Model thrombi formed under flow reveal the role of factor XIII-mediated cross-linking in resistance to fibrinolysis

Journal of Thrombosis and Haemostasis

Volumn 8, Issue 9, 2010, Pages 2017-2024

  Mutch, N J ^a,b   Koikkalainen, J S ^a   Fraser, S R ^a   Duthie, K M ^a   Griffin, M ^c   Mitchell, J ^a   Watson, H G ^d   Booth, N A ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c ASTON UNIVERSITY   (United Kingdom)

^d ABERDEEN ROYAL INFIRMARY   (United Kingdom)

Author keywords

Factor XIII; Fibrinolysis; Flow; Stability; Thrombi.

Indexed keywords

BLOOD CLOTTING FACTOR 13; BLOOD CLOTTING FACTOR 13 CONCENTRATE; ENZYME INHIBITOR; FIBRIN; FIBRINOGEN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; TISSUE PLASMINOGEN ACTIVATOR;

ARTICLE; BLOOD CLOT; BLOOD CLOTTING FACTOR 13 DEFICIENCY; BLOOD FLOW; CASE REPORT; DIMERIZATION; DRUG EFFECT; DRUG EFFICACY; ENDOTHELIUM CELL; ENZYME REPLACEMENT; ENZYME SYNTHESIS; FIBRINOLYSIS; FLUORESCENCE IMAGING; HUMAN; IN VIVO STUDY; MODEL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; THROMBOGENESIS;

CROSS-LINKING REAGENTS; DIMERIZATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FACTOR XIII; FIBRINOLYSIS; FIBRONECTINS; GTP-BINDING PROTEINS; HUMANS; INHIBITORY CONCENTRATION 50; PLASMINOGEN ACTIVATORS; THROMBOSIS; TIME FACTORS; TRANSGLUTAMINASES;

EID: 77956485373     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2010.03963.x     Document Type: Article

References (53)

1. Anwar R, Miloszewski KJ. Factor XIII deficiency. Br J Haematol 1999, 107:468-84.
2. Koseki-Kuno S, Yamakawa M, Dickneite G, Ichinose A. Factor XIII A subunit-deficient mice developed severe uterine bleeding events and subsequent spontaneous miscarriages. Blood 2003, 102:4410-12.
3. Ichinose A. Physiopathology and regulation of factor XIII. Thromb Haemost 2001, 86:57-65.
4. Lorand L. Sol Sherry lecture in thrombosis: research on clot stabilization provides clues for improving thrombolytic therapies. Arterioscler Thromb Vasc Biol 2000, 20:2-9.
5. Naski MC, Lorand L, Shafer JA. Characterization of the kinetic pathway for fibrin promotion of alpha-thrombin-catalyzed activation of plasma factor XIII. Biochemistry 1991, 30:934-41.
6. Chen R, Doolittle RF. Cross-linking sites in human and bovine fibrin. Biochemistry 1971, 10:4487-91.
7. McKee PA, Mattock P, Hill RL. Subunit structure of human fibrinogen, soluble fibrin, and cross-linked insoluble fibrin. Proc Natl Acad Sci USA 1970, 66:738-44.
8. Siebenlist KR, Mosesson MW. Progressive cross-linking of fibrin gamma chains increases resistance to fibrinolysis. J Biol Chem 1994, 269:28414-19.
9. Greenberg CS, Birckbichler PJ, Rice RH. Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues. FASEB J 1991, 5:3071-7.
10. Murthy SN, Wilson J, Guy SL, Lorand L. Intramolecular crosslinking of monomeric fibrinogen by tissue transglutaminase. Proc Natl Acad Sci USA 1991, 88:10601-4.
11. 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, 69:536-42.
12. Ritchie H, Robbie LA, Kinghorn S, Exley R, Booth NA. Monocyte plasminogen activator inhibitor 2 (PAI-2) inhibits u-PA-mediated fibrin clot lysis and is cross-linked to fibrin. Thromb Haemost 1999, 81:96-103.
13. Valnickova Z, Enghild JJ. Human procarboxypeptidase U, or thrombin-activable fibrinolysis inhibitor, is a substrate for transglutaminases. Evidence for transglutaminase-catalyzed cross-linking to fibrin. J Biol Chem 1998, 273:27220-4.
14. Robbie LA, Booth NA, Croll AM, Bennett B. The roles of α2-antiplasmin and plasminogen activator inhibitor 1 (PAI-1) in the inhibition of clot lysis. Thromb Haemost 1993, 70:301-6.
15. Standeven KF, Carter AM, Grant PJ, Weisel JW, Chernysh I, Masova L, Lord ST, Ariens RA. Functional analysis of fibrin {gamma}-chain cross-linking by activated factor XIII: determination of a cross-linking pattern that maximizes clot stiffness. Blood 2007, 110:902-7.
16. Mosesson MW, Finlayson JS. The search for the structure of fibrinogen. Prog Hemost Thromb 1976, 3:61-107.
17. Folk JE, Finlayson JS. The epsilon-(gamma-glutamyl)lysine crosslink and the catalytic role of transglutaminases. Adv Protein Chem 1977, 31:1-133.
18. Rampling MW. Factor XIII cross-linking and the rate of fibrinolysis induced by streptokinase and urokinase. Thromb Res 1978, 12:287-95.
19. Lorand JB, Pilkington TR, Lorand L. Inhibitors of fibrin cross-linking: relevance for thrombolysis. Nature 1966, 210:1273-4.
20. Schwartz ML, Pizzo SV, Hill RL, McKee PA. Human factor XIII from plasma and platelets. Molecular weights, subunit structures, proteolytic activation, and cross-linking of fibrinogen and fibrin. J Biol Chem 1973, 248:1395-407.
21. Francis CW, Marder VJ. Increased resistance to plasmic degradation of fibrin with highly crosslinked alpha-polymer chains formed at high factor XIII concentrations. Blood 1988, 71:1361-5.
22. Collet JP, Moen JL, Veklich YI, Gorkun OV, Lord ST, Montalescot G, Weisel JW. The alphaC domains of fibrinogen affect the structure of the fibrin clot, its physical properties, and its susceptibility to fibrinolysis. Blood 2005, 106:3824-30.
23. Robbie LA, Young SP, Bennett B, Booth NA. Thrombi formed in a Chandler loop mimic human arterial thrombi in structure and PAI-1 content and distribution. Thromb Haemost 1997, 77:510-15.
24. Mutch NJ, Thomas L, Moore NR, Lisiak KM, Booth NA. TAFIa, PAI-1 and α2-antiplasmin: complementary roles in regulating lysis of thrombi and plasma clots. J Thromb Haemost 2007, 5:812-17.
25. Booth NA, Simpson AJ, Croll A, Bennett B, MacGregor IR. Plasminogen activator inhibitor (PAI-1) in plasma and platelets. Br J Haematol 1988, 70:327-33.
26. Anwar R, Gallivan L, Miloszewski KJ, Markham AF. Splicing and missense mutations in the human FXIIIA gene causing FXIII deficiency: effects of these mutations on FXIIIA RNA processing and protein structure. Br J Haematol 1998, 103:425-8.
27. Mutch NJ, Moore NR, Wang E, Booth NA. Thrombus lysis by uPA, scuPA and tPA is regulated by plasma TAFI. J Thromb Haemost 2003, 1:2000-7.
28. Mutch NJ, Moore NR, Mattsson C, Jonasson H, Green AR, Booth NA. The use of the Chandler loop to examine the interaction potential of NXY-059 on the thrombolytic properties of rtPA on human thrombi in vitro. Br J Pharmacol 2008, 153:124-31.
29. Freund KF, Doshi KP, Gaul SL, Claremon DA, Remy DC, Baldwin JJ, Pitzenberger SM, Stern AM. Transglutaminase inhibition by 2-[(2-oxopropyl)thio]imidazolium derivatives: mechanism of factor XIIIa inactivation. Biochemistry 1994, 33:10109-19.
30. Auld GC, Ritchie H, Robbie LA, Booth NA. Thrombin upregulates tissue transglutaminase in endothelial cells: a potential role for tissue transglutaminase in stability of atherosclerotic plaque. Arterioscler Thromb Vasc Biol 2001, 21:1689-94.
31. Verderio E, Nicholas B, Gross S, Griffin M. Regulated expression of tissue transglutaminase in Swiss 3T3 fibroblasts: effects on the processing of fibronectin, cell attachment, and cell death. Exp Cell Res 1998, 239:119-38.
32. Raut S, Merton RE, Rigsby P, Muszbek L, Seitz R, Ariens RA, Barrowcliffe TW, Ichinose A. A collaborative study to establish the 1st international standard for factor XIII plasma. J Thromb Haemost 2007, 5:1923-9.
33. Booth NA, Bennett B, Wijngaards G, Grieve JH. A new life-long hemorrhagic disorder due to excess plasminogen activator. Blood 1983, 61:267-75.
34. Moir E, Booth NA, Bennett B, Robbie LA. Polymorphonuclear leucocytes mediate endogenous thrombus lysis via a u-PA-dependent mechanism. Br J Haematol 2001, 113:72-80.
35. Murthy SN, Lorand L. Cross-linked A alpha.gamma chain hybrids serve as unique markers for fibrinogen polymerized by tissue transglutaminase. Proc Natl Acad Sci USA 1990, 87:9679-82.
36. Jansen JW, Haverkate F, Koopman J, Nieuwenhuis HK, Kluft C, Boschman TA. Influence of factor XIIIa activity on human whole blood clot lysis in vitro. Thromb Haemost 1987, 57:171-5.
37. Bagoly Z, Fazakas F, Komaromi I, Haramura G, Toth E, Muszbek L. Cleavage of factor XIII by human neutrophil elastase results in a novel active truncated form of factor XIII A subunit. Thromb Haemost 2008, 99:668-74.
38. Greenberg CS, Sane DC, Lai T-S. Factor XIII and fibrin stabilization. Hemostasis and Thrombosis 2006, 317-34. Colman RW, Marder VJ, Clowes AWGeorge JNGoldhaber SJ. eds, 5th edn, Philadelphia, Lippincott Williams Wilkins
39. Levy JH, Gill R, Nussmeier NA, Olsen PS, Andersen HF, Booth FV, Jespersen CM. Repletion of factor XIII following cardiopulmonary bypass using a recombinant A-subunit homodimer. A preliminary report. Thromb Haemost 2009, 102:765-71.
40. Korte WC, Szadkowski C, Gahler A, Gabi K, Kownacki E, Eder M, Degiacomi P, Zoller N, Devay J, Lange J, Schnider T. Factor XIII substitution in surgical cancer patients at high risk for intraoperative bleeding. Anesthesiology 2009, 110:239-45.
41. Mockros LF, Roberts WW, Lorand L. Viscoelastic properties of ligation-inhibited fibrin clots. Biophys Chem 1974, 2:164-9.
42. Ryan EA, Mockros LF, Weisel JW, Lorand L. Structural origins of fibrin clot rheology. Biophys J 1999, 77:2813-26.
43. Ryan EA, Mockros LF, Stern AM, Lorand L. Influence of a natural and a synthetic inhibitor of factor XIIIa on fibrin clot rheology. Biophys J 1999, 77:2827-36.
44. Mosesson MW. Cross-linked gamma-chains in fibrin fibrils bridge 'transversely' between strands: yes. J Thromb Haemost 2004, 2:388-93.
45. Booth NA, Bachmann F. Plasminogen-plasmin system. Hemostasis and Thrombosis 2006, 335-65. Colman RW, Marder VJClowes AWGeorge JNGoldhaber SJ. eds, 5th edn, Philadelphia, Lippincott Williams Wilkins
46. Falls LA, Farrell DH. Resistance of gammaA/gamma′ fibrin clots to fibrinolysis. J Biol Chem 1997, 272:14251-6.
47. Sakharov DV, Rijken DC. Superficial accumulation of plasminogen during plasma clot lysis. Circulation 1995, 92:1883-90.
48. Reed GL, Houng AK. The contribution of activated factor XIII to fibrinolytic resistance in experimental pulmonary embolism. Circulation 1999, 99:299-304.
49. Siebenlist KR, Mosesson MW. Evidence of intramolecular cross-linked A alpha.gamma chain heterodimers in plasma fibrinogen. Biochemistry 1996, 35:5817-21.
50. Lee KN, Jackson KW, Christiansen VJ, Lee CS, Chun JG, McKee PA. Why α2-antiplasmin must be converted to a derivative form for optimal function. J Thromb Haemost 2007, 5:2095-104.
51. Mosesson MW, Siebenlist KR, Hernandez I, Lee KN, Christiansen VJ, McKee PA. Evidence that α2-antiplasmin becomes covalently ligated to plasma fibrinogen in the circulation: a new role for plasma factor XIII in fibrinolysis regulation. J Thromb Haemost 2008, 6:1565-70.
52. Haroon ZA, Wannenburg T, Gupta M, Greenberg CS, Wallin R, Sane DC. Localization of tissue transglutaminase in human carotid and coronary artery atherosclerosis: implications for plaque stability and progression. Lab Invest 2001, 81:83-93.
53. Robinson BR, Houng AK, Reed GL. Catalytic life of activated factor XIII in thrombi. Implications for fibrinolytic resistance and thrombus aging. Circulation 2000, 102:1151-7.