Fibrin accumulation secondary to loss of plasmin-mediated fibrinolysis drives inflammatory osteoporosis in mice

Arthritis and Rheumatology

Volumn 66, Issue 8, 2014, Pages 2222-2233

  Cole, Heather A ^a   Ohba, Tetsuro ^a   Nyman, Jeffry S ^a   Hirotaka, Haro ^b   Cates, Justin M M ^a   Flick, Matthew J ^c   Degen, Jay L ^c   Schoenecker, Jonathan G ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF YAMANASHI   (Japan)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRIN; FIBRINOGEN; GAMMA INTERFERON; INTEGRIN RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOCLAST DIFFERENTIATION FACTOR; PLASMIN; PLASMINOGEN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BIOSYNTHESIS; BONE ATROPHY; BONE REMODELING; BONE STRUCTURE; CELL STIMULATION; CHRONIC INFLAMMATION; COMPARATIVE STUDY; COMPRESSION; CONTROLLED STUDY; CORTICAL BONE; DENDRITIC CELL; FIBRIN DEPOSITION; FIBRINOGEN BLOOD LEVEL; FIBRINOLYSIS; FRAGILITY FRACTURE; HISTOPATHOLOGY; INFLAMMATION; INFLAMMATORY DISEASE; INFLAMMATORY OSTEOPOROSIS; INTERVERTEBRAL DISK; KYPHOSIS; LEUKOCYTE ACTIVATION; MACROPHAGE; MICRO-COMPUTED TOMOGRAPHY; MONOCYTE; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOCLAST ACTIVITY; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPOROSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; QUANTITATIVE ANALYSIS; RIGIDITY; SPINE RADIOGRAPHY; THICKNESS; VERTEBRA BODY; X RAY SYSTEM;

ANIMALS; FIBRIN; FIBRINOLYSIN; FIBRINOLYSIS; INFLAMMATION; MALE; MICE; OSTEOPOROSIS;

EID: 84905055000     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38639     Document Type: Article

References (42)

1. Raisz LG,. Pathogenesis of osteoporosis: concepts, conflicts, and prospects. J Clin Invest 2005; 115: 3318-25.
2. Canalis E, Giustina A, Bilezikian JP,. Mechanisms of anabolic therapies for osteoporosis. N Engl J Med 2007; 357: 905-16.
3. Mundy GR,. Osteoporosis and inflammation. Nutr Rev 2007; 65: S147-51.
4. Daniell HW,. Osteoporosis and smoking. JAMA 1972; 221: 509.
5. Hofbauer LC, Brueck CC, Singh SK, Dobnig H,. Osteoporosis in patients with diabetes mellitus. J Bone Miner Res 2007; 22: 1317-28.
6. Nielson CM, Srikanth P, Orwoll ES,. Obesity and fracture in men and women: an epidemiologic perspective. J Bone Miner Res 2012; 27: 1-10.
7. Arron JR, Choi Y,. Bone versus immune system. Nature 2000; 408: 535-6.
8. Ginaldi L, Di Benedetto MC, De Martinis M,. Osteoporosis, inflammation and ageing. Immun Ageing 2005; 2: 14.
9. Lacativa PG, Farias ML,. Osteoporosis and inflammation. Arq Bras Endocrinol Metabol 2010; 54: 123-32.
10. Manolagas SC, Jilka RL,. Bone marrow, cytokines, and bone remodeling: emerging insights into the pathophysiology of osteoporosis. N Engl J Med 1995; 332: 305-11.
11. Tilg H, Moschen AR, Kaser A, Pines A, Dotan I,. Gut, inflammation and osteoporosis: basic and clinical concepts. Gut 2008; 57: 684-94.
12. Stutz CM, O'Rear LD, O'Neill KR, Tamborski ME, Crosby CG, Devin CJ, et al. Coagulopathies in orthopaedics: links to inflammation and the potential of individualizing treatment strategies. J Orthop Trauma 2013; 27: 236-41.
13. Davalos D, Akassoglou K,. Fibrinogen as a key regulator of inflammation in disease. Semin Immunopathol 2012; 34: 43-62.
14. 2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest 2004; 113: 1596-606.
15. Todd RF III,. The continuing saga of complement receptor type 3 (CR3). J Clin Invest 1996; 98: 1-2.
16. Adams RA, Bauer J, Flick MJ, Sikorski SL, Nuriel T, Lassmann H, et al. The fibrin-derived γ377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J Exp Med 2007; 204: 571-82.
17. Davalos D, Ryu JK, Merlini M, Baeten KM, Le Moan N, Petersen MA, et al. Fibrinogen-induced perivascular microglial clustering is required for the development of axonal damage in neuroinflammation. Nat Commun 2012; 3: 1227.
18. 2 engagement of fibrinogen. Cancer Res 2010; 70: 2634-43.
19. 2 leukocyte integrin receptor. Hum Mol Genet 2012; 21: 1989-2004.
20. Alzahrani SH, Ajjan RA,. Coagulation and fibrinolysis in diabetes. Diab Vasc Dis Res 2010; 7: 260-73.
21. Billimoria JD, Pozner H, Metselaar B, Best FW, James DC,. Effect of cigarette smoking on lipids, lipoproteins, blood coagulation, fibrinolysis and cellular components of human blood. Atherosclerosis 1975; 21: 61-76.
22. De Pergola G, Pannacciulli N,. Coagulation and fibrinolysis abnormalities in obesity. J Endocrinol Invest 2002; 25: 899-904.
23. Dunn EJ, Ariens RA,. Fibrinogen and fibrin clot structure in diabetes. Herz 2004; 29: 470-9.
24. Paraskevas KI, Baker DM, Vrentzos GE, Mikhailidis DP,. The role of fibrinogen and fibrinolysis in peripheral arterial disease. Thromb Res 2008; 122: 1-12.
25. Undas A, Topor-Madry R, Tracz W, Pasowicz M,. Effect of cigarette smoking on plasma fibrin clot permeability and susceptibility to lysis. Thromb Haemost 2009; 102: 1289-91.
26. Romer J, Bugge TH, Pyke C, Lund LR, Flick MJ, Degen JL, et al. Impaired wound healing in mice with a disrupted plasminogen gene. Nat Med 1996; 2: 287-92.
27. Suh TT, Holmback K, Jensen NJ, Daugherty CC, Small K, Simon DI, et al. Resolution of spontaneous bleeding events but failure of pregnancy in fibrinogen-deficient mice. Genes Dev 1995; 9: 2020-33.
28. Bugge TH, Kombrinck KW, Flick MJ, Daugherty CC, Danton MJ, Degen JL,. Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell 1996; 87: 709-19.
29. Halleen JM, Tiitinen SL, Ylipahkala H, Fagerlund KM, Vaananen HK,. Tartrate-resistant acid phosphatase 5b (TRACP 5b) as a marker of bone resorption. Clin Lab 2006; 52: 499-509.
30. Takahashi N, Udagawa N, Suda T,. A new member of tumor necrosis factor ligand family, ODF/OPGL/TRANCE/RANKL, regulates osteoclast differentiation and function. Biochem Biophys Res Commun 1999; 256: 449-55.
31. Kanno Y, Ishisaki A, Kawashita E, Chosa N, Nakajima K, Nishihara T, et al. Plasminogen/plasmin modulates bone metabolism by regulating the osteoblast and osteoclast function. J Biol Chem 2011; 286: 8952-60.
32. Guzel S, Seven A, Kocaoglu A, Ilk B, Guzel EC, Saracoglu GV, et al. Osteoprotegerin, leptin and IL-6: association with silent myocardial ischemia in type 2 diabetes mellitus. Diab Vasc Dis Res 2013; 10: 25-31.
33. Armour KJ, Armour KE,. Inflammation-induced osteoporosis: the IMO model. Methods Mol Med 2003; 80: 353-60.
34. Bai P, Sun Y, Jin J, Hou J, Li R, Zhang Q, et al. Disturbance of the OPG/RANK/RANKL pathway and systemic inflammation in COPD patients with emphysema and osteoporosis. Respir Res 2011; 12: 157.
35. Breuil V, Ticchioni M, Testa J, Roux CH, Ferrari P, Breittmayer JP, et al. Immune changes in post-menopausal osteoporosis: the Immunos study. Osteoporos Int 2010; 21: 805-14.
36. Zhang Z, Fuentes NL, Fuller GM,. Characterization of the IL-6 responsive elements in the γ fibrinogen gene promoter. J Biol Chem 1995; 270: 24287-91.
37. Toriseva M, Kahari VM,. Proteinases in cutaneous wound healing. Cell Mol Life Sci 2009; 66: 203-24.
38. Jenkins G,. The role of proteases in transforming growth factor-β activation. Int J Biochem Cell Biol 2008; 40: 1068-78.
39. Roth D, Piekarek M, Paulsson M, Christ H, Bloch W, Krieg T, et al. Plasmin modulates vascular endothelial growth factor-A-mediated angiogenesis during wound repair. Am J Pathol 2006; 168: 670-84.
40. Jensen T, Kierulf P, Sandset PM, Klingenberg O, Joo GB, Godal HC, et al. Fibrinogen and fibrin induce synthesis of proinflammatory cytokines from isolated peripheral blood mononuclear cells. Thromb Haemost 2007; 97: 822-9.
41. Sitrin RG, Pan PM, Srikanth S, Todd RF III,. Fibrinogen activates NF-κB transcription factors in mononuclear phagocytes. J Immunol 1998; 161: 1462-70.
42. Manolagas SC,. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 2000; 21: 115-37.