Molecular mechanisms affecting fibrin structure and stability

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 3, 2011, Pages 494-499

  Lord, Susan T ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

fibrin; fibrinolysis; fibrinolytic agents; molecular mechanism; venous thrombosis

Indexed keywords

BLOOD CLOTTING FACTOR 13; BLOOD CLOTTING FACTOR 13A; FIBRIN; FIBRINOGEN; MONOMER; PLASMIN; PLASMINOGEN; TISSUE PLASMINOGEN ACTIVATOR;

ARTICLE; BINDING SITE; BLOOD VESSEL INJURY; CRYSTAL STRUCTURE; ENZYME DEGRADATION; FIBER; FIBRIN CLOT; FIBRINOLYSIS; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE; VEIN THROMBOSIS;

ANIMALS; BLOOD COAGULATION; FIBRIN; FIBRINOGEN; FIBRINOLYSIS; FIBRINOLYTIC AGENTS; HUMANS; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; VENOUS THROMBOSIS;

EID: 79952178145     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.110.213389     Document Type: Article

References (95)

1. Kaptoge S, White IR, Thompson SG, Wood AM, Lewington S, Lowe GD, Danesh J. Associations of plasma fibrinogen levels with established cardiovascular disease risk factors, inflammatory markers, and other characteristics: individual participant meta-analysis of 154,211 adults in 31 prospective studies: the fibrinogen studies collaboration. Am J Epidemiol. 2007;166:867-879. (Pubitemid 47511690)
2. Fatah K, Silveira A, Tornvall P, Karpe F, Blomback M, Hamsten A. Proneness to formation of tight and rigid fibrin gel structures in men with myocardial infarction at a young age. Thromb Haemost. 1996;76: 535-540. (Pubitemid 26372007)
3. Collet JP, Allali Y, Lesty C, Tanguy ML, Silvain J, Ankri A, Blanchet B, Dumaine R, Gianetti J, Payot L, Weisel JW, Montalescot G. Altered fibrin architecture is associated with hypofibrinolysis and premature coronary atherothrombosis. Arterioscler Thromb Vasc Biol. 2006;26: 2567-2573. (Pubitemid 44607482)
4. Mills JD, Ariens RA, Mansfield MW, Grant PJ. Altered fibrin clot structure in the healthy relatives of patients with premature coronary artery disease. Circulation. 2002;106:1938-1942. (Pubitemid 35176298)
5. Undas A, Zawilska K, Ciesla-Dul M, Lehmann-Kopydlowska A, Skubiszak A, Ciepluch K, Tracz W. Altered fibrin clot structure/function in patients with idiopathic venous thromboembolism and in their relatives. Blood. 2009;114:4272-4278.
6. Weisel JW, Stauffacher CV, Bullitt E, Cohen C. A model for fibrinogen: domains and sequence. Science. 1985;230:1388-1391. (Pubitemid 16105171)
7. Kollman JM, Pandi L, Sawaya MR, Riley M, Doolittle RF. Crystal structure of human fibrinogen. Biochemistry. 2009;48:3877-3886.
8. Doolittle RF. X-ray crystallographic studies on fibrinogen and fibrin. J Thromb Haemost. 2003;1:1559-1565.
9. Kostelansky MS, Betts L, Gorkun OV, Lord ST. 2.8 A crystal structures of recombinant fibrinogen fragment D with and without two peptide ligands: GHRP binding to the "b" site disrupts its nearby calcium-binding site. Biochemistry. 2002;41:12124-12132.
10. Pechik I, Madrazo J, Mosesson MW, Hernandez I, Gilliland GL, Medved L. Crystal structure of the complex between thrombin and the central "E" region of fibrin. Proc Natl Acad Sci U S A. 2004;101:2718-2723. (Pubitemid 38327677)
11. Burton RA, Tsurupa G, Hantgan RR, Tjandra N, Medved L. NMR solution structure, stability, and interaction of the recombinant bovine fibrinogen -C-domain fragment. Biochemistry. 2007;46:8550-8560. (Pubitemid 47106106)
12. Gorkun OV, Veklich YI, Medved LV, Henschen AH, Weisel JW. Role of the αC domains of fibrin in clot formation. Biochemistry. 1994;33: 6986-6997.
13. Lord ST. Fibrinogen and fibrin: scaffold proteins in hemostasis. Curr Opin Hematol. 2007;14:236-241. (Pubitemid 46597609)
14. Weisel JW, Nagaswami C. Computer modeling of fibrin polymerization kinetics correlated with electron microscope and turbidity observations: clot structure and assembly are kinetically controlled. Biophys J. 1992; 63:111-128.
15. Janus TJ, Lewis SD, Lorand L, Shafer JA. Promotion of thrombincatalyzed activation of factor XIII by fibrinogen. Biochemistry. 1983;22: 6269-6272. (Pubitemid 14175823)
16. Spraggon G, Everse SJ, Doolittle RF. Crystal structures of fragment D from human fibrinogen and its crosslinked counterpart from fibrin. Nature. 1997;389:455-462. (Pubitemid 27435313)
17. Bowley SR, Merenbloom BK, Okumura N, Betts L, Heroux A, Gorkun OV, Lord ST. Polymerization-defective fibrinogen variant γD364A binds knob "A" peptide mimic. Biochemistry. 2008;47:8607-8613.
18. Kudryk B, Blomback B, Blomback M. Fibrinogen Detroit: an abnormal fibrinogen with non-functinal NH2-terminal polymerization domain. Thrombosis Research. 1976;9:25-36.
19. Blomback B, Hessel B, Hogg D, Therkildsen L. A two-step fibrinogen-fibrin transition in blood coagulation. Nature. 1978;275:501-505. (Pubitemid 9020557)
20. Budzynski AZ, Olexa SA, Pandya BV. Fibrin polymerization sites in fibrinogen and fibrin fragments. Ann N Y Acad Sci. 1983;408:301-314. (Pubitemid 13072045)
21. Laudano AP, Doolittle RF. Studies on synthetic peptides that bind to fibrinogen and prevent fibrin polymerization: structural requirements, number of binding sites, and species differences. Biochemistry. 1980;19: 1013-1019. (Pubitemid 10112241)
22. Moen JL, Gorkun OV, Weisel JW, Lord ST. Recombinant BβArg14His fibrinogen implies participation of N-terminus of Bβ chain in desA fibrin polymerization. Blood. 2003;102:2466-2471. (Pubitemid 37193584)
23. Okumura N, Terasawa F, Haneishi A, Fujihara N, Hirota-Kawadobora M, Yamauchi K, Ota H, Lord ST. B:b interactions are essential for polymerization of variant fibrinogens with impaired holes 'a'. J Thromb Haemost. 2007;5:2352-2359. (Pubitemid 350154343)
24. Cierniewski CS, Budzynski AZ. Involvement of the α chain in fibrin clot formation: effect of monoclonal antibodies. Biochemistry. 1992;31: 4248-4253.
25. Collet JP, Moen JL, Veklich YI, Gorkun OV, Lord ST, Montalescot G, Weisel JW. The αC domains of fibrinogen affect the structure of the fibrin clot, its physical properties, and its susceptibility to fibrinolysis. Blood. 2005;106:3824-3830. (Pubitemid 41739019)
26. Yang Z, Mochalkin I, Doolittle RF. A model of fibrin formation based on crystal structures of fibrinogen and fibrin fragments complexed with synthetic peptides. Proc Natl Acad Sci U S A. 2000;97:14156-14161. (Pubitemid 32016546)
27. Doolittle RF. Structural basis of the fibrinogen-fibrin transformation: contributions from X-ray crystallography. Blood Rev. 2003;17:33-41. (Pubitemid 36176209)
28. Wolberg AS, Monroe DM, Roberts HR, Hoffman M. Elevated prothrombin results in clots with an altered fiber structure: a possible mechanism of the increased thrombotic risk. Blood. 2003;101: 3008-3013. (Pubitemid 36857988)
29. He S, Blomback M, Bark N, Johnsson H, Wallen NH. The direct thrombin inhibitors (argatroban, bivalirudin and lepirudin) and the indirect Xa-inhibitor (danaparoid) increase fibrin network porosity and thus facilitate fibrinolysis. Thromb Haemost. 2010;103:1076-1084.
30. Weisel JW, Litvinov RI. The biochemical and physical process of fibrinolysis and effects of clot structure and stability on the lysis rate. Cardiovasc Hematol Agents Med Chem. 2008;6:161-180.
31. Campbell RA, Overmyer KA, Selzman CH, Sheridan BC, Wolberg AS. Contributions of extravascular and intravascular cells to fibrin network formation, structure, and stability. Blood. 2009;114:4886-4896.
32. Van Hylckama Vlieg A, Komanasin N, Ariens RA, Poort SR, Grant PJ, Bertina RM, Rosendaal FR. Factor XIII Val34Leu polymorphism, factor XIII antigen levels and activity and the risk of deep venous thrombosis. Br J Haematol. 2002;119:169-175. (Pubitemid 35176517)
33. Ariens RA, Philippou H, Nagaswami C, Weisel JW, Lane DA, Grant PJ. The factor XIII V34L polymorphism accelerates thrombin activation of factor XIII and affects cross-linked fibrin structure. Blood. 2000;96: 988-995. (Pubitemid 30616865)
34. Trumbo TA, Maurer MC. Examining thrombin hydrolysis of the factor XIII activation peptide segment leads to a proposal for explaining the cardioprotective effects observed with the factor XIII V34L mutation. J Biol Chem. 2000;275:20627-20631. (Pubitemid 30457648)
35. Vossen CY, Rosendaal FR. The protective effect of the factor XIII Val34Leu mutation on the risk of deep venous thrombosis is dependent on the fibrinogen level. J Thromb Haemost. 2005;3:1102-1103. (Pubitemid 41632850)
36. Lim BC, Ariens RA, Carter AM, Weisel JW, Grant PJ. Genetic regulation of fibrin structure and function: complex gene-environment interactions may modulate vascular risk. Lancet. 2003;361:1424-1431. (Pubitemid 36515043)
37. Boekholdt SM, Sandhu MS, Wareham NJ, Luben R, Reitsma PH, Khaw KT. Fibrinogen plasma levels modify the association between the factor XIII Val34Leu variant and risk of coronary artery disease: the EPICNorfolk prospective population study. J Thromb Haemost. 2006;4: 2204-2209. (Pubitemid 44400299)
38. Gonzalez-Conejero R, Fernandez-Cadenas I, Iniesta JA, Marti-Fabregas J, Obach V, Alvarez-Sabin J, Vicente V, Corral J, Montaner J. Role of fibrinogen levels and factor XIII V34L polymorphism in thrombolytic therapy in stroke patients. Stroke. 2006;37:2288-2293. (Pubitemid 44337171)
39. Standeven KF, Uitte de Willige S, Carter AM, Grant PJ. Heritability of clot formation. Semin Thromb Hemost. 2009;35:458-467.
40. Standeven KF, Grant PJ, Carter AM, Scheiner T, Weisel JW, Ariens RA. Functional analysis of the fibrinogen Aα Thr312Ala polymorphism: effects on fibrin structure and function. Circulation. 2003;107: 2326-2330. (Pubitemid 36578503)
41. Ajjan R, Lim BC, Standeven KF, Harrand R, Dolling S, Phoenix F, Greaves R, Abou-Saleh RH, Connell S, Smith DA, Weisel JW, Grant PJ, Ariens RA. Common variation in the C-terminal region of the fibrinogen β-chain: effects on fibrin structure, fibrinolysis and clot rigidity. Blood. 2008;111:643-650.
42. Uitte de Willige S, Standeven KF, Philippou H, Ariens RA. The pleiotropic role of the fibrinogen β-chain in hemostasis. Blood. 2009;114: 3994-4001.
43. Cooper AV, Standeven KF, Ariens RA. Fibrinogen β-chain splice variant γ′ alters fibrin formation and structure. Blood. 2003;102:535-540. (Pubitemid 36841972)
44. Gersh KC, Nagaswami C, Weisel JW, Lord ST. The presence of β-chain impairs fibrin polymerization. Thromb Res. 2009;124:356-363.
45. Weisel JW. Structure of fibrin: impact on clot stability. J Thromb Haemost. 2007;5(suppl 1):116-124. (Pubitemid 46958824)
46. Rijken DC, Lijnen HR. New insights into the molecular mechanisms of the fibrinolytic system. J Thromb Haemost. 2009;7:4-13.
47. Falvo MR, Gorkun OV, Lord ST. The molecular origins of the mechanical properties of fibrin. Biophys Chem. 2010;152:15-20.
48. Lim BB, Lee EH, Sotomayor M, Schulten K. Molecular basis of fibrin clot elasticity. Structure. 2008;16:449-459.
49. Brown AE, Litvinov RI, Discher DE, Weisel JW. Forced unfolding of coiled-coils in fibrinogen by single-molecule AFM. Biophys J. 2007;92: L39-L41. (Pubitemid 46393457)
50. Brown AE, Litvinov RI, Discher DE, Purohit PK, Weisel JW. Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water. Science. 2009;325:741-744.
51. Averett LE, Geer CB, Fuierer RR, Akhremitchev BB, Gorkun OV, Schoenfisch MH. Complexity of "A-a" knob-hole fibrin interaction revealed by atomic force spectroscopy. Langmuir. 2008;24:4979-4988. (Pubitemid 351728051)
52. Falvo MR, Millard D, O'Brien ET III, Superfine R, Lord ST. Length of tandem repeats in fibrin's αC region correlates with fiber extensibility. J Thromb Haemost. 2008;6:1991-1993.
53. Weisel JW. The mechanical properties of fibrin for basic scientists and clinicians. Biophys Chem. 2004;112:267-276. (Pubitemid 39574429)
54. Liu W, Carlisle CR, Sparks EA, Guthold M. The mechanical properties of single fibrin fibers. J Thromb Haemost. 2010;8:1030-1036.
55. Houser JR, Hudson NE, Ping L, O'Brien ET III, Superfine R, Lord ST, Falvo MR. Evidence that αC region is origin of low modulus, high extensibility, and strain stiffening in fibrin fibers. Biophys J. 2010;99: 3038-3047.
56. Doolittle RF. Searching for differences between fibrinogen and fibrin that affect the initiation of fibrinolysis. Cardiovasc Hematol Agents Med Chem. 2008;6:181-189.
57. Nieuwenhuizen W, Vermond A, Voskuilen M, Traas DW, Verheijen JH. Identification of a site in fibrin(ogen) which is involved in the acceleration of plasminogen activation by tissue-type plasminogen activator. Biochim Biophys Acta. 1983;748:86-92. (Pubitemid 14244748)
58. Schielen WJ, Adams HP, van Leuven K, Voskuilen M, Tesser GI, Nieuwenhuizen W. The sequence γ-(312-324) is a fibrin-specific epitope. Blood. 1991;77:2169-2173.
59. Medved L, Nieuwenhuizen W. Molecular mechanisms of initiation of fibrinolysis by fibrin. Thromb Haemost. 2003;89:409-419. (Pubitemid 36329229)
60. Yakovlev S, Makogonenko E, Kurochkina N, Nieuwenhuizen W, Ingham K, Medved L. Conversion of fibrinogen to fibrin: mechanism of exposure of tPA-and plasminogen-binding sites. Biochemistry. 2000;39: 15730-15741. (Pubitemid 32038234)
61. Wilhelm SE, Lounes KC, Lord ST. Investigation of residues in the fibrin(ogen) γ chain involved in tissue plasminogen activator binding and plasminogen activation. Blood Coagul Fibrinolysis. 2004;15:451-461. (Pubitemid 39180229)
62. Ajjan RA, Standeven KF, Khanbhai M, Phoenix F, Gersh KC, Weisel JW, Kearney MT, Ariens RA, Grant PJ. Effects of aspirin on clot structure and fibrinolysis using a novel in vitro cellular system. Arterioscler Thromb Vasc Biol. 2009;29:712-717.
63. He S, Bark N, Wang H, Svensson J, Blomback M. Effects of acetylsalicylic acid on increase of fibrin network porosity and the consequent upregulation of fibrinolysis. J Cardiovasc Pharmacol. 2009; 53:24-29.
64. Longstaff C, Thelwell C, Williams SC, Silva MM, Szabo L, Kolev K. The interplay between tissue plasminogen activator domains and fibrin structures in the regulation of fibrinolysis: kinetic and microscopic studies. Blood. 2010. [Epub ahead of print].
65. Pandi L, Kollman JM, Lopez-Lira F, Burrows JM, Riley M, Doolittle RF. Two families of synthetic peptides that enhance fibrin turbidity and delay fibrinolysis by different mechanisms. Biochemistry. 2009;48:7201-7208.
66. Bowley SR, Lord ST. Fibrinogen variant BβD432A has normal polymerization but does not bind knob "B." Blood. 2009;113:4425-4430.
67. Holliday BA, Bowley SR, Lord ST. Plasmin-catalyzed lysis is enhanced in fibrin variants with weakened hole 'b'. J Thromb Haemost. 2009;7: Abstract OC-MO-117.
68. Medved L, Weisel JW. Recommendations for nomenclature on fibrinogen and fibrin. J Thromb Haemost. 2009;7:355-359.
69. Uitte de Willige S, Standeven KF, Philippou H, Ariens RA. The pleiotropic role of the fibrinogen β-chain in hemostasis. Blood. 2009;114: 3994-4001.
70. Cooper AV, Standeven KF, Ariens RA. Fibrinogen β-chain splice variant γ′ alters fibrin formation and structure. Blood. 2003;102:535-540. (Pubitemid 36841972)
71. Gersh KC, Nagaswami C, Weisel JW, Lord ST. The presence of β-chain impairs fibrin polymerization. Thromb Res. 2009;124:356-363.
72. Weisel JW. Structure of fibrin: impact on clot stability. J Thromb Haemost. 2007;5(suppl 1):116-124. (Pubitemid 46958824)
73. Rijken DC, Lijnen HR. New insights into the molecular mechanisms of the fibrinolytic system. J Thromb Haemost. 2009;7:4-13.
74. Falvo MR, Gorkun OV, Lord ST. The molecular origins of the mechanical properties of fibrin. Biophys Chem. 2010;152:15-20.
75. Lim BB, Lee EH, Sotomayor M, Schulten K. Molecular basis of fibrin clot elasticity. Structure. 2008;16:449-459.
76. Brown AE, Litvinov RI, Discher DE, Weisel JW. Forced unfolding of coiled-coils in fibrinogen by single-molecule AFM. Biophys J. 2007;92: L39-L41. (Pubitemid 46393457)
77. Brown AE, Litvinov RI, Discher DE, Purohit PK, Weisel JW. Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water. Science. 2009;325:741-744.
78. Averett LE, Geer CB, Fuierer RR, Akhremitchev BB, Gorkun OV, Schoenfisch MH. Complexity of "A-a" knob-hole fibrin interaction revealed by atomic force spectroscopy. Langmuir. 2008;24:4979-4988. (Pubitemid 351728051)
79. Falvo MR, Millard D, O'Brien ET III, Superfine R, Lord ST. Length of tandem repeats in fibrin's αC region correlates with fiber extensibility. J Thromb Haemost. 2008;6:1991-1993.
80. Weisel JW. The mechanical properties of fibrin for basic scientists and clinicians. Biophys Chem. 2004;112:267-276. (Pubitemid 39574429)
81. Liu W, Carlisle CR, Sparks EA, Guthold M. The mechanical properties of single fibrin fibers. J Thromb Haemost. 2010;8:1030-1036.
82. Houser JR, Hudson NE, Ping L, O'Brien ET III, Superfine R, Lord ST, Falvo MR. Evidence that αC region is origin of low modulus, high extensibility, and strain stiffening in fibrin fibers. Biophys J. 2010;99: 3038-3047.
83. Doolittle RF. Searching for differences between fibrinogen and fibrin that affect the initiation of fibrinolysis. Cardiovasc Hematol Agents Med Chem. 2008;6:181-189.
84. Nieuwenhuizen W, Vermond A, Voskuilen M, Traas DW, Verheijen JH. Identification of a site in fibrin(ogen) which is involved in the acceleration of plasminogen activation by tissue-type plasminogen activator. Biochim Biophys Acta. 1983;748:86-92. (Pubitemid 14244748)
85. Schielen WJ, Adams HP, van Leuven K, Voskuilen M, Tesser GI, Nieuwenhuizen W. The sequence γ-(312-324) is a fibrin-specific epitope. Blood. 1991;77:2169-2173.
86. Medved L, Nieuwenhuizen W. Molecular mechanisms of initiation of fibrinolysis by fibrin. Thromb Haemost. 2003;89:409-419. (Pubitemid 36329229)
87. Yakovlev S, Makogonenko E, Kurochkina N, Nieuwenhuizen W, Ingham K, Medved L. Conversion of fibrinogen to fibrin: mechanism of exposure of tPA-and plasminogen-binding sites. Biochemistry. 2000;39: 15730-15741. (Pubitemid 32038234)
88. Wilhelm SE, Lounes KC, Lord ST. Investigation of residues in the fibrin(ogen) γ chain involved in tissue plasminogen activator binding and plasminogen activation. Blood Coagul Fibrinolysis. 2004;15:451-461. (Pubitemid 39180229)
89. Ajjan RA, Standeven KF, Khanbhai M, Phoenix F, Gersh KC, Weisel JW, Kearney MT, Ariens RA, Grant PJ. Effects of aspirin on clot structure and fibrinolysis using a novel in vitro cellular system. Arterioscler Thromb Vasc Biol. 2009;29:712-717.
90. He S, Bark N, Wang H, Svensson J, Blomback M. Effects of acetylsalicylic acid on increase of fibrin network porosity and the consequent upregulation of fibrinolysis. J Cardiovasc Pharmacol. 2009; 53:24-29.
91. Longstaff C, Thelwell C, Williams SC, Silva MM, Szabo L, Kolev K. The interplay between tissue plasminogen activator domains and fibrin structures in the regulation of fibrinolysis: kinetic and microscopic studies. Blood. 2010. [Epub ahead of print].
92. Pandi L, Kollman JM, Lopez-Lira F, Burrows JM, Riley M, Doolittle RF. Two families of synthetic peptides that enhance fibrin turbidity and delay fibrinolysis by different mechanisms. Biochemistry. 2009;48:7201-7208.
93. Bowley SR, Lord ST. Fibrinogen variant BβD432A has normal polymerization but does not bind knob "B." Blood. 2009;113:4425-4430.
94. Holliday BA, Bowley SR, Lord ST. Plasmin-catalyzed lysis is enhanced in fibrin variants with weakened hole 'b'. J Thromb Haemost. 2009;7: Abstract OC-MO-117.
95. Medved L, Weisel JW. Recommendations for nomenclature on fibrinogen and fibrin. J Thromb Haemost. 2009;7:355-359.