Reactive oxygen species generation by copper(II) oxide nanoparticles determined by DNA damage assays and EPR spectroscopy

References

• Alves D, Santos CG, Paixao MW, Soares LC, De Souza D, Rodrigues OED, Braga AL. 2009. CuO nanoparticles: an efficient and recyclable catalyst for cross-coupling reactions of organic diselenides with aryl boronic acids. Tetrahedron Lett 50:6635–8.
   Web of Science ®Google Scholar
• Angelé-Martínez C, Goodman C, Brumaghim JL. 2014. Metal-mediated DNA damage and cell death: mechanisms, detection methods, and cellular consequences. Metallomics 6:1358–81.
   PubMed Web of Science ®Google Scholar
• Atha DH, Wang H, Petersen EJ, Cleveland D, Holbrook RD, Jaruga P, et al. 2012. Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environ Sci Technol 46:1819–27.
   PubMed Web of Science ®Google Scholar
• Bartosz G. 2006. Use of spectroscopic probes for detection of reactive oxygen species. Clin Chim Acta 368:53–76.
   PubMed Web of Science ®Google Scholar
• Bielski BHJ. 1978. Reevaluation of the spectral and kinetic properties of HO2 and O2- free radicals. Photochem Photobiol 28:645–9.
   Web of Science ®Google Scholar
• Blinova I, Ivask A, Heinlaan M, Mortimer M, Kahru A. 2010. Ecotoxicity of nanoparticles of CuO and ZnO in natural water. Environ Pollut 158:41–7.
   PubMed Web of Science ®Google Scholar
• Bondarenko O, Juganson K, Ivask A, Kasemets K, Mortimer M, Kahru A. 2013. Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review. Arch Toxicol 87:1181–200.
   PubMed Web of Science ®Google Scholar
• Burgess RC, Misteli T, Oberdoerffer P. 2012. DNA damage, chromatin, and transcription: the trinity of aging. Curr Opin Cell Biol 24:724–30.
   PubMed Web of Science ®Google Scholar
• Cadena E. 1997. Basic mechanisms of antioxidant activity. BioFactors 6:391–7.
   PubMed Web of Science ®Google Scholar
• Cho WS, Duffin R, Thielbeer F, Bradley M, Megson IL, Macnee W, et al. 2012. Zeta potential and solubility to toxic ions as mechanisms of lung inflammation caused by metal/metal oxide nanoparticles. Toxicol Sci 126:469–77.
   PubMed Web of Science ®Google Scholar
• Clément JL, Ferré N, Siri D, Karoui H, Rockenbauer A, Tordo P. 2004. Assignment of the EPR spectrum of 5,5-dimethyl-1-pyrroline N-oxide (DMPO) superoxide spin adduct. J Org Chem 70:1198–203.
   Web of Science ®Google Scholar
• Cooke MS, Evans MD, Dizdaroglu M, Lunec J. 2003. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 17:1195–214.
   PubMed Web of Science ®Google Scholar
• Cooney TE. 1995. Bactericidal activity of copper and noncopper paints. Infect Control Hosp Epidemiol 16:444–50.
   PubMed Web of Science ®Google Scholar
• Cronholm P, Karlsson HL, Hedberg J, Lowe TA, Winnberg L, Elihn K, et al. 2013. Intracellular uptake and toxicity of Ag and CuO nanoparticles: a comparison between nanoparticles and their corresponding metal ions. Small 9:970–82.
   PubMed Web of Science ®Google Scholar
• Cross JB, Currier RP, Torraco DJ, Vanderberg LA, Wagner GL, Gladen PD. 2003. Killing of Bacillus spores by aqueous dissolved oxygen, ascorbic acid, and copper ions. Appl Environ Microbiol 69:2245–52.
   PubMed Web of Science ®Google Scholar
• Dix TA, Hess KM, Medina MA, Sullivan RW, Tilly SL, Webb TL. 1996. Mechanism of site-selective DNA nicking by the hydrodioxyl (perhydroxyl) radical. Biochemistry 35:4578–783.
   PubMed Web of Science ®Google Scholar
• Eaton AD, Ciesceri LS, Rice EW, Greenberg AE. 2001. Standard Methods for the Examination of Water and Wastewater. Washington, D.C.: American Public Health Association.
   Google Scholar
• Fufezan C, Rutherford AW, Krieger-Liszkay A. 2002. Singlet oxygen production in herbicide-treated photosystem II. FEBS Lett 532:407–10.
   PubMed Web of Science ®Google Scholar
• Gaetke LM, Chow-Johnson HS, Chow CK. 2014. Copper: toxicological relevance and mechanisms. Arch Toxicol 88:1929–38.
   PubMed Web of Science ®Google Scholar
• Grassian VH. 2008. When size really matters: size-dependent properties and surface chemistry of metal and metal oxide nanoparticles in gas and liquid phase environments. J Phys Chem C 112:18303–13.
   Web of Science ®Google Scholar
• Gunawan C, Teoh WY, Marquis CP, Amal R. 2011. Cytotoxic origin of copper(II) oxide nanoparticles: comparative studies with micron-sized particles, leachate, and metal salts. ACS Nano 5:7214–25.
   PubMed Web of Science ®Google Scholar
• Heinlaan M, Ivask A, Blinova I, Dubourguier HC, Kahru A. 2008. Toxicity of nanosized and bulk ZnO, CuO and TiO2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere 71:1308–16.
   PubMed Web of Science ®Google Scholar
• Henle ES, Han Z, Tang N, Rai P, Luo Y, Linn S. 1999. Sequence-specific DNA cleavage by Fe2+-mediated fenton reactions has possible biological implications. J Biol Chem 274:962–71.
   PubMed Web of Science ®Google Scholar
• Hertzberg RP, Dervan PB. 1982. Cleavage of double helical DNA by methidium-propyl-EDTA-iron(II). J Am Chem Soc 104:313–15.
   Web of Science ®Google Scholar
• Ide T, Tsutsui H, Hayashidani S, Kang D, Suematsu N, Nakamura K, et al. 2001. Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res 88:529–35.
   PubMed Web of Science ®Google Scholar
• Isani G, Falcioni ML, Barucca G, Sekar D, Andreani G, Carpene E, Falcioni G. 2013. Comparative toxicity of CuO nanoparticles and CuSO4 in rainbow trout. Ecotoxicol Environ Saf 97:40–6.
   PubMed Web of Science ®Google Scholar
• Iyanagi T, Yamazaki I, Anan KF. 1985. One-electron oxidation-reduction properties of ascorbic acid. Biochim Biophys Acta 806:255–61.
   Web of Science ®Google Scholar
• Jameson RF, Blackburn NJ. 1982. The copper-catalysed oxidation of ascorbic acid by dioxygen. Part 4. The effect of chloride ions on the kinetics and mechanism. J Chem Soc Dalton Trans 9:9–13.
   Google Scholar
• Jo HJ, Choi JW, Lee SH, Hong SW. 2012. Acute toxicity of Ag and CuO nanoparticle suspensions against Daphnia magna: the importance of their dissolved fraction varying with preparation methods. J Hazard Mater 227–228:301–8.
   PubMed Web of Science ®Google Scholar
• Jose GP, Santra S, Mandal SK, Sengupta TK. 2011. Singlet oxygen mediated DNA degradation by copper nanoparticles: potential towards cytotoxic effect on cancer cells. J Nanobiotechnol 9:9 (1–8).
   PubMed Web of Science ®Google Scholar
• Karlsson HL, Cronholm P, Gustafsson J, Moller L. 2008a. Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21:1726–32.
   PubMed Web of Science ®Google Scholar
• Karlsson HL, Gustafsson J, Cronholm P, Moller L. 2009. Size-dependent toxicity of metal oxide particles-a comparison between nano- and micrometer size. Toxicol Lett 188:112–18.
   PubMed Web of Science ®Google Scholar
• Karlsson HL, Holgersson A, Moller L. 2008b. Mechanisms related to the genotoxicity of particles in the subway and from other sources. Chem Res Toxicol 21:726–31.
   PubMed Web of Science ®Google Scholar
• Kartal SN, Green Iii F, Clausen CA. 2009. Do the unique properties of nanometals affect leachability or efficacy against fungi and termites? Int Biodeterior Biodegrad 63:490–5.
   Web of Science ®Google Scholar
• Kasemets K, Ivask A, Dubourguier HC, Kahru A. 2009. Toxicity of nanoparticles of ZnO, CuO and TiO2 to yeast Saccharomyces cerevisiae. Toxicol In Vitro 23:1116–22.
   PubMed Web of Science ®Google Scholar
• Kehrer JP. 2000. The Haber-Weiss reaction and mechanisms of toxicity. Toxicology 149:43–50.
   PubMed Web of Science ®Google Scholar
• Keyer K, Gort AS, Imlay JA. 1995. Superoxide and the production of oxidative DNA damage. J Bacteriol 177:6782–90.
   PubMed Web of Science ®Google Scholar
• Khan AU, Kasha M. 1994. Singlet molecular oxygen in the Haber-Weiss reaction. Proc Natl Acad Sci USA 91:12365–7.
   PubMed Web of Science ®Google Scholar
• Kimoto E, Tanaka H, Ohmoto T, Choami M. 1993. Analysis of the transformation products of dehydro-L-ascorbic acid by ion-pairing high-performance liquid chromatography. Anal Biochem 214:38–44.
   PubMed Web of Science ®Google Scholar
• Koppenol WH. 1990. Oxyradical reactions: from bond-dissociation energies to reduction potentials. FEBS Lett 264:165–7.
   PubMed Web of Science ®Google Scholar
• Koppenol WH, Stanbury DM, Bounds PL. 2010. Electrode potentials of partially reduced oxygen species, from dioxygen to water. Free Radic Biol Med 49:317–22.
   PubMed Web of Science ®Google Scholar
• Li Y, Zhang W, Niu J, Chen Y. 2012a. Mechanism of photogenerated reactive oxygen species and correlation with the antibacterial properties of engineered metal-oxide nanoparticles. ACS Nano 6:5164–73.
   PubMed Web of Science ®Google Scholar
• Li Y, Zhu T, Zhao J, Xu B. 2012b. Interactive enhancements of ascorbic acid and iron in hydroxyl radical generation in quinone redox cycling. Environ Sci Technol 46:10302–9.
   PubMed Web of Science ®Google Scholar
• Lion Y, Van De Horst A. 1980. On the production of nitroxide radicals by singlet oxygen reaction. Photochem Photbiol 31:305–9.
   Web of Science ®Google Scholar
• Lowry JP, O’Neill RD. 1992. Homogeneous mechanism of ascorbic acid interference in hydrogen peroxide detection at enzyme-modified electrodes. Anal Chem 64:453–6.
   PubMed Web of Science ®Google Scholar
• Luijsterburg MS, Van Attikum H. 2011. Chromatin and the DNA damage response: the cancer connection. Mol Oncol 5:349–67.
   PubMed Web of Science ®Google Scholar
• Luyts K, Napierska D, Nemery B, Hoet PHM. 2013. How physico–chemical characteristics of nanoparticles cause their toxicity: complex and unresolved interrelations. Environ Sci Process Impacts 15:23–38.
   PubMed Web of Science ®Google Scholar
• Mani RG, Smet JH, Von Klitzing K, Narayanamurti V, Johnson WB, Umansky V. 2004. Demonstration of a 1/4-cycle phase shift in the radiation-induced oscillatory magnetoresistance in GaAs/AlGaAs devices. Phys Rev Lett 92:146801–5.
   PubMed Web of Science ®Google Scholar
• Maurer-Jones MA, Gunsolus IL, Murphy CJ, Haynes CL. 2013. Toxicity of engineered nanoparticles in the environment. Anal Chem 85:3036–49.
   PubMed Web of Science ®Google Scholar
• Morgan AR, Cone RL, Elgert TM. 1976. The mechanism of DNA strand breakage by vitamin C and superoxide and the protective roles of catalase and superoxide dismutase. Nucleic Acids Res 3:1139–49.
   PubMed Web of Science ®Google Scholar
• Moshe TB, Dror I, Berkowitz B. 2009. Oxidation of organic pollutants in aqueous solutions by nanosized copper oxide catalysts. Appl Cat B 85:207–11.
   Web of Science ®Google Scholar
• Mouithys-Mickalad A, Deby C, Deby-Dupont G, Lamy M. 1998. An electron spin resonance (ESR) study on the mechanism of ascorbyl radical production by metal-binding proteins. BioMetals 11:81–8.
   PubMed Web of Science ®Google Scholar
• Mystkowski EM. 1942. The oxidation of ascorbic acid in the presence of copper. Biochem J 36:494–500.
   PubMedGoogle Scholar
• Ren G, Hu D, Cheng EW, Vargas-Reus MA, Reip P, Allaker RP. 2009. Characterisation of copper oxide nanoparticles for antimicrobial applications. Int J Antimicrob Agents 33:587–90.
   PubMed Web of Science ®Google Scholar
• Rim KT, Song SW, Kim HY. 2013. Oxidative DNA damage from nanoparticle exposure and its application to workers’ health: a literature review. Saf Health Work 4:177–86.
   PubMedGoogle Scholar
• Sawyer DT, Valentine JS. 1981. How super is superoxide. Acc Chem Res 14:393–400.
   Web of Science ®Google Scholar
• Scherrer P. 1918. Bestimmung der grösse und der inneren struktur von kolloidteilchen mittels röntgenstrahlen. Göttinger Nachrichten Gessell 2:98–100.
   Google Scholar
• Schweigert N, Acero JL, Von Gunten U, Canonica S, Zehnder AJ, Eggen RI. 2000. DNA degradation by the mixture of copper and catechol is caused by DNA-copper-hydroperoxo complexes, probably DNA-Cu(I)OOH. Environ Mol Mutagen 36:5–12.
   PubMed Web of Science ®Google Scholar
• Selvakumar P, Suresh S. 2012. Conective performance of CuO/ater nanofluid in an electronic heat sink. Exp Thermal Fluid Sci 40:57–63.
   Web of Science ®Google Scholar
• Sestili P, Brandi G, Brambilla L, Cattabeni F, Cantoni O. 1996. Hydrogen peroxide mediates the killing of U937 tumor cells elicited by pharmacologically attainable concentrations of ascorbic acid: cell death prevention by extracellular catalase or catalase from cocultured erythrocytes or fibroblasts. J Pharmacol Exp Ther 277:1719–25.
   PubMed Web of Science ®Google Scholar
• Shi J, Abid AD, Kennedy IM, Hristova KR, Silk WK. 2011. To duckweeds (Landoltia punctata), nanoparticulate copper oxide is more inhibitory than the soluble copper in the bulk solution. Environ Pollut 159:1277–82.
   PubMed Web of Science ®Google Scholar
• Stockel J, Safar J, Wallace AC, Cohen FE, Prusiner SB. 1998. Prion protein selectively binds copper(II) ions. Biochemistry 37:7185–93.
   PubMed Web of Science ®Google Scholar
• Studer AM, Limbach LK, Van Duc L, Krumeich F, Athanassiou EK, Gerber LC, et al. 2010. Nanoparticle cytotoxicity depends on intracellular solubility: comparison of stabilized copper metal and degradable copper oxide nanoparticles. Toxicol Lett 197:169–74.
   PubMed Web of Science ®Google Scholar
• Thit A, Selck H, Bjerregaard HF. 2013. Toxicity of CuO nanoparticles and Cu ions to tight epithelial cells from Xenopus laevis (A6): effects on proliferation, cell cycle progression and cell death. Toxicol In Vitro 27:1596–601.
   PubMed Web of Science ®Google Scholar
• Ueda J, Takeshita K, Matsumoto S, Yazaki K, Kawaguchi M, Ozawa T. 2003. Singlet oxygen-mediated hydroxyl radical production in the presence of phenols: whether DMPO-*OH formation really indicates production of *OH? Photochem Photobiol 77:165–70.
   PubMed Web of Science ®Google Scholar
• Vajjha RS, Das DK, Kulkarni D. 2010. Development of new correlations for convective heat transfer and friction factor in turbulent regime for nanofluids. Int J Heat Mass Transfer 53:4607–18.
   Web of Science ®Google Scholar
• Valko M, Morris H, Cronin MT. 2005. Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–208.
   PubMed Web of Science ®Google Scholar
• Villamena FA, Zweier JL. 2004. Detection of reactive oxygen and nitrogen species by EPR spin trapping. Antioxid Redox Signal 6:619–29.
   PubMed Web of Science ®Google Scholar
• Wang Z, Li N, Zhao J, White JC, Qu P, Xing B. 2012. CuO nanoparticle interaction with human epithelial cells: cellular uptake, location, export, and genotoxicity. Chem Res Toxicol 25:1512–21.
   PubMed Web of Science ®Google Scholar
• Wood PM. 1974. The redox potential of the system oxygen-superoxide. FEBS Lett 44:22–4.
   PubMed Web of Science ®Google Scholar
• Yamamoto K, Kawanishi S. 1989. Hydroxyl free radical is not the main active species in site-specific DNA damage induced by copper (II) ion and hydrogen peroxide. J Biol Chem 264:15435–40.
   PubMed Web of Science ®Google Scholar
• Zhao MJ, Jung L. 1995. Kinetics of the competitive degradation of deoxyribose and other molecules by hydroxyl radicals produced by the Fenton reaction in the presence of ascorbic acid. Free Radic Res 23:229–43.
   PubMed Web of Science ®Google Scholar