Multi-platform genotoxicity analysis of silver nanoparticles in the model cell line CHO-K1

Toxicology Letters

Volumn 222, Issue 1, 2013, Pages 55-63

  Jiang, Xiumei ^a,b   Foldbjerg, Rasmus ^b   Miclaus, Teodora ^b   Wang, Liming ^a   Singh, Rajinder ^c   Hayashi, Yuya ^b   Sutherland, Duncan ^b   Chen, Chunying ^a   Autrup, Herman ^b   Beer, Christiane ^b  

^a NATIONAL CENTER FOR NANOSCIENCE AND TECHNOLOGY   (China)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

8 oxodG; Cytotoxicity; DNA adduct; Genotoxicity; Micronucleus assay; Silver nanoparticle

Indexed keywords

REACTIVE OXYGEN METABOLITE; SILVER NANOPARTICLE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE M PHASE; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CELLULAR DISTRIBUTION; CHROMOSOME DAMAGE; CONTROLLED STUDY; CYTOTOXICITY; DNA ADDUCT; DNA DAMAGE; ENDOSOME; FLUORESCENCE MICROSCOPE; GENOTOXICITY; LYSOSOME; MICRONUCLEUS TEST; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL;

8-OXODG; CYTOTOXICITY; DNA ADDUCT; GENOTOXICITY; MICRONUCLEUS ASSAY; SILVER NANOPARTICLE;

ANIMALS; APOPTOSIS; CELL CYCLE; CHO CELLS; COLORING AGENTS; CRICETINAE; CRICETULUS; DEOXYGUANOSINE; DNA ADDUCTS; FLOW CYTOMETRY; MASS SPECTROMETRY; MICRONUCLEUS TESTS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MUTAGENICITY TESTS; MUTAGENS; NANOPARTICLES; NECROSIS; REACTIVE OXYGEN SPECIES; SILVER; TETRAZOLIUM SALTS; THIAZOLES;

EID: 84881308119     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.07.011     Document Type: Article

References (61)

1. Ahamed M., Karns M., Goodson M., Rowe J., Hussain S.M., Schlager J.J., Hong Y. DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicology and Applied Pharmacology 2008, 233:404-410.
2. AshaRani P., Low Kah Mun G., Hande M.P., Valiyaveettil S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 2008, 3:279-290.
3. Bak H., Autrup H., Thomsen B.L., Tjønneland A., Overvad K., Vogel U., Raaschou-Nielsen O., Loft S. Bulky DNA adducts as risk indicator of lung cancer in a Danish case-cohort study. International Journal of Cancer 2005, 118:1618-1622.
4. Beer C., Foldbjerg R., Hayashi Y., Sutherland D.S., Autrup H. Toxicity of silver nanoparticles-nanoparticle or silver ion?. Toxicology Letters 2011, 208:286-292.
5. Bryce S.M., Bemis J.C., Avlasevich S.L., Dertinger S.D. In vitro micronucleus assay scored by flow cytometry provides a comprehensive evaluation of cytogenetic damage and cytotoxicity. Mutation Research - Genetic Toxicology and Environmental Mutagenesis 2007, 630:78-91.
6. Busolo M.A., Fernandez P., Ocio M.J., Lagaron J.M. Novel silver-based nanoclay as an antimicrobial in polylactic acid food packaging coatings. Food Additives and Contaminants A 2010, 27:1617-1626.
7. Cadet J., Delatour T., Douki T., Gasparutto D., Pouget J.P., Ravanat J.L., Sauvaigo S. Hydroxyl radicals and DNA base damage. Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis 1999, 424:9-21.
8. Chairuangkitti P., Lawanprasert S., Roytrakul S., Aueviriyavit S., Phummiratch D., Kulthong K., Chanvorachote P., Maniratanachote R. Silver nanoparticles induce toxicity in A549 cells via ROS-dependent and ROS-independent pathways. Toxicology in Vitro 2012, 27:330-338.
9. Chen C., Qu L., Li B., Xing L., Jia G., Wang T., Gao Y., Zhang P., Li M., Chen W. Increased oxidative DNA damage, as assessed by urinary 8-hydroxy-2'-deoxyguanosine concentrations, and serum redox status in persons exposed to mercury. Clinical Chemistry 2005, 51:759-767.
10. Chen J., Han C.-M., Lin X.-W., Tang Z.-J., Su S.-J. Effect of silver nanoparticle dressing on second degree burn wound. Zhonghua Wai Ke Za Zhi 2006, 44:50-52.
11. Cheng L.-C., Jiang X., Wang J., Chen C., Liu R.-S. Nano-bio effects: interaction of nanomaterials with cells. Nanoscale 2013, 5:3547-3569.
12. Chithrani B.D., Chan W.C.W. Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Letters 2007, 7:1542-1550.
13. Chithrani B.D., Stewart J., Allen C., Jaffray D.A. Intracellular uptake, transport, and processing of nanostructures in cancer cells. Nanomedicine - Nanotechnology 2009, 5:118-127.
14. Cohen M.S., Stern J.M., Vanni A.J., Kelley R.S., Baumgart E., Field D., Libertino J.A., Summerhayes I.C. In vitro analysis of a nanocrystalline silver-coated surgical mesh. Surgical Infections 2007, 8:397-404.
15. Dwivedi S., Saquib Q., Al-Khedhairy A.A., Musarrat J. Butachlor induced dissipation of mitochondrial membrane potential, oxidative DNA damage and necrosis in human peripheral blood mononuclear cells. Toxicology 2012, 302:77-87.
16. Fenech M. Cytokinesis-block micronucleus assay evolves into a "cytome" assay of chromosomal instability, mitotic dysfunction and cell death. Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis 2006, 600:58-66.
17. Fenech M. Cytokinesis-block micronucleus cytome assay. Nature Protocols 2007, 2:1084-1104.
18. Flower N., Brabu B., Revathy M., Gopalakrishnan C., Raja S., Murugan S., Kumaravel T. Characterization of synthesized silver nanoparticles and assessment of its genotoxicity potentials using the alkaline comet assay. Mutation Research - Genetic Toxicology and Environmental Mutagenesis 2012, 742:61-65.
19. Foldbjerg R., Dang D.A., Autrup H. Cytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549. Archives of Toxicology 2011, 85:743-750.
20. Foldbjerg R., Irving E., Hayashi Y., Sutherland D., Thorsen K., Autrup H., Beer C. Global gene expression profiling of human lung epithelial cells after exposure to nanosilver. Toxicological Sciences 2012, 130:145-157.
21. Foldbjerg R., Olesen P., Hougaard M., Dang D.A., Hoffmann H.J., Autrup H. PVP-coated silver nanoparticles and silver ions induce reactive oxygen species, apoptosis and necrosis in THP-1 monocytes. Toxicology Letters 2009, 190:156-162.
22. Fu J., Ji J., Fan D., Shen J. Construction of antibacterial multilayer films containing nanosilver via layer-by-layer assembly of heparin and chitosan-silver ions complex. Journal of Biomedical Materials Research A 2006, 79:665-674.
23. Hackenberg S., Scherzed A., Kessler M., Hummel S., Technau A., Froelich K., Ginzkey C., Koehler C., Hagen R., Kleinsasser N. Silver nanoparticles: evaluation of DNA damage, toxicity and functional impairment in human mesenchymal stem cells. Toxicology Letters 2011, 201:27-33.
24. Hayashi Y., Engelmann P., Foldbjerg R., Szabó M., Somogyi I., Pollák E., Molnár L., Autrup H., Sutherland D.S., Scott-Fordsmand J. Earthworms and humans in vitro: characterizing evolutionarily conserved stress and immune responses to silver nanoparticles. Environmental Science & Technology 2012, 46:4166-4173.
25. Hsin Y.H., Chen C.F., Huang S., Shih T.S., Lai P.S., Chueh P.J. The apoptotic effect of nanosilver is mediated by a ROS-and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicology Letters 2008, 179:130-139.
26. Ishikawa K., Ishii H., Saito T. DNA damage-dependent cell cycle checkpoints and genomic stability. DNA Cell Biology 2006, 25:406-411.
27. Karlsson H.L., Gustafsson J., Cronholm P., Möller L. Size-dependent toxicity of metal oxide particles - a comparison between nano-and micrometer size. Toxicology Letters 2009, 188:112-118.
28. Kasai H. Analysis of a form of oxidative DNA damage, 8-hydroxy-2'-deoxyguanosine, as a marker of cellular oxidative stress during carcinogenesis. Mutation Research 1997, 387:147-163.
29. Kim S., Choi J.E., Choi J., Chung K.H., Park K., Yi J., Ryu D.Y. Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicology in Vitro 2009, 23:1076-1084.
30. Kim T.H., Kim M., Park H.S., Shin U.S., Gong M.S., Kim H.W. Size-dependent cellular toxicity of silver nanoparticles. Journal of Biomedical Materials Research Part A 2012, 100:1033-1043.
31. Kim H.R., Kim M.J., Lee S.Y., Oh S.M., Chung K.H. Genotoxic effects of silver nanoparticles stimulated by oxidative stress in human normal bronchial epithelial (BEAS-2B) cells. Mutation Research-Genetic Toxicology and Environmental Mutagenesis 2011, 726:129-135.
32. Kim Y.S., Kim J.S., Cho H.S., Rha D.S., Kim J.M., Park J.D., Choi B.S., Lim R., Chang H.K., Chung Y.H. Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Sprague-Dawley rats. Inhalation Toxicology 2008, 20:575-583.
33. Kittler S., Greulich C., Diendorf J., Koller M., Epple M. Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions. Journal of Materials Chemistry 2010, 22:4548-4554.
34. Lao F., Chen L., Li W., Ge C., Qu Y., Sun Q., Zhao Y., Han D., Chen C. Fullerene nanoparticles selectively enter oxidation-damaged cerebral microvessel endothelial cells and inhibit JNK-related apoptosis. ACS Nano 2009, 3:3358-3368.
35. Lao F., Li W., Han D., Qu Y., Liu Y., Zhao Y., Chen C. Fullerene derivatives protect endothelial cells against NO-induced damage. Nanotechnology 2009, 20:225103.
36. Li Y., Liu Y., Fu Y., Wei T., Le Guyader L., Gao G., Liu R.-S., Chang Y.-Z., Chen C. The triggering of apoptosis in macrophages by pristine graphene through the MAPK and TGF-beta signaling pathways. Biomaterials 2012, 33:402-411.
37. Lima R., Seabra A.B., Duran N. Silver nanoparticles: a brief review of cytotoxicity and genotoxicity of chemically and biogenically synthesized nanoparticles. Journal of Applied Toxicology 2012, 32:867-879.
38. Liu J., Hurt R.H. Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environmental Science & Technology 2010, 44:2169-2175.
39. Liu Y., Li W., Lao F., Liu Y., Wang L., Bai R., Zhao Y., Chen C. Intracellular dynamics of cationic and anionic polystyrene nanoparticles without direct interaction with mitotic spindle and chromosomes. Biomaterials 2011, 32:8291-8303.
40. Lubick N. Nanosilver toxicity: ions, nanoparticles or both?. Environmental Science & Technology 2008, 42:8617.
41. Meng L., Jiang A., Chen R., Li C., Wang L., Qu Y., Wang P., Zhao Y., Chen C. Inhibitory effects of multiwall carbon nanotubes with high iron impurity on viability and neuronal differentiation in cultured PC12 cells. Toxicology 2012, doi:10.1016/j.tox.2012.1011.1011.
42. Midander K., Cronholm P., Karlsson H.L., Elihn K., Möller L., Leygraf C., Wallinder I.O. 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.
43. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods 1983, 65:55-63.
44. Musarrat J., Arezina-Wilson J., Wani A. Prognostic and aetiological relevance of 8-hydroxyguanosine in human breast carcinogenesis. European Journal of Cancer 1996, 32:1209-1214.
45. Nielsen P.S., De Pater N., Okkels H., Autrup H. Environmental air pollution and DNA adducts in Copenhagen bus drivers - effect of GSTM1 and NAT2 genotypes on adduct levels. Carcinogenesis 1996, 17:1021-1027.
46. OECD Guidelines for the Testing of Chemicals Test No. 487: In Vitro Mammalian Cell Micronucleus Test 2013.
47. Olinski R., Gackowski D., Rozalski R., Foksinski M., Bialkowski K. Oxidative DNA damage in cancer patients: a cause or a consequence of the disease development?. Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis 2003, 531:177-190.
48. Park E.J., Yi J., Kim Y., Choi K., Park K. Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicology in Vitro 2010, 24:872-878.
49. Peckys D.B., de Jonge N. Visualizing gold nanoparticle uptake in live cells with liquid scanning transmission electron microscopy. Nano Letters 2011, 11:1733-1738.
50. Porter A.E., Muller K., Skepper J., Midgley P., Welland M. Uptake of C60 by human monocyte macrophages, its localization and implications for toxicity: studied by high resolution electron microscopy and electron tomography. Acta Biomaterials 2006, 2:409-419.
51. Raoof M., Mackeyev Y., Cheney M.A., Wilson L.J., Curley S.A. Internalization of C60 fullerenes into cancer cells with accumulation in the nucleus via the nuclear pore complex. Biomaterials 2012, 33:2952-2960.
52. Samuel U., Guggenbichler J. Prevention of catheter-related infections: the potential of a new nano-silver impregnated catheter. International Journal of Antimicrobial Agents 2004, 23:75-78.
53. Singh R., Teichert F., Verschoyle R.D., Kaur B., Vives M., Sharma R.A., Steward W.P., Gescher A.J., Farmer P.B. Simultaneous determination of 8-oxo-2'-deoxyguanosine and 8-oxo-2'-deoxyadenosine in DNA using online column-switching liquid chromatography/tandem mass spectrometry. Rapid Communications in Mass Spectrometry 2009, 23:151-160.
54. Toduka Y., Toyooka T., Ibuki Y. Flow cytometric evaluation of nanoparticles using side-scattered light and reactive oxygen species-mediated fluorescence-correlation with genotoxicity. Environmental Science & Technology 2012, 46:7629-7636.
55. Van Engeland M., Ramaekers F.C., Schutte B., Reutelingsperger C.P. A novel assay to measure loss of plasma membrane asymmetry during apoptosis of adherent cells in culture. Cytometry 1996, 24:131-139.
56. Wang L., Liu Y., Li W., Jiang X., Ji Y., Wu X., Xu L., Qiu Y., Zhao K., Wei T. Selective targeting of gold nanorods at the mitochondria of cancer cells: implications for cancer therapy. Nano Letters 2010, 11:772-780.
57. Wei L., Tang J., Zhang Z., Chen Y., Zhou G., Xi T. Investigation of the cytotoxicity mechanism of silver nanoparticles in vitro. Biomedical Materials 2010, 5:044103.
58. Xu X., Yang Q., Bai J., Lu T., Li Y., Jing X. Fabrication of biodegradable electrospun poly(l-lactide-co-glycolide) fibers with antimicrobial nanosilver particles. Journal of Nanoscience and Nanotechnology 2008, 8:5066-5070.
59. Yang H., Liu C., Yang D., Zhang H., Xi Z. Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterials: the role of particle size, shape and composition. Journal of Applied Toxicology 2008, 29:69-78.
60. Zhao F., Zhao Y., Liu Y., Chang X., Chen C. Cellular uptake, intracellular trafficking, and cytotoxicity of nanomaterials. Small 2011, 7:1322-1337.
61. Zhou H., Zhao K., Li W., Yang N., Liu Y., Chen C., Wei T. The interactions between pristine graphene and macrophages and the production of cytokines/chemokines via TLR-and NF-κB-related signaling pathways. Biomaterials 2012, 33:6933-6942.