Determinants of fibrin formation, structure, and function

Current Opinion in Hematology

Volumn 19, Issue 5, 2012, Pages 349-356

  Wolberg, Alisa S ^a  

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

Author keywords

fibrinogen; hemostasis; infection; inflammation; thrombosis

Indexed keywords

BETA2 INTEGRIN; BLOOD CLOTTING FACTOR 12; BLOOD CLOTTING FACTOR 13; CD11B ANTIGEN; CD18 ANTIGEN; D DIMER; FIBRIN; FIBRINOGEN; FIBRONECTIN; HEPARIN BINDING PROTEIN; IMMUNOGLOBULIN; INTEGRIN; INTERLEUKIN 6; MICRORNA; PLASMIN; STAT3 PROTEIN; THROMBIN; VON WILLEBRAND FACTOR;

AFIBRINOGENEMIA; BLOOD CLOTTING; BLOOD CLOTTING DISORDER; BLOOD VESSEL INJURY; CELLULAR IMMUNITY; COGNITIVE DEFECT; DYSFIBRINOGENEMIA; FIBRIN FORMATION; FIBRIN FUNCTION; FIBRIN STRUCTURE; FIBRINOLYSIS; GENE EXPRESSION REGULATION; HEMOSTASIS; HUMAN; HYPOFIBRINOGENEMIA; INFECTION; INFLAMMATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; THROMBOSIS; WOUND HEALING;

BLOOD COAGULATION; FIBRIN; FIBRINOGEN; HOMEOSTASIS; HUMANS;

EID: 84865444722     PISSN: 10656251     EISSN: 15317048     Source Type: Journal    
DOI: 10.1097/MOH.0b013e32835673c2     Document Type: Review

References (90)

1. de Maat MP, Verschuur M. Fibrinogen heterogeneity: inherited and noninherited. Curr Opin Hematol 2005; 12:377-383. (Pubitemid 41284972)
2. Farrell DH, Thiagarajan P, Chung DW, Davie EW. Role of fibrinogen alpha and gamma chain sites in platelet aggregation. Proc Natl Acad Sci USA 1992; 89:10729-10732.
3. Farrell DH, Thiagarajan P. Binding of recombinant fibrinogen mutants to platelets. J Biol Chem 1994; 269:226-231. (Pubitemid 24026648)
4. Meh DA, Siebenlist KR, Brennan SO, et al. The amino acid sequence in fibrin responsible for high affinity thrombin binding. Thromb Haemost 2001; 85:470-474. (Pubitemid 32233021)
5. Meh DA, Siebenlist KR, Mosesson MW. Identification and characterization of the thrombin binding sites on fibrin. J Biol Chem 1996; 271:23121-23125. (Pubitemid 26314747)
6. Uitte de Willige S, Standeven KF, Philippou H, Ariens RA. The pleiotropic role of the fibrinogen gamma' chain in hemostasis. Blood 2009; 114:3994-4001.
7. Wilhelmsen L, Svardsudd K, Korsan-Bengsten K, et al. Fibrinogen as a risk factor for stroke and myocardial infarction. N Engl J Med 1984; 311:501-505. (Pubitemid 14059351)
8. Kannel WB, Wolf PA, Castelli WP, D'Agostino RB. Fibrinogen and risk of cardiovascular disease. The Framingham Study. JAMA 1987; 258:1183-1186.
9. Kamphuisen PW, Eikenboom JC, Vos HL, et al. Increased levels of factor VIII and fibrinogen in patients with venous thrombosis are not caused by acute phase reactions. Thromb Haemost 1999; 81:680-683. (Pubitemid 29216549)
10. Danesh J, Lewington S, Thompson SG, et al. Plasma fibrinogen level and the risk of major cardiovascular diseases and nonvascular mortality: an individual participant meta-analysis. JAMA 2005; 294:1799-1809. (Pubitemid 41434626)
11. Lovely RS, Falls LA, Al-Mondhiry HA, et al. Association of gammaA/gamma' fibrinogen levels and coronary artery disease. Thromb Haemost 2002; 88:26-31. (Pubitemid 34752262)
12. Uitte de Willige S, de Visser MC, Houwing-Duistermaat JJ, et al. Genetic variation in the fibrinogen gamma gene increases the risk for deep venous thrombosis by reducing plasma fibrinogen gamma' levels. Blood 2005; 106:4176-4183. (Pubitemid 41775924)
13. Mannila MN, Lovely RS, Kazmierczak SC, et al. Elevated plasma fibrinogen gamma' concentration is associated with myocardial infarction: effects of variation in fibrinogen genes and environmental factors. J Thromb Haemost 2007; 5:766-773. (Pubitemid 46563576)
14. Dalmon J, Laurent M, Courtois G. The human beta fibrinogen promoter contains a hepatocyte nuclear factor 1-dependent interleukin-6-responsive element. Mol Cell Biol 1993; 13:1183-1193. (Pubitemid 23040285)
15. Huber P, Laurent M, Dalmon J. Human beta-fibrinogen gene expression. Upstream sequences involved in its tissue specific expression and its dexamethasone and interleukin 6 stimulation. J Biol Chem 1990; 265:5695-5701.
16. Otto JM, Grenett HE, Fuller GM. The coordinated regulation of fibrinogen gene transcription by hepatocyte-stimulating factor and dexamethasone. J Cell Biol 1987; 105:1067-1072. (Pubitemid 18029832)
17. Fort A, Borel C, Migliavacca E, et al. Regulation of fibrinogen production by microRNAs. Blood 2010; 116:2608-2615.
18. Brock M, Trenkmann M, Gay RE, et al. MicroRNA-18a enhances the interleukin-6-mediated production of the acute-phase proteins fibrinogen and haptoglobin in human hepatocytes. J Biol Chem 2011; 286:40142-40150.
19. Lord ST. Molecular mechanisms affecting fibrin structure and stability. Arterioscler Thromb Vasc Biol 2011; 31:494-499.
20. Weisel JW. Fibrinogen and fibrin. Adv Protein Chem 2005; 70:247-299. (Pubitemid 40544785)
21. Chernysh IN, Nagaswami C, Weisel JW. Visualization and identification of the structures formed during early stages of fibrin polymerization. Blood 2011; 117:4609-4614.
22. Riedel T, Suttnar J, Brynda E, et al. Fibrinopeptides A and B release in the process of surface fibrin formation. Blood 2011; 117:1700-1706.
23. Nair CH, Shah GA, Dhall DP. Effect of temperature, pH and ionic strength and composition on fibrin network structure and its development. Thromb Res 1986; 42:809-816. (Pubitemid 16019838)
24. Blomback B, Carlsson K, Fatah K, et al. Fibrin in human plasma: gel architectures governed by rate and nature of fibrinogen activation. Thromb Res 1994; 75:521-538. (Pubitemid 24267336)
25. Ryan EA, Mockros LF, Weisel JW, Lorand L. Structural origins of fibrin clot rheology. Biophys J 1999; 77:2813-2826. (Pubitemid 29519524)
26. Glover CJ, McIntire LV, Brown CH 3rd, Natelson EA. Rheological properties of fibrin clots. Effects of fibrinogen concentration, factor XIII deficiency, and factor XIII inhibition. J Lab Clin Med 1975; 86:644-656.
27. Machlus KR, Cardenas JC, Church FC, Wolberg AS. Causal relationship between hyperfibrinogenemia, thrombosis, and resistance to thrombolysis in mice. Blood 2011; 117:4953-4963.
28. Francis CW, Marder VJ. Increased resistance to plasmic degradation of fibrin with highly crosslinked alpha-polymer chains formed at high factor-XIII concentrations. Blood 1988; 71:1361-1365.
29. Wolberg AS, Gabriel DA, Hoffman M. Analyzing fibrin clot structure using a microplate reader. Blood Coagul Fibrin 2002; 13:533-539.
30. Campbell RA, Aleman MM, Gray LD, et al. Flow profoundly influences fibrin network structure: implications for fibrin formation and clot stability in hemostasis. Thromb Haemost 2010; 104:1281-1284.
31. Gersh KC, Edmondson KE, Weisel JW. Flow rate and fibrin fiber alignment. J Thromb Haemost 2010; 8:2826-2828.
32. Bornikova L, Peyvandi F, Allen G, et al. Fibrinogen replacement therapy for congenital fibrinogen deficiency. J Thromb Haemost 2011; 9:1687-1704.
33. Lindahl B, Toss H, Siegbahn A, et al. Markers of myocardial damage and inflammation in relation to long-term mortality in unstable coronary artery disease. FRISC Study Group. Fragmin during Instability in Coronary Artery Disease. N Engl J Med 2000; 343:1139-1147.
34. Carrell N, Gabriel DA, Blatt PM, et al. Hereditary dysfibrinogenemia in a patient with thrombotic disease. Blood 1983; 62:439-447. (Pubitemid 13036097)
35. Collet J-P, Soria J, Mirshahi M, et al. Dusart syndrome: a new concept of the relationship between fibrin clot architecture and fibrin clot degradability: hypofibrinolysis related to an abnormal clot structure. Blood 1993; 82:2462-2469. (Pubitemid 23304270)
36. Tarumi T, Martincic D, Thomas A, et al. Familial thrombophilia associated with fibrinogen Paris V: Dusart syndrome. Blood 2000; 96:1191-1193. (Pubitemid 30616895)
37. Wada Y, Lord ST. A correlation between thrombotic disease and a specific fibrinogen abnormality (A alpha 554 Arg->Cys) in two unrelated kindred, Dusart and Chapel Hill III. Blood 1994; 84:3709-3714. (Pubitemid 24362467)
38. Koopman J, Haverkate F, Briet E, Lord ST. A congenitally abnormal fibrinogen (Vlissingen) with a 6-base deletion in the gamma-chain gene, causing defective calcium binding and impaired fibrin polymerization. J Biol Chem 1991; 266:13456-13461. (Pubitemid 21907366)
39. Marchi R, Lundberg U, Grimbergen J, et al. Fibrinogen Caracas V, an abnormal fibrinogen with an Aalpha 532 Ser->Cys substitution associated with thrombosis. Thromb Haemost 2000; 84:263-270. (Pubitemid 30601473)
40. Haverkate F, Samama M. Familial dysfibrinogenemia and thrombophilia. Report on a study of the SSC Subcommittee on Fibrinogen. Thromb Haemost 1995; 73:151-161.
41. Mosesson MW. Update on antithrombin I (fibrin). Thromb Haemost 2007; 98:105-108. (Pubitemid 47074184)
42. Pospisil CH, Stafford AR, Fredenburgh JC, Weitz JI. Evidence that both exosites on thrombin participate in its high affinity interaction with fibrin. J Biol Chem 2003; 278:21584-21591. (Pubitemid 36792557)
43. Fredenburgh JC, Stafford AR, Leslie BA, Weitz JI. Bivalent binding to gammaA/gamma'-fibrin engages both exosites of thrombin and protects it from inhibition by the antithrombin-heparin complex. J Biol Chem 2008; 283:2470-2477.
44. Pan CP, Shi Y, Amin K, et al. Wound healing monitoring using near infrared fluorescent fibrinogen. Biomed Opt Express 2010; 1:285-294.
45. Kerlin B, Cooley BC, Isermann BH, et al. Cause-effect relation between hyperfibrinogenemia and vascular disease. Blood 2004; 103:1728-1734. (Pubitemid 38268965)
46. Gulledge AA, Rezaee F, Verheijen JH, Lord ST. A novel transgenic mouse model of hyperfibrinogenemia. Thromb Haemost 2001; 86:511-516. (Pubitemid 32746937)
47. Holmback K, Danton MJ, Suh TT, et al. Impaired platelet aggregation and sustained bleeding in mice lacking the fibrinogen motif bound by integrin alpha IIb beta 3. EMBO J 1996; 15:5760-5771. (Pubitemid 26375497)
48. MosessonMW, Cooley BC, Hernandez I, et al. Thrombosis risk modification in transgenic mice containing the human fibrinogen thrombin-binding gamma' chain sequence. J Thromb Haemost 2009; 7:102-110.
49. Cheung EY, Vos HL, Kruip MJ, et al. Elevated fibrinogen gamma' ratio is associated with cardiovascular diseases and acute phase reaction but not with clinical outcome. Blood 2009; 114:4603-4604.
50. van den Herik EG, Cheung EY, de Lau LM, et al. gamma'/total fibrinogen ratio is associated with short-term outcome in ischaemic stroke. Thromb Haemost 2011; 105:430-434.
51. Alexander KS, Madden TE, Farrell DH. Association between gamma' fibrinogen levels and inflammation. Thromb Haemost 2011; 105:605-609.
52. Lovely RS, Yang Q, Massaro JM, et al. Assessment of genetic determinants of the association of gamma' fibrinogen in relation to cardiovascular disease. Arterioscler Thromb Vasc Biol 2011; 31:2345-2352.
53. Cheung EY, Uitte de Willige S, Vos HL, et al. Fibrinogen gamma' in ischemic stroke: a case-control study. Stroke 2008; 39:1033-1035. (Pubitemid 351619556)
54. Mosesson MW, Hernandez I, Raife TJ, et al. Plasma fibrinogen gamma' chain content in the thrombotic microangiopathy syndrome. J Thromb Haemost 2007; 5:62-69. (Pubitemid 44921068)
55. Hoffman M. Alterations of fibrinogen structure in human disease. Cardiovasc Hematol Agents Med Chem 2008; 6:206-211.
56. Sauls DL, Wolberg AS, Hoffman M. Elevated plasma homocysteine leads to alterations in fibrin clot structure and stability: implications for the mechanism of thrombosis in hyperhomocysteinemia. J Thromb Haemost 2003; 1:300-306.
57. Sauls DL, Warren M, Hoffman M. Homocysteinylated fibrinogen forms disulfide-linked complexes with albumin. Thromb Res 2011; 127:576-581.
58. Dunn EJ, Ariens RA, Grant PJ. The influence of type 2 diabetes on fibrin structure and function. Diabetologia 2005; 48:1198-1206. (Pubitemid 40909657)
59. Dunn EJ, Philippou H, Ariens RA, Grant PJ. Molecular mechanisms involved in the resistance of fibrin to clot lysis by plasmin in subjects with type 2 diabetes mellitus. Diabetologia 2006; 49:1071-1080.
60. da Costa G, Gomes RA, Guerreiro A, et al. Beyond genetic factors in familial amyloidotic polyneuropathy: protein glycation and the loss of fibrinogen's chaperone activity. PLoS One 2011; 6:e24850.
61. Tang H, Fu Y, Cui Y, et al. Fibrinogen has chaperone-like activity. Biochem Biophys Res Commun 2009; 378:662-667.
62. Tang H, Fu Y, Zhan S, Luo Y. Alpha(E)C, the C-terminal extension of fibrinogen, has chaperone-like activity. Biochemistry 2009; 48:3967-3976.
63. Smith KA, Adamson PJ, Pease RJ, et al. Interactions between factor XIII and the alphaC region of fibrinogen. Blood 2011; 117:3460-3468.
64. Vu TT, Stafford AR, Leslie BA, et al. Histidine-rich glycoprotein binds fibrin(ogen) with high affinity and competes with thrombin for binding to the gamma'-chain. J Biol Chem 2011; 286:30314-30323.
65. Tsuchida-Straeten N, Ensslen S, Schafer C, et al. Enhanced blood coagulation and fibrinolysis in mice lacking histidine-rich glycoprotein (HRG). J Thromb Haemost 2005; 3:865-872. (Pubitemid 41632812)
66. Renne T, Pozgajova M, Gruner S, et al. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med 2005; 202:271-281. (Pubitemid 41043823)
67. Konings J, Govers-Riemslag JW, Philippou H, et al. Factor XIIa regulates the structure of the fibrin clot independently of thrombin generation through direct interaction with fibrin. Blood 2011; 118:3942-3951.
68. Ahn HJ, Zamolodchikov D, Cortes-Canteli M, et al. Alzheimer's disease peptide beta-amyloid interacts with fibrinogen and induces its oligomerization. Proc Natl Acad Sci USA 2010; 107:21812-21817.
69. Cortes-Canteli M, Paul J, Norris EH, et al. Fibrinogen and beta-amyloid association alters thrombosis and fibrinolysis: a possible contributing factor to Alzheimer's disease. Neuron 2010; 66:695-709.
70. Zamolodchikov D, Strickland S. Abeta delays fibrin clot lysis by altering fibrin structure and attenuating plasminogen binding to fibrin. Blood 2012; 119:3342-3351.
71. de la Torre JC. Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol 2004; 3:184-190. (Pubitemid 38232669)
72. Smith SA, Mutch NJ, Baskar D, et al. Polyphosphate modulates blood coagulation and fibrinolysis. Proc Natl Acad Sci USA 2006; 103:903-908. (Pubitemid 43212194)
73. Muller F, Mutch NJ, Schenk WA, et al. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 2009; 139:1143-1156.
74. Choi SH, Smith SA, Morrissey JH. Polyphosphate is a cofactor for the activation of factor XI by thrombin. Blood 2011; 118:6963-6970.
75. Smith SA, Morrissey JH. Polyphosphate enhances fibrin clot structure. Blood 2008; 112:2810-2816.
76. Mutch NJ, Engel R, Uitte de Willige S, et al. Polyphosphate modifies the fibrin network and down-regulates fibrinolysis by attenuating binding of tPA and plasminogen to fibrin. Blood 2010; 115:3980-3988.
77. Herwald H, Cramer H, Morgelin M, et al. M protein, a classical bacterial virulence determinant, forms complexes with fibrinogen that induce vascular leakage. Cell 2004; 116:367-379. (Pubitemid 38366314)
78. Macheboeuf P, Buffalo C, Fu CY, et al. Streptococcal M1 protein constructs a pathological host fibrinogen network. Nature 2011; 472:64-68.
79. Collet JP, Montalescot G, Lesty C, et al. Effects of abciximab on the architecture of platelet-rich clots in patients with acute myocardial infarction undergoing primary coronary intervention. Circulation 2001; 103:2328-2331. (Pubitemid 32448794)
80. Collet JP, Montalescot G, Lesty C, et al. Disaggregation of in vitro preformed platelet-rich clots by abciximab increases fibrin exposure and promotes fibrinolysis. Arterioscler Thromb Vasc Biol 2001; 21:142-148. (Pubitemid 32061939)
81. Collet JP, Montalescot G, Lesty C, Weisel JW. A structural and dynamic investigation of the facilitating effect of glycoprotein IIb/IIIa inhibitors in dissolving platelet-rich clots. Circ Res 2002; 90:428-434. (Pubitemid 34633912)
82. Jerome WG, Handt S, Hantgan RR. Endothelial cells organize fibrin clots into structures that are more resistant to lysis. Microsc Microanal 2005; 11:268-277. (Pubitemid 40870196)
83. Campbell RA, Overmyer KA, Bagnell CR, Wolberg AS. Cellular procoagulant activities dictate clot structure and stability as a function of distance from the cell surface. Arter Thromb Vasc Biol 2008; 28:2247-2254.
84. Campbell RA, Overmyer KA, Selzman CH, et al. Contributions of extravascular and intravascular cells to fibrin network formation, structure, and stability. Blood 2009; 114:4886-4896.
85. Aleman MM, Gardiner C, Harrison P, Wolberg AS. Unique contributions of monocyte-and platelet-derived microparticles to thrombin generation and fibrin formation and stability. J Thromb Haemost 2011; 9:2251-2261.
86. Wu X, Helfrich MH, Horton MA, et al. Fibrinogen mediates platelet-polymorphonuclear leukocyte cooperation during immune-complex glomerulonephritis in rats. J Clin Invest 1994; 94:928-936. (Pubitemid 24286432)
87. Ugarova TP, Lishko VK, Podolnikova NP, et al. Sequence gamma 377-395(P2), but not gamma 190-202(P1), is the binding site for the alpha MI-domain of integrin alpha M beta 2 in the gamma C-domain of fibrinogen. Biochemistry 2003; 42:9365-9373. (Pubitemid 36959244)
88. Flick MJ, Du X, Degen JL. Fibrin(ogen)-alpha M beta 2 interactions regulate leukocyte function and innate immunity in vivo. Exp Biol Med (Maywood) 2004; 229:1105-1110. (Pubitemid 39602252)
89. Flick MJ, Du X, Witte DP, et al. Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest 2004; 113:1596-1606. (Pubitemid 39071683)
90. Steinbrecher KA, Horowitz NA, Blevins EA, et al. Colitis-associated cancer is dependent on the interplay between the hemostatic and inflammatory systems and supported by integrin alpha(M)beta(2) engagement of fibrinogen. Cancer Res 2010; 70:2634-2643.