Cobalt alloy implant debris induces inflammation and bone loss primarily through danger signaling, not TLR4 activation: Implications for DAMP-ening implant related inflammation

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Samelko, Lauryn ^a   Landgraeber, Stefan ^b   McAllister, Kyron ^a   Jacobs, Joshua ^a   Hallab, Nadim James ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOY; COBALT; CRYOPYRIN; HISTIDINE; INFLAMMASOME; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; INTERLEUKIN 1BETA; TLR4 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALVARIA; CONTROLLED STUDY; GRAM NEGATIVE BACTERIUM; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MALE; METAL BINDING; MONOCYTE; MOUSE; NONHUMAN; OSTEOLYSIS; PARTICLE SIZE; SIGNAL TRANSDUCTION; AGONISTS; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; INFLAMMATION; METABOLISM; OSTEOPOROSIS; PROSTHESES AND ORTHOSES;

ALLOYS; ANIMALS; COBALT; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MONOCYTES; OSTEOPOROSIS; PROSTHESES AND IMPLANTS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84982693502     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0160141     Document Type: Article

References (57)

1. Bosker BH, Ettema HB, van RM, Boomsma MF, Kollen BJ, Maas M, et al. Pseudotumor formation and serum ions after large head metal-on-metal stemmed total hip replacement. Risk factors, time course and revisions in 706 hips. Arch Orthop Trauma Surg 2015 Mar; 135(3):417-25. doi:10.1007/s00402-015-2165-2 PMID: 25663048
2. Madl AK, Liong M, Kovochich M, Finley BL, Paustenbach DJ, Oberdorster G. Toxicology of wear particles of cobalt-chromium alloy metal-on-metal hip implants Part I: Physicochemical properties in patient and simulator studies. Nanomedicine 2015 Mar 3.
3. Samelko L, Caicedo MS, Lim SJ, la-Valle C, Jacobs J, Hallab NJ. Cobalt-alloy implant debris induce HIF-1alpha hypoxia associated responses: a mechanism for metal-specific orthopedic implant failure. PLoS One 2013; 8(6):e67127. doi:10.1371/journal.pone.0067127 PMID: 23840602
4. Dalal A, Pawar V, McAllister K, Weaver C, Hallab NJ. Orthopedic implant cobalt-alloy particles produce greater toxicity and inflammatory cytokines than titanium alloy and zirconium alloy-based particles in vitro, in human osteoblasts, fibroblasts, and macrophages. J Biomed Mater Res A 2012 Aug; 100 (8):2147-58. doi:10.1002/jbm.a.34122 PMID: 22615169
5. Hallab NJ, McAllister K, Brady M, Jarman-Smith M. Macrophage reactivity to different polymers demonstrates particle size- and material-specific reactivity: PEEK-OPTIMA((R)) particles versus UHMWPE particles in the submicron, micron, and 10 micron size ranges. J Biomed Mater Res B Appl Biomater 2011 Nov 21.
6. Caicedo MS, Desai R, McAllister K, Reddy A, Jacobs JJ, Hallab NJ. Soluble and particulate Co-Cr-Mo alloy implant metals activate the inflammasome danger signaling pathway in human macrophages: A novel mechanism for implant debris reactivity. J Orthop Res 2008 Dec 22; 27(7):847-54.
7. Goodman SB. Wear particles, periprosthetic osteolysis and the immune system. Biomater 2007 Dec; 28(34):5044-8.
8. Jacobs JJ, Hallab NJ, Urban RM, Wimmer MA. Wear particles. J Bone Joint Surg Am 2006 Apr; 88 Suppl 2:99-102. PMID: 16595453
9. Dostert C, Petrilli V, Van BR, Steele C, Mossman BT, Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008 May 2; 320(5876):674-7. doi:10.1126/science.1156995 PMID: 18403674
10. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, Reinheckel T, et al. The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 2008 Aug; 9(8):857-65. doi:10.1038/ni.1636 PMID: 18604209
11. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 2008 Aug; 9(8):847-56. doi:10.1038/ni.1631 PMID: 18604214
12. Petrilli V, Papin S, Dostert C, Mayor A, Martinon F, Tschopp J. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ 2007 Sep; 14(9):1583-9. PMID: 17599094
13. Petrilli V, Dostert C, Muruve DA, Tschopp J. The inflammasome: a danger sensing complex triggering innate immunity. Curr Opin Immunol 2007 Dec; 19(6):615-22. PMID: 17977705
14. Caicedo M, Jacobs JJ, Reddy A, Hallab NJ. Analysis of metal ion-induced DNA damage, apoptosis, and necrosis in human (Jurkat) T-cells demonstrates Ni(2+) and V(3+) are more toxic than other metals: Al(3+), Be(2+), Co(2+), Cr(3+), Cu(2+), Fe(3+), Mo(5+), Nb(5+), Zr(2+). J Biomed Mater Res A 2007 Nov 29; 86:905-13.
15. Ting JP, Willingham SB, Bergstralh DT. NLRs at the intersection of cell death and immunity. Nat Rev Immunol 2008 May; 8(5):372-9. doi:10.1038/nri2296 PMID: 18362948
16. Janeway CA Jr., Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002; 20:197-216. PMID: 11861602
17. Schmidt M, Raghavan B, Muller V, Vogl T, Fejer G, Tchaptchet S, et al. Crucial role for human Toll-like receptor 4 in the development of contact allergy to nickel. Nat Immunol 2010Sep; 11(9):814-9. doi:10.1038/ni.1919 PMID: 20711192
18. Raghavan B, Martin SF, Esser PR, Goebeler M, Schmidt M. Metal allergens nickel and cobalt facilitate TLR4 homodimerization independently of MD2. EMBO Rep 2012 Dec; 13(12):1109-15. doi:10.1038/embor.2012.155 PMID: 23059983
19. Oblak A, Pohar J, Jerala R. MD-2 Determinants of Nickel and Cobalt-Mediated Activation of Human TLR4. PLoS One 2015; 10(3):e0120583. doi:10.1371/journal.pone.0120583 PMID: 25803856
20. Greenfield EM, Beidelschies MA, Tatro JM, Goldberg VM, Hise AG. Bacterial pathogen-associated molecular patterns stimulate biological activity of orthopaedic wear particles by activating cognate Toll-like receptors. J Biol Chem 2010 Oct 15; 285(42):32378-84. doi:10.1074/jbc.M110.136895 PMID: 20729214
21. Pearl JI, Ma T, Irani AR, Huang Z, Robinson WH, Smith RL, et al. Role of the Toll-like receptor pathway in the recognition of orthopedic implant wear-debris particles. Biomater 2011 Aug; 32(24):5535-42.
22. Lahdeoja T, Pajarinen J, Kouri VP, Sillat T, Salo J, Konttinen YT. Toll-like receptors and aseptic loosening of hip endoprosthesis - a potential to respond against danger signals? J Orthop Res 2010 Feb; 28(2):184-90. doi:10.1002/jor.20979 PMID: 19725103
23. Tamaki Y, Takakubo Y, Hirayama T, Konttinen YT, Goodman SB, Yamakawa M, et al. Expression of Toll-like receptors and their signaling pathways in rheumatoid synovitis. J Rheumatol 2011 May; 38(5):810-20. doi:10.3899/jrheum.100732 PMID: 21324962
24. Caicedo MS, Samelko L, McAllister K, Jacobs JJ, Hallab NJ. Increasing both CoCrMo-alloy particle size and surface irregularity induces increased macrophage inflammasome activation in vitro potentially through lysosomal destabilization mechanisms. J Orthop Res 2013 Oct; 31(10):1633-42. doi:10.1002/jor.22411 PMID: 23794526
25. Lamkanfi M, Sarkar A, Vande WL, Vitari AC, Amer AO, Wewers MD, et al. Inflammasome-dependent release of the alarmin HMGB1 in endotoxemia. J Immunol 2010 Oct 1; 185(7):4385-92. doi:10.4049/jimmunol.1000803 PMID: 20802146
26. Lu B, Wang H, Andersson U, Tracey KJ. Regulation of HMGB1 release by inflammasomes. Protein Cell 2013 Mar; 4(3):163-7. doi:10.1007/s13238-012-2118-2 PMID: 23483477
27. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 2007Jan; 81(1):1-5.
28. Hirsiger S, Simmen HP, Werner CM, Wanner GA, Rittirsch D. Danger signals activating the immune response after trauma. Mediators Inflamm 2012; 2012:315941. doi:10.1155/2012/315941 PMID: 22778496
29. Sloane JA, Blitz D, Margolin Z, Vartanian T. A clear and present danger: endogenous ligands of Toll-like receptors. Neuromolecular Med 2010 Jun; 12(2):149-63. doi:10.1007/s12017-009-8094-x PMID: 19830599
30. Park JS, Gamboni-Robertson F, He Q, Svetkauskaite D, Kim JY, Strassheim D, et al. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol 2006Mar; 290(3):C917-C924. PMID: 16267105
31. Vabulas RM, hmad-Nejad P, da CC, Miethke T, Kirschning CJ, Hacker H, et al. Endocytosed HSP60s use toll-like receptor 2 (TLR2) and TLR4 to activate the toll/interleukin-1 receptor signaling pathway in innate immune cells. J Biol Chem 2001 Aug 17; 276(33):31332-9. PMID: 11402040
32. Hallab NJ, Jacobs JJ. Biologic effects of implant debris. Bull NYU Hosp Jt Dis 2009; 67(2):182-8. PMID: 19583551
33. Caicedo MS, Pennekamp PH, McAllister K, Jacobs JJ, Hallab NJ. Soluble ions more than particulate cobalt-alloy implant debris induce monocyte costimulatory molecule expression and release of proinflammatory cytokines critical to metal-induced lymphocyte reactivity. J Biomed Mater Res A 2010 Jun 15; 93(4):1312-21. doi:10.1002/jbm.a.32627 PMID: 19844976
34. Casey LC, Balk RA, Bone RC. Plasma cytokine and endotoxin levels correlate with survival in patients with the sepsis syndrome. Ann Intern Med 1993 Oct 15; 119(8):771-8. PMID: 8379598
35. Opal SM, Scannon PJ, Vincent JL, White M, Carroll SF, Palardy JE, et al. Relationship between plasma levels of lipopolysaccharide (LPS) and LPS-binding protein in patients with severe sepsis and septic shock. J Infect Dis 1999 Nov; 180(5):1584-9. PMID: 10515819
36. Paladini F, Cocco E, Potolicchio I, Fazekasova H, Lombardi G, Fiorillo MT, et al. Divergent effect of cobalt and beryllium salts on the fate of peripheral blood monocytes and T lymphocytes. Toxicol Sci 2011Feb; 119(2):257-69. doi:10.1093/toxsci/kfq328 PMID: 20974702
37. Takashiba S, Van Dyke TE, Amar S, Murayama Y, Soskolne AW, Shapira L. Differentiation of monocytes to macrophages primes cells for lipopolysaccharide stimulation via accumulation of cytoplasmic nuclear factor kappaB. Infect Immun 1999Nov; 67(11):5573-8. PMID: 10531202
38. Bauernfeind F, Hornung V. Of inflammasomes and pathogens - sensing of microbes by the inflammasome. EMBO Mol Med 2013 Jun; 5(6):814-26. doi:10.1002/emmm.201201771 PMID: 23666718
39. Bauernfeind FG, Horvath G, Stutz A, Alnemri ES, MacDonald K, Speert D, et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol 2009 Jul 15; 183(2):787-91. doi:10.4049/jimmunol.0901363 PMID: 19570822
40. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010 Apr 29; 464(7293):1357-61. doi:10.1038/nature08938 PMID: 20428172
41. Green JM, Hallab NJ, Liao YS, Narayan V, Schwarz EM, Xie C. Anti-oxidation treatment of ultra high molecular weight polyethylene components to decrease periprosthetic osteolysis: evaluation of osteolytic and osteogenic properties of wear debris particles in a murine calvaria model. Curr Rheumatol Rep 2013 May; 15(5):325. doi:10.1007/s11926-013-0325-3 PMID: 23532463
42. 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 Jan; 154(1):203-10. PMID: 9916934
43. Greenfield EM, Bi Y, Ragab AA, Goldberg VM, Nalepka JL, Seabold JM. Does endotoxin contribute to aseptic loosening of orthopedic implants? J Biomed Mater Res B Appl Biomater 2005 Jan 15; 72(1):179-85. PMID: 15449253
44. Ward JR, West PW, Ariaans MP, Parker LC, Francis SE, Crossman DC, et al. Temporal interleukin-1beta secretion from primary human peripheral blood monocytes by P2X7-independent and P2X7-dependent mechanisms. J Biol Chem 2010 Jul 23; 285(30):23147-58. doi:10.1074/jbc.M109.072793 PMID: 20495003
45. Burton L, Paget D, Binder NB, Bohnert K, Nestor BJ, Sculco TP, et al. Orthopedic wear debris mediated inflammatory osteolysis is mediated in part by NALP3 inflammasome activation. J Orthop Res 2013 Jan; 31(1):73-80. doi:10.1002/jor.22190 PMID: 22933241
46. Caicedo MS, Samelko L, McAllister K, Jacobs JJ, Hallab NJ. Increasing both CoCrMo-alloy particle size and surface irregularity induces increased macrophage inflammasome activation in vitro potentially through lysosomal destabilization mechanisms. J Orthop Res 2013 Oct; 31(10):1633-42. doi:10.1002/jor.22411 PMID: 23794526
47. Guarda G, Braun M, Staehli F, Tardivel A, Mattmann C, Forster I, et al. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 2011 Feb 25; 34(2):213-23. doi:10.1016/j.immuni.2011.02.006 PMID: 21349431
48. Grutz G. New insights into the molecular mechanism of interleukin-10-mediated immunosuppression. J Leukoc Biol 2005 Jan; 77(1):3-15. PMID: 15522916
49. Gurung P, Li B, Subbarao Malireddi RK, Lamkanfi M, Geiger TL, Kanneganti TD. Chronic TLR Stimulation Controls NLRP3 Inflammasome Activation through IL-10 Mediated Regulation of NLRP3 Expression and Caspase-8 Activation. Sci Rep 2015; 5:14488. doi:10.1038/srep14488 PMID: 26412089
50. Tyson-Capper AJ, Lawrence H, Holland JP, Deehan DJ, Kirby JA. Metal-on-metal hips: cobalt can induce an endotoxin-like response. Ann Rheum Dis 2013 Mar; 72(3):460-1. doi:10.1136/annrheumdis-2012-202468 PMID: 23076072
51. Bi Y, Collier TO, Goldberg VM, Anderson JM, Greenfield EM. Adherent endotoxin mediates biological responses of titanium particles without stimulating their phagocytosis. J Orthop Res 2002 Jul; 20(4):696-703. PMID: 12168657
52. Gordon A, Greenfield EM, Eastell R, Kiss-Toth E, Wilkinson JM. Individual susceptibility to periprosthetic osteolysis is associated with altered patterns of innate immune gene expression in response to pro-inflammatory stimuli. J Orthop Res 2010 Sep; 28(9):1127-35. doi:10.1002/jor.21135 PMID: 20225323
53. Gordon A, Kiss-Toth E, Stockley I, Eastell R, Wilkinson JM. Polymorphisms in the interleukin-1 receptor antagonist and interleukin-6 genes affect risk of osteolysis in patients with total hip arthroplasty. Arthritis Rheum 2008Oct; 58(10):3157-65. doi:10.1002/art.23863 PMID: 18821666
54. Hallab NJ, Vermes C, Messina C, Roebuck KA, Glant TT, Jacobs JJ. Concentration- and composition-dependent effects of metal ions on human MG-63 osteoblasts. J Biomed Mater Res 2002 Jun 5; 60(3):420-33. PMID: 11920666
55. Lawrence H, Deehan D, Holland J, Kirby J, Tyson-Capper A. The immunobiology of cobalt: demonstration of a potential aetiology for inflammatory pseudotumours after metal-on-metal replacement of the hip. Bone Joint J 2014 Sep; 96-B(9):1172-7. doi:10.1302/0301-620X.96B9.33476 PMID: 25183586
56. Kim SY, Choi YJ, Joung SM, Lee BH, Jung YS, Lee JY. Hypoxic stress up-regulates the expression of Toll-like receptor 4 in macrophages via hypoxia-inducible factor. Immunology 2010 Apr; 129(4):516-24. doi:10.1111/j.1365-2567.2009.03203.x PMID: 20002786
57. Mishra KP, Jain S, Ganju L, Singh SB. Hypoxic Stress Induced TREM-1 and Inflammatory Chemokines in Human Peripheral Blood Mononuclear Cells. Indian J Clin Biochem 2014 Apr; 29(2):133-8. doi:10.1007/s12291-013-0345-9 PMID: 24757292