Neuronal cytotoxicity and genotoxicity induced by zinc oxide nanoparticles

Environment International

Volumn 55, Issue , 2013, Pages 92-100

  Valdiglesias, Vanessa ^a,b   Costa, Carla ^c   Kiliç, Gözde ^a   Costa, Solange ^c   Pásaro, Eduardo ^a   Laffon, Blanca ^a   Teixeira, João Paulo ^c  

^a UNIVERSITY OF A CORUÑA   (Spain)

^b IRCCS SAN RAFFAELE PISANA   (Italy)

^c NATIONAL INSTITUTE OF HEALTH   (Portugal)

Author keywords

Cytotoxicity; Genotoxicity; Oxidative damage; SHSY5Y cells; Zinc oxide nanoparticles

Indexed keywords

CELL DEATH; CONSUMER PRODUCTS; CYTOTOXICITY; FLOW CYTOMETRY; MEDICAL APPLICATIONS; NANOPARTICLES; NEURONS; TISSUE; ZINC;

ACTION MECHANISMS; BIOMEDICAL APPLICATIONS; EXPOSURE CONDITIONS; GENOTOXIC EFFECTS; GENOTOXICITIES; OXIDATIVE DAMAGE; SH-SY5Y CELLS; ZINC OXIDE NANOPARTICLES;

ZINC OXIDE;

HISTONE H2AX; NANOPARTICLE; UNCLASSIFIED DRUG; ZINC ION; ZINC OXIDE NANOPARTICLE;

DAMAGE; FLOW CYTOMETRY; ION; NERVOUS SYSTEM; OXIDE; PARTICULATE MATTER; POLLUTION EFFECT; POLLUTION EXPOSURE; TOXICITY; TOXICOLOGY; ZINC;

APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY TEST; DNA DAMAGE; GENOTOXICITY; HUMAN; HUMAN CELL; MICRONUCLEUS; NERVE CELL; NEUROTOXICITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 84875611485     PISSN: 01604120     EISSN: 18736750     Source Type: Journal    
DOI: 10.1016/j.envint.2013.02.013     Document Type: Article

References (58)

1. Akhtar M.J., Ahamed M., Kumar S., Khan M.M., Ahmad J., Alrokayan S.A. Zinc oxide nanoparticles selectively induce apoptosis in human cancer cells through reactive oxygen species. Int J Nanomedicine 2012, 7:845-857.
2. Avlasevich S.L., Bryce S.M., Cairns S.E., Dertinger S.D. In vitro micronucleus scoring by flow cytometry: differential staining of micronuclei versus apoptotic and necrotic chromatin enhances assay reliability. Environ Mol Mutagen 2006, 47:56-66.
3. Block M.L., Wu X., Pei Z., Li G., Wang T., Qin L., et al. Nanometer size diesel exhaust particles are selectively toxic to dopaminergic neurons: the role of microglia, phagocytosis, and NADPH oxidase. FASEB J 2004, 18:1618.
4. Borenfreund E., Puerner J.A. Toxicity determined in vitro by morphological alterations and neutral red absorption. Toxicol Lett 1985, 24:119-124.
5. Chiang H.M., Xia Q., Zou X., Wang C., Wang S., Miller B.J., et al. Nanoscale ZnO induces cytotoxicity and DNA damage in human cell lines and rat primary neuronal cells. J Nanosci Nanotechnol 2012, 12:2126-2135.
6. Costa S., Coelho P., Costa C., Silva S., Mayan O., Santos L.S., et al. Genotoxic damage in pathology anatomy laboratory workers exposed to formaldehyde. Toxicology 2008, 252:40-48.
7. Daniels W., Hendricks J., Salie R., Rensburg S. A mechanism for zinc toxicity in neuroblastoma cells. Metab Brain Dis 2004, 19:79-88.
8. De Berardis B., Civitelli G., Condello M., Lista P., Pozzi R., Arancia G., et al. Exposure to ZnO nanoparticles induces oxidative stress and cytotoxicity in human colon carcinoma cells. Toxicol Appl Pharmacol 2010, 246:116-127.
9. Deng X., Luan Q., Chen W., Wang Y., Wu M., Zhang H., et al. Nanosized zinc oxide particles induce neural stem cell apoptosis. Nanotechnology 2009, 20:115101.
10. 2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environ Sci Technol 2007, 41:8484-8490.
11. Fukui H., Horie M., Endoh S., Kato H., Fujita K., Nishio K., et al. Association of zinc ion release and oxidative stress induced by intratracheal instillation of ZnO nanoparticles to rat lung. Chem Biol Interact 2012, 198:29-37.
12. Han D., Tian Y., Zhang T., Ren G., Yang Z. Nano-zinc oxide damages spatial cognition capability via over-enhanced long-term potentiation in hippocampus of Wistar rats. Int J Nanomedicine 2011, 6:1453-1461.
13. Hanley C., Layne J., Punnoose A., Reddy K.M., Coombs I., Coombs A., et al. Preferential killing of cancer cells and activated human T cells using ZnO nanoparticles. Nanotechnology 2008, 19:295103.
14. Hao L., Chen L. Oxidative stress responses in different organs of carp (Cyprinus carpio) with exposure to ZnO nanoparticles. Ecotoxicol Environ Saf 2012, 80:103-110.
15. Hsiao I.L., Huang Y.J. Effects of various physicochemical characteristics on the toxicities of ZnO and TiO nanoparticles toward human lung epithelial cells. Sci Total Environ 2011, 409(7):1219-1228.
16. Hu Y.L., Gao J.Q. Potential neurotoxicity of nanoparticles. Int J Pharm 2010, 394:115-121.
17. Jeng H.A., Swanson J. Toxicity of metal oxide nanoparticles in mammalian cells. J Environ Sci Health A 2006, 41:2699-2711.
18. Kao Y.Y., Cheng T.J., Yang D.M., Wang C.T., Chiung Y.M., Liu P.S. Demonstration of an olfactory bulb-brain translocation pathway for ZnO nanoparticles in rodent cells in vitro and in vivo. J Mol Neurosci 2012, 48:464-471.
19. Kao Y.Y., Chen Y.C., Cheng T.J., Chiung Y.M., Liu P.S. Zinc oxide nanoparticles interfere with zinc ion homeostasis to cause cytotoxicity. Toxicol Sci 2012, 125(2):462-472.
20. Kim Y.H., Fazlollahi F., Kennedy I.M., Yacobi N.R., Hamm-Alvarez S.F., Borok Z., et al. Alveolar epithelial cell injury due to zinc oxide nanoparticle exposure. Am J Respir Crit Care Med 2010, 182:1398-1409.
21. Kim J.A., Åberg C., Salvati A., Dawson K.A. Role of cell cycle on the cellular uptake and dilution of nanoparticles in a cell population. Nat Nanotechnol 2011, 7:62-68.
22. Kozik M.B., Maziarz L., Godlewski A. Morphological and histochemical changes occurring in the brain of rats fed large doses of zinc oxide. Folia Histochem Cytochem (Krakow) 1980, 18:201-206.
23. Lai J.C., Lai M.B., Jandhyam S., Dukhande V.V., Bhushan A., Daniels C.K., et al. Exposure to titanium dioxide and other metallic oxide nanoparticles induces cytotoxicity on human neural cells and fibroblasts. Int J Nanomedicine 2008, 3(4):533-545.
24. Lee C.M., Jeong H.J., Kim D.W., Sohn M.H., Lim S.T. The effect of fluorination of zinc oxide nanoparticles on evaluation of their biodistribution after oral administration. Nanotechnology 2012, 23:205102.
25. Lesniak A., Campbell A., Monopoli M.P., Lynch I., Salvati A., Dawson K.A. Serum heat inactivation affects protein corona composition and nanoparticle uptake. Biomaterials 2010, 31:9511-9518.
26. Li J., Liu X., Zhang Y., Tian F., Zhao G., Yu Q., et al. Toxicity of nano zinc oxide to mitochondria. Toxicol Res 2012, 1:137.
27. Lin W., Xu Y., Huang C.-C., Ma Y., Shannon K.B., Chen D.-R., et al. Toxicity of nano- and micro-sized ZnO particles in human lung epithelial cells. J Nanopart Res 2009, 11:25-39.
28. Mosmann T. Rapid colorimetric assay for cellular growth and survival, application to proliferation and cytotoxicity assays. J Immunol Methods 1983, 65:55-63.
29. Nair S., Sasidharan A., Rani V.V.D., Menon D., Nair S., Manzoor K., et al. Role of size scale of ZnO nanoparticles and microparticles on toxicity toward bacteria and osteoblast cancer cells. J Mater Sci Mater Med 2009, 20:235-241.
30. Nüsse M., Beisker W., Kramer J., Miller B.M., Schreiber G.A., Viaggi S., et al. Measurement of micronuclei by flow cytometry. Methods Cell Biol 1994, 42:149-158.
31. Oberdörster G., Sharp Z., Atudorei V., Elder A., Gelein R., Kreyling W., et al. Inhal Toxicol 2004, 16:437.
32. Osman I.F., Baumgartner A., Cemeli E., Fletcher J.N., Anderson D. Genotoxicity and cytotoxicity of zinc oxide and titanium dioxide in HEp-2 cells. Nanomedicine (Lond) 2010, 5:1193-1203.
33. Ostrovsky S., Kazimirsky G., Gedanken A., Brodie C. Selective cytotoxic effect of ZnO nanoparticles on glioma cells. Nano Res 2009, 2:882-890.
34. Pasupuleti S., Alapati S., Ganapathy S., Anumolu G., Pully N.R., Prakhya B.M. Toxicity of zinc oxide nanoparticles through oral route. Toxicol Ind Health 2012, 28:675-686.
35. Pavlica S., Gaunitz F., Gebhardt R. Comparative in vitro toxicity of seven zinc-salts towards neuronal PC12 cells. Toxicol in Vitro 2009, 23:653-659.
36. Peters A., Veronesi B., Calderon-GarciduenasL Gehr P., Chen L.C., Geiser M., Reed W., et al. Translocation and potential neurological effects of fine and ultrafine particles a critical update. Part Fibre Toxicol 2006, 3:13.
37. Premanathan M., Karthikeyan K., Jeyasubramanian K., Manivannan G. Selective toxicity of ZnO nanoparticles toward Gram positive bacteria and cancer cells by apoptosis through lipid peroxidation. Nanomedicine: NBM 2011, 7:184-192.
38. Qiang J.L. The surface properties and photocatalytic activities of ZnO ultrafine particles. Appl Surf Sci 2001, 180:308-314.
39. Reed R.B., Ladner D.A., Higgins C.P., Westerhoff P., Ranville J.F. Solubility of nano-zinc oxide in environmentally and biologically important matrices. Environ Toxicol Chem 2012, 31:93-99.
40. Roman D., Locher F., Suter W., Cordier A., Bobadilla M. Evaluation of a new procedure for the flow cytometric analysis of in vitro, chemically induced micronuclei in V79 cells. Environ Mol Mutagen 1998, 32:387-396.
41. Seil J.T., Webster T.J. Decreased astroglial cell adhesion and proliferation on zinc oxide nanoparticle polyurethane composites. Int J Nanomedicine 2008, 3:523-531.
42. Sharma V., Shukla R.K., Saxena N., Parmar D., Das M., Dhawan A. DNA damaging potential of zinc oxide nanoparticles in human epidermal cells. Toxicol Lett 2009, 185:211-218.
43. Sharma V., Singh S.K., Anderson D., Tobin D.J., Dhawan A. Zinc oxide nanoparticle induced genotoxicity in primary human epidermal keratinocytes. J Nanosci Nanotechnol 2011, 11:3782-3788.
44. Sharma V., Singh P., Pandey A.K., Dhawan A. Induction of oxidative stress, DNA damage and apoptosis in mouse liver after sub-acute oral exposure to zinc oxide nanoparticles. Mutat Res 2012, 745:84-91.
45. Sharma V., Anderson D., Dhawan A. Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria mediated apoptosis in human liver cells (HepG2). Apoptosis 2012, 17:852-870.
46. Singh N.P., McCoy M.T., Tice R.R., Schneider E.L. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 1988, 175:184-191.
47. Smith C.C., O'Donovan M.R., Martin E.A. hOGG1 recognizes oxidative damage using the comet assay with greater specificity than FPG or ENDOIII. Mutagenesis 2006, 21:185-190.
48. Suzuki H., Toyooka T., Ibuki Y. Simple and easy method to evaluate uptake potential of nanoparticles in mammalian cells using a flow cytometric light scatter analysis. Environ Sci Technol 2007, 41:3018-3024.
49. Tanaka T., Halicka D., Traganos F., Darzynkiewicz Z. Cytometric analysis of DNA damage, phosphorylation of histone H2AX as a marker of DNA double-strand breaks (DSBs). Methods Mol Biol 2009, 523:161-168.
50. Valdiglesias V., Laffon B., Pásaro E., Méndez J. Okadaic acid induces morphological changes, apoptosis and cell cycle alterations in different human cell types. J Environ Monit 2011, 13(6):1831-1840.
51. Valdiglesias V., Laffon B., Pásaro E., Méndez J. Okadaic acid-induced genotoxicity in human cells evaluated by micronucleus test and γH2AX analysis. J Toxicol Environ Health 2011, 74:980-992.
52. Vandebriel R.J., De Jong W.H. A review of mammalian toxicity of ZnO nanoparticles. Nanotechnol Sci Appl 2012, 5:61-71.
53. Wahab R., Kaushik N.K., Verma A.K., Mishra A., Hwang I.H., Yang Y.B., et al. Fabrication and growth mechanism of ZnO nanostructures and their cytotoxic effect on human brain tumor U87, cervical cancer HeLa, and normal HEK cells. J Biol Inorg Chem 2011, 16:431-442.
54. Wang L., Wang L., Ding W., Zhang F. Acute toxicity of ferric oxide and zinc oxide nanoparticles in rats. J Nanosci Nanotechnol 2010, 10:8617-8624.
55. Wong S.W., Leung P.T., Djurisić A.B., Leung K.M. Toxicities of nano zinc oxide to five marine organisms: influences of aggregate size and ion solubility. Anal Bioanal Chem 2010, 396:609-618.
56. 2, ZnO and their bulk counterparts on zebrafish: acute toxicity, oxidative stress and oxidative damage. Sci Total Environ 2011, 409:1444-1452.
57. Yin Y., Lin Q., Sun H., Chen D., Wu Q., Chen X., et al. Cytotoxic effects of ZnO hierarchical architectures on RSC96 Schwann cells. Nanoscale Res Lett 2012, 7:439.
58. Zhao J., Xu L., Zhang T., Ren G., Yang Z. Influences of nanoparticle zinc oxide on acutely isolated rat hippocampal CA3 pyramidal neurons. Neurotoxicology 2009, 30:220-230.