Macrophage migration inhibitory factor is essential for osteoclastogenic mechanisms in vitro and in vivo mouse model of arthritis

Cytokine

Volumn 72, Issue 2, 2015, Pages 135-145

  Gu, Ran ^a   Santos, Leilani L ^a   Ngo, Devi ^a   Fan, HuaPeng ^a   Singh, Preetinder P ^b   Fingerle Rowson, Gunter ^c   Bucala, Richard ^d   Xu, Jiake ^e   Quinn, Julian M W ^a,b   Morand, Eric F ^a  

^a MONASH UNIVERSITY   (Australia)

^b HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Bone; Cell signals; Cytokines; Inflammation; Transcription factors

Indexed keywords

CD74 ANTIGEN; MACROPHAGE MIGRATION INHIBITION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; OSTEOCLAST DIFFERENTIATION FACTOR; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR RELA; B LYMPHOCYTE ANTIGEN; HLA ANTIGEN CLASS 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INVARIANT CHAIN; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE; BONE EROSION; CONTROLLED STUDY; DNA POLYMORPHISM; ENZYME PHOSPHORYLATION; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MALE; MOUSE; MOUSE MODEL; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; PROMOTER REGION; PROTEIN PHOSPHORYLATION; RHEUMATOID ARTHRITIS; SYNOVIUM; TRANSCRIPTION INITIATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DEFICIENCY; DISEASE MODEL; GENETICS; IMMUNOLOGY; METABOLISM; OSTEOLYSIS; PATHOPHYSIOLOGY; PHYSIOLOGY;

MUS;

ANIMALS; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; ARTHRITIS, RHEUMATOID; BONE RESORPTION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HISTOCOMPATIBILITY ANTIGENS CLASS II; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MICE; MICE, INBRED C57BL; NF-KAPPA B; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; RANK LIGAND; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; SYNOVIAL MEMBRANE;

EID: 84922068493     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2014.11.015     Document Type: Article

References (52)

1. Morand E.F., Leech M., Bernhagen J. MIF: a new cytokine link between rheumatoid arthritis and atherosclerosis. Nat Rev Drug Discov 2006, 5:399-410.
2. Bernhagen J., Calandra T., Mitchell R.A., Martin S.B., Tracey K.J., Voelter W., et al. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 1993, 365:756-759.
3. Santos L., Hall P., Metz C., Bucala R., Morand E.F. Role of macrophage migration inhibitory factor (MIF) in murine antigen-induced arthritis: interaction with glucocorticoids. Clin Exp Immunol 2001, 123:309-314.
4. Gregory J.L., Morand E.F., McKeown S.J., Ralph J.A., Hall P., Yang Y.H., et al. Macrophage migration inhibitory factor induces macrophage recruitment via CC chemokine ligand 2. J Immunol 2006, 177:8072-8079.
5. Fan H., Hall P., Santos L.L., Gregory J.L., Fingerle-Rowson G., Bucala R., et al. Macrophage migration inhibitory factor and CD74 regulate macrophage chemotactic responses via MAPK and Rho GTPase. J Immunol 2011, 186:4915-4924.
6. Lacey D., Sampey A., Mitchell R., Bucala R., Santos L., Leech M., et al. Control of fibroblast-like synoviocyte proliferation by macrophage migration inhibitory factor. Arthritis Rheum 2003, 48:103-109.
7. Sampey A.V., Hall P.H., Mitchell R.A., Metz C.N., Morand E.F. Regulation of synoviocyte phospholipase A2 and cyclooxygenase 2 by macrophage migration inhibitory factor. Arthritis Rheum 2001, 44:1273-1280.
8. Onodera S., Kaneda K., Mizue Y., Koyama Y., Fujinaga M., Nishihira J. Macrophage migration inhibitory factor up-regulates expression of matrix metalloproteinases in synovial fibroblasts of rheumatoid arthritis. J Biol Chem 2000, 275:444-450.
9. Morand E.F., Leech M., Weedon H., Metz C., Bucala R., Smith M.D. Macrophage migration inhibitory factor in rheumatoid arthritis: clinical correlations. Rheumatology (Oxford) 2002, 41:558-562.
10. Mikulowska A., Metz C.N., Bucala R., Holmdahl R. Macrophage migration inhibitory factor is involved in the pathogenesis of collagen type II-induced arthritis in mice. J Immunol 1997, 158:5514-5517.
11. Santos L.L., Fan H., Hall P., Ngo D., Mackay C.R., Fingerle-Rowson G., et al. Macrophage migration inhibitory factor regulates neutrophil chemotactic responses in inflammatory arthritis in mice. Arthritis Rheum 2011, 63:960-970.
12. Leng L., Metz C.N., Fang Y., Xu J., Donnelly S., Baugh J., et al. MIF signal transduction initiated by binding to CD74. J Exp Med 2003, 197:1467-1476.
13. Shi X., Leng L., Wang T., Wang W., Du X., Li J., et al. CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 2006, 25:595-606.
14. Takahashi K., Koga K., Linge H.M., Zhang Y., Lin X., Metz C.N., et al. Macrophage CD74 contributes to MIF-induced pulmonary inflammation. Respir Res 2009, 10:33.
15. Nakashima T., Takayanagi H. New regulation mechanisms of osteoclast differentiation. Ann N Y Acad Sci 2011, 1240:E13-E18.
16. Blair H.C., Robinson L.J., Zaidi M. Osteoclast signalling pathways. Biochem Biophys Res Commun 2005, 328:728-738.
17. Romas E., Bakharevski O., Hards D.K., Kartsogiannis V., Quinn J.M., Ryan P.F., et al. Expression of osteoclast differentiation factor at sites of bone erosion in collagen-induced arthritis. Arthritis Rheum 2000, 43:821-826.
18. Pettit A.R., Ji H., Stechow von D., Müller R., Goldring S.R., Choi Y., et al. TRANCE/RANKL knockout mice are protected from bone erosion in a serum transfer model of arthritis. Am J Pathol 2001, 159:1689-1699.
19. Schett G. Effects of inflammatory and anti-inflammatory cytokines on the bone. Eur J Clin Invest 2011, 41:1361-1366.
20. Radstake T.R.D.J., Sweep F.C.G.J., Welsing P., Franke B., Vermeulen S.H.H.M., Geurts-Moespot A., et al. Correlation of rheumatoid arthritis severity with the genetic functional variants and circulating levels of macrophage migration inhibitory factor. Arthritis Rheum 2005, 52:3020-3029.
21. Oshima S., Onodera S., Amizuka N., Li M., Irie K., Watanabe S., et al. Macrophage migration inhibitory factor-deficient mice are resistant to ovariectomy-induced bone loss. FEBS Lett 2006, 580:1251-1256.
22. Madeira M.F.M., Queiroz C.M., Costa G.M., Santos P.C., Silveira E.M., Garlet G.P., et al. MIF induces osteoclast differentiation and contributes to progression of periodontal disease in mice. Microbes Infect 2012, 14:198-206.
23. Kobayashi T., Onodera S., Kondo E., Tohyama H., Fujiki H., Yokoyama A., et al. Impaired fracture healing in macrophage migration inhibitory factor-deficient mice. Osteoporos Int 2011, 22:1955-1965.
24. Onodera S., Sasaki S., Ohshima S., Amizuka N., Li M., Udagawa N., et al. Transgenic mice overexpressing macrophage migration inhibitory factor (MIF) exhibit high-turnover osteoporosis. J Bone Miner Res 2006, 21:876-885.
25. Jacquin C., Koczon-Jaremko B., Aguila H.L., Leng L., Bucala R., Kuchel G.A., et al. Macrophage migration inhibitory factor inhibits osteoclastogenesis. Bone 2009, 45:640-649.
26. Mun S.H., Won H.Y., Hernandez P., Aguila H.L., Lee S.-K. Deletion of CD74, a putative MIF receptor, in mice enhances osteoclastogenesis and decreases bone mass. J Bone Miner Res 2013, 28:948-959.
27. Fingerle-Rowson G., Petrenko O., Metz C.N., Forsthuber T.G., Mitchell R., Huss R., et al. The p53-dependent effects of macrophage migration inhibitory factor revealed by gene targeting. Proc Natl Acad Sci USA 2003, 100:9354-9359.
28. Cook A.D., Turner A.L., Braine E.L., Pobjoy J., Lenzo J.C., Hamilton J.A. Regulation of systemic and local myeloid cell subpopulations by bone marrow cell-derived granulocyte-macrophage colony-stimulating factor in experimental inflammatory arthritis. Arthritis Rheum 2011, 63:2340-2351.
29. Aeberli D., Yang Y., Mansell A., Santos L., Leech M., Morand E.F. Endogenous macrophage migration inhibitory factor modulates glucocorticoid sensitivity in macrophages via effects on MAP kinase phosphatase-1 and p38 MAP kinase. FEBS Lett 2006, 580:974-981.
30. Wang C., Steer J.H., Joyce D.A., Yip K.H.M., Zheng M.H., Xu J. 12-O-tetradecanoylphorbol-13-acetate (TPA) inhibits osteoclastogenesis by suppressing RANKL-induced NF-kappaB activation. J Bone Miner Res 2003, 18:2159-2168.
31. Singh P.P., van der Kraan A.G.J., Xu J., Gillespie M.T., Quinn J.M.W. Membrane-bound receptor activator of NFκB ligand (RANKL) activity displayed by osteoblasts is differentially regulated by osteolytic factors. Biochem Biophys Res Commun 2012, 422:48-53.
32. Mitchell R.A., Liao H., Chesney J., Fingerle-Rowson G., Baugh J., David J., et al. Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc Natl Acad Sci USA 2002, 99:345-350.
33. Leech M., Metz C., Hall P., Hutchinson P., Gianis K., Smith M., et al. Macrophage migration inhibitory factor in rheumatoid arthritis: evidence of proinflammatory function and regulation by glucocorticoids. Arthritis Rheum 1999, 42:1601-1608.
34. Leech M., Metz C., Santos L., Peng T., Holdsworth S.R., Bucala R., et al. Involvement of macrophage migration inhibitory factor in the evolution of rat adjuvant arthritis. Arthritis Rheum 1998, 41:910-917.
35. Onodera S., Oshima S., Nishihira J., Yasuda K., Tohyama H., Irie K., et al. Active immunization against macrophage migration inhibitory factor using a novel DNA vaccine prevents ovariectomy-induced bone loss in mice. Vaccine 2008, 26:829-836.
36. Onodera S., Suzuki K., Matsuno T., Kaneda K., Kuriyama T., Nishihira J. Identification of macrophage migration inhibitory factor in murine neonatal calvariae and osteoblasts. Immunology 1996, 89:430-435.
37. Toh M.-L., Aeberli D., Lacey D., Yang Y., Santos L.L., Clarkson M., et al. Regulation of IL-1 and TNF receptor expression and function by endogenous macrophage migration inhibitory factor. J Immunol 2006, 177:4818-4825.
38. Vaira S., Alhawagri M., Anwisye I., Kitaura H., Faccio R., Novack D.V. RelA/p65 promotes osteoclast differentiation by blocking a RANKL-induced apoptotic JNK pathway in mice. J Clin Invest 2008, 118:2088-2097.
39. Nakamura H., Hirata A., Tsuji T., Yamamoto T. Role of osteoclast extracellular signal-regulated kinase (ERK) in cell survival and maintenance of cell polarity. J Bone Miner Res 2003, 18:1198-1205.
40. Matsumoto M., Sudo T., Saito T., Osada H., Tsujimoto M. Involvement of p38 mitogen-activated protein kinase signaling pathway in osteoclastogenesis mediated by receptor activator of NF-kappa B ligand (RANKL). J Biol Chem 2000, 275:31155-31161.
41. Li H., Zhai Z., Liu G., Tang T., Lin Z., Zheng M., et al. Sanguinarine inhibits osteoclast formation and bone resorption via suppressing RANKL-induced activation of NF-κB and ERK signaling pathways. Biochem Biophys Res Commun 2013, 430:951-956.
42. Ralph J.A., Ahmed A.U., Santos L.L., Clark A.R., McMorrow J., Murphy E.P., et al. Identification of NURR1 as a mediator of MIF signaling during chronic arthritis: effects on glucocorticoid-induced MKP1. Am J Pathol 2010, 177:2366-2378.
43. Jeffrey K.L., Camps M., Rommel C., Mackay C.R. Targeting dual-specificity phosphatases: manipulating MAP kinase signalling and immune responses. Nat Rev Drug Discov 2007, 6:391-403.
44. Greven D., Leng L., Bucala R. Autoimmune diseases: MIF as a therapeutic target. Expert Opin Ther Targets 2010, 14:253-264.
45. Honma N., Koseki H., Akasaka T., Nakayama T., Taniguchi M., Serizawa I., et al. Deficiency of the macrophage migration inhibitory factor gene has no significant effect on endotoxaemia. Immunology 2000, 100:84-90.
46. Ohkawara T., Koyama Y., Onodera S., Takeda H., Kato M., Asaka M., et al. DNA vaccination targeting macrophage migration inhibitory factor prevents murine experimental colitis. Clin Exp Immunol 2011, 163:113-122.
47. Herrero L.J., Nelson M., Srikiatkhachorn A., Gu R., Anantapreecha S., Fingerle-Rowson G., et al. Critical role for macrophage migration inhibitory factor (MIF) in Ross River virus-induced arthritis and myositis. Proc Natl Acad Sci USA 2011, 108:12048-12053.
48. Santos L.L., Dacumos A., Yamana J., Sharma L., Morand E.F. Reduced arthritis in MIF deficient mice is associated with reduced T cell activation: down-regulation of ERK MAP kinase phosphorylation. Clin Exp Immunol 2008, 152:372-380.
49. Bucala R. MIF, MIF alleles, and prospects for therapeutic intervention in autoimmunity. J Clin Immunol 2013, 33(Suppl 1):S72-S78.
50. Hertig A., Rondeau E. Role of the coagulation/fibrinolysis system in fibrin-associated glomerular injury. J Am Soc Nephrol 2004, 15:844-853.
51. Quinn J.M.W., Sims N.A., Saleh H., Mirosa D., Thompson K., Bouralexis S., et al. IL-23 inhibits osteoclastogenesis indirectly through lymphocytes and is required for the maintenance of bone mass in mice. J Immunol 2008, 181:5720-5729.
52. Chen L., Wei X.-Q., Evans B., Jiang W., Aeschlimann D. IL-23 promotes osteoclast formation by up-regulation of receptor activator of NF-kappaB (RANK) expression in myeloid precursor cells. Eur J Immunol 2008, 38:2845-2854.