Fibrinogen and fibrin polymerization: Appraisal of the binding events that accompany fibrin generation and fibrin clot assembly

Blood Coagulation and Fibrinolysis

Volumn 8, Issue 5, 1997, Pages 257-267

  Mosesson, M W ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Crosslinking; Endot helial cells; Factor XIII; Fibrin; Fibrinogen; Fibrinolysis; Platelets; Thrombin; TPA

Indexed keywords

BLOOD CLOTTING FACTOR 13; FIBRIN; FIBRINOGEN; FIBRINOPEPTIDE B; PLASMINOGEN; THROMBIN; TISSUE PLASMINOGEN ACTIVATOR;

BINDING SITE; ENDOTHELIUM CELL; FIBRIN CLOT; FIBRIN POLYMERIZATION; FIBRINOLYSIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN STRUCTURE; REVIEW; THROMBOCYTE;

EID: 0030803827     PISSN: 09575235     EISSN: None     Source Type: Journal    
DOI: 10.1097/00001721-199707000-00001     Document Type: Review

References (127)

1. Henschen A, Lottspeich F, Kehl M, Southan C. Covalent structure of fibrinogen. Ann NY Acad Sci 1983; 408: 28-43.
2. Mosesson MW, Siebenlist KR, Hainfeld JF, Wall JS. The covalent structure of factor XIIIa-crosslinked fibrinogen fibrils. J Struct Biol 1995; 115: 88-101.
3. Mosesson MW, Siebenlist KR, DiOrio JP, Matsuda M, Hainfeld JF, Wall JS. The role of fibrinogen D domain intermolecular association sites in the polymerization of fibrin and fibrinogen Tokyo II (γ275arg → cys). J Clin Invest 1995; 96: 1053-1058.
4. Siebenlist KR, Meh DA, Wall JS, Hainfeld JF, Mosesson MW. Orientation of the C-terminal regions of fibrin y chain dimers determined from the crosslinked products formed in mixtures of fibrin, fragment D, and factor XIIIa. Thromb Haemostas 1995; 74: 1113-1119.
5. 2-terminal part of human fibrinogen. Thromb Res 1976; 8: 639-658.
6. Huang S, Cao Z, Davie EW. The role of aminoterminal disulfide bonds in the structure and assembly of human fibrinogen. Biochem Biophys Res Comm 1993; 190: 488-495.
7. Zhang J-Z, Redman CM. Role of interchain disulfide bonds on the assembly and secretion of human fibrinogen. J Biol Chem 1994; 269: 652-658.
8. Hoeprich PD, Jr, Doolittle RF. Dimeric half-molecules of human fibrinogen are joined through disulfide bonds in an antiparallel orientation. Biochemistry 1983; 22: 2049-2055.
9. Mosesson MW, Hainfeld JF, Haschemeyer RH, Wall JS. Identification and mass analysis of human fibrinogen molecules and their domains by scanning transmission electron microscopy. J Mol Biol 1981; 153: 695-718.
10. Williams RC. Morphology of fibrinogen monomers and of fibrin polymers. Ann NY Acad Sci 1983; 408: 180-193.
11. Méndez JA, Alvarez MV, Aznárez JA, González-Rodríguez J. Two fold symmetry of human fibrinogen proved at the βchain distal domains by monoclonal-immunoelectron microscopy and image analysis. Biochemistry 1996; 35: 634-637.
12. 2-terminal portions of fibrinogen Metz (Aα16Arg → Cys) Aα chains are oriented in the same direction. In: Müller-Berghaus G, Scheefers-Borchel U, Selmayr E, Henschen A, eds. Fibrinogen and Its Derivatives. Amsterdam: Elsevier, 1986: 3-15.
13. Miyata T, Terukina S, Matsuda M, Takeda Y, Murakami T, Iwanaga S. Fibrinogens Kawaguchi and Osaka: an animo acid substitution of Aα arginine-16 to cysteine which forms an extra interchain disulfide bridge between the two Aα chains. J Biochem (Tokyo) 1987; 102:93-101.
14. Kanaide H, Shainoff JR. Cross-linking of fibrinogen and fibrin by fibrin-stabilizing factor (factor XIIIa). J Lab Clin Med 1975; 85: 574-597.
15. Chen R, Doolittle RF. Identification of the polypeptide chains involved in the cross-linking of fibrin. Proc Natl Acad Sci USA 1969; 63: 420-427.
16. Chen R, Doolittle RF. γ-γ cross-linking sites in human and bovine fibrin. Biochemistry 1971; 10: 4486-4491.
17. Doolittle RF, Chen R, Lau F. Hybrid fibrin: proof of the intermolecular nature of γ-γ crosslinking units. Biochem Biophys Res Comm 1971; 44: 94-100.
18. Fowler WE, Erickson HP, Hantgan RR, McDonagh J, Hermans J. Crosslinked fibrinogen dimers demonstrate a feature of molecular packing in fibrin fibers. Science 1981; 211: 287-289.
19. Selmayr E, Thiel W, Müller-Berghaus G. Crosslinking of fibrinogen to immobilized des AA-fibrin. Thromb Res 1985; 39: 459-465.
20. Selmayr E, Deffner M, Bachmann L, Müller-Berghaus G. Chromatography and electron microscopy of cross-linked fibrin polymers - a new model describing the cross-linking at the DD-trans contact of the fibrin molecules. Biopolymers 1988; 27: 1733-1748.
21. Mosesson MW, Siebenlist KR, Amrani DL, DiOrio JP. Identification of covalently linked trimeric and tetrameric D domains in crosslinked fibrin. Proc Natl Acad Sci USA 1989; 86: 1113-1117.
22. Shainoff JR, Dardik BN. Fibrinopeptide B in fibrin assembly and metabolism: physiologic significance in delayed release of the peptide. Ann NY Acad Sci 1983; 408: 254-267.
23. Rozenfel'd MA, Vasil'eva MV. Mechanism of aggregation of fibrinogen molecules: the influence of fibrin-stabilizing factor. Biomed Sci 1991; 2: 155-161.
24. Mega JI, Shainoff JR, Dreasher DA. Dissociation of α-fibrin at elevated temperatures. In: Mosesson MW, Amrani DL, DiOrio JP, Siebenlist KR, eds. Fibrinogen 3. Biochemistry, Biology, Gene Regulation and Expression. New York: Elsevier, 1988: 83-86.
25. Scheraga HA, Laskowski M, Jr. The fibrinogen-fibrin conversion. Adv Prot Chem 1957; 12: 1-131.
26. Blombäck B. Studies on the action of thrombic enzymes on bovine fibrinogen as measured by N-terminal analysis. Arkiv Kemi 1958; 12: 321-335.
27. Blombäck B, Hessel B, Hogg D, Therkildsen I., A two-step fibrinogen-fibrin transition in blood coagulation. Nature (London) 1978; 275: 501-505.
28. Laudano AP, Doolittle RF. Studies on synthetic peptides that bind to fibrinogen and prevent fibrin polymerization. Proc Natl Acad Sci USA 1978; 75: 3085-3089.
29. Laudano AP, Doolittle RP. Studies on synthetic peptides that bind to fibrinogen and prevent fibrin polymerization: structural requirements and species differences. Biochemistry 1980; 19: 1013-1019.
30. Shimizu A, Saito Y, Inada Y. Distinctive role of histidine-16 of the Bβ chain of fibrinogen in the end-to-end association of fibrin. Proc Natl Acad Sci USA 1986; 83: 591-593.
31. Liu CY, Nossel HL. Kaplan KL. Defective thrombin binding by abnormal fibrin associated with recurrent thrombosis. Thromb Haemostas 1979; 42: 79 (abstract).
32. Liu CY, Koehn JA, Morgan FJ. Characterization of fibrinogen New York I. A dysfunctional fibrinogen with a deletion of Bβ 9-72 corresponding exactly to exon 2 of the gene. J Biol Chem 1985; 260: 4390-4396.
33. 2-terminus. J Biol Chem 1985; 260: 2994-3000.
34. Siebenlist KR, DiOrio JP, Budzynski AZ, Mosesson MW. The polymerization and thrombin-binding properties of des-(Bβ1-42)-fibrin. J Biol Chem 1990; 265: 18650-18655.
35. Pandya BV, Gabriel JL, O'Brien JO, Budzynski AZ. Polymerization site in the β chain of fibrin: mapping of the Bβ1-55 sequence. Biochemistry 1991; 30: 162-168.
36. Kudryk B, Collen D, Woods KR, Blombäck B. Evidence for localization of polymerization sites in fibrinogen. J Biol Chem 1974; 249: 3322-3325.
37. Kudryk B, Reuterby J, Blombäck B. Adsorption of plasmic fragment D to thrombin modified fibrinogen-sepharose. Thromb Res 1973; 2: 297-304.
38. Olexa SA, Budzynski AZ. Evidence for four different polymerization sites involved in human fibrin formation. Proc Natl Acad Sci USA 1980; 77: 1374-1378.
39. Olexa SA, Budzynski AZ, Doolittle RF, Cottrell BA, Greene TC. Structure of fragment E species from human cross-linked fibrin. Biochemistry 1981; 21: 6139-6145.
40. Shimizu A, Nagel GM, Doolittle RF. Photoaffinity labeling of the primary fibrin polymerization site: isolation of a CNBr fragment corresponding to γ337-379. Proc Natl Acad Sci USA 1992; 89: 2888-2892.
41. Yamazumi K, Doolittle RF. Photoaffinity labeling of the primary polymerization site: localization of the label to γ-chain tyr-363. Proc Natl Acad Sci USA 1992; 89: 2893-2896.
42. Ferry JD. The mechanism of polymerization of fibrinogen. Proc Natl Acad Sci USA 1952; 38: 566-569.
43. Krakow W, Endres GF, Siegel BM, Scheraga HA. An electron microscopic investigation of the polymerization of bovine fibrin monomer. J Mol Biol 1972; 71: 95-103.
44. Fowler WE, Hantgan RR, Hermans J, Erickson HP. Structure of the fibrin protofibril. Proc Natl Acad Sci USA 1981; 78:4872-4876.
45. Hantgan R, McDonagh J, Hermans J. Fibrin assembly. Ann NY Acad Sci 1993; 408: 344-365.
46. Hewat EA, Tranqui L, Wade RH. Electron microscope structural study of modified fibrin and a related modified fibrinogen aggregate. J Mol Biol 1983; 170:203-222.
47. Mosesson MW, DiOrio JP, Siebenlist KR, Wall JS, Hainfeld JF. Evidence for a second type of branch point in fibrin polymer networks, the trimolecular junction. Blood 1993; 82: 1517-1521.
48. Matačić S. Loewy AG. The identification of isopeptide crosslinks in insoluble fibrin. Biochem Biophys Res Commun 1968; 30: 356-362.
49. Pisano JJ, Finlayson JS, Peyton MP. Crosslink in fibrin polymerized by factor XIII: ε-(γ-glutamyl)lysine. Science 1968; 160: 892-893.
50. Shimizu A, Ferry JD. Ligation of fibrinogen by factor XIIIa with dithiothreitol: mechanical properties of ligated fibrinogen gels. Biopolymers 1988; 27: 703-713.
51. Purves LR, Purves M, Brandt W. Cleavage of fibrin-derived D-dimer into monomers by endopeptidase from puff adder venom (bitis arietans) acting at cross-linked sites of the γ-chain. Sequence of carboxy-terminal cyanogen bromide γ-chain fragments. Biochemistry 1987; 26: 4640-4646.
52. 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: 738-744.
53. Shainoff JR, Urbanic DA, DiBello PM. Immunoelectrophoretic characterization of the crosslinking of fibrinogen and fibrin by factor XIIIa and tissue transglutaminase. J Biol Chem 1991; 166: 6429-6437.
54. 2-plasmin inhibitor and fibronectin to fibrin by fibrin-stabilizing factor. Biochim Biophys Acta 1981; 661: 280-286.
55. 2-plasmin inhibitor. J Biol Chem 1986; 261: 15591-15595.
56. Stathakis NE, Mosesson MW, Chen AB, Galanakis DK. Cryoprecipitation of fibrin-fibrinogen complexes induced by the cold-insoluble globulin of plasma. Blood 1978; 51: 1211-1222.
57. Sobel JH, Ehrlich PH, Birken S, Saffron AJ, Canfield RE. Monoclonal antibody to the region of fibronectin involved in cross-linking to human fibrin. Biochemistry 1983; 22: 4175-4183.
58. Siebenlist KR, Mosesson MW. Factors affecting γ-chain multimer formation in cross-linked fibrin. Biochemistry 1992; 31: 936-941.
59. Shainoff JR, Dardik BN. Fibrinopeptide B and aggregation of fibrinogen. Science 1979; 204: 200-202.
60. Medved LV, Litvinovich SV, Ugarova TP, Lukinova NI, Kilikhevich VN, Ardemasova ZA. Localization of a fibrin polymerization site complementary to Gly-His-Arg sequence. FEBS Lett 1993; 320: 239-242.
61. Mosesson MW, DiOrio JP, Müller MF, et al. Studies on the ultrastructure of fibrin lacking fibrinopeptide B (β-fibrin). Blood 1987; 69: 1073-1081.
62. Mosesson MW, Sherry S. Preparation and properties of human fibrinogen of relatively high solubility. Biochemistry 1966; 5: 2829-2835.
63. Hasegawa N, Sasaki S. Location of the binding site 'b' for lateral polymerization of fibrin. Thromb Res 1990; 57: 183-195.
64. Veklich YI, Gorkun OV, Medved LV, Nieuwenhuizen W, Weisel JW. Carboxyl-terminal portions of the α chains of fibrinogen and fibrin. J Biol Chem 1993; 268: 13577-13585.
65. Gorkun OV, Veklich YI, Medved LV, Henschen A, Weisel JW. Role of the αC domains of fibrin in clot formation. Biochemistry 1994; 33: 6986-6997.
66. Sporn LA, Bunce LA, Francis CW. Cell proliferation of fibrin: modulation by fibrinopeptide cleavage. Blood 1995; 86: 1801-1810.
67. Bunce LA, Sporn LA, Francis CW. Endothelial cell spreading on fibrin requires fibrinopeptide-B cleavage and amino acid residues 15-42 of the beta chain. J Clin Invest 1992; 89: 842-850.
68. Chalupowicz DG, Chowdhury ZA, Bach TL, Barsigian C, Martinez J. Fibrin II induces endothelial cell capillary tube formation. J Cell Biol 1995; 130: 207-215.
69. Ribes JA, Bunce LA, Francis CW. Mediation of fibrin-induced release of von Willebrand factor from cultured endothelial cells by fibrin β chain. J Clin Invest 1989; 84: 435-441.
70. Francis CW, Bunce LA, Sporn LA. Endothelial cell responses to fibrin mediated by FPB cleavage and the amino acid terminus of the β chain. Blood Cells 1993; 19:291-307.
71. Simpson-Haidaris PJ, Odrljin TM, Frances CW, et al. Heparin binding domain of fibrin mediates its binding to endothelial cells. Fibrinolysis 1996; 10 (suppl 4); 20 (abstract).
72. Odrljin TM, Shainoff JR, Lawrence SO, Simpson-Haidaris PJ. Thrombin cleavage enhances exposure of a heparin binding domain in the N-terminus of the fibrin β chain. Blood 1996; 88: 2050-2061.
73. Erban JK, Wagner DD. A 130-kDa protein in endothelial cells binds to amino acids 15-42 of the Bβ chain of fibrinogen. J Biol Chem 1992; 267: 2451-2458.
74. Hamaguchi M, Bunce LA, Sporn LA, Francis CW. Spreading of platelets on fibrin is mediated by the amino terminus of the β chain including peptide β15-42. Blood 1993; 81: 2348-2356.
75. Mosesson MW, Finlayson JS, Umfleet RA. Heterogeneities of human fibrinogen. III Identification of γ chain variants. J Biol Chem 1972; 247: 5223-5227.
76. Mosesson MW, Finlayson JS. Subfractions of human fibrinogen - preparation and analysis. J Lab Clin Med 1963; 62: 663-674.
77. Wolfenstein-Todel C, Mosesson MW. Human plasma fibrinogen heterogeneity: evidence for an extended carboxyl-terminal sequence in a normal fibrinogen variant (γ′). Proc Natl Acad Sci USA 1980; 77: 5069-5073.
78. Stathakis NE, Mosesson MW, Galanakis DK, Ménaché D. Human fibrinogen heterogeneities. Preparation and characterization of γ and γ′ chains. Thromb Res 1978; 13:467-475.
79. A and γ′ chains of human fibrinogen are produced by alternative mRNA splicing. Biochemistry 1984; 23: 4232-4236.
80. Wolfenstein-Todel C, Mosesson MW. Carboxy-terminal amino acid sequence of a human fibrinogen γ chain variant (γ′). Biochemistry 1981; 20: 6146-6149.
81. Harfenist EJ, Packham MA, Mustard JF. Effect of variant y chains and sialic acid content of fibrinogen upon its interactions with ADP-stimulated platelet aggregation. Blood 1984; 64: 1163-1168.
82. Amrani DL, Newman PJ, Meh D, Mosesson MW. The role of fibrinogen Aα chains in ADP-induced platelet aggregation in the presence of fibrinogen molecules containing γ′ chains. Blood 1988; 72: 919-924.
83. Kirschbaum NE, Mosesson MW, Amrani DL. Characterization of the y chain platelet binding site on fibrinogen fragment D. Blood 1992; 79: 2643-2648.
84. Farrell DH, Thiagarajan P. Binding of recombinant fibrinogen mutants to platelets. J Biol Chem 1994; 269:226-231.
85. Siebenlist KR, Meh DA, Mosesson MW. Plasma factor XIII binds specifically to fibrinogen molecules containing γ′ chains. Biochemistry 1996; 35: 10448-10453.
86. Fenton JW, II, Olson TA, Zabinski MP, Wilner GD. Anion-binding exosite of human α-thrombin and fibrin(ogen) recognition. Biochemistry 1988; 27: 7106-7112.
87. Stubbs MT, Bode W. A player of many parts: the spotlight falls on thrombin's structure. Thromb Res 1993; 69: 1-58.
88. Noé G, Hofsteenge J, Rovelli G, Stone SR. The use of sequence-specific antibodies to identify a secondary binding site in thrombin. J Biol Chem 1988; 263: 11729-11735.
89. T -thrombin. Identification of lysyl residues in α-thrombin that are critical for heparin and fibrin(ogen) interactions. J Biol Chem 1989; 264: 18419-18425.
90. Esmon CT, Lollar P. Involvement of thrombin anion-binding exosites 1 and 2 in the activation of factor V and factor VIII. J Biol Chem 1996; 271: 13882-13887.
91. Herbert J-M, Dupuy E, Laplace M-C, Zini J-M, Bar Shavit R, Tobelem G. Thrombin induces endothelial cell growth via both a proteolytic and non-proteolytic pathway. Biochem J 1994; 303: 227-231.
92. Tsiang M, Lentz SR, Dittman WA, Wen D, Scarpati EM, Sadler JE. Equilibrium binding of thrombin to recombinant human thrombomodulin: effect of hirudin, fibrinogen, factor Va and peptide analogues. Biochemistry 1990; 26: 10602-10612.
93. Suzuki K, Nishioka J. A thrombin-based peptide corresponding to the sequence of the thrombomodulin-binding site blocks the procoagulant activities of thrombin. J Boil Chem 1991; 266: 18498-18501.
94. De Marco L, Mazzucato M, Masotti A, Ruggeri ZM. Location and characterization of an α-thrombin binding site in platelet glycoprotein Ibα. J Biol Chem 1994; 269: 6478-6484.
95. Scheraga HA. Interaction of thrombin and fibrinogen and the polymerization of fibrin monomer. Ann NY Acad Sci 1983; 408: 330-343.
96. Martinelli RA, Scheraga HA. Steady-state kinetic study of the bovine thrombin-fibrinogen interaction. Biochemistry 1980; 19: 2343-2350.
97. Hurlet-Jensen A, Cummins HZ, Nossel HL, Liu CY. Fibrin polymerization and release of fibrinopeptide B by thrombin. Thromb Res 1982; 27: 419-427.
98. Ruf W, Bender A, Lane DA, Preissner KT, Selmayr E, Müller-Berghaus G. Thrombin-induced fibrinopeptide B release from normal and variant fibrinogens: influence of inhibitors of fibrin polymerization. Biochim Biophys Acta 1988; 965: 169-175.
99. Liu CY, Nossel HL, Kaplan KL. The binding of thrombin by fibrin. J Biol Chem 1979; 254: 10421-10425.
100. Meh DA, Siebenlist KR, Mosesson MW. Identification and characterization of the thrombin binding sites on fibrin. J Biol Chem 1996; 271: 23121-23125.
101. Kaminski M, McDonagh J. Inhibited thrombins. Interactions with fibrinogen and fibrin. Biochem J 1987; 242: 881-887.
102. Liu CY, Wallen P, Handley DA. Fibrinogen New York I: the structural, functional, and genetic defects and an hypothesis of the role of fibrin in the regulation of coagulation and fibrinolysis. In: Lane D, Henschen A, Jasani M, eds. Fibrinogen, Fibrin Formation, and Fibrinolysis, Vol 4. Berlin: Walter de Gruyter, 1986; 79-90.
103. Koopman J, Haverkate F, Lord ST, Grimbergen J, Mannucci PM. Molecular basis of fibrinogen Naples associated with defective thrombin binding and thrombophilia. J Clin Invest 1992; 90: 238-244.
104. Di Minno G, Martinez J, Cirillo F, et al. A role for platelets and thrombin in the juvenile stroke of two siblings with defective thrombin adsorbing capacity of fibrinogen. Arterioscl Thromb 1991; 11: 785-796.
105. Vali Z, Scheraga HA. Localization of the binding site on fibrin for the secondary binding site of thrombin. Biochemistry 1988; 27: 1956-1963.
106. Binnie CG, Lord ST. A synthetic analog of fibrinogen α27-50 is an inhibitor of thrombin. Thromb Haemostas 1994; 65: 165-168.
107. Collen D. On the regulation and control of fibrinolysis. Thromb Haemostas 1980; 43: 77-89.
108. Levin E. Latent tissue plasminogen activator produced by human endothelial cells in culture: evidence for an enzyme-inhibitor complex. Proc Natl Acad Sci USA 1983; 80: 6804-6808.
109. Wallén P. Activation of plasminogen with urokinase and tissue activator. In: Paoletti R, Sherry S, eds. Thrombosis and Urokinase, Vol. 9. London: Academic Press, 1977: 91-102.
110. Hoylaerts M, Rijken DC, Lijnen HR, Collen D. Kinetics of the activation of plasminogen by human tissue plasminogen activator: role of fibrin. J Biol Chem 1982; 257: 2912-2919.
111. Rånby M. Studies of the kinetics of plasminogen activation by tissue plasminogen activator. Biochim Biophys Acta 1982; 704: 461-469.
112. Suenson E, Petersen LC. Fibrin and plasminogen structures essential to stimulation of plasmin formation by tissue-type plasminogen activator. Biochim Biophys Acta 1986; 870: 510-519.
113. Nicuwenhuizen 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.
114. Schielen WJG, Adams HPHM, Voskuilen M, Tesser GI, Nieuwenhuizen W. The sequence Aα-(154-159) of fibrinogen is capable of accelerating the tPA catalyzed activation of plasminogen. Blood Coag Fibrinol 1991; 2: 465-470.
115. Schielen WJG, Adams HPHM, Voskuilen M, Tesser GI, Nieuwenhuizen W. Structural requirements of position Aα-157 in fibrinogen for the fibrin-induced rate enhancement of the plasminogen activation by tPA. Biochem J 1991; 276: 655-659.
116. Yonekawa O, Voskuilen M, Nieuwenhuizen W. Localization in the fibrinogen γ-chain of a new site that is involved in the acceleration of the tissue-type plasminogen activator-catalysed activation of plasminogen. Biochem J 1992; 283: 187-191.
117. 152Val of fibrinogen Aα-chain in the fibrin-induced rate enhancement of the plasminogen activation by tPA. Fibrinolysis 1993; 7: 63-67.
118. Nieuwenhuizen W. Sites in fibrin involved in the acceleration of plasminogen activation by tPA. Possible role of fibrin polymerization. Thromb Res 1994; 75: 343-347.
119. Schielen WJG, Voskuilen M, Tesser GI, Nieuwenhuizen W. The sequence Aα-(148-160) in fibrin, but not in fibrinogen, is accessible to monoclonal antibodies. Proc Natl Acad Sci USA 1989; 86: 8951-8954.
120. Schielen WJG, Adams HPHM, van Leuven K, Voskuilen M, Tesser GI, Nieuwenhuizen W. The sequence γ-(312-324) is a fibrin-specific epitope. Blood 1991; 77: 2169-2173.
121. Haddeland U, Bennick A, Brosstad F. Stimulating effect on tissue-type plasminogen activation - a new and sensitive indicator of denatured fibrinogen. Thromb Res 1995; 77: 329-336.
122. Haddeland U, Sletten K, Bennick A, Nieuwenhuizen W, Brosstad F. Aggregated conformationally changed fibrinogen exposes the stimulatory sites for t-PA catalysed plasminogen activation. Thromb Haemostas 1996; 75: 326-331.
123. Verheijen JH, Nieuwenhuizen W, Wijngaards G. Activation of plasminogen by tissue activator is increased specifically in the presence of certain soluble fibrin(ogen) fragments. Thromb Res 1982; 27: 377-385.
124. Voskuilen M, Vermond A, Veeneman GH, et al. Fibrinogen lysine residue Aα157 plays a crucial role in the fibrin-induced acceleration of plasminogen activation catalyzed by tissue-type plasminogen activator. J Biol Chem 1987; 262: 5944-5946.
125. Nieuwenhuizen W, Verheijcn JH, Vermond A, Chang GTG. Plasminogen activation by tissue activator is accelerated in the presence of fibrin(ogen) cyanogen bromide fragment FCB-2. Biochim Biophys Acta 1983; 755: 531-533.
126. Grailhe P, Nieuwenhuizen W, Anglés-Cano E. Study of tissue-type plasminogen activator binding sites on fibrin using distinct fragments of fibrinogen. Eur J Biochem 1994; 219: 961-967.
127. Mosesson MW, Siebenlist KR, Voskuilen M, Nieuwenhuizen W. Evaluation of the factors contributing to fibrin-dependent tissue plasminogen activator-mediated plasminogen activation (submitted).