Evidence that fibrinogen γ′ directly interferes with protofibril growth: Implications for fibrin structure and clot stiffness

Journal of Thrombosis and Haemostasis

Volumn 10, Issue 6, 2012, Pages 1072-1080

  Allan, P ^a   Uitte de Willige, S ^a   Abou Saleh, R H ^a   Connell, S D ^a   Ariens R A S ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Clot rheology; Fibrin structure; Fibrinogen; FXIII; Splice variation; Thrombin

Indexed keywords

FIBRINOGEN; FIBRINOGEN GAMMA'; TRANSCRIPTION FACTOR IIIA; UNCLASSIFIED DRUG;

ANION EXCHANGE CHROMATOGRAPHY; ARTICLE; ATOMIC FORCE MICROSCOPY; BLOOD CLOTTING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CROSS LINKING; FIBRIN FORMATION; FLOW MEASUREMENT; MAGNETIC MICRORHEOMETRY; MOLECULAR MECHANICS; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTOFIBRIL FORMATION; SCANNING ELECTRON MICROSCOPY; TURBIDITY; VISCOELASTICITY;

ALTERNATIVE SPLICING; BLOOD COAGULATION; BLOOD COAGULATION TESTS; CHROMATOGRAPHY, ION EXCHANGE; ELASTICITY; FACTOR XIIIA; FIBRIN; FIBRINOGENS, ABNORMAL; HUMANS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; NEPHELOMETRY AND TURBIDIMETRY; POLYMERIZATION; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; TIME FACTORS; VISCOSITY;

EID: 84861707362     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2012.04717.x     Document Type: Article

References (36)

1. Henschen A, Lottspeich F, Kehl M, Southan C. Covalent structure of fibrinogen. Ann NY Acad Sci 1983; 408: 28-43.
2. Chung DW, Davie EW. Gamma and γ' chains of human fibrinogen are produced by alternative mRNA processing. Biochemistry 1984; 23: 4232-6.
3. Wolfenstein-Todel C, Mosesson MW. Carboxy-terminal amino acid sequence of a human fibrinogen γ-chain variant (γ'). Biochemistry 1981; 20: 6146-9.
4. Mosesson MW, Finlayson JS. Subfractions of human fibrinogen; preparation and analysis. J Lab Clin Med 1963; 62: 663-74.
5. Mosesson MW, Finlayson JS, Umfleet RA. Human fibrinogen heterogeneities: 3. Identification of chain variants. J Biol Chem 1972; 247: 5223-7.
6. Uitte de Willige S, Standeven KF, Philippou H, Ariëns RAS. The pleiotropic role of the fibrinogen gamma' chain in hemostasis. Blood 2009; 114: 3994-4001.
7. Lovely RS, Falls LA, Al-Mondhiry HA, Chambers CE, Sexton GJ, Ni H, Farrell DH. Association of γA/γ' Fibrinogen Levels and Coronary Artery Disease. Thromb Haemost 2002; 88: 26-31.
8. Mannila MN, Lovely RS, Kazmierczak SC, Eriksson P, Samnegård A, Farrell DH, Hamsten A, Silveira A. Elevated plasma fibrinogen gamma' concentration is associated with myocardial infarction: effects of variation in fibrinogen genes and environmental factors. J Thromb Haemost 2007; 5: 766-73.
9. Cheung EY, Uitte de Willige S, Vos HL, Leebeek FW, Dippel DW, Bertina RM, De Maat MP. Fibrinogen gamma' in ischemic stroke: a case-control study. Stroke 2008; 39: 1033-5.
10. Uitte de Willige S, De Visser MCH, Houwing-Duistermaat JJ, Rosendaal FR, Vos HL, Bertina RM. Genetic variation in the fibrinogen gamma gene increases the risk for deep venous thrombosis by reducing plasma fibrinogen gamma' levels. Blood 2005; 106: 4176-83.
11. Mosesson M, Hernandez I, Raife T, Medved L, Yakovlev S, Simpson-Haidaris P. Plasma fibrinogen gamma prime chain content in the thrombotic microangiopathy syndrome. J Thromb Haemost 2007; 5: 62-9.
12. Siebenlist KR, Mosesson MW, Hernandez I, Bush LA, Di Cera E, Shainoff JR, Di Orio JP, Stojanovic L. Studies on the basis for the properties of fibrin produced from fibrinogen-containing gamma' chains. Blood 2005; 106: 2730-6.
13. Cooper AV, Standeven KF, Ariëns RAS. Fibrinogen gamma-chain splice variant gamma' alters fibrin formation and structure. Blood 2003; 102: 535-40.
14. Gersh KC, Nagaswami C, Weisel JW, Lord ST. The presence of γ' chain impairs fibrin polymerization. Thromb Res 2009; 124: 356-63.
15. Collet JP, Nagaswami C, Farrell DH, Montalescot G, Weisel JW. Influence of gamma' fibrinogen splice variant on fibrin physical properties and fibrinolysis rate. Arterioscler Thromb Vasc Biol 2004; 24: 382-6.
16. Falls LA, Farrell DH. Resistance of γA/γ' fibrin clots to fibrinolysis. J Biol Chem 1997; 272: 14251-6.
17. Moaddel M, Farrell DH, Daugherty MA, Fried MG. Interactions of human fibrinogens with factor XIII: roles of calcium and the γ' peptide. Biochemistry 2000; 39: 6698-705.
18. Moaddel M, Falls LA, Farrell DH. The role of γA/γ' fibrinogen in plasma factor XIII activation. J Biol Chem 2000; 275: 32135-40.
19. Meh DA, Siebenlist KR, Mosesson MW. Identification and characterization of the thrombin binding sites on fibrin. J Biol Chem 1996; 271: 23121-5.
20. Lovely RS, Moaddel M, Farrell DH. Fibrinogen γ' chain binds thrombin exosite II. J Thromb Haemost 2003; 1: 124-31.
21. Meh DA, Siebenlist KR, Brennan SO, Holyst T, Mosesson MW. The amino acid sequence in fibrin responsible for high affinity thrombin binding. Thromb Haemost 2001; 85: 470-4.
22. Siebenlist KR, Meh DA, Mosesson MW. Plasma factor XIII binds specifically to fibrinogen molecules containing γ' chains. Biochemistry 1996; 35: 10448-53.
23. Kazama M, McDonagh J, Wagner RH, Langdell RD, McDonagh RP. Purification and immunochemical characterization of human plasma factor XIII. Pathophysiol Haemost Thromb 1976; 5: 329-40.
24. Gersh KC, Lord ST. An investigation of Factor XIII binding to recombinant γ'/γ' and γA/γ' fibrinogen. Blood 2006; 108: 1705. [abstract].
25. Standeven KF, Carter AM, Grant PJ, Weisel JW, Chernysh I, Masova L, Lord ST, Ariëns 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.
26. Mihalyi E. Physicochemical studies of bovine fibrinogen. IV. Ultraviolet absorption and its relation to the structure of the molecule. Biochemistry 1968; 7: 208-23.
27. 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: 111-28.
28. Abou-Saleh RH, Connell SD, Harrand R, Ajjan RA, Mosesson MW, Smith DA, Grant PJ, Ariëns RA. Nanoscale probing reveals that reduced stiffness of clots from fibrinogen lacking 42N-terminal Bbeta-chain residues is due to the formation of abnormal oligomers. Biophys J 2009; 96: 2415-27.
29. Billingsley DJ, Kirkham J, Bonass WA, Thomson NH. Atomic force microscopy of DNA at high humidity: irreversible conformational switching of supercoiled molecules. Phys Chem Chem Phys 2010; 12: 14727-34.
30. 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, Ariëns RA. Common variation in the C-terminal region of the fibrinogen-chain: effects on fibrin structure, fibrinolysis and clot rigidity. Blood 2008; 111: 643-50.
31. Evans RML, Tassieri M, Auhl D, Waigh TA. Direct conversion of rheological compliance measurements into storage and loss moduli. Phys Rev E 2009; 80: 012501.
32. Chernysh IN, Weisel JW. Dynamic imaging of fibrin network formation correlated with other measures of polymerization. Blood 2008; 111: 4854-61.
33. Jones RAL. Soft Condensed Matter. USA: Oxford University Press, 2002.
34. Ryan EA, Mockros LF, Weisel JW, Lorand L. Structural origins of fibrin clot rheology. Biophys J 1999; 77: 2813-26.
35. Medved L, Nieuwenhuizen W. Molecular mechanisms of initiation of fibrinolysis by fibrin. Thromb Haemost 2003; 89: 409-19.
36. Litvinov RI, Gorkun OV, Owen SF, Shuman H, Weisel JW. Polymerization of fibrin: specificity, strength, and stability of knob-hole interactions studied at the single-molecule level. Blood 2005; 106: 2944-51.