Ionic cobalt but not metal particles induces ROS generation in immune cells in vitro
Kathrin Chamaon
Department of Orthopaedic Surgery, Otto-von-Guericke University, Leipziger Str. 44, 39120, Magdeburg, Germany
Search for more papers by this authorPeter Schönfeld
Institute for Biochemistry and Cell Biology, Otto-von-Guericke University, Leipziger Str. 44, 39120, Magdeburg, Germany
Search for more papers by this authorFriedemann Awiszus
Department of Orthopaedic Surgery, Otto-von-Guericke University, Leipziger Str. 44, 39120, Magdeburg, Germany
Search for more papers by this authorJessica Bertrand
Department of Orthopaedic Surgery, Otto-von-Guericke University, Leipziger Str. 44, 39120, Magdeburg, Germany
These authors contributed equally to this work.Search for more papers by this authorCorresponding Author
Christoph H. Lohmann
Department of Orthopaedic Surgery, Otto-von-Guericke University, Leipziger Str. 44, 39120, Magdeburg, Germany
These authors contributed equally to this work.Correspondence to: C. H. Lohmann; e-mail: [email protected]Search for more papers by this authorKathrin Chamaon
Department of Orthopaedic Surgery, Otto-von-Guericke University, Leipziger Str. 44, 39120, Magdeburg, Germany
Search for more papers by this authorPeter Schönfeld
Institute for Biochemistry and Cell Biology, Otto-von-Guericke University, Leipziger Str. 44, 39120, Magdeburg, Germany
Search for more papers by this authorFriedemann Awiszus
Department of Orthopaedic Surgery, Otto-von-Guericke University, Leipziger Str. 44, 39120, Magdeburg, Germany
Search for more papers by this authorJessica Bertrand
Department of Orthopaedic Surgery, Otto-von-Guericke University, Leipziger Str. 44, 39120, Magdeburg, Germany
These authors contributed equally to this work.Search for more papers by this authorCorresponding Author
Christoph H. Lohmann
Department of Orthopaedic Surgery, Otto-von-Guericke University, Leipziger Str. 44, 39120, Magdeburg, Germany
These authors contributed equally to this work.Correspondence to: C. H. Lohmann; e-mail: [email protected]Search for more papers by this authorAbstract
Total joint replacement is one of the most successful procedures in orthopedic surgery today. However, metal implant materials undergo wear and corrosion processes. Generated particles and ions can cause a variety of cellular reactions. Cobalt-containing alloys are used frequently in implant materials. Some studies suggest that cobalt exhibits potential cytotoxic effects, for example, via generation of reactive oxygen species (ROS). To further elucidate the effects of cobalt on human cells, we determined cell viability and cytosolic and mitochondrial superoxide formation after incubation of either ions or particles with different cells. MM-6 and Jurkat cell lines were treated for 24, 48 and 72 h with either CoCrMo particles or cobalt ions (supplied as CoCl2). A total of 24 h exposure of both forms of cobalt did not induce cell death using terminal deoxynucleotidyl transferase (TUNEL) and trypan blue assay. Interestingly, the formation of superoxide (O2.−) is evoked mainly by ionic CoCl2 but not cobalt particles. Cobalt alloy particles are likely to even suppress O2.− formation in mitochondria in both used cell lines. Furthermore, we did not observe any effect of cobalt particles on O2.− formation in peripheral blood mononuclear cells (PBMCs) from healthy donors. We also found that the O2− formation by CoCl2 within mitochondria is a generalized effect for all cell types used, while the formation of superoxide in cytosolic compartment is cell-type dependent. In summary, our data suggest that cobalt ions specifically induce the formation of O2.−, whereas the cobalt particles were better tolerated. © 2018 Wiley Periodicals, Inc. J Biomed Mater Res Part B: Appl Biomater 107B: 1246–1253, 2019.
REFERENCES
- 1Learmonth ID, Young C, Rorabeck C. The operation of the century: Total hip replacement. Lancet 2007; 370(9597): 1508–1519.
- 2Doorn PF, Campbell PA, Worrall J, Benya PD, McKellop HA, Amstutz HC. Metal wear particle characterization from metal on metal total hip replacements: Transmission electron microscopy study of periprosthetic tissues and isolated particles. J Biomed Mater Res 1998; 42(1): 103–111.
10.1002/(SICI)1097-4636(199810)42:1<103::AID-JBM13>3.0.CO;2-M CAS PubMed Web of Science® Google Scholar
- 3Pourzal R, Catelas I, Theissmann R, Kaddick C, Fischer A. Characterization of wear particles generated from CoCrMo alloy under sliding wear conditions. Wear 2011; 271(9–10): 1658–1666.
- 4Hallab NJ, Jacobs JJ. Chemokines associated with pathologic responses to orthopedic implant debris. Front Endocrinol (Lausanne) 2017; 8: 5.
- 5Meyer H, Mueller T, Goldau G, Chamaon K, Ruetschi M, Lohmann CH. Corrosion at the cone/taper interface leads to failure of large-diameter metal-on-metal total hip arthroplasties. Clin Orthop Relat Res 2012; 470(11): 3101–3108.
- 6Simonsen LO, Harbak H, Bennekou P. Cobalt metabolism and toxicology – A brief update. Sci Total Environ 2012; 432: 210–215.
- 7Kanaji A, Orhue V, Caicedo MS, Virdi AS, Sumner DR, Hallab NJ, Yoshiaki T, Sena K. Cytotoxic effects of cobalt and nickel ions on osteocytes in vitro. J Orthop Surg Res 2014; 9: 91.
- 8Willert HG, Semlitsch M. Reactions of the articular capsule to wear products of artificial joint prostheses. J Biomed Mater Res 1977; 11(2): 157–164.
- 9Willert HG, Buchhorn GH, Fayyazi A, Flury R, Windler M, Koster G, Lohmann CH. Metal-on-metal bearings and hypersensitivity in patients with artificial hip joints. A clinical and histomorphological study. J Bone Joint Surg Am 2005; 87(1): 28–36.
- 10Lohmann CH, Meyer H, Nuechtern JV, Singh G, Junk-Jantsch S, Schmotzer H, Morlock MM, Pfluger G. Periprosthetic tissue metal content but not serum metal content predicts the type of tissue response in failed small-diameter metal-on-metal total hip arthroplasties. J Bone Joint Surg Am 2013; 95(17): 1561–1568.
- 11Leonard SS, Harris GK, Shi X. Metal-induced oxidative stress and signal transduction. Free Radic Biol Med 2004; 37(12): 1921–1942.
- 12Valko M, Morris H, Cronin MT. Metals, toxicity and oxidative stress. Curr Med Chem 2005; 12(10): 1161–1208.
- 13Cobelli N, Scharf B, Crisi GM, Hardin J, Santambrogio L. Mediators of the inflammatory response to joint replacement devices. Nat Rev Rheumatol 2011; 7(10): 600–608.
- 14Dyskova T, Gallo J, Kriegova E. The role of the chemokine system in tissue response to prosthetic by-products leading to periprosthetic osteolysis and aseptic loosening. Front Immunol 2017; 8: 1026.
- 15Anderson JA, Lamichhane S, Mani G. Macrophage responses to 316L stainless steel and cobalt chromium alloys with different surface topographies. J Biomed Mater Res A 2016; 104(11): 2658–2672.
- 16Kinov P, Leithner A, Radl R, Bodo K, Khoschsorur GA, Schauenstein K, Windhager R. Role of free radicals in aseptic loosening of hip arthroplasty. J Orthop Res 2006; 24(1): 55–62.
- 17Scharf B, Clement CC, Zolla V, Perino G, Yan B, Elci SG, Purdue E, Goldring S, Macaluso F, Cobelli N, Vachet RW, Santambrogio L. Molecular analysis of chromium and cobalt-related toxicity. Sci Rep 2014; 4: 5729.
- 18Valko M, Jomova K, Rhodes CJ, Kuca K, Musilek K. Redox- and non-redox-metal-induced formation of free radicals and their role in human disease. Arch Toxicol 2016; 90(1): 1–37.
- 19Anderson JM, McNally AK. Biocompatibility of implants: Lymphocyte/macrophage interactions. Semin Immunopathol 2011; 33(3): 221–233.
- 20Akbar M, Brewer JM, Grant MH. Effect of chromium and cobalt ions on primary human lymphocytes in vitro. J Immunotoxicol 2011; 8(2): 140–149.
- 21Ziegler-Heitbrock HW, Thiel E, Futterer A, Herzog V, Wirtz A, Riethmuller G. Establishment of a human cell line (Mono Mac 6) with characteristics of mature monocytes. Int J Cancer 1988; 41(3): 456–461.
- 22Lohmann CH, Singh G, Willert HG, Buchhorn GH. Metallic debris from metal-on-metal total hip arthroplasty regulates periprosthetic tissues. World J Orthop 2014; 5(5): 660–666.
- 23Buchhorn GH, Willert HG, Semlitsch M, Schoen R, Steinemann S, Schmidt M. Preparation, characterization, and animal testing for biocompatibility of metal particles of iron-, cobalt-, and titanium-based implant alloys, K.R.S. John (Ed.), Particulate debris from medical implants: mechanisms of formation and biological consequences, ASTM STP 1144, Philadelphia 1998. pp 177-188.
- 24Hallab NJ, Jacobs JJ. Biologic effects of implant debris. Bull NYU Hosp Jt Dis 2009; 67(2): 182–188.
- 25Wojtala A, Bonora M, Malinska D, Pinton P, Duszynski J, Wieckowski MR. Methods to monitor ROS production by fluorescence microscopy and fluorometry. Methods Enzymol 2014; 542: 243–262.
- 26Berridge MV, Tan AS. High-capacity redox control at the plasma membrane of mammalian cells: Trans-membrane, cell surface, and serum NADH-oxidases. Antioxid Redox Signal 2000; 2(2): 231–242.
- 27Domingo JL. Metal-induced developmental toxicity in mammals: A review. J Toxicol Environ Health 1994; 42(2): 123–141.
- 28Jomova K, Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology 2011; 283(2–3): 65–87.
- 29Kirkland D, Brock T, Haddouk H, Hargeaves V, Lloyd M, Mc Garry S, Proudlock R, Sarlang S, Sewald K, Sire G, Sokolowski A, Ziemann C. New investigations into the genotoxicity of cobalt compounds and their impact on overall assessment of genotoxic risk. Regul Toxicol Pharmacol 2015; 73(1): 311–338.
- 30Van den Broeke LT, Graslund A, Nilsson JL, Wahlberg JE, Scheynius A, Karlberg AT. Free radicals as potential mediators of metal-allergy: Ni2+- and Co2+-mediated free radical generation. Eur J Pharm Sci 1998; 6(4): 279–286.
- 31Patel E, Lynch C, Ruff V, Reynolds M. Co-exposure to nickel and cobalt chloride enhances cytotoxicity and oxidative stress in human lung epithelial cells. Toxicol Appl Pharmacol 2012; 258(3): 367–375.
- 32Andrews RE, Shah KM, Wilkinson JM, Gartland A. Effects of cobalt and chromium ions at clinically equivalent concentrations after metal-on-metal hip replacement on human osteoblasts and osteoclasts: Implications for skeletal health. Bone 2011; 49(4): 717–723.
- 33Catelas I, Petit A, Vali H, Fragiskatos C, Meilleur R, Zukor DJ, Antoniou J, Huk OL. Quantitative analysis of macrophage apoptosis vs. necrosis induced by cobalt and chromium ions in vitro. Biomaterials 2005; 26(15): 2441–2453.
- 34Baldwin EL, Byl JA, Osheroff N. Cobalt enhances DNA cleavage mediated by human topoisomerase II alpha in vitro and in cultured cells. Biochemistry 2004; 43(3): 728–735.
- 35Colognato R, Bonelli A, Ponti J, Farina M, Bergamaschi E, Sabbioni E, Migliore L. Comparative genotoxicity of cobalt nanoparticles and ions on human peripheral leukocytes in vitro. Mutagenesis 2008; 23(5): 377–382.
- 36Lojk J, Bregar VB, Rajh M, Mis K, Kreft ME, Pirkmajer S, Veranic P, Pavlin M. Cell type-specific response to high intracellular loading of polyacrylic acid-coated magnetic nanoparticles. Int J Nanomed 2015; 10: 1449–1462.
- 37Zou W, Yan M, Xu W, Huo H, Sun L, Zheng Z, Liu X. Cobalt chloride induces PC12 cells apoptosis through reactive oxygen species and accompanied by AP-1 activation. J Neurosci Res 2001; 64(6): 646–653.
- 38Battaglia V, Compagnone A, Bandino A, Bragadin M, Rossi CA, Zanetti F, Colombatto S, Grillo MA, Toninello A. Cobalt induces oxidative stress in isolated liver mitochondria responsible for permeability transition and intrinsic apoptosis in hepatocyte primary cultures. Int J Biochem Cell Biol 2009; 41(3): 586–594.
- 39Kubrak OI, Husak VV, Rovenko BM, Storey JM, Storey KB, Lushchak VI. Cobalt-induced oxidative stress in brain, liver and kidney of goldfish Carassius auratus. Chemosphere 2011; 85(6): 983–999.
- 40Baskaran R, Kalaiselvi P, Huang CY, Padma VV. Neferine, a bisbenzylisoquinoline alkaloid, offers protection against cobalt chloride-mediated hypoxia-induced oxidative stress in muscle cells. Integr Med Res 2015; 4(4): 231–241.
- 41Zhu H, Liu Y, Hong H, Wang W, Liu F. Protective effects of Zn2+ against cobalt nanoparticles and cobalt chloride-induced cytotoxicity of RAW 264.7 cells via ROS pathway. Biochem Biophys Res Commun 2017; 486(2): 357–363.
- 42Petit A, Mwale F, Zukor DJ, Catelas I, Antoniou J, Huk OL. Effect of cobalt and chromium ions on bcl-2, bax, caspase-3, and caspase-8 expression in human U937 macrophages. Biomaterials 2004; 25(11): 2013–2018.
- 43Petit A, Mwale F, Tkaczyk C, Antoniou J, Zukor DJ, Huk OL. Cobalt and chromium ions induce nitration of proteins in human U937 macrophages in vitro. J Biomed Mater Res A 2006; 79(3): 599–605.
- 44Higashi Y, Jitsuiki D, Chayama K, Yoshizumi M. Edaravone (3-methyl-1-phenyl-2-pyrazolin-5-one), a novel free radical scavenger, for treatment of cardiovascular diseases. Recent Pat Cardiovasc Drug Discov 2006; 1(1): 85–93.
- 45Fukai T, Ushio-Fukai M. Superoxide dismutases: Role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 2011; 15(6): 1583–1606.
- 46Cathcart MK. Regulation of superoxide anion production by NADPH oxidase in monocytes/macrophages: Contributions to atherosclerosis. Arterioscler Thromb Vasc Biol 2004; 24(1): 23–28.
- 47Jackson SH, Devadas S, Kwon J, Pinto LA, Williams MS. T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat Immunol 2004; 5(8): 818–827.
- 48Kobayashi Y, Okahata S, Sakano T, Tanabe K, Usui T. Superoxide dismutase activity of T lymphocytes and non-T lymphocytes. FEBS Lett 1979; 98(2): 391–393.
- 49Brand MD. The sites and topology of mitochondrial superoxide production. Exp Gerontol 2010; 45(7–8): 466–472.
- 50Porwol T, Ehleben W, Zierold K, Fandrey J, Acker H. The influence of nickel and cobalt on putative members of the oxygen-sensing pathway of erythropoietin-producing Hep G2 cells. Eur J Biochem 1998; 256(1): 16–23.
- 51Ehleben W, Porwol T, Fandrey J, Kummer W, Acker H. Cobalt and desferrioxamine reveal crucial members of the oxygen sensing pathway in HepG2 cells. Kidney Int 1997; 51(2): 483–491.
- 52Bragadin M, Toninello A, Mancon M, Manente S. The interactions of cobalt(II) with mitochondria from rat liver. J Biol Inorg Chem 2007; 12(5): 631–635.
- 53Hervouet E, Pecina P, Demont J, Vojtiskova A, Simonnet H, Houstek J, Godinot C. Inhibition of cytochrome c oxidase subunit 4 precursor processing by the hypoxia mimic cobalt chloride. Biochem Biophys Res Commun 2006; 344(4): 1086–1093.
- 54Manke A, Wang L, Rojanasakul Y. Mechanisms of nanoparticle-induced oxidative stress and toxicity. Biomed Res Int 2013; 2013: 942916.
- 55Raghunathan VK, Devey M, Hawkins S, Hails L, Davis SA, Mann S, Chang IT, Ingham E, Malhas A, Vaux DJ, Lane JD, Case CP. Influence of particle size and reactive oxygen species on cobalt chrome nanoparticle-mediated genotoxicity. Biomaterials 2013; 34 (14): 3559–3570.
- 56Liu YK, Deng XX, Yang HL. Cytotoxicity and genotoxicity in liver cells induced by cobalt nanoparticles and ions. Bone Joint Res 2016; 5(10): 461–469.
- 57Posada OM, Tate RJ, Grant MH. Toxicity of cobalt-chromium nanoparticles released from a resurfacing hip implant and cobalt ions on primary human lymphocytes in vitro. J Appl Toxicol 2015; 35(6): 614–622.