Fibrinogen post-translational modifications are biochemical determinants of fibrin clot properties and interactions.
fibrin clot properties
fibrinogen
post‐translational modifications
thrombosis
Journal
The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646
Informations de publication
Date de publication:
23 Aug 2024
23 Aug 2024
Historique:
revised:
31
05
2024
received:
16
11
2023
accepted:
23
07
2024
medline:
24
8
2024
pubmed:
24
8
2024
entrez:
24
8
2024
Statut:
aheadofprint
Résumé
The structure of fibrinogen and resulting fibrin formed during the coagulation process have important biological functions in human physiology and pathology. Fibrinogen post-translational modifications (PTMs) increase the complexity of the protein structure and many studies have emphasized the potential associations of post-translationally altered fibrinogen with the formation of a fibrin clot with a prothrombotic phenotype. However, the mechanisms by which PTMs exert their action on fibrinogen, and their causal association with disease pathogenesis are relatively unexplored. Moreover, the significance of fibrinogen PTMs in health has yet to be appreciated. In this review, the impact of fibrinogen PTMs on fibrinogen functionality is discussed from a biochemical perspective, emphasizing the potential mechanisms by which PTMs mediate the acquisition of altered fibrinogen properties. A brief discussion on dysfibrinogenemias of genetic origin, attributed to single point variations of the fibrinogen molecule is also provided, highlighting the influence that amino acid properties have on fibrinogen structure, properties, and molecular interactions that arise during thrombus formation.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 The Author(s). The FEBS Journal published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
Références
Forrester JM (1995) Malpighi's De polypo cordis: an annotated translation. Med Hist 39, 477–492.
Bayer IS (2002) Advances in fibrin‐based materials in wound repair: a review. Molecules 27, 4504.
Kearney KJ, Ariëns RAS & Macrae FL (2022) The role of fibrin(ogen) in wound healing and infection control. Semin Thromb Hemost 48, 174–187.
Macrae FL, Duval C, Papareddy P, Baker SR, Yuldasheva N, Kearney KJ, McPherson LR, Asquith N, Konings J, Casini A et al. (2018) A fibrin biofilm covers blood clots and protects from microbial invasion. J Clin Invest 128, 3356–3368.
Ko YP & Flick MJ (2016) Fibrinogen is at the interface of host defense and pathogen virulence in Staphylococcus aureus infection. Semin Thromb Hemost 42, 408–421.
Litvinov RI & Wiesel JW (2016) What is the biological and clinical relevance of fibrin? Semin Thromb Hemost 42, 333–343.
Litvinov RI, Pieters M, de Lange‐Loots Z & Weisel JW (2021) Fibrinogen and fibrin. In Macromolecular Protein Complexes III: Structure and Function. Subcellular Biochemistry 96. (Robin Harris J & Marles‐Wright J, eds), pp. 471–501. Springer Nature, Cham.
Weisel JW & Litvinov RI (2017) Fibrin formation, structure and properties. Subcell Biochem 82, 405–456.
Kattula S, Byrnes JR & Wolberg AS (2017) Fibrinogen and fibrin in hemostasis and thrombosis. Arterioscler Thromb Vasc Biol 37, e13–e21.
Spraggon G, Everse SJ & Doolittle SF (1997) Crystalstructures of fragment D from human fibrinogen and its cross linked counterpart from fibrin. Nature 389, 455–462.
Weisel JW & Medved L (2001) The structure and function of the αC domains of fibrinogen. Ann N Y Acad Sci 936, 312–327.
Litvinov RI, Yakovlev S, Tsurupa G, Gorkun OV, Medved L & Weisel JW (2007) Direct evidence for specific interactions of the fibrinogen αC domains with the central E region and with each other. Biochemistry 46, 9133–9142.
Veklich YI, Gorkunz OV, Medved LV, Nieuwenhuizenll W & Weisel JW (1993) Carboxyl‐terminal portions of the α chains of fibrinogen and fibrin. Localization by electron microscopy and the effects of isolated ac fragments on polymerization. J Biol Chem 268, 13577–13585.
Doolittle RF, Watt KWK, Cottrell BA, Strong DD & Riley M (1979) The amino acid sequence of the A‐chain of human fibrinogen. Nature 280, 464–468.
Doolittle RF (1981) Fibrinogen and fibrin. Sci Am 245, 126–135.
Litvinov RI, Gorkun OV, Owen SF, Shuman H & Weisel JW (2005) Polymerization of fibrin: specificity, strength, and stability of knob‐hole interactions studied at the single‐molecule level. Blood 106, 2944–2951.
Ferry JD (1983) The conversion of fibrinogen to fibrin: events and recollections from 1942 to 1982. Ann N Y Acad Sci 408, 1–10.
Pratt KP, Cote HCF, Chung DW, Stenkamp RE & Davie DW (1997) The primary fibrin polymerization pocket: three‐dimensional structure of a 30‐kDa C‐terminal chain fragment complexed with the peptide Gly‐Pro‐Arg‐Pro. Proc Natl Acad Sci USA 94, 7176–7181.
Erickson HP & Fowler WE (1983) Electron microscopy of fibrinogen, its plasmic fragments and small polymers. Ann N Y Acad Sci 408, 146–163.
Lorand L (2005) Factor XIII and the clotting of fibrinogen: from basic research to medicine. J Thromb Haemost 3, 1337–1348.
Fogelson AL & Keener JP (2010) Toward an understanding of fibrin branching structure. Phys Rev E Stat Nonlin Soft Matter Phys 81, 051922.
Mosesson MW (2005) Fibrinogen and fibrin structure and functions. J Thromb Haemost 3, 1894–1904.
Cierniewski CS & Budzynski AZ (1992) Involvement of the alpha chain in fibrin clot formation. Effect of monoclonal antibodies. Biochemistry 31, 4248–4253.
Gorkun OV, Henschen‐Edman AH, Ping LF & Lord ST (1998) 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, 15434–15441.
Kostelansky MS, Lounes KC, Ping LF, Dickerson SK, Gorkun OV & Lord ST (2004) Calcium‐binding site beta 2, adjacent to the “b” polymerization site, modulates lateral aggregation of protofibrils during fibrin polymerization. Biochemistry 43, 2475–2483.
Laurens N, Koolwijk P & de Maat MP (2006) Fibrin structure and wound healing. J Thromb Haemost 4, 932–939.
Ritchie H, Lawrie LC, Crombie PW, Mosesson MW & Booth NA (2000) Cross‐linking of plasminogen activator inhibitor 2 and α2‐antiplasmin to fibrin(ogen). J Biol Chem 275, 24915–24920.
Valnickova Z & Enghild JJ (1998) Human procarboxypeptidase U, or thrombin‐activable fibrinolysis inhibitor, is a substrate for transglutaminases: evidence for transglutaminase‐catalyzed cross‐linking to fibrin. J Biol Chem 273, 27220–27224.
Fuchs TA, Brilla A, Duerschmied D, Schatzberga D, Monestierd M, Myers DD Jr, Wrobleskie SK, Wakefielde TW, Hartwigg JH & WagnerBok DD (2010) Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA 107, 15880–15885.
Bok RA & Mangel WF (1985) Quantitative characterization of the binding of plasminogen to intact fibrin clots, lysine‐sepharose, and fibrin cleaved by plasmin. Biochemistry 24, 3279–3286.
Tsurupa G & Medved L (2001) Identification and characterization of novel tPA‐ and plasminogen‐binding sites within fibrin(ogen) alpha C‐domains. Biochemistry 40, 801–808.
Cieslik J, Mrozinska S, Broniatowska E & Undas A (2018) Altered plasma clot properties increase the risk of recurrent deep vein thrombosis: a cohort study. Blood 131, 797–807.
Undas A (2014) Fibrin clot properties and their modulation in thrombotic disorders. Thromb Haemost 112, 32–42.
Brown AEX, Litvinov RI, Discher DE, Purohit PK & Weisel JW (2009) Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water. Science 325, 741–744.
Guy RD, Fogelson AL & Keener JP (2007) Fibrin gel formation in a shear flow. Math Med Biol 24, 111–130.
Galanakis DK, Agnes Henschen A, Peerschke EIB & Kehlt M (1989) Fibrinogen stony brook, a heterozygous Aa16Arg – Cys dysfibrinogenemia evaluation of diminished platelet aggregation support and of enhanced inhibition of fibrin assembly. J Clin Invest 84, 295–304.
Flood VH, Hamid A, Al‐Mondhiry HA & Farrell DH (2006) The fibrinogen Aalpha R16C mutation results in fibrinolytic resistance. Br J Haematol 134, 220–226.
Soria J, Soria C, Samama M, Tabori S, Kehl M, Henschen A, Nieuwenhuizen W, Rimon A & Tatarski I (1987) Fibrinogen Haifa: fibrinogen variant with absence of protective effect of calcium on plasmin degradation of gamma chains. Thromb Haemost 57, 310–313.
Collet JP, Soria J, Mirshahi M, Hirsch M, Dagonnet FB, Caen J & Soria C (1993) Dusart syndrome: a new concept of the relationship between fibrin clot architecture and fibrin clot degradability: hypofibrinolysis related to an abnormal clot structure. Blood 82, 2462–2469.
Collet JP, Woodhead JL, Soria J, Soria C, Mirshahi M, Caen JP & Weisel JW (1996) Fibrinogen dusart: electron microscopy of molecules, fibers and clots, and viscoelastic properties of clots. Biophys J 70, 500–510.
Ramanathan R, Gram J, Feddersen S, Nybo M, Larsen A & Sidelmann JJ (2013) Dusart Syndrome in a Scandinavian family characterized by arterial and venous thrombosis at young age. Scand J Clin Lab Invest 73, 585–590.
Koopman J, Haverkate F, Grimbergen J, Lord ST, Mosesson MW, DiOrio JP, Siebenlist KS, Legrand C, Soria J, Soria C et al. (1993) Molecular basis for fibrinogen Dusart (A alpha 554 Arg‐‐>Cys) and its association with abnormal fibrin polymerization and thrombophilia. J Clin Invest 91, 1637–1643.
Koopman J, Haverkate F, Lord ST, Grimbergen J & Mannucci PM (1992) Molecular basis of fibrinogen Naples associated with defective thrombin binding and thrombophilia. Homozygous substitution of B beta 68 Ala‐‐‐‐Thr. J Clin Invest 90, 238–244.
Klykov O, van der Zwaan C, Heck AJR, Meijer AB & Scheltema RA (2020) Missing regions within the molecular architecture of human fibrin clots structurally resolved by XL‐MS and integrative structural modeling. Proc Natl Acad Sci USA 117, 1976–1987.
Lounes KC, Lefkowitz JB, Henschen‐Edman AH, Coates AI, Hantgan RR & Lord ST (2001) The impaired polymerization of fibrinogen Longmont (Bbeta166Arg‐‐>Cys) is not improved by removal of disulfide‐linked dimers from a mixture of dimers and cysteine‐linked monomers. Blood 98, 661–666.
Morris TA, Marsh JJ, Chiles PG, Magaña MM, Liang NC, Soler X, Desantis DJ, Ngo D & Woods VL Jr (2009) High prevalence of dysfibrinogenemia among patients with chronic thromboembolic pulmonary hypertension. Blood 27, 1929–1936.
Borrell M, Garí M, Coll I, Vallvé C, Tirado I, Soria JM, Sala N, Muñoz C, Oliver A, García A et al. (1995) Abnormal polymerization and normal binding of plasminogen and t‐PA in three new dysfibrinogenaemias: Barcelona III and IV (gamma Arg 275‐‐>His) and Villajoyosa (gamma Arg 275‐‐>Cys). Blood Coagul Fibrinolysis 6, 198–206.
Ishikawa S, Hirota‐Kawadobora M, Tozuka M, Ishii K, Terasawa F & Okumura N (2004) Recombinant fibrinogen, gamma275Arg‐‐>Cys, exhibits formation of disulfide bond with cysteine and severely impaired D:D interactions. J Thromb Haemost 2, 468–475.
Lounes KC, Soria C, Mirshahi SS, Desvignes P, Mirshahi M, Bertrand O, Bonnet P, Koopman J & Soria J (2000) Fibrinogen Ale's: a homozygous case of dysfibrinogenemia (g‐Asp330 3Val) characterized by a defective fibrin polymerization site “a”. Blood 96, 3473–3479.
Bantia S, Mane SM, Bell WR & Dang CV (1990) Fibrinogen Baltimore I: polymerization defect associated with a y292Gly‐Val (GGC‐GTC) mutation. Blood 76, 2279–2283.
Carter AM, Catto AJ, Kohler HP, Ariëns RA, Stickland MH & Grant PJ (2000) Alpha‐fibrinogen Thr312Ala polymorphism and venous thromboembolism. Blood 96, 1177–1179.
Standeven KF, Grant PJ, Carter AM, Scheiner T, Weisel JW & Ariëns RA (2003) Functional analysis of the fibrinogen Aalpha Thr312Ala polymorphism: effects on fibrin structure and function. Circulation 107, 2326–2330.
Standeven KF, Carter AM, Grant PJ, Weisel JW, Chernysh I, Masova L, Lord ST & Ariëns RA (2007) Functional analysis of fibrin {gamma}‐chain cross‐linking by activated factor XIII: determination of a cross‐linking pattern that maximizes clot stiffness. Blood 110, 902–907.
Mann M & Jensen ON (2003) Proteomic analysis of post‐translational modifications. Nature 21, 255–261.
Witze ES, Old WM, Resing KA & Ahn NG (2007) Mapping protein post‐translational modifications with mass spectrometry. Nat Methods 4, 798–806.
Shacter E, Williams JA, Lim M & Levine RL (1994) Differential susceptibility of plasma proteins to oxidative modification: examination by western blot immunoassay. Free Radic Biol Med 17, 429–437.
Martinez M, Weisel JW & Ischiropoulos H (2013) Functional impact of oxidative posttranslational modifications on fibrinogen and fibrin clots. Free Radic Biol Med 65, 411–418.
Galanakis DK, Laurent P & Janoff A (1982) Cigarette smoke contains anticoagulants against fibrin aggregation and factor XIIIa in plasma. Science 217, 642–645.
Shacter E, Williams JA & Levine RL (1995) Oxidative modification of fibrinogen inhibits thrombin‐catalyzed clot formation. Free Radic Biol Med 18, 815–821.
Amici A, Levine RL, Tsai L & Stadtman ER (1989) Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal‐catalyzed oxidation reactions. J Biol Chem 264, 3341–3346.
Belisario MA, Di Domenico C, Pelagalli A, Della Morte R & Staiano N (1997) Metal‐ion catalyzed oxidation affects fibrinogen activity on platelet aggregation and adhesion. Biochimie 79, 449–455.
Ramdev N, Walsh MT & Loscalzo J (1998) Protrothrombotic consequences of the oxidation of fibrinogen and their inhibition by aspirin. J Thromb Thrombolysis 5, 9–14.
Rosenfeld MA, Shchegolikhin AN, Bychkova AV, Leonova VB, Biryukova MI & Kostanova EA (2014) Ozone‐induced oxidative modification of fibrinogen: role of the D regions. Free Radic Biol Med 77, 106–120.
Yurina LV, Vasilyeva AD, Bugrova AE, Indeykina MI, Kononikhin AS, Nikolaev EN & Rosenfeld MA (2019) Hypochlorite‐induced oxidative modification of fibrinogen. Dokl Biochem Biophys 484, 37–41.
Yurina LV, Vasilyeva AD, Vasserman LA, Podoplelova NA, Panteleev MA & Rosenfeld MA (2021) Effect of hypochlorite‐ and peroxide‐induced oxidation of fibrinogen on the fibrin structure. Dokl Biochem Biophys 499, 242–246.
Stadtman ER, Van Remmen H, Richardson A, Wehr NB & Levine RL (2005) Methionine oxidation and aging. Biochim Biophys Acta 1703, 135–140.
Ferrer‐Sueta G, Campolo N, Trujillo M, Bartesaghi S, Carballal S, Romero N, Alvarez B & Radi R (2018) Biochemistry of peroxynitrite and protein tyrosine nitration. Chem Rev 118, 1338–1408.
Brot N & Weissbach H (1983) Biochemistry and physiological role of methionine sulfoxide residues in proteins. Arch Biochem Biophys 223, 271–281.
Weigandt KM, White N, Chung D, Ellingson E, Wang Y, Fu X & Pozzo DC (2012) Fibrin clot structure and mechanics associated with specific oxidation of methionine residues in fibrinogen. Biophys J 103, 2399–2407.
Bychkova AV, Vasilyeva AD, Bugrova AE, Indeykina MI, Kononikhin AS, Nikolaev EN, Konstantinova ML & Rosenfeld MA (2017) Oxidation‐induced modification of the fibrinogen polypeptide chains. Dokl Biochem Biophys 474, 173–177.
Zhang XH & Weissbach H (2008) Origin and evolution of the protein‐repairing enzymes methionine sulphoxide reductases. Biol Rev Camb Philos Soc 83, 249–257.
Fedorova M, Bollineni RC & Hoffmann R (2014) Protein carbonylation as a major hallmark of oxidative damage: update of analytical strategies. Mass Spectrom Rev 33, 79–97.
Błaż M, Natorska J, Bembenek JP, Członkowska A, Ząbczyk M, Polak M & Undas A (2023) Protein carbonylation contributes to prothrombotic fibrin clot phenotype in acute ischemic stroke: clinical associations. Stroke 54, 2804–2813.
Becatti M, Emmi G, Silvestri E, Bruschi G, Ciucciarelli L, Squatrito D, Vaglio A, Taddei N, Abbate R, Emmi L et al. (2016) Neutrophil activation promotes fibrinogen oxidation and thrombus formation in Behçet disease. Circulation 133, 302–311.
Pignatelli B, Li CQ, Boffetta P, Chen Q, Ahrens W, Nyberg F, Mukeria A, Bruske‐Hohlfeld I, Fortes C, Constantinescu V et al. (2001) Nitrated and oxidized plasma proteins in smokers and lung cancer patients. Cancer Res 61, 778–784.
Becatti M, Marcucci R, Bruschi G, Taddei N, Bani D, Gori AM, Giusti B, Gensini GF, Abbate R & Fiorillo C (2014) Oxidative modification of fibrinogen is associated with altered function and structure in the subacute phase of myocardial infarction. Arterioscler Thromb Vasc Biol 34, 1355–1361.
Larsen JB & Hvas AM (2021) Fibrin clot properties in coronary artery disease: new determinants and prognostic markers. Pol Arch Intern Med 131, 16113.
Ząbczyk M, Ariëns RAS & Undas A (2023) Fibrin clot properties in cardiovascular disease: from basic mechanisms to clinical practice. Cardiovasc Res 119, 94–111.
Seydewitz HH & Witt I (1985) Increased phosphorylation of human fibrinopeptide A under acute phase conditions. Thromb Res 40, 29–39.
Heldin P (1987) Phosphorylation in vitro of human fibrinogen with casein kinase TS and characterization of phosphorylated sites. Arch Biochem Biophys 257, 269–275.
Heldin P & Humble E (1987) Phosphorylation of human fibrinogen in vitro with protein kinase C: characterization of the phosphorylated sites. Arch Biochem Biophys 252, 49–59.
Forsberg PO & Martin SC (1990) Plasmin digestion of human fibrinogen previously phosphorylated by protein kinase C or dephosphorylated by alkaline phosphatase in vitro. Thromb Res 58, 119–127.
Martin SC & Björk I (1990) Conformational changes in human fibrinogen after in vitro phosphorylation and their relation to fibrinogen behaviour. FEBS Lett 272, 103–105.
Martin SC, Ekman P, Forsberg PO & Ersmark H (1992) Increased phosphate content of fibrinogen in vivo correlates with alteration in fibrinogen behaviour. Thromb Res 68, 467–473.
Castegna A, Thongboonkerd V, Klein JB, Lynn B, Markesbery WR & Butterfield DA (2003) Proteomic identification of nitrated proteins in Alzheimer's disease brain. J Neurochem 85, 1394–1401.
Ischiropoulos H (1998) Biological tyrosine nitration: a pathophysiological function of nitric oxide and reactive oxygen species. Arch Biochem Biophys 356, 1–11.
Shishehbor MH, Aviles RJ, Brennan ML, Fu X, Goormastic M, Pearce GL, Gokce N, Keaney JF Jr, Penn MS, Sprecher DL et al. (2003) Association of nitrotyrosine levels with cardiovascular disease and modulation by statin therapy. JAMA 289, 1675–1680.
Reynolds MR, Reyes JF, Fu Y, Bigio EH, Guillozet‐Bongaarts AL, Berry RW & Binder LI (2006) Tau nitration occurs at tyrosine 29 in the fibrillar lesions of Alzheimer's disease and other tauopathies. J Neurosci 26, 10634–10645.
Thomson L, Tenopoulou M, Lightfoot R, Tsika E, Parastatidis I, Martinez M, Greco TM, Doulias PT, Wu Y, Tang WH et al. (2012) Immunoglobulins against tyrosine‐nitrated epitopes in coronary artery disease. Circulation 126, 2392–2401.
Vadseth C, Souza JM, Thomson L, Seagraves A, Nagaswami C, Scheiner T, Torbet J, Vilaire G, Bennett JS, Murciano JC et al. (2004) Pro‐thrombotic state induced by post‐translational modification of fibrinogen by reactive nitrogen species. J Biol Chem 279, 8820–8826.
Martinez M, Cuker A, Mills A, Lightfoot R, Fan Y, Tang WH, Hazen SL & Ischiropoulos H (2012) Nitrated fibrinogen is a biomarker of oxidative stress in venous thromboembolism. Free Radic Biol Med 53, 230–236.
Souza JM, Peluffo G & Radi R (2008) Protein tyrosine nitration—functional alteration or just a biomarker? Free Radic Biol Med 45, 357–366.
van der Vliet A, Eiserich JP, Halliwell B & Cross CE (1997) Formation of reactive nitrogen species during peroxidase‐catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide‐dependent toxicity. J Biol Chem 272, 7617–7625.
Wu W, Chen Y & Hazen SL (1999) Eosinophil peroxidase nitrates protein tyrosyl residues. Implications for oxidative damage by nitrating intermediates in eosinophilic inflammatory disorders. J Biol Chem 274, 25933–25944.
Gaut JP, Byun J, Tran HD, Lauber WM, Carroll JA, Hotchkiss RS, Belaaouaj A & Heinecke JW (2013) Myeloperoxidase produces nitrating oxidants in vivo. J Clin Invest 109, 1311–1319.
Radi R (2013) Protein tyrosine nitration: biochemical mechanisms and structural basis of functional effects. Acc Chem Res 46, 550–559.
Radi R (2018) Oxygen radicals, nitric oxide, and peroxynitrite: redox pathways in molecular medicine. Proc Natl Acad Sci USA 115, 5839–5848.
Parastatidis I, Thomson L, Burke A, Chernysh I, Nagaswami C, Visser J, Stamer S, Liebler DC, Koliakos G, Heijnen HF et al. (2008) Fibrinogen beta‐chain tyrosine nitration is a prothrombotic risk factor. J Biol Chem 283, 33846–33853.
Heffron SP, Parastatidis I, Cuchel M, Wolfe ML, Tadesse MG, Mohler ER 3rd, Ischiropoulos H, Rader DJ & Reilly MP (2009) Inflammation induces fibrinogen nitration in experimental human endotoxemia. Free Radic Biol Med 47, 1140–1146.
Medeiros R, Sousa B, Rossi S, Afonso C, Bonino L, Pitt A, López E, Spickett C & Borthagaray G (2021) Identification and relative quantification of 3‐nitrotyrosine residues in fibrinogen nitrated in vitro and fibrinogen from ischemic stroke patient plasma using LC‐MS/MS. Free Radic Biol Med 165, 334–347.
Griswold‐Prenner I, Kashyap AK, Mazhar S, Hall ZW, Fazelinia H & Ischiropoulos H (2023) Unveiling the human nitroproteome: protein tyrosine nitration in cell signaling and cancer. J Biol Chem 299, 105038.
Blomback B, Blomback M, Finkbeiner W, Holmgren A, Kowalska‐Loth B & Olovson G (1974) Enzymatic reduction of disulfide bonds in fibrin‐ogen by the thioredoxin system. I. identification of reduced bonds and studies on reoxidation process. Thromb Res 4, 55–75.
Butera D & Hogg PJ (2020) Fibrinogen function achieved through multiple covalent states. Nat Commun 11, 5468.
Hoffman M (2008) Alterations of fibrinogen structure in human disease. Cardiovasc Hematol Agents Med Chem 6, 206–211.
Pieters M, van Zyl DG, Rheeder P, Jerling JC, Loots du T, van der Westhuizen FH, Gottsche LT & Weisel JW (2007) Glycation of fibrinogen in uncontrolled diabetic patients and the effects of glycaemic control on fibrinogen glycation. Thromb Res 120, 439–446.
Hammer MR, John PN, Flynn MD, Bellingham AJ & Leslie RD (1989) Glycated fibrinogen: a new index of short‐term diabetic control. Ann Clin Biochem 26, 58–62.
Jörneskog G, Egberg N, Fagrell B, Fatah K, Hessel B, Johnsson H, Brismar K & Blombäck M (1996) Altered properties of the fibrin gel structure in patients with IDDM. Diabetologia 39, 1519–1523.
Svensson J, Bergman AC, Adamson U, Blombäck M, Wallén H & Jörneskog G (2012) Acetylation and glycation of fibrinogen in vitro occur at specific lysine residues in a concentration dependent manner: a mass spectrometric and isotope labeling study. Biochem Biophys Res Commun 421, 335–342.
Bryk AH, Zettl K, Wiśniewski JR & Undas A (2021) Glycation and acetylation sites on fibrinogen in plasma fibrin clot of patients with type 2 diabetes: effects of low‐dose acetylsalicylic acid. Thromb Res 198, 93–98.
de Vries JJ, Snoek CJM, Rijken DC & de Maat MPM (2020) Effects of post‐translational modifications of fibrinogen on clot formation, clot structure, and fibrinolysis: a systematic review. Arterioscler Thromb Vasc Biol 40, 554–569.
Henschen‐Edman AH (2001) Fibrinogen non‐inherited heterogeneity and its relationship to function in health and disease. Ann N Y Acad Sci 936, 580–593.
Dunn EJ, Philippou H, Ariëns RA & Grant PJ (2006) Molecular mechanisms involved in the resistance of fibrin to clot lysis by plasmin in subjects with type 2 diabetes mellitus. Diabetologia 49, 1071–1080.
Undas A & Ariëns RA (2011) Fibrin clot structure and function: a role in the pathophysiology of arterial and venous thromboembolic diseases. Arterioscler Thromb Vasc Biol 31, e88–e99.
Ajjan RA, Standeven KF, Khanbhai M, Phoenix F, Gersh KC, Weisel JW, Kearney MT, Ariëns RA & Grant PJ (2009) Effects of aspirin on clot structure and fibrinolysis using a novel in vitro cellular system. Arterioscler Thromb Vasc Biol 29, 712–717.
Williams S, Fatah K, Ivert T & Blombäck M (1995) The effect of acetylsalicylic acid on fibrin gel lysis by tissue plasminogen activator. Blood Coagul Fibrinolysis 6, 718–725.
Undas A, Brummel‐Ziedins K & Mann KG (2014) Why does aspirin decrease the risk of venous thromboembolism? On old and novel antithrombotic effects of acetyl salicylic acid. J Thromb Haemost 12, 1776–1787.
Lauricella AM, Quintana IL & Kordich LC (2002) Effects of homocysteine thiol group on fibrin networks: another possible mechanism of harm. Thromb Res 15, 75–79.
Sauls DL, Wolberg AS & Hoffman M (2003) Elevated plasma homocysteine leads to alterations in fibrin clot structure and stability: implications for the mechanism of thrombosis in hyperhomocysteinemia. J Thromb Haemost 1, 300–306.
Sikora M, Marczak Ł, Kubalska J, Graban A & Jakubowski H (2014) Identification of N‐homocysteinylation sites in plasma proteins. Amino Acids 46, 235–244.
Lentz SR (1998) Mechanisms of thrombosis in hyperhomocysteinemia. Curr Opin Hematol 5, 343–349.
Aronow WS, Ahn C & Gutstein H (2000) Increased plasma homocysteine is an independent predictor of new atherothrombotic brain infarction in older persons. Am J Cardiol 86, 585–586.
Sauls DL, Lockhart E, Warren ME, Lenkowski A, Wilhelm SE & Hoffman M (2006) Modification of fibrinogen by homocysteine thiolactone increases resistance to fibrinolysis: a potential mechanism of the thrombotic tendency in hyperhomocysteinemia. Biochemistry 45, 2480–2487.
Sauls DL, Warren M & Hoffman M (2011) Homocysteinylated fibrinogen forms disulfide‐linked complexes with albumin. Thromb Res 27, 576–581.
Jakubowski H (1997) Metabolism of homocysteine thiolactone in human cell cultures. Possible mechanism for pathological consequences of elevated homocysteine levels. J Biol Chem 272, 1935–1942.
Jakubowski H (1999) Protein homocysteinylation: possible mechanism underlying pathological consequences of elevated homocysteine levels. FASEB J 13, 2277–2283.
Jakubowski H (2000) Homocysteine thiolactone: metabolic origin and protein homocysteinylation in humans. J Nutr 130, 377S–381S.
Genoud V, Lauricella AM, Kordich LC & Quintana I (2014) Impact of homocysteine‐thiolactone on plasma fibrin networks. J Thromb Thrombolysis 38, 540–545.
Marchi R, Carvajal Z & Weisel JW (2008) Comparison of the effect of different homocysteine concentrations on clot formation using human plasma and purified fibrinogen. Thromb Haemost 99, 451–452.
Townsend RR, Hilliker E, Li YT, Laine RA, Bell WR & Lee YC (1982) Carbohydrate structure of human fibrinogen. Use of 300‐MHz 1H‐NMR to characterize glycosidase‐treated glycopeptides. J Biol Chem 257, 9704–9710.
Brennan SO (2015) Variation of fibrinogen oligosaccharide structure in the acute phase response: possible haemorrhagic implications. BBA Clin 3, 221–226.
Langer BG, Weisel JW, Dinauer PA, Nagaswami C & Bell WR (1988) Deglycosylation of fibrinogen accelerates polymerization and increases lateral aggregation of fibrin fibers. J Biol Chem 263, 15056–15063.
Martinez J, Palascak JE & Kwasniak D (1978) Abnormal sialic acid content of the dysfibrinogenemia associated with liver disease. J Clin Invest 61, 535–538.
Lisman T & Ariëns RA (2016) Alterations in fibrin structure in patients with liver diseases. Semin Thromb Hemost 42, 389–396.
Martinez J, MacDonald KA & Palascak JE (1983) The role of sialic acid in the dysfibrinogenemia associated with liver disease: distribution of sialic acid on the constituent chains. Blood 61, 1196–1202.
Brownlee M, Vlassara H & Cerami A (1983) Nonenzymatic glycosylation reduces the susceptibility of fibrin to degradation by plasmin. Diabetes 32, 680–684.
Nakayama‐Hamada M, Suzuki A, Furukawa H, Yamada R & Yamamoto K (2008) Citrullinated fibrinogen inhibits thrombin‐catalysed fibrin polymerization. J Biochem 144, 393–398.
Damiana T, Damgaard D, Sidelmann JJ, Nielsen CH, de Maat MPM, Münster AB & Palarasah Y (2020) Citrullination of fibrinogen by peptidylarginine deiminase 2 impairs fibrin clot structure. Clin Chim Acta 501, 6–11.
Nakayama‐Hamada M, Suzuki A, Kubota K, Takazawa T, Ohsaka M, Kawaida R, Ono M, Kasuya A, Furukawa H, Yamada R et al. (2005) Comparison of enzymatic properties between hPADI2 and hPADI4. Biochem Biophys Res Commun 327, 192–200.
Geer CB, Stasko NA, Rus IA, Lord ST & Schoenfisch MH (2008) Influence of glutathione and its derivatives on fibrin polymerization. Biomacromolecules 9, 1876–1882.
Akhter S, Vignini A, Wen Z, English A, Wang PG & Mutus B (2002) Evidence for S‐nitrosothiol‐dependent changes in fibrinogen that do not involve transnitrosation or thiolation. Proc Natl Acad Sci USA 99, 9172–9177.
Sovova Z, Suttnar J & Dyr JE (2020) Molecular dynamic simulations suggest that metabolite‐induced post‐translational modifications alter the behavior of the fibrinogen coiled‐coil domain. Metabolites 11, 307.