Functional impact of oxidative posttranslational modifications on fibrinogen and fibrin clots

Free Radical Biology and Medicine

Volumn 65, Issue , 2013, Pages 411-418

  Martinez, Marissa ^a   Weisel, John W ^b   Ischiropoulos, Harry ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Coagulation; Fibrin; Fibrinogen; Free radicals; Nitrotyrosine; Oxidation; Thrombosis

Indexed keywords

CYSTEINE; DITHIOTHREITOL; FIBRINOGEN; GLUTATHIONE; HEMATOPORPHYRIN; MONOMER; PEROXYNITRITE; PLASMIN; PLASMINOGEN; THIOREDOXIN; THROMBIN; TISSUE PLASMINOGEN ACTIVATOR; FIBRIN;

ADULT RESPIRATORY DISTRESS SYNDROME; ATHEROGENESIS; ATHEROSCLEROSIS; BINDING SITE; BLOOD CLOTTING; BLOOD CLOTTING TIME; CARBONYLATION; CORONARY ARTERY DISEASE; FIBRIN CLOT; FIBRIN POLYMERIZATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IN VITRO STUDY; ISCHEMIC HEART DISEASE; LIVER CELL; MASS SPECTROMETRY; MOLECULAR WEIGHT; NERVE DEGENERATION; NITRATION; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PATHOGENESIS; PLASMINOGEN ACTIVATION; POLYMERIZATION; POROSITY; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; SCANNING ELECTRON MICROSCOPY; SHEAR STRESS; THROMBOCYTE AGGREGATION; THROMBOCYTE POOR PLASMA; THROMBOELASTOGRAPHY; THROMBOEMBOLISM; TURBIDITY; VEIN THROMBOSIS; WESTERN BLOTTING; ANIMAL; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ANIMALS; BLOOD COAGULATION; FIBRIN; FIBRINOGEN; HUMANS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84881507608     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.06.039     Document Type: Review

References (84)

1. G.H. Whipple, and S.H. Hurwitz Fibrinogen of the blood as influenced by the liver necrosis of chloroform poisoning J. Exp. Med. 13 1911 136 161
2. T.P. Stein, M.J. Leskiw, and H.W. Wallace Measurement of half-life human plasma fibrinogen Am. J. Physiol. 234 1978 D504 510
3. C.E. Hall, and H.S. Slayter The fibrinogen molecule: its size, shape, and mode of polymerization J. Biophys. Biochem. Cytol. 5 1959 11 16
4. J.M. Kollman, L. Pandi, M.R. Sawaya, M. Riley, and R.F. Doolittle Crystal structure of human fibrinogen Biochemistry 48 2009 3877 3886
5. Z. Yang, J.M. Kollman, L. Pandi, and R.F. Doolittle Crystal structure of native chicken fibrinogen at 2.7 A resolution Biochemistry 40 2001 12515 12523 (Pubitemid 32979704)
6. J.H. Brown, N. Volkmann, G. Jun, A.H. Henschen-Edman, and C. Cohen The crystal structure of modified bovine fibrinogen Proc. Natl. Acad. Sci. USA 97 2000 85 90 (Pubitemid 30055788)
7. L. Lorand 'Fibrino-peptide'; new aspects of the fibrinogen-fibrin transformation Nature 167 1951 992 993
8. B. Blomback, B. Hessel, D. Hogg, and L. Therkildsen A two-step fibrinogen - fibrin transition in blood coagulation Nature 275 1978 501 505 (Pubitemid 9020557)
9. 2-terminal fragments of the ("A") chain J. Biol. Chem. 247 1972 1496 1512
10. F.R. Bettelheim The clotting of fibrinogen. II. Fractionation of peptide material liberated Biochim. Biophys. Acta 19 1956 121 130
11. A.Z. Budzynski, S.A. Olexa, and B.V. Pandya Fibrin polymerization sites in fibrinogen and fibrin fragments Ann. N. Y. Acad. Sci. 408 1983 301 314 (Pubitemid 13072045)
12. K.P. Pratt, H.C. Cote, D.W. Chung, R.E. Stenkamp, and E.W. Davie The primary fibrin polymerization pocket: three-dimensional structure of a 30-kDa C-terminal gamma chain fragment complexed with the peptide gly-pro-arg-pro Proc. Natl. Acad. Sci. USA 94 1997 7176 7181
13. G. Spraggon, S.J. Everse, and R.F. Doolittle Crystal structures of fragment D from human fibrinogen and its crosslinked counterpart from fibrin Nature 389 1997 455 462 (Pubitemid 27435313)
14. W. Krakow, G.F. Endres, B.M. Siegel, and H.A. Scheraga An electron microscopic investigation of the polymerization of bovine fibrin monomer J. Mol. Biol. 71 1972 95 103
15. W.E. Fowler, R.R. Hantgan, J. Hermans, and H.P. Erickson Structure of the fibrin protofibril Proc. Natl. Acad. Sci. USA 78 1981 4872 4876 (Pubitemid 12225583)
16. E.A. Hewat, L. Tranqui, and R.H. Wade Electron microscope structural study of modified fibrin and a related modified fibrinogen aggregate J. Mol. Biol. 170 1983 203 222 (Pubitemid 13013748)
17. R.R. Hantgan, and J. Hermans Assembly of fibrin: a light scattering study J. Biol. Chem. 254 1979 11272 11281 (Pubitemid 10136141)
18. A.S. Ng, S.D. Lewis, and J.A. Shafer Quantifying thrombin-catalyzed release of fibrinopeptides from fibrinogen using high-performance liquid chromatography Methods Enzymol. 222 1993 341 358
19. E.A. Ryan, L.F. Mockros, J.W. Weisel, and L. Lorand Structural origins of fibrin clot rheology Biophys. J. 77 1999 2813 2826 (Pubitemid 29519524)
20. J.P. Collet, D. Park, C. Lesty, J. Soria, C. Soria, G. Montalescot, and J.W. Weisel Influence of fibrin network conformation and fibrin fiber diameter on fibrinolysis speed: dynamic and structural approaches by confocal microscopy Arterioscler. Thromb. Vasc. Biol. 20 2000 1354 1361 (Pubitemid 30262939)
21. C. Gerth, W.W. Roberts, and J.D. Ferry Rheology of fibrin clots. II. Linear viscoelastic behavior in shear creep Biophys. Chem. 2 1974 208 217
22. A.E. Brown, R.I. Litvinov, D.E. Discher, P.K. Purohit, and J.W. Weisel Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water Science 325 2009 741 744
23. L. Lorand, and A. Jacobsen Accelerated lysis of blood clots Nature 195 1962 911 912
24. S. Nakamura, S. Iwanaga, and T. Suzuki On the activation of bovine plasma factor XIII: amino acid sequence of the peptide released by thrombin and the terminal residues of the subunit polypeptides J. Biochem 78 1975 1247 1266
25. J.H. Sobel, and M.A. Gawinowicz Identification of the alpha chain lysine donor sites involved in factor XIIIa fibrin cross-linking J. Biol. Chem. 271 1996 19288 19297 (Pubitemid 26271597)
26. B.A. Cottrell, D.D. Strong, K.W. Watt, and R.F. Doolittle Amino acid sequence studies on the alpha chain of human fibrinogen: exact location of cross-linking acceptor sites Biochemistry 18 1979 5405 5410 (Pubitemid 10140282)
27. K.C. Robbins, L. Summaria, B. Hsieh, and R.J. Shah The peptide chains of human plasmin: mechanism of activation of human plasminogen to plasmin J. Biol. Chem. 242 1967 2333 2342
28. M. Hoylaerts, D.C. Rijken, H.R. Lijnen, and D. Collen Kinetics of the activation of plasminogen by human tissue plasminogen activator: role of fibrin J. Biol. Chem. 257 1982 2912 2919 (Pubitemid 12118804)
29. R.A. Bok, and W.F. Mangel Quantitative characterization of the binding of plasminogen to intact fibrin clots, lysine-sepharose, and fibrin cleaved by plasmin Biochemistry 24 1985 3279 3286 (Pubitemid 15028730)
30. G. Tsurupa, and L. Medved Identification and characterization of novel tPA- and plasminogen-binding sites within fibrin(ogen) alpha C-domains Biochemistry 40 2001 801 808 (Pubitemid 32096865)
31. J.P. Collet, Y. Allali, C. Lesty, M.L. Tanguy, J. Silvain, A. Ankri, B. Blanchet, R. Dumaine, J. Gianetti, L. Payot, J.W. Weisel, and G. Montalescot Altered fibrin architecture is associated with hypofibrinolysis and premature coronary atherothrombosis Arterioscler. Thromb. Vasc. Biol. 26 2006 2567 2573 (Pubitemid 44607482)
32. I. Parastatidis, L. Thomson, A. Burke, I. Chernysh, C. Nagaswami, J. Visser, S. Stamer, D.C. Liebler, G. Koliakos, H.F. Heijnen, G.A. Fitzgerald, J.W. Weisel, and H. Ischiropoulos Fibrinogen beta-chain tyrosine nitration is a prothrombotic risk factor J. Biol. Chem. 283 2008 33846 33853
33. M. Pieters, N. Covic, F.H. van der Westhuizen, C. Nagaswami, Y. Baras, D. Toit Loots, J.C. Jerling, D. Elgar, K.S. Edmondson, D.G. van Zyl, P. Rheeder, and J.W. Weisel Glycaemic control improves fibrin network characteristics in type 2 diabetes - a purified fibrinogen model Thromb. Haemostasis 99 2008 691 700 (Pubitemid 351694225)
34. D.H. Farrell, and P. Thiagarajan Binding of recombinant fibrinogen mutants to platelets J. Biol. Chem. 269 1994 226 231 (Pubitemid 24026648)
35. W.B. Kannel, P.A. Wolf, W.P. Castelli, and R.B. D'Agostino Fibrinogen and risk of cardiovascular disease. the Framingham Study JAMA 258 1987 1183 1186
36. L. Wilhelmsen, K. Svardsudd, K. Korsan-Bengtsen, B. Larsson, L. Welin, and G. Tibblin Fibrinogen as a risk factor for stroke and myocardial infarction N. Engl. J. Med. 311 1984 501 505 (Pubitemid 14059351)
37. Emerging Risk Factors Collaboration S. Kaptoge, E. Di Angelantonio, L. Pennells, A.M. Wood, I.R. White, P. Gao, M. Walker, A. Thompson, N. Sarwar, M. Caslake, A.S. Butterworth, P. Amouyel, G. Assmann, S.J. Bakker, E.L. Barr, E. Barrett-Connor, E.J. Benjamin, C. Bjorkelund, H. Brenner, E. Brunner, R. Clarke, J.A. Cooper, P. Cremer, M. Cushman, G.R. Dagenais, R.B.S. D'Agostino, R. Dankner, G. Davey-Smith, D. Deeg, J.M. Dekker, G. Engstrom, A.R. Folsom, F.G. Fowkes, J. Gallacher, J.M. Gaziano, S. Giampaoli, R.F. Gillum, A. Hofman, B.V. Howard, E. Ingelsson, H. Iso, T. Jorgensen, S. Kiechl, A. Kitamura, Y. Kiyohara, W. Koenig, D. Kromhout, L.H. Kuller, D.A. Lawlor, T.W. Meade, A. Nissinen, B.G. Nordestgaard, A. Onat, D.B. Panagiotakos, B.M. Psaty, B. Rodriguez, A. Rosengren, V. Salomaa, J. Kauhanen, J.T. Salonen, J.A. Shaffer, S. Shea, I. Ford, C.D. Stehouwer, T.E. Strandberg, R.W. Tipping, A. Tosetto, S. Wassertheil-Smoller, P. Wennberg, R.G. Westendorp, P.H. Whincup, L. Wilhelmsen, M. Woodward, G.D. Lowe, N.J. Wareham, K.T. Khaw, N. Sattar, C.J. Packard, V. Gudnason, P.M. Ridker, M.B. Pepys, S.G. Thompson, and J. Danesh C-reactive protein, fibrinogen, and cardiovascular disease prediction N. Engl. J. Med. 367 2012 1310 1320
38. J.J. Stec, H. Silbershatz, G.H. Tofler, T.H. Matheney, P. Sutherland, I. Lipinska, J.M. Massaro, P.F. Wilson, J.E. Muller, and R.B.S. D'Agostino Association of fibrinogen with cardiovascular risk factors and cardiovascular disease in the Framingham offspring population Circulation 102 2000 1634 1638
39. B. Pignatelli, C.Q. Li, P. Boffetta, Q. Chen, W. Ahrens, F. Nyberg, A. Mukeria, I. Bruske-Hohlfeld, C. Fortes, V. Constantinescu, H. Ischiropoulos, and H. Ohshima Nitrated and oxidized plasma proteins in smokers and lung cancer patients Cancer Res. 61 2001 778 784 (Pubitemid 32128646)
40. R.S. Barua, F. Sy, S. Srikanth, G. Huang, U. Javed, C. Buhari, D. Margosan, and J.A. Ambrose Effects of cigarette smoke exposure on clot dynamics and fibrin structure: an ex vivo investigation Arterioscler. Thromb. Vasc. Biol. 30 2010 75 79
41. M. van Oijen, J.C. Witteman, A. Hofman, P.J. Koudstaal, and M.M. Breteler Fibrinogen is associated with an increased risk of Alzheimer disease and vascular dementia Stroke 36 2005 2637 2641
42. M. Thambisetty, A. Simmons, A. Hye, J. Campbell, E. Westman, Y. Zhang, L.O. Wahlund, A. Kinsey, M. Causevic, R. Killick, I. Kloszewska, P. Mecocci, H. Soininen, M. Tsolaki, B. Vellas, C. Spenger, and S. Lovestone AddNeuroMed Consortium. Plasma biomarkers of brain atrophy in Alzheimer's disease PLoS One 6 2011 e28527
43. G. Xu, H. Zhang, S. Zhang, X. Fan, and X. Liu Plasma fibrinogen is associated with cognitive decline and risk for dementia in patients with mild cognitive impairment Int. J. Clin. Pract. 62 2008 1070 1075 (Pubitemid 351793581)
44. K. Hensley, N. Hall, R. Subramaniam, P. Cole, M. Harris, M. Aksenov, M. Aksenova, S.P. Gabbita, J.F. Wu, and J.M. Carney Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation J. Neurochem. 65 1995 2146 2156
45. J. Choi, C.A. Malakowsky, J.M. Talent, C.C. Conrad, and R.W. Gracy Identification of oxidized plasma proteins in Alzheimer's disease Biochem. Biophys. Res. Commun. 293 2002 1566 1570 (Pubitemid 34681057)
46. P.D. Zieve, and H.M. Solomon Effect of hematoporphyrin and light on human fibrinogen Am. J. Physiol. 210 1966 1391 1395
47. Y. Inada, B. Hessel, and B. Blomback Photooxidation of fibrinogen in the presence of methylene blue and its effect on polymerization Biochim. Biophys. Acta 532 1978 161 170 (Pubitemid 8251069)
48. A. Shimizu, Y. Saito, and Y. Inada Distinctive role of histidine-16 of the B beta chain of fibrinogen in the end-to-end association of fibrin Proc. Natl. Acad. Sci. USA 83 1986 591 593 (Pubitemid 16035520)
49. S.J. Everse, G. Spraggon, L. Veerapandian, M. Riley, and R.F. Doolittle Crystal structure of fragment double-D from human fibrin with two different bound ligands Biochemistry 37 1998 8637 8642 (Pubitemid 28299601)
50. T.W. Stief Oxidized fibrin stimulates the activation of pro-urokinase and is the preferential substrate of human plasmin Blood Coagulation Fibrinolysis 4 1993 117 121 (Pubitemid 23064927)
51. M.A. Belisario, C. Di Domenico, A. Pelagalli, R. Della Morte, and N. Staiano Metal-ion catalyzed oxidation affects fibrinogen activity on platelet aggregation and adhesion Biochimie 79 1997 449 455 (Pubitemid 27462528)
52. E. Shacter, J.A. Williams, and R.L. Levine Oxidative modification of fibrinogen inhibits thrombin-catalyzed clot formation Free Radic. Biol. Med. 18 1995 815 821
53. A. Amici, R.L. Levine, L. Tsai, and E.R. Stadtman Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal-catalyzed oxidation reactions J. Biol. Chem. 264 1989 3341 3346 (Pubitemid 19063388)
54. D.K. Galanakis, P. Laurent, and A. Janoff Cigarette smoke contains anticoagulants against fibrin aggregation and factor XIIIa in plasma Science 217 1982 642 645 (Pubitemid 12041291)
55. G.R. Upchurch Jr, N. Ramdev, M.T. Walsh, and J. Loscalzo Prothrombotic consequences of the oxidation of fibrinogen and their inhibition by aspirin J. Thromb. Thrombolysis 5 1998 9 14 (Pubitemid 28075248)
56. K.M. Weigandt, N. White, D. Chung, E. Ellingson, Y. Wang, X. Fu, and D.C. Pozzo Fibrin clot structure and mechanics associated with specific oxidation of methionine residues in fibrinogen Biophys. J. 103 2012 2399 2407
57. O.V. Gorkun, A.H. Henschen-Edman, L.F. Ping, and S.T. Lord Analysis of A alpha 251 fibrinogen: the alpha C domain has a role in polymerization, albeit more subtle than anticipated from the analogous proteolytic fragment X Biochemistry 37 1998 15434 15441 (Pubitemid 28516005)
58. M.D. Gole, J.M. Souza, I. Choi, C. Hertkorn, S. Malcolm, R.F. Foust 3rd, B. Finkel, P.N. Lanken, and H. Ischiropoulos Plasma proteins modified by tyrosine nitration in acute respiratory distress syndrome Am. J. Physiol. Lung Cell. Mol. Physiol. 278 2000 L961 L967
59. M. Piroddi, A. Palmese, F. Pilolli, A. Amoresano, P. Pucci, C. Ronco, and F. Galli Plasma nitroproteome of kidney disease patients Amino Acids 40 2011 653 667
60. C. Vadseth, J.M. Souza, L. Thomson, A. Seagraves, C. Nagaswami, T. Scheiner, J. Torbet, G. Vilaire, J.S. Bennett, J.C. Murciano, V. Muzykantov, M.S. Penn, S.L. Hazen, J.W. Weisel, and H. Ischiropoulos Pro-thrombotic state induced by post-translational modification of fibrinogen by reactive nitrogen species J. Biol. Chem. 279 2004 8820 8826 (Pubitemid 38295940)
61. M. Martinez, A. Cuker, A. Mills, R. Lightfoot, Y. Fan, W.H. Tang, S.L. Hazen, and H. Ischiropoulos Nitrated fibrinogen is a biomarker of oxidative stress in venous thromboembolism Free Radic. Biol. Med. 53 2012 230 236
62. A.M. Mitchell, K.E. Nordenholz, and J.A. Kline Tandem measurement of D-dimer and myeloperoxidase or C-reactive protein to effectively screen for pulmonary embolism in the emergency department Acad. Emerg. Med 15 2008 800 805
63. M.L. Brennan, W. Wu, X. Fu, Z. Shen, W. Song, H. Frost, C. Vadseth, L. Narine, E. Lenkiewicz, M.T. Borchers, A.J. Lusis, J.J. Lee, N.A. Lee, H.M. Abu-Soud, H. Ischiropoulos, and S.L. Hazen A tale of two controversies: defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species J. Biol. Chem. 277 2002 17415 17427 (Pubitemid 34967541)
64. M.L. von Bruhl, K. Stark, A. Steinhart, S. Chandraratne, I. Konrad, M. Lorenz, A. Khandoga, A. Tirniceriu, R. Coletti, M. Kollnberger, R.A. Byrne, I. Laitinen, A. Walch, A. Brill, S. Pfeiler, D. Manukyan, S. Braun, P. Lange, J. Riegger, J. Ware, A. Eckart, S. Haidari, M. Rudelius, C. Schulz, K. Echtler, V. Brinkmann, M. Schwaiger, K.T. Preissner, D.D. Wagner, N. Mackman, B. Engelmann, and S. Massberg Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo J. Exp. Med. 209 2012 819 835
65. F.K. Swirski, P. Libby, E. Aikawa, P. Alcaide, F.W. Luscinskas, R. Weissleder, and M.J. Pittet Ly-6Chi monocytes dominate hypercholesterolemia- associated monocytosis and give rise to macrophages in atheromata J. Clin. Invest. 117 2007 195 205 (Pubitemid 46048466)
66. M. Drechsler, R.T. Megens, M. van Zandvoort, C. Weber, and O. Soehnlein Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis Circulation 122 2010 1837 1845
67. S.P. Heffron, I. Parastatidis, M. Cuchel, M.L. Wolfe, M.G. Tadesse, E.R. Mohler 3rd, H. Ischiropoulos, D.J. Rader, and M.P. Reilly Inflammation induces fibrinogen nitration in experimental human endotoxemia Free Radic. Biol. Med. 47 2009 1140 1146
68. I. Parastatidis, L. Thomson, D.M. Fries, R.E. Moore, J. Tohyama, X. Fu, S.L. Hazen, H.F. Heijnen, M.K. Dennehy, D.C. Liebler, D.J. Rader, and H. Ischiropoulos Increased protein nitration burden in the atherosclerotic lesions and plasma of apolipoprotein A-I deficient mice Circ. Res. 101 2007 368 376 (Pubitemid 47267705)
69. Anonymous Oral contraceptives and stroke in young women: associated risk factors JAMA 231 1975 718 722
70. T. Nakayama, D.F. Church, and W.A. Pryor Quantitative analysis of the hydrogen peroxide formed in aqueous cigarette tar extracts Free Radic. Biol. Med. 7 1989 9 15 (Pubitemid 19165149)
71. P. Nowak, H.M. Zbikowska, M. Ponczek, J. Kolodziejczyk, and B. Wachowicz Different vulnerability of fibrinogen subunits to oxidative/nitrative modifications induced by peroxynitrite: functional consequences Thromb. Res. 121 2007 163 174 (Pubitemid 350138069)
72. G. Lupidi, M. Angeletti, A.M. Eleuteri, L. Tacconi, M. Coletta, and E. Fioretti Peroxynitrite-mediated oxidation of fibrinogen inhibits clot formation FEBS Lett. 462 1999 236 240
73. P. Nowak, and B. Wachowicz Peroxynitrite-mediated modification of fibrinogen affects platelet aggregation and adhesion Platelets 13 2002 293 299 (Pubitemid 34864513)
74. R. Radi, J.S. Beckman, K.M. Bush, and B.A. Freeman Peroxynitrite oxidation of sulfhydryls: the cytotoxic potential of superoxide and nitric oxide J. Biol. Chem. 266 1991 4244 4250 (Pubitemid 21909347)
75. H. Ischiropoulos, and A.B. al-Mehdi Peroxynitrite-mediated oxidative protein modifications FEBS Lett. 364 1995 279 282
76. A. Henschen Number and reactivity of disulfide bonds in fibrinogen and fibrin Ark. Kemi 22 1964 355 373
77. B. Blomback, M. Blomback, W. Finkbeiner, A. Holmgren, B. Kowalska-Loth, and G. Olovson Enzymatic reduction of disulfide bonds in fibrinogen by the thioredoxin system. I. Identification of reduced bonds and studies on reoxidation process Thromb. Res. 4 1974 55 75
78. R. Procyk, and B. Blomback Disulfide bond reduction in fibrinogen: calcium protection and effect on clottability Biochemistry 29 1990 1501 1507 (Pubitemid 20063381)
79. R. Procyk, L. Medved, K.J. Engelke, B. Kudryk, and B. Blomback Nonclottable fibrin obtained from partially reduced fibrinogen: characterization and tissue plasminogen activator stimulation Biochemistry 31 1992 2273 2278
80. C.B. Geer, N.A. Stasko, I.A. Rus, S.T. Lord, and M.H. Schoenfisch Influence of glutathione and its derivatives on fibrin polymerization Biomacromolecules 9 2008 1876 1882
81. S. Akhter, A. Vignini, Z. Wen, A. English, P.G. Wang, and B. Mutus Evidence for S-nitrosothiol-dependent changes in fibrinogen that do not involve transnitrosation or thiolation Proc. Natl. Acad. Sci. USA 99 2002 9172 9177 (Pubitemid 34764586)
82. R.M. Bateman, C.G. Ellis, M. Suematsu, and K.R. Walley S-nitrosoglutathione acts as a small molecule modulator of human fibrin clot architecture PLoS One 7 2012 e43660
83. J. Konings, J.W. Govers-Riemslag, H. Philippou, N.J. Mutch, J.I. Borissoff, P. Allan, S. Mohan, G. Tans, H. Ten Cate, and R.A. Ariens Factor XIIa regulates the structure of the fibrin clot independently of thrombin generation through direct interaction with fibrin Blood 118 2011 3942 3951
84. M. Bilzer, and B.H. Lauterburg Glutathione metabolism in activated human neutrophils: stimulation of glutathione synthesis and consumption of glutathione by reactive oxygen species Eur. J. Clin. Invest 21 1991 316 322