Cytotoxicity and genotoxicity of nano - and microparticulate copper oxide: Role of solubility and intracellular bioavailability

Particle and Fibre Toxicology

Volumn 11, Issue 1, 2014, Pages

  Semisch, Annetta ^a   Ohle, Julia ^a   Witt, Barbara ^a   Hartwig, Andrea ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

Apoptosis; Bioavailability; Copper chloride; Copper oxide microparticles; Copper oxide nanoparticles; Cytotoxicity; Genotoxicity; Intracellular distribution; Poly(ADP ribosyl)ation

Indexed keywords

APOPTOSIS INDUCING FACTOR; CELL DNA; COPPER CHLORIDE; COPPER ION; COPPER OXIDE; COPPER OXIDE MICROPARTICLE; COPPER OXIDE NANOPARTICLE; HYDROGEN PEROXIDE; METAL NANOPARTICLE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; UNCLASSIFIED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; BIOAVAILABILITY; CATALYSIS; CELL DEATH; CELL FRACTIONATION; CELL NUCLEUS; CELL STRAIN; CELL STRAIN A549; CELL STRAIN HELA S3; COLONY FORMATION; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; DIPLOIDY; DISSOLUTION; DNA STRAND BREAKAGE; GENOTOXICITY; HUMAN; HUMAN CELL; LYSOSOME; PRIORITY JOURNAL; PROTEIN TRANSPORT;

APOPTOSIS; BIOLOGICAL AVAILABILITY; CASPASE 3; CASPASE 7; CELL NUCLEUS; CELL SURVIVAL; COPPER; DNA DAMAGE; ENDOTOXINS; HELA CELLS; HUMANS; INDICATORS AND REAGENTS; METAL NANOPARTICLES; MICRONUCLEUS TESTS; MICROSCOPY, ELECTRON, SCANNING; MUTAGENS; PARTICLE SIZE; POLY ADENOSINE DIPHOSPHATE RIBOSE; SOLUBILITY; TRANSLOCATION, GENETIC; VISCOSITY;

EID: 84893710296     PISSN: None     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/1743-8977-11-10     Document Type: Article

References (50)

1. Linder MC. Copper and genomic stability in mammals. Mutat Res/Fundam Mol Mech Mutagen 2001, 475:141-152.
2. Rana SVS. Metals and apoptosis: recent developments. J Trace Elem Med Biol 2008, 22:262-284. 10.1016/j.jtemb.2008.08.002, 19013355.
3. Festa RA, Thiele DJ. Copper: an essential metal in biology. Curr Biol 2011, 21:877-883.
4. Jomova K, Baros S, Valko M. Redox active metal-induced oxidative stress in biological systems. Transit Met Chem 2012, 37:127-134.
5. Hartwig A. Metal interaction with redox regulation: an integrating concept in metal carcinogenesis?. Free Radic Biol Med 2013, 55:63-72.
6. Schwerdtle T, Hamann I, Jahnke G, Walter I, Richter C, Parsons JL, Dianov GL, Hartwig A. Impact of copper on the induction and repair of oxidative DNA damage, poly(ADP-ribosyl)ation and PARP-1 activity. Mol Nutr Food Res 2007, 51:201-210. 10.1002/mnfr.200600107, 17230584.
7. Reddy VP, Kumar AV, Swapna K, Rao KR. Copper oxide nanoparticle-catalyzed coupling of diaryl diselenide with aryl halides under ligand-free conditions. Org Lett 2009, 11:951-953. 10.1021/ol802734f, 19182886.
8. Gabbay J, Borkow G, Mishal J, Magen E, Zatcoff R, Shemer-Avni Y. Copper oxide impregnated textiles with potent biocidal activities. J Ind Text 2006, 35:323-335.
9. Ben-Moshe T, Dror I, Berkowitz B. Oxidation of organic pollutants in aqueous solutions by nanosized copper oxide catalysts. Appl Catal B Environ 2009, 85:207-211.
10. Shah ID, Ruzzi PL, Schluter RB. Decomposition of cupric oxide using a reducing scavenger. United States Pat 1978, 4:080,430.
11. Nel AE, Madler L, Velegol D, Xia T, Hoek EMV, Somasundaran P, Klaessig F, Castranova V, Thompson M. Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater 2009, 8:543-557. 10.1038/nmat2442, 19525947.
12. Monopoli MP, Aberg C, Salvati A, Dawson KA. Biomolecular coronas provide the biological identity of nanosized materials. Nat Nano 2012, 7:779-786.
13. Sayes CM, Warheit DB. Characterization of nanomaterials for toxicity assessment. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2009, 1:660-670. 10.1002/wnan.58, 20049823.
14. Wang Y, Hodgkinson V, Zhu S, Weisman GA, Petris MJ. Advances in the understanding of mammalian copper transporters. Adv Nutr Res: Int Rev J 2011, 2:129-137.
15. Canton I, Battaglia G. Endocytosis at the nanoscale. Chem Soc Rev 2012, 41:2718-2739. 10.1039/c2cs15309b, 22389111.
16. Hanagata N, Zhuang F, Connolly S, Li J, Ogawa N, Xu M. Molecular responses of human lung epithelial cells to the toxicity of copper oxide nanoparticles inferred from whole genome expression analysis. ACS nano 2011, 5:9326-9338. 10.1021/nn202966t, 22077320.
17. Wang Z, Li N, Zhao J, White JC, Qu P, Xing B. CuO nanoparticle interaction with human epithelial cells: cellular uptake, location, export, and genotoxicity. Chem Res Toxicol 2012, 25:1512-1521. 10.1021/tx3002093, 22686560.
18. Cronholm P, Karlsson HL, Hedberg J, Lowe TA, Winnberg L, Elihn K, Wallinder IO, Möller L. Intracellular uptake and toxicity of Ag and CuO nanoparticles: a comparison between nanoparticles and their corresponding metal ions. Small 2013, 9:970-982. 10.1002/smll.201201069, 23296910.
19. Karlsson HL, Cronholm P, Gustafsson J, Möller L. Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 2008, 21:1726-1732. 10.1021/tx800064j, 18710264.
20. Karlsson H, Gustafsson J, Cronholm P, Möller L. Size-dependent toxicity of metal oxide particles-a comparison between nano- and micrometer size. Toxicol Lett 2009, 188:112-118. 10.1016/j.toxlet.2009.03.014, 19446243.
21. Midander K, Cronholm P, Karlsson HL, Elihn K, Möller L, Leygraf C, Wallinder IO. Surface characteristics, copper release, and toxicity of nano- and micrometer-sized copper and copper(II) oxide particles: a cross-disciplinary study. Small 2009, 5:389-399. 10.1002/smll.200801220, 19148889.
22. Song MF, Li YS, Kasai H, Kawai K. Metal nanoparticle-induced micronuclei and oxidative DNA damage in mice. J clin biochem nutr 2012, 50:211-216. 10.3164/jcbn.11-70, 3334374, 22573923.
23. Perreault F, Melegari SP, da Costa CH, de Oliveira Franco Rossetto AL, Popovic R, Matias WG. Genotoxic effects of copper oxide nanoparticles in Neuro 2A cell cultures. Sci Total Environ 2012, 441:117-124.
24. Di Bucchianico S, Fabbrizi MR, Misra SK, Valsami-Jones E, Berhanu D, Reip P, Bergamaschi E, Migliore L. Multiple cytotoxic and genotoxic effects induced in vitro by differently shaped copper oxide nanomaterials. Mutagenesis 2013, 28:287-299. 10.1093/mutage/get014, 23462852.
25. Semisch A, Hartwig A. Copper ions interfere with the reduction of the water soluble tetrazolium salt-8. Chem Res Toxicol 2014, epub ahead of print, doi:10.1021/tx400414c.
26. Bryce SM, Bemis JC, Avlasevich SL, Dertinger SD. In vitro micronucleus assay scored by flow cytometry provides a comprehensive evaluation of cytogenetic damage and cytotoxicity. Mutat Res 2007, 630:78-91. 10.1016/j.mrgentox.2007.03.002, 1950716, 17434794.
27. Berntsen P, Park CY, Rothen-Rutishauser B, Tsuda A, Sager TM, Molina RM, Donaghey TC, Alencar AM, Kasahara DI, Ericsson T, Millet EJ, Swenson J, Tschumperlin DJ, Butler JP, Brain JD, Fredberg JJ, Gehr P, Zhou EH. Biomechanical effects of environmental and engineered particles on human airway smooth muscle cells. J R Soc Interface 2010, 7(Suppl 3):331-340.
28. Studer AM, Limbach LK, Van Duc L, Krumeich F, Athanassiou EK, Gerber LC, Moch H, Stark WJ. Nanoparticle cytotoxicity depends on intracellular solubility: comparison of stabilized copper metal and degradable copper oxide nanoparticles. Toxicol Lett 2010, 197:169-174. 10.1016/j.toxlet.2010.05.012, 20621582.
29. Huang C-C, Hwu JR, Su W-C, Shieh D-B, Tzeng Y, Yeh C-S. Surfactant-assisted hollowing of Cu nanoparticles involving halide-induced corrosion-oxidation processes. Chem Eur J 2006, 12:3805-3810. 10.1002/chem.200501484, 16528773.
30. Seiffert JM, Baradez M-O, Nischwitz V, Lekishvili T, Goenaga-Infante H, Marshall D. Dynamic monitoring of metal oxide nanoparticle toxicity by label free impedance sensing. Chem Res Toxicol 2011, 25:140-152.
31. Lynch I, Dawson KA. Protein-nanoparticle interactions. Nano Today 2008, 3:40-47.
32. Schwerdtle T, Hartwig A. Bioavailability and genotoxicity of soluble and particulate nickel compounds in cultured human lung cells. Mater Werkst 2006, 37:521-525.
33. Ralle M, Huster D, Vogt S, Schirrmeister W, Burkhead JL, Capps TR, Gray L, Lai B, Maryon E, Lutsenko S. Wilson disease at a single cell level: intracellular copper trafficking activates compartment-specific responses in hepatocytes. J Biol Chem 2010, 285:30875-30883. 10.1074/jbc.M110.114447, 2945580, 20647314.
34. Fabisiak JP, Pearce LL, Borisenko GG, Tyhurina YY, Tyurin VA, Razzack J, Lazo JS, Pitt BR, Kagan VE. Bifunctional anti/prooxidant potential of metallothionein: redox signaling of copper binding and release. Antioxid Redox Signal 1999, 1:349-364. 10.1089/ars.1999.1.3-349, 11229446.
35. Bai P, Cantó C. The role of PARP-1 and PARP-2 enzymes in metabolic regulation and disease. Cell Metab 2012, 16:290-295.
36. Krishnakumar R, Kraus WL. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol Cell 2010, 39:8-24. 10.1016/j.molcel.2010.06.017, 2923840, 20603072.
37. Langelier M-F, Servent KM, Rogers EE, Pascal JM. A third zinc-binding domain of human poly(ADP-ribose) polymerase-1 coordinates DNA-dependent enzyme activation. J Biol Chem 2008, 283:4105-4114. 10.1074/jbc.M708558200, 18055453.
38. Woodhouse BC, Dianov GL. Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair 2008, 7:1077-1086. 10.1016/j.dnarep.2008.03.009, 18468963.
39. Rhun YL, Kirkland JB, Shah GM. Cellular responses to DNA damage in the absence of poly(ADP-ribose) polymerase. Biochem Biophys Res Commun 1998, 245:1-10. 10.1006/bbrc.1998.8257, 9535773.
40. Gradwohl G, de Murcia JM M, Molinete M, Simonin F, Koken M, Hoeijmakers JH, de Murcia G. The second zinc-finger domain of poly(ADP-ribose) polymerase determines specificity for single-stranded breaks in DNA. Proc Natl Acad Sci 1990, 87:2990-2994. 10.1073/pnas.87.8.2990, 53819, 2109322.
41. Weibel A, Bouchet R, Boulc'h F, Knauth P. The big problem of small particles: a comparison of methods for determination of particle size in nanocrystalline anatase powders. Chem Mater 2005, 17:2378-2385.
42. Schulze C, Kroll A, Lehr C-M, Schäfer UF, Becker K, Schnekenburger J, Schulze Isfort C, Landsiedel R, Wohlleben W. Not ready to use - overcoming pitfalls when dispersing nanoparticles in physiological media. Nanotoxicology 2008, 2:51-61.
43. Ladelfe PC, Czanderna AW, Biegen JR. Optical constants of cupric oxide from 450 to 800 mμ. Thin Solid Films 1972, 10:403-411.
44. Brunauer S, Emmett PH, Teller E. Adsorption of gases in multimolecular layers. J Am Chem Soc 1938, 60:309-319.
45. Stopford W, Turner J, Cappellini D, Brock T. Bioaccessibility testing of cobalt compounds. J Environ Monit 2003, 5:675-680. 10.1039/b302257a, 12948248.
46. Midander K, Wallinder IO, Leygraf C. In vitro studies of copper release from powder particles in synthetic biological media. Environ Pollut 2007, 145:51-59. 10.1016/j.envpol.2006.03.041, 16714077.
47. Hartwig A, Klyszcz-Nasko H, Schlepegrell R, Beyersmann D. Cellular damage by ferric nitrilotriacetate and ferric citrate in V79 cells: interrelationship between lipid peroxidation, DNA strand breaks and sister-chromatid exchanges. Carcinogenesis 1993, 14:107-112. 10.1093/carcin/14.1.107, 8425256.
48. Hartwig A, Pelzer A, Asmuss M, Bürkle A. Very low concentrations of arsenite suppress poly(ADP-ribosyl)ation in mammalian cells. Int J Cancer 2003, 104:1-6. 10.1002/ijc.10911, 12532412.
49. Kawamitsu H, Hoshino H, Okada H, Miwa M, Momoi H, Sugimura T. Monoclonal antibodies to poly(adenosine diphosphate ribose) recognize different structures. Biochemistry 1984, 23:3771-3777. 10.1021/bi00311a032, 6206890.
50. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.