Targeting the coagulation factor fibrinogen for arthritis therapy

Current Pharmaceutical Biotechnology

Volumn 12, Issue 9, 2011, Pages 1497-1506

  Raghu, Harini ^a   Flick, Matthew J ^a  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

Author keywords

Arthritis; Fibrinogen; Inflammation; M 2

Indexed keywords

BLOOD CLOTTING FACTOR; CELL SURFACE RECEPTOR; FIBRIN; FIBRINOGEN; INTEGRIN; INTEGRIN RECEPTOR; INTEGRIN RECEPTOR ALPHAMBETA2; PROTEINASE; THROMBIN; UNCLASSIFIED DRUG;

ARTHRITIS; ARTICLE; ARTICULAR CARTILAGE; BLOOD CLOTTING; BLOOD VESSEL INJURY; FIBRIN DEPOSITION; HEMOSTASIS; HUMAN; INFLAMMATION; NONHUMAN; PATHOGENESIS; POLYMERIZATION; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; RHEUMATOID ARTHRITIS; SYNOVIAL FLUID; SYNOVIUM; TISSUE INJURY;

EID: 80052218979     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920111798281144     Document Type: Article

References (125)

1. Davie, E.W.; Fujikawa, K.; Kisiel, W. The coagulation cascade: initiation, maintenance, and regulation. Biochemistry, 1991, 30(43), 10363-10370.
2. Mosesson, M.W. The roles of fibrinogen and fibrin in hemostasis and thrombosis. Semin. Hematol., 1992, 29(3), 177-188.
3. Ryu, J.K.; Davalos, D.; Akassoglou, K. Fibrinogen signal transduction in the nervous system. J. Thromb. Haemost., 2009, 7 (Suppl 1), 151-154.
4. Cortes-Canteli, M.; Strickland, S. Fibrinogen, a possible key player in Alzheimer's disease. J. Thromb. Haemost., 2009, 7 (Suppl 1), 146-150.
5. Tang, L.; Ugarova, T.P.; Plow, E.F.; Eaton, J.W. Molecular determinants of acute inflammatory responses to biomaterials. J. Clin. Invest., 1996, 97(5), 1329-1334.
6. Esmon, C.T. Crosstalk between inflammation and thrombosis. Maturitas, 2004, 47(4), 305-314.
7. Danesh, J.; Collins, R.; Appleby, P.; Peto, R. Association of fibrinogen, C-reactive protein, albumin, or leukocyte count with coronary heart disease: meta-analyses of prospective studies. JAMA, 1998, 279(18), 1477-1482.
8. Koenig, W. Fibrin(ogen) in cardiovascular disease: an update. Thromb. Haemost., 2003, 89(4), 601-609.
9. Park, C.S.; Ihm, S.H.; Yoo, K.D.; Kim, D.B.; Lee, J.M.; Kim, H.Y.; Chung, W.S.; Seung, K.B.; Kim, J.H. Relation between Creactive protein, homocysteine levels, fibrinogen, and lipoprotein levels and leukocyte and platelet counts, and 10-year risk for cardiovascular disease among healthy adults in the USA. Am. J. Cardiol., 2010, 105(9), 1284-1288.
10. Aliberti, G.; Proietta, M.; Pulignano, I.; Del Porto, F.; Tammeo, A.; Trappolini, M. Association between fibrinogen plasma levels and platelet counts in an outpatient population and in patients with coronary heart disease. Blood Coagul. Fibrinolysis, 2010, 21(3), 216-220.
11. Danesh, J.; Lewington, S.; Thompson, S.G.; Lowe, G.D.; Collins, R.; Kostis, J.B.; Wilson, A.C.; Folsom, A.R.; Wu, K.; Benderly, M.; Goldbourt, U.; Willeit, J.; Kiechl, S.; Yarnell, J.W.; Sweetnam, P.M.; Elwood, P.C.; Cushman, M.; Psaty, B.M.; Tracy, R.P.; Tybjaerg-Hansen, A.; Haverkate, F.; de Maat, M.P.; Fowkes, F.G.; Lee, A.J.; Smith, F.B.; Salomaa, V.; Harald, K.; Rasi, R.; Vahtera, E.; Jousilahti, P.; Pekkanen, J.; D'Agostino, R.; Kannel, W.B.; Wilson, P.W.; Tofler, G.; Arocha-Pinango, C.L.; Rodriguez-Larralde, A.; Nagy, E.; Mijares, M.; Espinosa, R.; Rodriquez-Roa, E.; Ryder, E.; Diez-Ewald, M.P.; Campos, G.; Fernandez, V.; Torres, E.; Marchioli, R.; Valagussa, F.; Rosengren, A.; Wilhelmsen, L.; Lappas, G.; Eriksson, H.; Cremer, P.; Nagel, D.; Curb, J.D.; Rodriguez, B.; Yano, K.; Salonen, J.T.; Nyyssonen, K.; Tuomainen, T.P.; Hedblad, B.; Lind, P.; Loewel, H.; Koenig, W.; Meade, T.W.; Cooper, J.A.; De Stavola, B.; Knottenbelt, C.; Miller, G.J.; Bauer, K.A.; Rosenberg, R.D.; Sato, S.; Kitamura, A.; Naito, Y.; Palosuo, T.; Ducimetiere, P.; Amouyel, P.; Arveiler, D.; Evans, A.E.; Ferrieres, J.; Juhan-Vague, I.; Bingham, A.; Schulte, H.; Assmann, G.; Cantin, B.; Lamarche, B.; Despres, J.P.; Dagenais, G.R.; Tunstall-Pedoe, H.; Woodward, M.; Ben-Shlomo, Y.; Davey Smith, G.; Palmieri, V.; Yeh, J.L.; Rudnicka, A.; Ridker, P.; Rodeghiero, F.; Tosetto, A.; Shepherd, J.; Ford, I.; Robertson, M.; Brunner, E.; Shipley, M.; Feskens, E.J.; Kromhout, D.; Dickinson, A.; Ireland, B.; Juzwishin, K.; Kaptoge, S.; Memon, A.; Sarwar, N.; Walker, M.; Wheeler, J.; White, I.; Wood, A. Plasma fibrinogen level and the risk of major cardiovascular diseases and nonvascular mortality: an individual participant meta-analysis. JAMA, 2005, 294(14), 1799-1809.
12. Isenegger, J.; Meier, N.; Lammle, B.; Alberio, L.; Fischer, U.; Nedeltchev, K.; Gralla, J.; Kohler, H.P.; Mattle, H.P.; Arnold, M., D-dimers predict stroke subtype when assessed early. Cerebrovasc. Dis., 2010, 29(1), 82-86.
13. del Zoppo, G.J.; Levy, D.E.; Wasiewski, W.W.; Pancioli, A.M.; Demchuk, A.M.; Trammel, J.; Demaerschalk, B.M.; Kaste, M.; Albers, G.W.; Ringelstein, E.B. Hyperfibrinogenemia and functional outcome from acute ischemic stroke. Stroke, 2009, 40(5), 1687-1691.
14. Rothwell, P.M.; Howard, S.C.; Power, D.A.; Gutnikov, S.A.; Algra, A.; van Gijn, J.; Clark, T.G.; Murphy, M.F.; Warlow, C.P. Fibrinogen concentration and risk of ischemic stroke and acute coronary events in 5113 patients with transient ischemic attack and minor ischemic stroke. Stroke, 2004, 35(10), 2300-2305.
15. Bloom, B.J.; Alario, A.J.; Miller, L.C. Persistent elevation of fibrin D-dimer predicts longterm outcome in systemic juvenile idiopathic arthritis. J. Rheumatol., 2009, 36(2), 422-426.
16. Yildirim, K.; Karatay, S.; Melikoglu, M.A.; Gureser, G.; Ugur, M.; Senel, K. Associations between acute phase reactant levels and disease activity score (DAS28) in patients with rheumatoid arthritis. Ann. Clin. Lab. Sci., 2004, 34(4), 423-426.
17. Ichikawa, Y.; Yamada, C.; Horiki, T.; Hoshina, Y.; Uchiyama, M. Serum matrix metalloproteinase-3 and fibrin degradation product levels correlate with clinical disease activity in rheumatoid arthritis. Clin. Exp. Rheumatol., 1998, 16(5), 533-540.
18. Bloom, B.J.; Tucker, L.B.; Miller, L.C.; Schaller, J.G.; Fibrin Ddimer as a marker of disease activity in systemic onset juvenile rheumatoid arthritis. J. Rheumatol., 1998, 25(8), 1620-1625.
19. Beckham, J.C.; Caldwell, D.S.; Peterson, B.L.; Pippen, A.M.; Currie, M.S.; Keefe, F.J.; Weinberg, J.B. Disease severity in rheumatoid arthritis: relationships of plasma tumor necrosis factoralpha, soluble interleukin 2-receptor, soluble CD4/CD8 ratio, neopterin, and fibrin D-dimer to traditional severity and functional measures. J. Clin. Immunol., 1992, 12(5), 353-361.
20. Shen, J.; Ran, Z.H.; Zhang, Y.; Cai, Q.; Yin, H.M.; Zhou, X.T.; Xiao, S.D. Biomarkers of altered coagulation and fibrinolysis as measures of disease activity in active inflammatory bowel disease: a gender-stratified, cohort analysis. Thromb. Res., 2009, 123(4), 604-611.
21. Biancone, L.; Scopinaro, F.; Maletta, M.; Monteleone, G.; Luzza, F.; Banci, M.; Mercantini, P.; Renda, T.; Pallone, F. Circulating D dimer in inflammatory bowel disease. Ital. J. Gastroenterol., 1994, 26(3), 116-120.
22. Lake, A.M.; Stauffer, J.Q.; Stuart, M.J. Hemostatic alterations in inflammatory bowel disease: response to therapy. Am. J. Dig. Dis., 1978, 23(10), 897-902.
23. Aksungar, F.B.; Topkaya, A.E.; Yildiz, Z.; Sahin, S.; Turk, U. Coagulation status and biochemical and inflammatory markers in multiple sclerosis. J. Clin. Neurosci., 2008, 15(4), 393-397.
24. Flick, M.J.; Du, X.; Degen, J.L. Fibrin(ogen)-alpha M beta 2 interactions regulate leukocyte function and innate immunity in vivo. Exp. Biol. Med., (Maywood), 2004, 229(11), 1105-1110.
25. Degen, J.L.; Bugge, T.H.; Goguen, J.D. Fibrin and fibrinolysis in infection and host defense. J. Thromb. Haemost., 2007, 5 (Suppl 1), 24-31.
26. Rothfork, J.M.; Dessus-Babus, S.; Van Wamel, W.J.; Cheung, A.L.; Gresham, H.D. Fibrinogen depletion attenuates Staphyloccocus aureus infection by preventing density-dependent virulence gene up-regulation. J. Immunol., 2003, 171(10), 5389-5395.
27. Szaba, F.M.; Smiley, S.T. Roles for thrombin and fibrin(ogen) in cytokine/chemokine production and macrophage adhesion in vivo. Blood, 2002, 99(3), 1053-1059.
28. Flick, M.J.; Lajeunesse, C.M.; Talmage, K.E.; Witte, D.P.; Palumbo, J.S.; Pinkerton, M.D.; Thornton, S.; Degen, J.L. Fibrin(ogen) exacerbates inflammatory joint disease through a mechanism linked to the integrin alpha(M)beta(2) binding motif. J. Clin. Invest., 2007, 117(11), 3224-3235.
29. Adams, R.A.; Schachtrup, C.; Davalos, D.; Tsigelny, I.; Akassoglou, K. Fibrinogen signal transduction as a mediator and therapeutic target in inflammation: lessons from multiple sclerosis. Curr. Med. Chem., 2007, 14(27), 2925-2936.
30. Adams, R.A.; Bauer, J.; Flick, M.J.; Sikorski, S.L.; Nuriel, T.; Lassmann, H.; Degen, J.L.; Akassoglou, K. The fibrin-derived gamma377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J. Exp. Med., 2007, 204(3), 571-582.
31. Steinbrecher, K.A.; Horowitz, N.A.; Blevins, E.A.; Barney, K.A.; Shaw, M.A.; Harmel-Laws, E.; Finkelman, F.D.; Flick, M.J.; Pinkerton, M.D.; Talmage, K.E.; Kombrinck, K.W.; Witte, D.P.; Palumbo, J.S. 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(7), 2634-2643.
32. Floer, M.; Gotte, M.; Wild, M.K.; Heidemann, J.; Gassar, E.S.; Domschke, W.; Kiesel, L.; Luegering, A.; Kucharzik, T. Enoxaparin improves the course of dextran sodium sulfate-induced colitis in syndecan-1-deficient mice. Am. J. Pathol., 2010, 176(1), 146-157.
33. Yoshida, H.; Russell, J.; Granger, D.N. Thrombin mediates the extraintestinal thrombosis associated with experimental colitis. Am. J. Physiol. Gastrointest Liver Physiol., 2008, 295(5), G904-G908.
34. Tanne, D.; Katzav, A.; Beilin, O.; Grigoriadis, N.C.; Blank, M.; Pick, C.G.; Landenberg, P.; Shoenfeld, Y.; Chapman, J. Interaction of inflammation, thrombosis, aspirin and enoxaparin in CNS experimental antiphospholipid syndrome. Neurobiol. Dis., 2008, 30(1), 56-64.
35. Slofstra, S.H.; van 't Veer, C.; Buurman, W.A.; Reitsma, P.H.; ten Cate, H.; Spek, C.A. Low molecular weight heparin attenuates multiple organ failure in a murine model of disseminated intravascular coagulation. Crit. Care Med., 2005, 33(6), 1365-1370.
36. Frizelle, S.; Schwarz, J.; Huber, S.A.; Leslie, K. Evaluation of the effects of low molecular weight heparin on inflammation and collagen deposition in chronic coxsackievirus B3-induced myocarditis in A/J mice. Am. J. Pathol., 1992, 141(1), 203-209.
37. Varisco, P.A.; Peclat, V.; van Ness, K.; Bischof-Delaloye, A.; So, A.; Busso, N. Effect of thrombin inhibition on synovial inflammation in antigen induced arthritis. Ann. Rheum. Dis., 2000, 59(10), 781-787.
38. Niessen, F.; Furlan-Freguia, C.; Fernandez, J.A.; Mosnier, L.O.; Castellino, F.J.; Weiler, H.; Rosen, H.; Griffin, J.H.; Ruf, W. Endogenous EPCR/aPC-PAR1 signaling prevents inflammationinduced vascular leakage and lethality. Blood, 2009, 113(12), 2859-2866.
39. Busso, N.; Chobaz-Peclat, V.; Hamilton, J.; Spee, P.; Wagtmann, N.; So, A. Essential role of platelet activation via protease activated receptor 4 in tissue factor-initiated inflammation. Arthritis Res. Ther., 2008, 10(2), R42.
40. Han, M.H.; Hwang, S.I.; Roy, D.B.; Lundgren, D.H.; Price, J.V.; Ousman, S.S.; Fernald, G.H.; Gerlitz, B.; Robinson, W.H.; Baranzini, S.E.; Grinnell, B.W.; Raine, C.S.; Sobel, R.A.; Han, D.K.; Steinman, L. Proteomic analysis of active multiple sclerosis lesions reveals therapeutic targets. Nature, 2008, 451(7182), 1076-1081.
41. Paul, J.; Strickland, S.; Melchor, J.P. Fibrin deposition accelerates neurovascular damage and neuroinflammation in mouse models of Alzheimer's disease. J. Exp. Med., 2007, 204(8), 1999-2008.
42. Akassoglou, K.; Adams, R.A.; Bauer, J.; Mercado, P.; Tseveleki, V.; Lassmann, H.; Probert, L.; Strickland, S. Fibrin depletion decreases inflammation and delays the onset of demyelination in a tumor necrosis factor transgenic mouse model for multiple sclerosis. Proc. Natl. Acad. Sci. USA, 2004, 101(17), 6698-6703.
43. Busso, N.; Peclat, V.; Van Ness, K.; Kolodziesczyk, E.; Degen, J.; Bugge, T.; So, A. Exacerbation of antigen-induced arthritis in urokinase-deficient mice. J. Clin. Invest., 1998, 102(1), 41-50.
44. Cantwell, A.M.; Di Cera, E. Rational design of a potent anticoagulant thrombin. J. Biol. Chem., 2000, 275(51), 39827-39830.
45. Gruber, A.; Cantwell, A.M.; Di Cera, E.; Hanson, S.R. The thrombin mutant W215A/E217A shows safe and potent anticoagulant and antithrombotic effects in vivo. J. Biol. Chem., 2002, 277(31), 27581-27584.
46. Bernard, G.R.; Vincent, J.L.; Laterre, P.F.; LaRosa, S.P.; Dhainaut, J.F.; Lopez-Rodriguez, A.; Steingrub, J.S.; Garber, G.E.; Helterbrand, J.D.; Ely, E.W.; Fisher, C.J. Jr., Efficacy and safety of recombinant human activated protein C for severe sepsis. N. Engl. J. Med., 2001, 344(10), 699-709.
47. Kerschen, E.J.; Fernandez, J.A.; Cooley, B.C.; Yang, X.V.; Sood, R.; Mosnier, L.O.; Castellino, F.J.; Mackman, N.; Griffin, J.H.; Weiler, H. Endotoxemia and sepsis mortality reduction by nonanticoagulant activated protein C. J. Exp. Med., 2007, 204(10), 2439-2448.
48. Mosnier, L.O.; Yang, X.V.; Griffin, J.H. Activated protein C mutant with minimal anticoagulant activity, normal cytoprotective activity, and preservation of thrombin activable fibrinolysis inhibitor-dependent cytoprotective functions. J. Biol. Chem., 2007, 282(45), 33022-33033.
49. Bach, T.L.; Barsigian, C.; Yaen, C.H.; Martinez, J. Endothelial cell VE-cadherin functions as a receptor for the beta15-42 sequence of fibrin. J. Biol. Chem., 1998, 273(46), 30719-30728.
50. Dejana, E.; Languino, L.R.; Polentarutti, N.; Balconi, G.; Ryckewaert, J.J.; Larrieu, M.J.; Donati, M.B.; Mantovani, A.; Marguerie, G. Interaction between fibrinogen and cultured endothelial cells. Induction of migration and specific binding. J. Clin. Invest., 1985, 75(1), 11-18.
51. Gross, T.J.; Leavell, K.J.; Peterson, M.W. CD11b/CD18 mediates the neutrophil chemotactic activity of fibrin degradation product D domain. Thromb. Haemost., 1997, 77(5), 894-900.
52. Holmback, K.; Danton, M.J.; Suh, T.T.; Daugherty, C.C.; Degen, J.L. Impaired platelet aggregation and sustained bleeding in mice lacking the fibrinogen motif bound by integrin alpha IIb beta 3. EMBO J., 1996, 15(21), 5760-5771.
53. Lishko, V.K.; Kudryk, B.; Yakubenko, V.P.; Yee, V.C.; Ugarova, T.P. Regulated unmasking of the cryptic binding site for integrin alpha M beta 2 in the gamma C-domain of fibrinogen. Biochemistry, 2002, 41(43), 12942-12951.
54. May, A.E.; Kalsch, T.; Massberg, S.; Herouy, Y.; Schmidt, R.; Gawaz, M. Engagement of glycoprotein IIb/IIIa (alpha(IIb)beta3) on platelets upregulates CD40L and triggers CD40L-dependent matrix degradation by endothelial cells. Circulation, 2002, 106(16), 2111-2117.
55. Rubel, C.; Gomez, S.; Fernandez, G.C.; Isturiz, M.A.; Caamano, J.; Palermo, M.S. Fibrinogen-CD11b/CD18 interaction activates the NF-kappa B pathway and delays apoptosis in human neutrophils. Eur. J. Immunol., 2003, 33(5), 1429-1438.
56. Sherman, L.A.; Lee, J. Specific binding of soluble fibrin to macrophages. J. Exp. Med., 1977, 145(1), 76-85.
57. Suehiro, K.; Gailit, J.; Plow, E.F. Fibrinogen is a ligand for integrin alpha5beta1 on endothelial cells. J. Biol. Chem., 1997, 272(8), 5360-5366.
58. Vidal, B.; Serrano, A.L.; Tjwa, M.; Suelves, M.; Ardite, E.; De Mori, R.; Baeza-Raja, B.; Martinez de Lagran, M.; Lafuste, P.; Ruiz-Bonilla, V.; Jardi, M.; Gherardi, R.; Christov, C.; Dierssen, M.; Carmeliet, P.; Degen, J.L.; Dewerchin, M.; Munoz-Canoves, P. Fibrinogen drives dystrophic muscle fibrosis via a TGFbeta/alternative macrophage activation pathway. Genes Dev., 2008, 22(13), 1747-1752.
59. Fowler, W.E.; Fretto, L.J.; Erickson, H.P.; McKee, P.A. Electron microsocpy of plasmic fragments of human fibrinogen as related to trinodular structure of the intact molecule. J. Clin. Invest., 1980, 66(1), 50-56.
60. Weisel, J.W.; Phillips, G.N. Jr.; Cohen, C. A model from electron microscopy for the molecular structure of fibrinogen and fibrin. Nature, 1981, 289(5795), 263-267.
61. Kant, J.A.; Fornace, A.J., Jr.; Saxe, D.; Simon, M.I.; McBride, O.W.; Crabtree, G.R. Evolution and organization of the fibrinogen locus on chromosome 4: gene duplication accompanied by transposition and inversion. Proc. Natl. Acad. Sci. USA, 1985, 82(8), 2344-2348.
62. Duan, H.O.; Simpson-Haidaris, P.J. Cell type-specific differential induction of the human gamma-fibrinogen promoter by interleukin-6. J. Biol. Chem., 2006, 281(18), 12451-12457.
63. Lawrence, S.O.; Simpson-Haidaris, P.J. Regulated de novo biosynthesis of fibrinogen in extrahepatic epithelial cells in response to inflammation. Thromb Haemost, 2004, 92(2), 234-243.
64. Fu, Y.; Weissbach, L.; Plant, P.W.; Oddoux, C.; Cao, Y.; Liang, T.J.; Roy, S.N.; Redman, C.M.; Grieninger, G. Carboxy-terminalextended variant of the human fibrinogen alpha subunit: a novel exon conferring marked homology to beta and gamma subunits. Biochemistry, 1992, 31(48), 11968-11972.
65. Fu, Y.; Grieninger, G. Fib420: a normal human variant of fibrinogen with two extended alpha chains. Proc. Natl. Acad. Sci. USA, 1994, 91(7), 2625-2628.
66. Chung, D.W.; Davie, E.W. Gamma and gamma' chains of human fibrinogen are produced by alternative mRNA processing. Biochemistry, 1984, 23(18), 4232-4236.
67. Uitte de Willige, S.; Standeven, K.F.; Philippou, H.; Ariens, R.A. The pleiotropic role of the fibrinogen gamma' chain in hemostasis. Blood, 2009, 114(19), 3994-4001.
68. Katagiri, Y.; Hiroyama, T.; Akamatsu, N.; Suzuki, H.; Yamazaki, H.; Tanoue, K. Involvement of alpha v beta 3 integrin in mediating fibrin gel retraction. J. Biol. Chem., 1995, 270(4), 1785-1790.
69. Ugarova, T.P.; Solovjov, D.A.; Zhang, L.; Loukinov, D.I.; Yee, V.C.; Medved, L.V.; Plow, E.F. Identification of a novel recognition sequence for integrin alphaM beta2 within the gammachain of fibrinogen. J. Biol. Chem., 1998, 273(35), 22519-22527.
70. Loike, J.D.; Sodeik, B.; Cao, L.; Leucona, S.; Weitz, J.I.; Detmers, P.A.; Wright, S.D.; Silverstein, S.C. CD11c/CD18 on neutrophils recognizes a domain at the N terminus of the A alpha chain of fibrinogen. Proc. Natl. Acad. Sci. USA, 1991, 88(3), 1044-1048.
71. Lishko, V.K.; Podolnikova, N.P.; Yakubenko, V.P.; Yakovlev, S.; Medved, L.; Yadav, S.P.; Ugarova, T.P. Multiple binding sites in fibrinogen for integrin alphaMbeta2 (Mac-1). J. Biol. Chem., 2004, 279(43), 44897-44906.
72. Ugarova, T.P.; Yakubenko, V.P. Recognition of fibrinogen by leukocyte integrins. Ann. N Y. Acad. Sci., 2001, 936, 368-385.
73. Rubel, C.; Fernandez, G.C.; Rosa, F.A.; Gomez, S.; Bompadre, M.B.; Coso, O.A.; Isturiz, M.A.; Palermo, M.S. Soluble fibrinogen modulates neutrophil functionality through the activation of an extracellular signal-regulated kinase-dependent pathway. J. Immunol., 2002, 168(7), 3527-3535.
74. Pluskota, E.; Soloviev, D.A.; Szpak, D.; Weber, C.; Plow, E.F. Neutrophil apoptosis: selective regulation by different ligands of integrin alphaMbeta2. J. Immunol., 2008, 181(5), 3609-3619.
75. Cheresh, D.A.; Berliner, S.A.; Vicente, V.; Ruggeri, Z.M. Recognition of distinct adhesive sites on fibrinogen by related integrins on platelets and endothelial cells. Cell, 1989, 58(5), 945-953.
76. Yokoyama, K.; Zhang, X.P.; Medved, L.; Takada, Y. Specific binding of integrin alpha v beta 3 to the fibrinogen gamma and alpha E chain C-terminal domains. Biochemistry, 1999, 38(18), 5872-5877.
77. Farrell, D.H.; Thiagarajan, P.; Chung, D.W.; Davie, E.W. Role of fibrinogen alpha and gamma chain sites in platelet aggregation. Proc. Natl. Acad. Sci. USA, 1992, 89(22), 10729-10732.
78. Farrell, D.H.; Thiagarajan, P. Binding of recombinant fibrinogen mutants to platelets. J. Biol. Chem., 1994, 269(1), 226-231.
79. Hettasch, J.M.; Bolyard, M.G.; Lord, S.T. The residues AGDV of recombinant gamma chains of human fibrinogen must be carboxyterminal to support human platelet aggregation. Thromb. Haemost., 1992, 68(6), 701-706.
80. Ugarova, T.P.; Lishko, V.K.; Podolnikova, N.P.; Okumura, N.; Merkulov, S.M.; Yakubenko, V.P.; Yee, V.C.; Lord, S. T.; Haas, T.A. 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(31), 9365-9373.
81. Lishko, V.K.; Yakubenko, V.P.; Hertzberg, K.M.; Grieninger, G.; Ugarova, T.P. The alternatively spliced alpha(E)C domain of human fibrinogen-420 is a novel ligand for leukocyte integrins alpha(M)beta(2) and alpha(X)beta(2). Blood, 2001, 98(8), 2448-2455.
82. Wright, S.D.; Weitz, J.I.; Huang, A.J.; Levin, S.M.; Silverstein, S.C.; Loike, J.D. Complement receptor type three (CD11b/CD18) of human polymorphonuclear leukocytes recognizes fibrinogen. Proc. Natl. Acad. Sci. USA, 1988, 85(20), 7734-7738.
83. Altieri, D.C.; Bader, R.; Mannucci, P.M.; Edgington, T.S. Oligospecificity of the cellular adhesion receptor Mac-1 encompasses an inducible recognition specificity for fibrinogen. J. Cell Biol., 1988, 107(5), 1893-1900.
84. Altieri, D.C.; Plescia, J.; Plow, E.F. The structural motif glycine 190-valine 202 of the fibrinogen gamma chain interacts with CD11b/CD18 integrin (alpha M beta 2, Mac-1) and promotes leukocyte adhesion. J. Biol. Chem., 1993, 268(3), 1847-1853.
85. Flick, M.J.; Du, X.; Witte, D.P.; Jirouskova, M.; Soloviev, D.A.; Busuttil, S.J.; Plow, E.F.; Degen, J.L. 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(11), 1596-1606.
86. Doolittle, R.F.; Yang, Z.; Mochalkin, I. Crystal structure studies on fibrinogen and fibrin. Ann. N. Y. Acad. Sci., 2001, 936, 31-43.
87. Alonzi, T.; Fattori, E.; Lazzaro, D.; Costa, P.; Probert, L.; Kollias, G.; De Benedetti, F.; Poli, V.; Ciliberto, G. Interleukin 6 is required for the development of collagen-induced arthritis. J. Exp. Med., 1998, 187(4), 461-468.
88. Brennan, F.M.; Maini, R.N.; Feldmann, M. Role of proinflammatory cytokines in rheumatoid arthritis. Springer Semin. Immunopathol., 1998, 20(1-2), 133-147.
89. Douni, E.; Akassoglou, K.; Alexopoulou, L.; Georgopoulos, S.; Haralambous, S.; Hill, S.; Kassiotis, G.; Kontoyiannis, D.; Pasparakis, M.; Plows, D.; Probert, L.; Kollias, G. Transgenic and knockout analyses of the role of TNF in immune regulation and disease pathogenesis. J. Inflamm., 1995, 47(1-2), 27-38.
90. Feldmann, M.; Brennan, F.M.; Maini, R.N. Rheumatoid arthritis. Cell, 1996, 85(3), 307-310.
91. Feldmann, M.; Maini, R.N. The role of cytokines in the pathogenesis of rheumatoid arthritis. Rheumatology, (Oxford), 1999, 38 (Suppl 20), 3-7.
92. Joosten, L.A.; Helsen, M.M.; Saxne, T.; van De Loo, F.A.; Heinegard, D.; van Den Berg, W.B. IL-1 alpha beta blockade prevents cartilage and bone destruction in murine type II collageninduced arthritis, whereas TNF-alpha blockade only ameliorates joint inflammation. J. Immunol., 1999, 163(9), 5049-5055.
93. Kollias, G.; Douni, E.; Kassiotis, G.; Kontoyiannis, D. The function of tumour necrosis factor and receptors in models of multi-organ inflammation, rheumatoid arthritis, multiple sclerosis and inflammatory bowel disease. Ann. Rheum. Dis., 1999, 58 (Suppl 1), 32-139.
94. Luross, J.A.; Williams, N.A. The genetic and immunopathological processes underlying collagen-induced arthritis. Immunology, 2001, 103(4), 407-416.
95. Mori, L.; Iselin, S.; De Libero, G.; Lesslauer, W. Attenuation of collagen-induced arthritis in 55-kDa TNF receptor type 1 (TNFR1)-IgG1-treated and TNFR1-deficient mice. J. Immunol., 1996, 157(7), 3178-3182.
96. Redlich, K.; Hayer, S.; Ricci, R.; David, J.P.; Tohidast-Akrad, M.; Kollias, G.; Steiner, G.; Smolen, J.S.; Wagner, E.F.; Schett, G. Osteoclasts are essential for TNF-alpha-mediated joint destruction. J. Clin. Invest., 2002, 110(10), 1419-1427.
97. Scatena, M.; Liaw, L.; Giachelli, C.M. Osteopontin: a multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler Thromb. Vasc. Biol., 2007, 27(11), 2302-2309.
98. Scheinecker, C.; Redlich, K.; Smolen, J.S. Cytokines as therapeutic targets: advances and limitations. Immunity, 2008, 28(4), 440-444.
99. van de Loo, F.A.; Joosten, L.A.; van Lent, P.L.; Arntz, O.J.; van den Berg, W.B. Role of interleukin-1, tumor necrosis factor alpha, and interleukin-6 in cartilage proteoglycan metabolism and destruction. Effect of in situ blocking in murine antigen- and zymosan-induced arthritis. Arthritis Rheum., 1995, 38(2), 164-172.
100. Williams, R.O.; Feldmann, M.; Maini, R.N. Cartilage destruction and bone erosion in arthritis: the role of tumour necrosis factor alpha. Ann. Rheum. Dis., 2000, 59 Suppl 1, i75-i180.
101. Williams, R.O.; Ghrayeb, J.; Feldmann, M.; Maini, R.N. Successful therapy of collagen-induced arthritis with TNF receptor-IgG fusion protein and combination with anti-CD4. Immunology, 1995, 84(3), 433-439.
102. Arend, W.P.; Dayer, J.M. Inhibition of the production and effects of interleukin-1 and tumor necrosis factor alpha in rheumatoid arthritis. Arthritis Rheum., 1995, 38(2), 151-160.
103. Emery, P.; Fleischmann, R.; Filipowicz-Sosnowska, A.; Schechtman, J.; Szczepanski, L.; Kavanaugh, A.; Racewicz, A.J.; van Vollenhoven, R.F.; Li, N.F.; Agarwal, S.; Hessey, E.W.; Shaw, T.M. The efficacy and safety of rituximab in patients with active rheumatoid arthritis despite methotrexate treatment: results of a phase IIB randomized, double-blind, placebo-controlled, doseranging trial. Arthritis Rheum., 2006, 54(5), 1390-1400.
104. Kremer, J.M.; Genant, H.K.; Moreland, L.W.; Russell, A.S.; Emery, P.; Abud-Mendoza, C.; Szechinski, J.; Li, T.; Ge, Z.; Becker, J.C.; Westhovens, R. Effects of abatacept in patients with methotrexate-resistant active rheumatoid arthritis: a randomized trial. Ann. Intern. Med., 2006, 144(12), 865-876.
105. Smiley, S.T.; King, J.A.; Hancock, W.W. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J. Immunol., 2001, 167(5), 2887-2894.
106. Qi, J.; Kreutzer, D.L. Fibrin activation of vascular endothelial cells. Induction of IL-8 expression. J. Immunol., 1995, 155(2), 867-876.
107. Drew, A.F.; Tucker, H.L.; Liu, H.; Witte, D.P.; Degen, J.L.; Tipping, P.G. Crescentic glomerulonephritis is diminished in fibrinogen-deficient mice. Am. J. Physiol. Renal. Physiol., 2001, 281(6), 1157-1163.
108. Perez, R.L.; Roman, J. Fibrin enhances the expression of IL-1 beta by human peripheral blood mononuclear cells. Implications in pulmonary inflammation. J. Immunol., 1995, 154(4), 1879-1887.
109. Jensen, T.; Kierulf, P.; Sandset, P.M.; Klingenberg, O.; Joo, G.B.; Godal, H.C.; Skjonsberg, O.H. Fibrinogen and fibrin induce synthesis of proinflammatory cytokines from isolated peripheral blood mononuclear cells. Thromb. Haemost., 2007, 97(5), 822-829.
110. Fan, S.T.; Edgington, T.S. Integrin regulation of leukocyte inflammatory functions. CD11b/CD18 enhancement of the tumor necrosis factor-alpha responses of monocytes. J. Immunol., 1993, 150(7), 2972-2980.
111. Liu, X.; Piela-Smith, T.H. Fibrin(ogen)-induced expression of ICAM-1 and chemokines in human synovial fibroblasts. J. Immunol., 2000, 165(9), 5255-5261.
112. Takami, M.; Terry, V.; Petruzzelli, L. Signaling pathways involved in IL-8-dependent activation of adhesion through Mac-1. J. Immunol., 2002, 168(9), 4559-4566.
113. Weinberg, J.B.; Pippen, A.M.; Greenberg, C.S. Extravascular fibrin formation and dissolution in synovial tissue of patients with osteoarthritis and rheumatoid arthritis. Arthritis Rheum., 1991, 34(8), 996-1005.
114. Zacharski, L.R.; Brown, F.E.; Memoli, V.A.; Kisiel, W.; Kudryk, B.J.; Rousseau, S.M.; Hunt, J.A.; Dunwiddie, C.; Nutt, E.M. Pathways of coagulation activation in situ in rheumatoid synovial tissue. Clin. Immunol. Immunopathol., 1992, 63(2), 155-162.
115. Marty, I.; Peclat, V.; Kirdaite, G.; Salvi, R.; So, A.; Busso, N. Amelioration of collagen-induced arthritis by thrombin inhibition. J. Clin. Invest., 2001, 107(5), 631-640.
116. Yang, Y.H.; Carmeliet, P.; Hamilton, J.A. Tissue-type plasminogen activator deficiency exacerbates arthritis. J. Immunol., 2001, 167(2), 1047-1052.
117. Rantapaa-Dahlqvist, S.; de Jong, B.A.; Berglin, E.; Hallmans, G.; Wadell, G.; Stenlund, H.; Sundin, U.; van Venrooij, W.J. Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum., 2003, 48(10), 2741-2749.
118. Ronnelid, J.; Wick, M.C.; Lampa, J.; Lindblad, S.; Nordmark, B.; Klareskog, L.; van Vollenhoven, R.F. Longitudinal analysis of citrullinated protein/peptide antibodies (anti-CP) during 5 year follow up in early rheumatoid arthritis: anti-CP status predicts worse disease activity and greater radiological progression. Ann. Rheum. Dis., 2005, 64(12), 1744-1749.
119. Hammer, J.; Gallazzi, F.; Bono, E.; Karr, R.W.; Guenot, J.; Valsasnini, P.; Nagy, Z.A.; Sinigaglia, F. Peptide binding specificity of HLA-DR4 molecules: correlation with rheumatoid arthritis association. J. Exp. Med., 1995, 181(5), 1847-1855.
120. Schellekens, G.A.; de Jong, B.A.; van den Hoogen, F.H.; van de Putte, L. B.; van Venrooij, W.J. Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritisspecific autoantibodies. J. Clin. Invest., 1998, 101(1), 273-281.
121. Girbal-Neuhauser, E.; Durieux, J.J.; Arnaud, M.; Dalbon, P.; Sebbag, M.; Vincent, C.; Simon, M.; Senshu, T.; Masson-Bessiere, C.; Jolivet-Reynaud, C.; Jolivet, M.; Serre, G. The epitopes targeted by the rheumatoid arthritis-associated antifilaggrin autoantibodies are posttranslationally generated on various sites of (pro)filaggrin by deimination of arginine residues. J. Immunol., 1999, 162(1), 585-594.
122. van Venrooij, W.J.; Hazes, J.M.; Visser, H. Anticitrullinated protein/peptide antibody and its role in the diagnosis and prognosis of early rheumatoid arthritis. Neth. J. Med., 2002, 60(10), 383-388.
123. Kuhn, K.A.; Kulik, L.; Tomooka, B.; Braschler, K.J.; Arend, W.P.; Robinson, W.H.; Holers, V.M. Antibodies against citrullinated proteins enhance tissue injury in experimental autoimmune arthritis. J. Clin. Invest., 2006, 116(4), 961-973.
124. Hill, J.A.; Bell, D.A.; Brintnell, W.; Yue, D.; Wehrli, B.; Jevnikar, A.M.; Lee, D.M.; Hueber, W.; Robinson, W.H.; Cairns, E. Arthritis induced by posttranslationally modified (citrullinated) fibrinogen in DR4-IE transgenic mice. J. Exp. Med., 2008, 205(4), 967-979.
125. Ho, P.P.; Lee, L.Y.; Zhao, X.; Tomooka, B.H.; Paniagua, R.T.; Sharpe, O.; BenBarak, M.J.; Chandra, P.E.; Hueber, W.; Steinman, L.; Robinson, W.H. Autoimmunity against fibrinogen mediates inflammatory arthritis in mice. J. Immunol., 2010, 184(1), 379-390.