Biocompatibility of implantable materials: An oxidative stress viewpoint

Biomaterials

Volumn 109, Issue , 2016, Pages 55-68

  Mouthuy, Pierre Alexis ^a,b   Snelling, Sarah J B ^b   Dakin, Stephanie G ^b   Milković, Lidija ^a   Gašparović, Ana Čipak ^a   Carr, Andrew J ^b   Žarković, Neven ^a  

^a RUDER BO KOVI INSTITUTE   (Croatia)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Biocompatibility; Biomaterials; Lipid peroxidation products; Oxidative stress; RNS; ROS

Indexed keywords

BIOCOMPATIBILITY; BIOMATERIALS; CELL SIGNALING; CELLS; CYTOLOGY; DEGRADATION; LIPIDS; MOLECULES; NEURODEGENERATIVE DISEASES; OXIDANTS; OXIDATION; PATHOLOGY; RADON;

ANTIOXIDANT CAPACITY; BIOMATERIAL IMPLANTATION; DEGRADATION PRODUCTS; EXTRACELLULAR MATRICES; IMPLANTABLE MATERIALS; LIPID PEROXIDATION; PATHOLOGICAL CONDITIONS; SIGNALLING MOLECULES;

OXIDATIVE STRESS;

BIOMATERIAL; GLASS; MATRIX METALLOPROTEINASE; POLYMER; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; ANTIOXIDANT; OXIDIZING AGENT;

BIOCOMPATIBILITY; CELL COMMUNICATION; CERAMIC PROSTHESIS; COMPOSITE MATERIAL; DEGRADATION; DENDRITIC CELL; EQUIPMENT DESIGN; EXTRACELLULAR MATRIX; GIANT CELL; HUMAN; HYPOXIA; IMPLANT; IMPLANTATION; INFLAMMATION; INTRACELLULAR SIGNALING; LIPID PEROXIDATION; LYMPHOCYTE; MACROPHAGE; MAST CELL; MECHANICAL STRESS; METAL IMPLANT; NEUTROPHIL; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SURFACE PROPERTY; SURGICAL WOUND; TISSUE ENGINEERING; TISSUE REPAIR; WEIGHT, MASS AND SIZE; WETTABILITY; WOUND HEALING; ANIMAL; CHEMICALLY INDUCED; CHEMISTRY; METABOLISM; PHYSIOLOGY; PROSTHESES AND ORTHOSES;

ANIMALS; ANTIOXIDANTS; BIOCOMPATIBLE MATERIALS; HUMANS; INFLAMMATION; LIPID PEROXIDATION; OXIDANTS; OXIDATIVE STRESS; PROSTHESES AND IMPLANTS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; TISSUE ENGINEERING; WOUND HEALING;

EID: 84988484554     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2016.09.010     Document Type: Review

References (162)

1. [1] The Global Market for Medical Devices, sixth ed., 2015, Kalorama Information, 205.
2. [2] Williams, D., Revisiting the definition of biocompatibility. Med. Device Technol. 14:8 (2003), 10–13.
3. [3] Oliva, N., et al. Regulation of dendrimer/dextran material performance by altered tissue microenvironment in inflammation and neoplasia. Sci. Transl. Med., 7(272), 2015 p. 272ra11-272ra11.
4. [4] Selvam, S., et al. Minimally invasive, longitudinal monitoring of biomaterial-associated inflammation by fluorescence imaging. Biomaterials 32:31 (2011), 7785–7792.
5. [5] Suri, S., et al. In vivo fluorescence imaging of biomaterial-associated inflammation and infection in a minimally invasive manner. J. Biomed. Mater. Res. A 103:1 (2015), 76–83.
6. [6] Kim, M.S., et al. An in vivo study of the host tissue response to subcutaneous implantation of PLGA- and/or porcine small intestinal submucosa-based scaffolds. Biomaterials 28:34 (2007), 5137–5143.
7. [7] Yoon, S.J., et al. Reduction of inflammatory reaction of poly(d,l-lactic-co-glycolic Acid) using demineralized bone particles. Tissue Eng. Part A 14:4 (2008), 539–547.
8. [8] Niethammer, P., et al. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459:7249 (2009), 996–999.
9. [9] Wattamwar, P.P., Dziubla, T.D., Modulation of the wound healing response through oxidation active materials. Bhatia, K.S., (eds.) Engineering Biomaterials for Regenerative Medicine: Novel Technologies for Clinical Applications, 2012, Springer, New York, NY, 161–192 New York.
10. [10] Lugrin, J., et al. The role of oxidative stress during inflammatory processes. Biol. Chem. 395:2 (2014), 203–230.
11. [11] Chang, H.H., et al. Stimulation of glutathione depletion, ROS production and cell cycle arrest of dental pulp cells and gingival epithelial cells by HEMA. Biomaterials 26:7 (2005), 745–753.
12. [12] Lefeuvre, M., et al. TEGDMA induces mitochondrial damage and oxidative stress in human gingival fibroblasts. Biomaterials 26:25 (2005), 5130–5137.
13. [13] Ozmen, I., Naziroglu, M., Okutan, R., Comparative study of antioxidant enzymes in tissues surrounding implant in rabbits. Cell Biochem. Funct. 24:3 (2006), 275–281.
14. [14] Tsaryk, R., et al. The role of oxidative stress in the response of endothelial cells to metals. Antoniac, I., (eds.) Biologically Responsive Biomaterials for Tissue Engineering, 2013, Springer, New York, NY, 65–88 New York.
15. [15] Lin, T.H., et al. Chronic inflammation in biomaterial-induced periprosthetic osteolysis: NF-kappaB as a therapeutic target. Acta Biomater. 10:1 (2014), 1–10.
16. [16] Dziubla, T., Butterfield, D.A., Oxidative Stress and Biomaterials. 2016, Academic Press, 404.
17. [17] Mittal, M., et al. Reactive oxygen species in inflammation and tissue injury. Antioxid. Redox Signal 20:7 (2014), 1126–1167.
18. [18] Holmstrom, K.M., Finkel, T., Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat. Rev. Mol. Cell Biol. 15:6 (2014), 411–421.
19. [19] Brieger, K., et al. Reactive oxygen species: from health to disease. Swiss Med. Wkly., 142, 2012, w13659.
20. [20] Pham-Huy, L.A., He, H., Pham-Huy, C., Free radicals, antioxidants in disease and health. Int. J. Biomed. Sci. IJBS 4:2 (2008), 89–96.
21. [21] Halliwell, B., Reactive species and antioxidants. Redox biology is a fundamental theme of Aerobic life. Plant Physiol. 141:2 (2006), 312–322.
22. [22] Sorci, G., Faivre, B., Inflammation and oxidative stress in vertebrate host–parasite systems. Philosophical Trans. R. Soc. Lond. B Biol. Sci. 364:1513 (2009), 71–83.
23. [23] Frijhoff, J., et al. Clinical relevance of Biomarkers of oxidative stress. Antioxidants Redox Signal. 23:14 (2015), 1144–1170.
24. [24] Schaur, R.J., Basic aspects of the biochemical reactivity of 4-hydroxynonenal. Mol. Asp. Med. 24:4–5 (2003), 149–159.
25. [25] Augustyniak, A., et al. Natural and synthetic antioxidants: an updated overview. Free Radic. Res. 44:10 (2010), 1216–1262.
26. [26] Reuter, S., et al. Oxidative stress, inflammation, and cancer: how are they linked?. Free Radic. Biol. Med. 49:11 (2010), 1603–1616.
27. [27] Finkel, T., Holbrook, N.J., Oxidants, oxidative stress and the biology of ageing. Nature 408:6809 (2000), 239–247.
28. [28] Pacher, P., Beckman, J.S., Liaudet, L., Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 87:1 (2007), 315–424.
29. [29] Li, X., et al. Targeting mitochondrial reactive oxygen species as novel therapy for inflammatory diseases and cancers. J. Hematol. Oncol., 6, 2013 19–19.
30. [30] Eming, S.A., Krieg, T., Davidson, J.M., Inflammation in wound repair: molecular and cellular mechanisms. J. Investig. Dermatol 127:3 (2007), 514–525.
31. [31] Trachootham, D., et al. Redox regulation of cell survival. Antioxid. Redox Signal 10:8 (2008), 1343–1374.
32. [32] Bartling, T.R., et al. Redox-sensitive gene-regulatory events controlling aberrant matrix metalloproteinase-1 expression. Free Radic. Biol. Med. 74 (2014), 99–107.
33. [33] Morita, K., et al. Reactive oxygen species induce chondrocyte hypertrophy in endochondral ossification. J. Exp. Med. 204:7 (2007), 1613–1623.
34. [34] Wang, Z., Li, Y., Sarkar, F.H., Signaling mechanism(s) of reactive oxygen species in Epithelial-Mesenchymal Transition reminiscent of cancer stem cells in tumor progression. Curr. Stem Cell Res. Ther. 5:1 (2010), 74–80.
35. [35] Bigelow, D.J., Squier, T.C., Redox modulation of cellular signaling and metabolism through reversible oxidation of methionine sensors in calcium regulatory proteins. Biochim. Biophys. Acta 1703:2 (2005), 121–134.
36. [36] Ayala, A., Muñoz, M.F., Argüelles, S., Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-Hydroxy-2-Nonenal. Oxidative Med. Cell. Longev., 2014, 2014, 31.
37. [37] Volinsky, R., Kinnunen, P.K., Oxidized phosphatidylcholines in membrane-level cellular signaling: from biophysics to physiology and molecular pathology. Febs J. 280:12 (2013), 2806–2816.
38. [38] Aiken, C.T., et al. Oxidative stress-mediated regulation of proteasome complexes. Mol. Cell Proteomics, 10(5), 2011 p. R110.006924.
39. [39] Lizarbe, T.R., et al. Nitric oxide elicits functional MMP-13 protein-tyrosine nitration during wound repair. Faseb J. 22:9 (2008), 3207–3215.
40. [40] Zuo, Y., et al. Oxidative modification of caspase-9 facilitates its activation via disulfide-mediated interaction with Apaf-1. Cell Res. 19:4 (2009), 449–457.
41. [41] Franz, S., et al. Immune responses to implants – a review of the implications for the design of immunomodulatory biomaterials. Biomaterials 32:28 (2011), 6692–6709.
42. [42] Ratner, B.D., et al. Biomaterials Science: an Introduction to Materials in Medicine. third ed., 2013, Elsevier.
43. [43] Bonnans, C., Chou, J., Werb, Z., Remodelling the extracellular matrix in development and disease. Nat. Rev. Mol. Cell Biol. 15:12 (2014), 786–801.
44. [44] Nisimoto, Y., et al. Nox4: a hydrogen peroxide-generating oxygen sensor. Biochemistry 53:31 (2014), 5111–5120.
45. [45] Gough, D.R., Cotter, T.G., Hydrogen peroxide: a Jekyll and Hyde signalling molecule. Cell Death Dis., 2, 2011, e213.
46. [46] Li, J., et al. Reciprocal activation between IL-6/STAT3 and NOX4/Akt signalings promotes proliferation and survival of non-small cell lung cancer cells. Oncotarget 6:2 (2015), 1031–1048.
47. [47] Manea, A., et al. Transcriptional regulation of NADPH oxidase isoforms, Nox1 and Nox4, by nuclear factor-kappaB in human aortic smooth muscle cells. Biochem. Biophys. Res. Commun. 396:4 (2010), 901–907.
48. [48] Manea, S.A., et al. Regulation of Nox enzymes expression in vascular pathophysiology: focusing on transcription factors and epigenetic mechanisms. Redox Biol. 5 (2015), 358–366.
49. [49] Kim, J., Keum, Y.-S., NRF2, a key regulator of antioxidants with two faces towards Cancer. Oxidative Med. Cell. Longev., 2016, 2016, 7.
50. [50] Mansouri, L., et al. NF-kappaB activation in chronic lymphocytic leukemia: a point of convergence of external triggers and intrinsic lesions. Semin. Cancer Biol. 39 (August 2016), 40–48, 10.1016/j.semcancer.2016.07.005.
51. [51] Williams, D.F., Zhong, S.P., Talking point. Are free radicals involved in biodegradation of implanted polymers?. Adv. Mater. 3:12 (1991), 623–626.
52. [52] Dakin, S.G., et al. Inflammation activation and resolution in human tendon disease. Sci. Transl. Med., 7(311), 2015 p. 311ra173.
53. [53] Razzell, W., et al. Calcium flashes orchestrate the wound inflammatory response through DUOX activation and hydrogen peroxide release. Curr. Biol. 23:5 (2013), 424–429.
54. [54] Kono, H., Rock, K.L., How dying cells alert the immune system to danger. Nat. Rev. Immunol. 8:4 (2008), 279–289.
55. [55] Bryan, N., et al. Reactive oxygen species (ROS)–a family of fate deciding molecules pivotal in constructive inflammation and wound healing. Eur. Cell Mater. 24 (2012), 249–265.
56. [56] Kuper, C., Beck, F.X., Neuhofer, W., Toll-like receptor 4 activates NF-kappaB and MAP kinase pathways to regulate expression of proinflammatory COX-2 in renal medullary collecting duct cells. Am. J. Physiol. Ren. Physiol. 302:1 (2012), F38–F46.
57. [57] Buxade, M., et al. Gene expression induced by Toll-like receptors in macrophages requires the transcription factor NFAT5. J. Exp. Med. 209:2 (2012), 379–393.
58. [58] Motterlini, R., et al. Oxidative-stress response in vascular endothelial cells exposed to acellular hemoglobin solutions. Am. J. Physiol. 269:2 Pt 2 (1995), H648–H655.
59. [59] Everse, J., Hsia, N., The toxicities of native and modified hemoglobins. Free Radic. Biol. Med. 22:6 (1997), 1075–1099.
60. [60] Clanton, T.L., Hypoxia-induced reactive oxygen species formation in skeletal muscle. J. Appl. Physiol. 102:6 (2007), 2379–2388.
61. [61] Brueckl, C., et al. Hyperoxia-induced reactive oxygen species formation in pulmonary capillary endothelial cells in situ. Am. J. Respir. Cell Mol. Biol. 34:4 (2006), 453–463.
62. [62] Tan, S., et al. Peritoneal air exposure elicits an intestinal inflammation resulting in postoperative ileus. Mediat. Inflamm., 2014, 2014, 11.
63. [63] Collard, C.D., et al. Complement activation after oxidative stress: role of the lectin complement pathway. Am. J. Pathol. 156:5 (2000), 1549–1556.
64. [64] Anderson, J.M., Rodriguez, A., Chang, D.T., Foreign body reaction to biomaterials. Semin. Immunol. 20:2 (2008), 86–100.
65. [65] Amini, A.R., Wallace, J.S., Nukavarapu, S.P., Short-term and long-term effects of orthopedic biodegradable implants. J. Long. Term. Eff. Med. Implants 21:2 (2011), 93–122.
66. [66] Buckley, C.D., Why does chronic inflammation persist: an unexpected role for fibroblasts. Immunol. Lett. 138:1 (2011), 12–14.
67. [67] Chu, C.-C., von Fraunhofer, J.A., Greisler, H.P., Wound Closure Biomaterials and Devices. 1996, CRC Press, 416.
68. [68] Kirkham, P., Oxidative stress and macrophage function: a failure to resolve the inflammatory response. Biochem. Soc. Trans. 35:Pt 2 (2007), 284–287.
69. [69] Murray, P.J., et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41:1 (2014), 14–20.
70. [70] Brown, B.N., et al. Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials. Acta biomater. 8:3 (2012), 978–987.
71. [71] Basil, M.C., Levy, B.D., Specialized pro-resolving mediators: endogenous regulators of infection and inflammation. Nat. Rev. Immunol. 16:1 (2016), 51–67.
72. [72] Zhang, Y., et al. ROS play a critical role in the differentiation of alternatively activated macrophages and the occurrence of tumor-associated macrophages. Cell Res. 23:7 (2013), 898–914.
73. [73] Helming, L., Gordon, S., Macrophage fusion induced by IL-4 alternative activation is a multistage process involving multiple target molecules. Eur. J. Immunol. 37:1 (2007), 33–42.
74. [74] Sharma, P., et al. Redox regulation of interleukin-4 signaling. Immunity 29:4 (2008), 551–564.
75. [75] Park, J., Babensee, J.E., Differential functional effects of biomaterials on dendritic cell maturation. Acta Biomater. 8:10 (2012), 3606–3617.
76. [76] Cheong, T.-C., et al. Functional manipulation of dendritic cells by photoswitchable generation of intracellular reactive oxygen species. ACS Chem. Biol. 10:3 (2015), 757–765.
77. [77] Batal, I., et al. The mechanisms of up-regulation of dendritic cell activity by oxidative stress. J. Leukoc. Biol. 96:2 (2014), 283–293.
78. [78] Pearce, E.J., Everts, B., Dendritic cell metabolism. Nat. Rev. Immunol. 15:1 (2015), 18–29.
79. [79] Matsue, H., et al. Generation and function of reactive oxygen species in dendritic cells during antigen presentation. J. Immunol. 171:6 (2003), 3010–3018.
80. [80] Chiarugi, P., et al. Reactive oxygen species as essential mediators of cell adhesion: the oxidative inhibition of a FAK tyrosine phosphatase is required for cell adhesion. J. Cell Biol. 161:5 (2003), 933–944.
81. [81] Day, R.M., Suzuki, Y.J., Cell proliferation, reactive oxygen and cellular glutathione. Dose-Response 3:3 (2005), 425–442.
82. [82] Giannoni, E., et al. Intracellular reactive oxygen species activate src tyrosine kinase during cell adhesion and Anchorage-dependent cell growth. Mol. Cell. Biol. 25:15 (2005), 6391–6403.
83. [83] Bigarella, C.L., Liang, R., Ghaffari, S., Stem cells and the impact of ROS signaling. Development 141:22 (2014), 4206–4218.
84. [84] Ji, A.-R., et al. Reactive oxygen species enhance differentiation of human embryonic stem cells into mesendodermal lineage. Exp. Mol. Med. 42 (2010), 175–186.
85. [85] Vieira, H.L.A., Alves, P.M., Vercelli, A., Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species. Prog. Neurobiol. 93:3 (2011), 444–455.
86. [86] Milkovic, L., Cipak Gasparovic, A., Zarkovic, N., Overview on major lipid peroxidation bioactive factor 4-hydroxynonenal as pluripotent growth-regulating factor. Free Radic. Res. 49:7 (2015), 850–860.
87. [87] Dalleau, S., et al. Cell death and diseases related to oxidative stress: 4-hydroxynonenal (HNE) in the balance. Cell Death Differ. 20:12 (2013), 1615–1630.
88. [88] Liu, W.F., et al. Real-time in vivo detection of biomaterial-induced reactive oxygen species. Biomaterials 32:7 (2011), 1796–1801.
89. [89] Janda, J., et al. Modulation of ROS levels in fibroblasts by altering mitochondria regulates the process of wound healing. Arch. Dermatol Res. 308:4 (2016), 239–248.
90. [90] Wlaschek, M., Scharffetter-Kochanek, K., Oxidative stress in chronic venous leg ulcers. Wound Repair Regen. 13:5 (2005), 452–461.
91. [91] Midwood, K.S., Williams, L.V., Schwarzbauer, J.E., Tissue repair and the dynamics of the extracellular matrix. Int. J. Biochem. Cell Biol. 36:6 (2004), 1031–1037.
92. [92] Siwik, D.A., Pagano, P.J., Colucci, W.S., Oxidative stress regulates collagen synthesis and matrix metalloproteinase activity in cardiac fibroblasts. Am. J. Physiol. Cell Physiol. 280:1 (2001), C53–C60.
93. [93] Boudreau, H.E., et al. Nox4 involvement in TGF-beta and SMAD3-driven induction of the epithelial-to-mesenchymal transition and migration of breast epithelial cells. Free Radic. Biol. Med. 53:7 (2012), 1489–1499.
94. [94] Cucoranu, I., et al. NAD(P)H oxidase 4 mediates transforming growth factor-beta1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ. Res. 97:9 (2005), 900–907.
95. [95] Bondi, C.D., et al. NAD(P)H oxidase mediates TGF-beta1-induced activation of kidney myofibroblasts. J. Am. Soc. Nephrol. 21:1 (2010), 93–102.
96. [96] Kurtz, S., UHMWPE Biomaterials Handbook. Ultra High Molecular Weight Polyethylene in Total Joint Replacement and Medical Devices. 2015, William Andrew.
97. [97] Ali, S.A., et al. Mechanisms of polymer degradation in implantable devices. I. Poly(caprolactone). Biomaterials 14:9 (1993), 648–656.
98. [98] Ali, S.A.M., Doherty, P.J., Williams, D.F., The mechanisms of oxidative degradation of biomedical polymers by free radicals. J. Appl. Polym. Sci. 51:8 (1994), 1389–1398.
99. [99] Tamariz, E., Rios-Ramírez, A., Biodegradation of medical purpose polymeric materials and their impact on biocompatibility. Chamy, R., (eds.) Biodegradation – Life of Science, 2013, InTech.
100. [100] van Lith, R., Developing biomaterials for the Attenuation of oxidative stress. Biomedical Engineering, 2014, Northwestern university Evanston, Illinois.
101. [101] Bakopoulou, A., Papadopoulos, T., Garefis, P., Molecular toxicology of substances released from resin-based dental restorative materials. Int. J. Mol. Sci. 10:9 (2009), 3861–3899.
102. [102] Krifka, S., et al. A review of adaptive mechanisms in cell responses towards oxidative stress caused by dental resin monomers. Biomaterials 34:19 (2013), 4555–4563.
103. [103] Ulbricht, J., Jordan, R., Luxenhofer, R., On the biodegradability of polyethylene glycol, polypeptoids and poly(2-oxazoline)s. Biomaterials 35:17 (2014), 4848–4861.
104. [104] Bladen, C.L., et al. Analysis of wear, wear particles, and reduced inflammatory potential of vitamin E ultrahigh-molecular-weight polyethylene for use in total joint replacement. J. Biomed. Mater. Res. B Appl. Biomater. 101:3 (2013), 458–466.
105. [105] Abbott, D.A., et al. Catalase overexpression reduces lactic acid-induced oxidative stress in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 75:8 (2009), 2320–2325.
106. [106] Jiang, W.W., et al. Phagocyte responses to degradable polymers. J. Biomed. Mater. Res. A 82:2 (2007), 492–497.
107. [107] Lardner, A., The effects of extracellular pH on immune function. J. Leukoc. Biol. 69:4 (2001), 522–530.
108. [108] Singh, B.R., et al. ROS-mediated apoptotic cell death in prostate cancer LNCaP cells induced by biosurfactant stabilized CdS quantum dots. Biomaterials 33:23 (2012), 5753–5767.
109. [109] Serrano, M.C., et al. Transitory oxidative stress in L929 fibroblasts cultured on poly(epsilon-caprolactone) films. Biomaterials 26:29 (2005), 5827–5834.
110. [110] Surendran, D., et al. Long term effect of biodegradable polymer on oxidative stress and genotoxicity. BIO 2 (2012), 37–46.
111. [111] Badylak, S.F., Gilbert, T.W., Immune response to biologic scaffold materials. Seminars Immunol. 20:2 (2008), 109–116.
112. [112] Adair-Kirk, T.L., Senior, R.M., Fragments of extracellular matrix as mediators of inflammation. Int. J. Biochem. Cell Biol. 40:6–7 (2008), 1101–1110.
113. [113] Moroni, F., Mirabella, T., Decellularized matrices for cardiovascular tissue engineering. Am. J. Stem Cells 3:1 (2014), 1–20.
114. [114] Campo, G.M., et al. Efficacy of treatment with glycosaminoglycans on experimental collagen-induced arthritis in rats. Arthritis Res. Ther. 5:3 (2003), R122–R131.
115. [115] Sansone, V., Pagani, D., Melato, M., The effects on bone cells of metal ions released from orthopaedic implants. A review. Clin. Cases Min. Bone Metab. 10:1 (2013), 34–40.
116. [116] Tsaryk, R., et al. Response of human endothelial cells to oxidative stress on Ti6Al4V alloy. Biomaterials 28:5 (2007), 806–813.
117. [117] Valko, M., Morris, H., Cronin, M.T., Metals, toxicity and oxidative stress. Curr. Med. Chem. 12:10 (2005), 1161–1208.
118. [118] Ercal, N., Gurer-Orhan, H., Aykin-Burns, N., Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr. Top. Med. Chem. 1:6 (2001), 529–539.
119. [119] Thrivikraman, G., Madras, G., Basu, B., In vitro/In vivo assessment and mechanisms of toxicity of bioceramic materials and its wear particulates. RSC Adv. 4:25 (2014), 12763–12781.
120. [120] Hallab, N.J., Jacobs, J.J., Biologic effects of implant debris. Bull. NYU Hosp. Jt. Dis. 67:2 (2009), 182–188.
121. [121] Luo, G., et al. Resveratrol protects against titanium particle-induced aseptic loosening through reduction of oxidative stress and inactivation of NF-kappaB. Inflammation 39:2 (2016), 775–785.
122. [122] Kinov, P., et al. Role of free radicals in aseptic loosening of hip arthroplasty. J. Orthop. Res. 24:1 (2006), 55–62.
123. [123] Doorn, P.F., Campbell, P., Amstutz, H., Particle disease in metal-on-metal total hip replacements. Rieker, C.B., Windler, M., Wyss, U., (eds.) Metasul: a Metal-on-metal Bearing, 1999, Huber, Bern, 113–119.
124. [124] Gilbert, J.L., et al. Direct in vivo inflammatory cell-induced corrosion of CoCrMo alloy orthopedic implant surfaces. J. Biomed. Mater. Res. A 103:1 (2015), 211–223.
125. [125] Gilbert, J.L., Kubacki, G.W., Chapter three - oxidative stress, inflammation, and the corrosion of metallic biomaterials: corrosion causes biology and biology causes corrosion A2-dziubla, thomas. Butterfield, D.A., (eds.) Oxidative Stress and Biomaterials, 2016, Academic Press, 59–88.
126. [126] Bearinger, J.P., Orme, C.A., Gilbert, J.L., Effect of hydrogen peroxide on titanium surfaces: in situ imaging and step-polarization impedance spectroscopy of commercially pure titanium and titanium, 6-aluminum, 4-vanadium. J. Biomed. Mater. Res. A 67:3 (2003), 702–712.
127. [127] Jebahi, S., et al. Biological therapy of strontium-substituted bioglass for soft tissue wound-healing: responses to oxidative stress in ovariectomised rats. Ann. Pharm. Fr. 71:4 (2013), 234–242.
128. [128] Wu, C., et al. Hypoxia-mimicking mesoporous bioactive glass scaffolds with controllable cobalt ion release for bone tissue engineering. Biomaterials 33:7 (2012), 2076–2085.
129. [129] Milkovic, L., et al. Effects of Cu-doped 45S5 bioactive glass on the lipid peroxidation-associated growth of human osteoblast-like cells in vitro. J. Biomed. Mater. Res. A 102:10 (2014), 3556–3561.
130. [130] Samira, J., et al. Accelerated bone ingrowth by local delivery of Zinc from bioactive glass: oxidative stress status, mechanical property, and microarchitectural characterization in an ovariectomized rat model. Libyan J. Med., 10, 2015, 28572.
131. [131] Mrakovcic, L., et al. Lipid peroxidation product 4-hydroxynonenal as factor of oxidative homeostasis supporting bone regeneration with bioactive glasses. Acta Biochim. Pol. 57:2 (2010), 173–178.
132. [132] Canton, I., et al. Real-time detection of stress in 3D tissue-engineered constructs using NF-kappaB activation in transiently transfected human dermal fibroblast cells. Tissue Eng. 13:5 (2007), 1013–1024.
133. [133] Merrell, J.G., et al. Curcumin loaded poly(ε-caprolactone) nanofibers: diabetic wound dressing with antioxidant and anti-inflammatory properties. Clin. Exp. Pharmacol. Physiol. 36:12 (2009), 1149–1156.
134. [134] Eliaz, N., Degradation of Implant Materials. 2012, Springer, 516.
135. [135] Sheikh, Z., et al. Macrophages, foreign body giant cells and their response to implantable biomaterials. Materials, 8(9), 2015, 5269.
136. [136] Khanna, P., et al. Nanotoxicity: an interplay of oxidative stress, inflammation and cell death. Nanomaterials 5:3 (2015), 1163–1180.
137. [137] Park, E.J., Park, K., Oxidative stress and pro-inflammatory responses induced by silica nanoparticles in vivo and in vitro. Toxicol. Lett. 184:1 (2009), 18–25.
138. [138] Avalos, A., et al. Cytotoxicity and ROS production of manufactured silver nanoparticles of different sizes in hepatoma and leukemia cells. J. Appl. Toxicol. 34:4 (2014), 413–423.
139. [139] Misawa, M., Takahashi, J., Generation of reactive oxygen species induced by gold nanoparticles under x-ray and UV Irradiations. Nanomedicine 7:5 (2011), 604–614.
140. [140] Bhattacharjee, S., et al. Role of membrane disturbance and oxidative stress in the mode of action underlying the toxicity of differently charged polystyrene nanoparticles. RSC Adv. 4:37 (2014), 19321–19330.
141. [141] Frohlich, E., et al. Cytotoxicity of nanoparticles independent from oxidative stress. J. Toxicol. Sci. 34:4 (2009), 363–375.
142. [142] Manke, A., Wang, L., Rojanasakul, Y., Mechanisms of nanoparticle-induced oxidative stress and toxicity. BioMed Res. Int., 2013, 2013, 15.
143. [143] Fu, P.P., et al. Mechanisms of nanotoxicity: generation of reactive oxygen species. J. Food Drug Analysis 22:1 (2014), 64–75.
144. [144] Sarkar, A., Ghosh, M., Sil, P.C., Nanotoxicity: oxidative stress mediated toxicity of metal and metal oxide nanoparticles. J. Nanosci. Nanotechnol. 14:1 (2014), 730–743.
145. [145] Cochran, D.B., et al. Suppressing iron oxide nanoparticle toxicity by vascular targeted antioxidant polymer nanoparticles. Biomaterials 34:37 (2013), 9615–9622.
146. [146] Halliwell, B., Free Radicals in Biology and Medicine [electronic Resource]. fifth ed., 2015, Oxford University Press, Oxford ed. Oxford scholarship online, ed. J.M.C. Gutteridge and p. Oxford University Press.
147. [147] Napoli, A., et al. Oxidation-responsive polymeric vesicles. Nat. Mater. 3:3 (2004), 183–189.
148. [148] Wattamwar, P.P., et al. Synthesis and characterization of poly(antioxidant beta-amino esters) for controlled release of polyphenolic antioxidants. Acta Biomater. 8:7 (2012), 2529–2537.
149. [149] Xu, Q., et al. Reactive oxygen species (ROS) responsive polymers for biomedical applications. Macromol. Biosci. 16:5 (2016), 635–646.
150. [150] de Gracia Lux, C., et al. Biocompatible polymeric nanoparticles degrade and release cargo in response to biologically relevant levels of hydrogen peroxide. J. Am. Chem. Soc. 134:38 (2012), 15758–15764.
151. [151] Yang, J., et al. A thermoresponsive biodegradable polymer with intrinsic antioxidant properties. Biomacromolecules 15:11 (2014), 3942–3952.
152. [152] Udipi, K., et al. Modification of inflammatory response to implanted biomedical materials in vivo by surface bound superoxide dismutase mimics. J. Biomed. Mater. Res. 51:4 (2000), 549–560.
153. [153] Hood, E.D., et al. Endothelial targeting of nanocarriers loaded with antioxidant enzymes for protection against vascular oxidative stress and inflammation. Biomaterials 35:11 (2014), 3708–3715.
154. [154] Gallorini, M., et al. Activation of the Nrf2-regulated antioxidant cell response inhibits HEMA-induced oxidative stress and supports cell viability. Biomaterials 56 (2015), 114–128.
155. [155] Somasuntharam, I., et al. Delivery of Nox2-NADPH oxidase siRNA with polyketal nanoparticles for improving cardiac function following myocardial infarction. Biomaterials 34:31 (2013), 7790–7798.
156. [156] Drummond, G.R., et al. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat. Rev. Drug Discov. 10:6 (2011), 453–471.
157. [157] Liu, Z., et al. Oxidation-induced degradable nanogels for iron chelation. Sci. Rep., 6, 2016, 20923.
158. [158] van Lith, R., et al. Engineering biodegradable polyester elastomers with antioxidant properties to attenuate oxidative stress in tissues. Biomaterials 35:28 (2014), 8113–8122.
159. [159] Fan, J., et al. Direct evidence for catalase and peroxidase activities of ferritin-platinum nanoparticles. Biomaterials 32:6 (2011), 1611–1618.
160. [160] Taylor, G.C., et al. Influence of titanium oxide and titanium peroxy gel on the breakdown of hyaluronan by reactive oxygen species. Biomaterials 17:13 (1996), 1313–1319.
161. [161] Miguez-Pacheco, V., et al. Bioactive glasses in soft tissue repair. Am. Ceram. Soc. Bull., 94(6), 2009.
162. [162] Placek, L., Wren, A.W., Cytocompatibility of Y2O3 and CeO2 containing bioactive glasses to aid spinal cord recovery. 41st Annual Northeast Biomedical Engineering Conference (NEBEC), 2015, IEEE.