Wear debris inhibition of anti-osteoclastogenic signaling by interleukin-6 and interferon-γ: Mechanistic insights and implications for periprosthetic osteolysis

Journal of Bone and Joint Surgery

Volumn 88, Issue 4, 2006, Pages 788-799

  Rakshit, Diptendu S ^a   Ly, Khanh ^a   Sengupta, Tapas K ^b   Nestor, Bryan J ^a   Sculco, Thomas P ^a   Ivashkiv, Lionel B ^a   Purdue, P Edward ^a  

^a HOSPITAL FOR SPECIAL SURGERY   (United States)

^b Philip Morris USA Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BONE CEMENT; COLONY STIMULATING FACTOR 1; GAMMA INTERFERON; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38; OSTEOCLAST DIFFERENTIATION FACTOR; POLY(METHYL METHACRYLATE); STAT1 PROTEIN; STAT3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; SUPPRESSOR OF CYTOKINE SIGNALING 1; SUPPRESSOR OF CYTOKINE SIGNALING 3; TITANIUM; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL DIFFERENTIATION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MACROPHAGE; OSTEOCLAST; OSTEOLYSIS; PERIPROSTHETIC OSTEOLYSIS; PRIORITY JOURNAL; PROSTHESIS FAILURE; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELL; TOTAL HIP PROSTHESIS;

EID: 33645678219     PISSN: 00219355     EISSN: None     Source Type: Journal    
DOI: 10.2106/JBJS.E.00711     Document Type: Article

References (42)

1. Saleh KJ, Thongtrangan I, Schwarz EM. Osteolysis: medical and surgical approaches. Clin Orthop Relat Res. 2004;427:138-47.
2. Jacobs JJ, Roebuck KA, Archibeck M, Hallab NJ, Glant TT. Osteolysis: basic science. Clin Orthop Relat Res. 2001;393:71-7.
3. Wooley PH, Schwarz EM. Aseptic loosening. Gene Ther. 2004;11:402-7.
4. Blaine TA, Rosier RN, Puzas JE, Looney RJ, Reynolds PR, Reynolds SD, O'Keefe RJ. Increased levels of tumor necrosis factor-alpha and interleukin-6 protein and messenger RNA in human peripheral blood monocytes due to titanium particles. J Bone Joint Surg Am. 1996;78:1181-92.
5. Nakashima Y, Sun DH, Trindade MC, Maloney WJ, Goodman SB, Schurman DJ, Smith RL. Signaling pathways for tumor necrosis factor-alpha and interleukin-6 expression in human macrophages exposed to titanium-alloy particulate debris in vitro. J Bone Joint Surg Am. 1999;81:603-15.
6. Merkel KD, Erdmann JM, McHugh KP, Abu-Amer Y, Ross FP, Teitelbaum SL. Tumor necrosis factor-alpha mediates orthopedic implant osteolysis. Am J Pathol. 1999;154:203-10.
7. Ingham E, Green TR, Stone MH, Kowalski R, Watkins N, Fisher J. Production of TNF-alpha and bone resorbing activity by macrophages in response to different types of bone cement particles. Biomaterials. 2000;21:1005-13.
8. Chiba J, Rubash HE, Kim KJ, Iwaki Y. The characterization of cytokines in the interface tissue obtained from failed cementless total hip arthroplasty with and without femoral osteolysis. Clin Orthop Relat Res. 1994;300:304-12.
9. Stea S, Visentin M, Granchi D, Ciapetti G, Donati ME, Sudanese A, Zanotti C, Toni A. Cytokines and osteolysis around total hip prostheses. Cytokine. 2000;12:1575-9.
10. Takayanagi H, Ogasawara K, Hida S, Chiba T, Murata S, Sato K, Takaoka A, Yokochi T, Oda H, Tanaka K, Nakamura K, Taniguchi T. T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-gamma. Nature. 2000;408:600-5.
11. Hernigou P, Intrator L, Bahrami T, Bensussan A, Farcet JP. Interleukin-6 in the blood of patients with total hip arthroplasty without loosening. Clin Orthop Relat Res. 1999;366:147-54.
12. Sims NA, Jenkins BJ, Quinn JM, Nakamura A, Glatt M, Gillespie MT, Ernst M, Martin TJ. Glycoprotein 130 regulates bone turnover and bone size by distinct downstream signaling pathways. J Clin Invest. 2004;113:379-89.
13. Ohishi M, Matsumura Y, Aki D, Mashima R, Taniguchi K, Kobayashi T, Kukita T, Iwamoto Y, Yoshimura A. Suppressors of cytokine signaling-1 and -3 regulate osteoclastogenesis in the presence of inflammatory cytokines. J Immunol. 2005;174:3024-31.
14. Sengupta TK, Talbot ES, Scherle PA, Ivashkiv LB. Rapid inhibition of interleukin-6 signaling and Stat3 activation mediated by mitogen-activated protein kinases. Proc Natl Acad Sci USA. 1998;95:11107-12.
15. Ahmed ST, Ivashkiv LB. Inhibition of IL-6 and IL-10 signaling and Stat activation by inflammatory and stress pathways. J Immunol. 2000;165:5227-37.
16. Kubo M, Hanada T, Yoshimura A. Suppressors of cytokine signaling and immunity. Nat Immunol. 2003;4:1169-76.
17. Sengupta TK, Schmitt EM, Ivashkiv LB. Inhibition of cytokines and JAK-STAT activation by distinct signaling pathways. Proc Natl Acad Sci USA. 1996;93:9499-504.
18. Huang W, Drissi MH, O'Keefe RJ, Schwarz EM. A rapid multiparameter approach to study factors that regulate osteoclastogenesis: demonstration of the combinatorial dominant effects of TNF-alpha and TGF-ss in RANKL-mediated osteoclastogenesis. Calcif Tissue Int. 2003;73:584-93.
19. Clohisy JC, Hirayama T, Frazier E, Han SK, Abu-Amer Y. NF-kB signaling blockade abolishes implant particle-induced osteoclastogenesis. J Orthop Res. 2004;22:13-20.
20. Karsdal MA, Hjorth P, Henriksen K, Kirkegaard T, Nielsen KL, Lou H, Delaisse JM, Foged NT. Transforming growth factor-beta controls human osteoclastogenesis through the p38 MAPK and regulation of RANK expression. J Biol Chem. 2003;278:44975-87.
21. Nicholson GC, Malakellis M, Collier FM, Cameron PU, Holloway WR, Gough TJ, Gregorio-King C, Kirkland MA, Myers DE. Induction of osteoclasts from CD14-positive human peripheral blood mononuclear cells by receptor activator of nuclear factor kappaB ligand (RANKL). Clin Sci (Lond). 2000;99:133-40.
22. Hu X, Li WP, Meng C, Ivashkiv LB. Inhibition of IFN-gamma signaling by glucocorticoids. J Immunol. 2003;170:4833-9.
23. Antoniv TT, Park-Min KH, Ivashkiv LB. Kinetics of IL-10-induced gene expression in human macrophages. Immunobiology. 2005;210:87-95.
24. Wooley PH, Morren R, Andary J, Sud S, Yang SY, Mayton L, Markel D, Sieving A, Nasser S. Inflammatory responses to orthopaedic biomaterials in the murine air pouch. Biomaterials. 2002;23:517-26.
25. Childs LM, Goater JJ, O'Keefe RJ, Schwarz EM. Efficacy of etanercept for wear debris-induced osteolysis. J Bone Miner Res. 2001;16:338-47.
26. Bukata SV, Gelinas J, Wei X, Rosier RN, Puzas JE, Zhang X, Schwarz EM, Song XY, Griswold DE, O'Keefe RJ. PGE2 and IL-6 production by fibroblasts in response to titanium wear debris particles is mediated through a Cox-2 dependent pathway. J Orthop Res. 2004;22:6-12.
27. Manlapaz M, Maloney WJ, Smith RL. In vitro activation of human fibroblasts by retrieved titanium alloy wear debris. J Orthop Res. 1996;14:465-72.
28. Wang ML, Tuli R, Manner PA, Sharkey PF, Hall DJ, Tuan RS. Direct and indirect induction of apoptosis in human mesenchymal stem cells in response to titanium particles. J Orthop Res. 2003;21:697-707.
29. Vermes C, Chandrasekaran R, Jacobs JJ, Galante JO, Roebuck KA, Glant TT. The effects of particulate wear debris, cytokines, and growth factors on the functions of MG-63 osteoblasts. J Bone Joint Surg Am. 2001;83:201-11.
30. Sandhu J, Waddell JE, Henry M, Boynton EL. The role of T cells in polyethylene particulate induced inflammation. J Rheumatol. 1998;25:1794-9.
31. Taki N, Tatro JM, Nalepka JL, Togawa O, Goldberg VM, Rimnac CM, Greenfield EM. Polyethylene and titanium particles induce osteolysis by similar, lymphocyte-independent, mechanisms. J Orthop Res. 2005;23:376-83.
32. Hallab NJ, Anderson S, Caicedo M, Skipor A, Campbell P, Jacobs JJ. Immune responses correlate with serum-metal in metal-on-metal hip arthroplasty. J Arthroplasty. 2004;19(8 Suppl 3):88-93.
33. Teng YT, Mahamed D, Singh B. Gamma interferon positively modulates Actinobacillus actinomycetemcomitans-specific RANKL+ CD4+ Th-cell-mediated alveolar bone destruction in vivo. Infect Immun. 2005;73:3453-61.
34. Kamimura D, Ishihara K, Hirano T. IL-6 signal transduction and its physiological roles: the signal orchestration model. Rev Physiol Biochem Pharmacol. 2003;149:1-38.
35. Kudo O, Sabokbar A, Pocock A, Itonaga I, Fujikawa Y, Athanasou NA. Interleukin-6 and interleukin-11 support human osteoclast formation by a RANKL-independent mechanism. Bone. 2003;32:1-7.
36. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, Morony S, Oliveira-dos-Santos AJ, Van G, Itie A, Khoo W, Wakeham A, Dunstan CR, Lacey DL, Mak TW, Boyle WJ, Penninger JM. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 1999;397:315-23.
37. Childs LM, Paschalis EP, Xing L, Dougall WC, Anderson D, Boskey AL, Puzas JE, Rosier RN, O'Keefe RJ, Boyce BF, Schwarz EM. In vivo RANK signaling blockade using the receptor activator of NF-kappaB:Fc effectively prevents and ameliorates wear debris-induced osteolysis via osteoclast depletion without inhibiting osteogenesis. J Bone Miner Res. 2002;17:192-9.
38. Goater JJ, O'Keefe RJ, Rosier RN, Puzas JE, Schwarz EM. Efficacy of ex vivo OPG gene therapy in preventing wear debris induced osteolysis. J Orthop Res. 2002;20:169-73.
39. Sutherland MK, Brady H, Gayo-Fung LM, Leisten J, Lipps SG, McKie JA, O'Leary E, Patnaik N, Anderson DW, Bhagwat SS, Stein B. Effects of SP500263, a novel selective estrogen receptor modulator, on bone, uterus, and serum cholesterol in the ovariectomized rat. Calcif Tissue Int. 2003;72:710-6.
40. Shuai K, Liu B. Regulation of JAK-STAT signalling in the immune system. Nat Rev Immunol. 2003;3:900-11.
41. Fox SW, Haque SJ, Lovibond AC, Chambers TJ. The possible role of TGF-beta-induced suppressors of cytokine signaling expression in osteoclast/macrophage lineage commitment in vitro. J Immunol. 2003;170:3679-87.
42. Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature. 2003;423:337-42.