, Tekelenburg W, et al.: Inreased fibrinolytic activity during use of oral contraceptives is counteracted by an enhanced factor XI-independent downregulation of fibrinolysis: a randomized crossover study of two-low dose oral contraceptives. Thromb Haemost 2000, 84:9-14.
49. 49 Bouma BN, von dem Borne PAK, Meijers JCM: Factor XI and protection of the fibrin clot against lysis - a role for the intrinsic pathway of coagulation in fibrinolysis. Thromb Haemost 1998, 80:24-27.
50. 50 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 1997, 74:5260-5264.
51. 51 Marlar RA, Kleiss AJ, Griffin JH: An alternative extrinsic pathway of human blood coagulation. Blood 1982, 60:1353-1358.
52. 52 Broze GJ: The role of tissue factor pathway inhibitor in a revised coagulation cascade. Semin Haematol 1992, 29:159-169.
53. 53 Rand MD, Lock JB, van't Veer C, et al.: Blood clotting in minimally altered whole blood. Blood 1996, 88:3432-3445.
54. 54 Hu CJ, Baglia FA, Mills DCB, et al.: Tissue-specific expression of functional platelet factor XI is independent of plasma factor XI expression. Blood 1998, 91:3800-3807.
55. 55 Hsu TC, Shore SK, Seshsmma T, et al.: Molecular cloning of platelet factor XI, an alternative splicing product of the plasma factor XI gene. J Biol Chem 1998, 273:13787-13793.
56. 56 Martincic D, Kravtsov V, Gailani D: Factor XI messenger RNA in human platelets. Blood 1999, 94:3397-3404. The results described in this article contrast those described in ref 55. Normal platelets, bone marrow and megakaryocyte cell lines contained factor XI mRNA that is identical to the mRNA found in the liver whereas in ref 55 an alternatively spliced factor XI mRNA lacking the fifth exon is reported to be present in platelets. The discrepancy between these studies remains unexplained.
57. th percentile of the distribution of factor XI values in control subjects. The mechanism by which high levels of factor XI cause thrombosis is postulated to be via sustained thrombin generation which leads to protection of fibrin for fibrinolysis.
58. 58 Klement P, Liao P, Bajzar L: A novel approach to arterial thrombolysis. Blood 1999, 94:2735-2743. This is an interesting study. Using a rabbit arterial thrombolysis model it is demonstrated that inhibitors of TAFI improve thrombolytic therapy. A similar mechanism is expected to take place when inhibitors of factor XI will be used, because the generation of thrombin needed for the activation of TAFI will be decreased. The advantage of the inhibition of factor XI and TAFI is that the generation of thrombin via the extrinsic system can still provide a hemostatic plug. We have to keep in mind that TAFI is a carboypeptidase that might have other functions outside of the coagulation system and it is not known what the effect of TAFI inhibition is.