In vivo genotoxicity assessment of titanium, zirconium and aluminium nanoparticles, and their microparticulated forms, in Drosophila

Chemosphere

Volumn 93, Issue 10, 2013, Pages 2304-2310

  Demir, Eşref ^a   Turna, Fatma ^a   Vales, Gerard ^b   Kaya, Bülent ^a   Creus, Amadeu ^b,c   Marcos, Ricard ^b,c  

^a AKDENIZ UNIVERSITY   (Turkey)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Aluminium oxide nanoparticles; Drosophila melanogaster; Genotoxicity; Titanium dioxide nanoparticles; Wing spot assay; Zirconium oxide nanoparticles

Indexed keywords

ALUMINA; ALUMINUM OXIDE; NANOPARTICLES; TITANIUM DIOXIDE; ZIRCONIA;

ALUMINIUM OXIDE; DROSOPHILA MELANOGASTER; GENOTOXIC ACTIVITY; GENOTOXIC EVALUATION; GENOTOXICITIES; NANOPARTICLE EXPOSURES; OXIDE NANOPARTICLES; TITANIUM DIOXIDES (TIO2);

TIO2 NANOPARTICLES;

ALUMINUM OXIDE; NANOPARTICLE; TITANIUM DIOXIDE; ZIRCONIUM OXIDE; MUTAGENIC AGENT; TITANIUM; ZIRCONIUM;

ADULT; ALUMINUM; BIOASSAY; DATABASE; FLY; GENOTOXICITY; MUTATION; TITANIUM; WING; ZIRCONIUM;

ARTICLE; CONTROLLED STUDY; DIGESTIVE SYSTEM; DROSOPHILA MELANOGASTER; FORELIMB; GENE EXPRESSION; GENOTOXICITY; HAIR; HETEROZYGOSITY; IN VIVO STUDY; LARVA; NONHUMAN; SOMATIC MUTATION; ANIMAL; MUTAGEN TESTING; TOXICITY;

DROSOPHILA MELANOGASTER;

ALUMINUM OXIDE; ANIMALS; DROSOPHILA MELANOGASTER; MUTAGENICITY TESTS; MUTAGENS; NANOPARTICLES; TITANIUM; ZIRCONIUM;

EID: 84886945940     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2013.08.022     Document Type: Article

References (55)

1. Adams M.D., Celniker S.E., Holt R.A., Evans C.A., Gocayne J.D., Amanatides P.G., Scherer S.E., Li P.W., Hoskins R.A., Galle R.F., et al. The genome sequence of Drosophila melanogaster. Science 2000, 287:2185-2195.
2. Ahamed M., Posgai R., Gorey T.J., Nielsen M., Hussain S.M., Rowe J.J. Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster. Toxicol. Appl. Pharmacol. 2010, 242:263-269.
3. Ai J., Biazar E., Jafarpour M., Montazeri M., Majdi A., Aminifard S., Zafari M., Akbari H.R., Rad H.G. Nanotoxicology and nanoparticle safety in biomedical designs. Int. J. Nanomed. 2011, 6:1117-1127.
4. Alonso-Moraga A., Graf U. Genotoxicity testing of antiparasitic nitrofurans in the Drosophila wing somatic mutation and recombination test. Mutagenesis 1989, 4:105-110.
5. ATSDR (Agency for Toxic Substances and Disease Registry), 1999. Agency for toxic substances and disease registry toxicological profile of aluminium, U.S. Department of health and human services, public health service http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=191&tid=34.
6. Baan R.A. Carcinogenic hazards from inhaled carbon black, titanium dioxide, and talc not containing asbestos or asbestiform fibers: recent evaluations by an IARC Monographs Working Group. Inhal. Toxicol. 2007, 19:213-228.
7. Balasubramanyam A., Sailaja N., Mahboob M., Rahman M.F., Hussain S.M., Grover P. In vivo genotoxicity assessment of aluminium oxide nanomaterials in rat peripheral blood cells using the comet assay and micronucleus test. Mutagenesis 2009, 24:245-251.
8. Balasubramanyam A., Sailaja N., Mahboob M., Rahman M.F., Misra S., Hussain S.M., Grover P. Evaluation of genotoxic effects of oral exposure to aluminium oxide nanomaterials in rat bone marrow. Mutat. Res. 2009, 676:41-47.
9. Banasik A., Lankoff A., Piskulak A., Adamowska K., Lisowska H., Wojcik A. Aluminum-induced micronuclei and apoptosis in human peripheral-blood lymphocytes treated during different phases of the cell cycle. Environ. Toxicol. 2005, 20:402-406.
10. Bermudez E., Mangum J.B., Wong B.A., Asgharian B., Hext P.M., Warheit D.B., Everitt J.I. Pulmonary responses of mice, rats, and hamsters to subchronic inhalation of ultrafine titanium dioxide particles. Toxicol. Sci. 2004, 77:347-357.
11. Bhattacharya K., Davoren M., Boertz J., Schins R.P.F., Hoffmann E., Dopp E. Titanium dioxide nanoparticles induce oxidative stress and DNA adduct formation but not DNA breakage in human lung cells. Part Fibre Toxicol. 2009, 21:6-17.
12. Braz M.G., De Castro Marcondes J.P., Matsumoto M.A., Duarte M.H., Salvadori D.M.F., Ribeiro D.A. Genotoxicity in primary human peripheral lymphocytes after exposure to radiopacifiers in vitro. J. Mater. Sci. Mater. M 2008, 19:601-605.
13. Carmona E.R., Kossatz E., Creus A., Marcos R. Genotoxic evaluation of two mercury compounds in the Drosophila wing spot test. Chemosphere 2008, 70:1910-1914.
14. Dalal A., Pawar V., McAllister K., Weaver C., Hallab N.J. Orthopedic implant cobalt-alloy particlesproduce greater toxicity and inflammatory cytokines than titanium alloy and zirconium alloy-based particles in vitro, in human osteoblasts, fibroblasts, and macrophages. J. Biomed. Mater. Res. Part A 2012, 100A:2147-2158.
15. Demir E., Vales G., Kaya B., Creus A., Marcos R. Genotoxic analysis of silver nanoparticles in Drosophila. Nanotoxicology 2011, 5:417-424.
16. Di Virgilio A.L., Reigosa M., Arnal P.M., de Mele M.F.L. Comparative study of the cytotoxic and genotoxic effects of titanium oxide and aluminium oxide nanoparticles in Chinese hamster ovary (CHO-K1) cells. J. Hazard. Mater. 2010, 177:711-718.
17. Frei H., Würgler F.E. Statistical methods to decide whether mutagenicity test data from Drosophila assays indicate a positive, negative, or inconclusive result. Mutat. Res. 1988, 203:297-308.
18. Ginebra M.P., Albuixech L., Fernández-Barragán E., Aparicio C., Gil F.J., San R.J., Vázquez B., Planell J.A. Mechanical performance of acrylic bone cements containing different radiopacifying agents. Biomaterials 2002, 23:1873-1882.
19. Gorth D.J., Rand D.M., Webster T.J. Silver nanoparticle toxicity in Drosophila: size does matter. Int. J. Nanomed. 2011, 6:343-350.
20. Gurr J.R., Wang A.S., Chen C.H., Jan K.Y. Ultrafine titanium dioxide particles in the absence of photoactivation can induce oxidative damage to human bronchial epithelial cells. Toxicology 2005, 213:66-73.
21. Hackenberg S., Friehs G., Froelich K., Ginzkey C., Koehler C., Scherzed A., Burghartz M., Hagen R., Kleinsasser N. Intracellular distribution, geno- and cytotoxic effects of nanosized titanium dioxide particles in the anatase crystal phase on human nasal mucosa cells. Toxicol. Lett. 2010, 195:9-14.
22. Holland P.W. More genes in vertebrates?. J. Struct. Funct. Genom. 2003, 3(1-4):75-84.
23. Kasai Y., Cagan R. Drosophila as a tool for personalized medicine: a primer. Per. Med. 2010, 7:621-632.
24. Kastenbaum M.A., Bowman K.O. Tables for determining the statistical significance of mutation frequencies. Mutat. Res. 1970, 9:527-549.
25. Kaun K.R., Devineni R.V., Heberlein U. Drosophila melanogaster as a model to study drug addiction. Hum. Genet. 2012, 131:959-975.
26. Kennedy S.R., Loeb L.A., Herr A.J. Somatic mutations in aging, cancer and neurodegeneration. Mech. Ageing Dev. 2012, 133:118-126.
27. Kounatidis I., Ligoxygakis P. Drosophila as a model system to unravel the layers of innate immunity to infection. Open Biol. 2012, 2:120075.
28. Landsiedel R., Kapp M.D., Schulz M., Wiench K., Oesch F. Genotoxicity investigations on nanomaterials: methods, preparation and characterization of test material, potential artifacts and limitations-many questions, some answers. Mutat. Res. 2009, 681:241-258.
29. Lankoff A., Banasik A., Duma A., Ochniak E., Lisowska H., Kuszewski T., Góźdź S., Wojcik A. A comet assay study reveals that aluminium induces DNA damage and inhibits the repair of radiation-induced lesions in human peripheral blood lymphocytes. Toxicol. Lett. 2006, 161:27-36.
30. Lima P.D.L., Leite D.S., Vasconcellos M.C., Cavalcanti B.C., Santos R.A., Costa-Lotufo L.V., Pessoa C., Moraes M.O., Burbano R.R. Genotoxic effect of aluminium chloride in cultured human lymphocytes treated in different phases of cells cycle. Food Chem. Toxicol. 2007, 45:1154-1159.
31. Lindsley D.L., Zimm G.G. The Genome of Drosophila melanogaster 1992, Academic Press, San Diego, CA.
32. Linnainmaa K., Kiveipensa P., Vainio H. Toxicity and cytogenetic studies of ultrafine titanium dioxide in cultured rat liver epithelial cells. Toxicol. In Vitro 1997, 11:329-335.
33. Long T.C., Saleh N., Tilton R.D., Lowry G.V., Veronesi B. Titanium dioxide (P25) produces reactive oxygen species in immortalized brain microglia (BV2): implications for nanoparticle neurotoxicity. Environ. Sci. Technol. 2006, 40:4346-4352.
34. Mitchell W., Bridget M.J., Stone M.H., Fisher J., Ingham E. Comparison of the response of human peripheral blood mononuclear cells to challenge with particles of three bone cements in vitro. Biomaterials 2003, 24:737-748.
35. Nakagawa Y., Wakuri S., Sakamoto K., Tanaka N. The photogenotoxicity of titanium dioxide particles. Mutat. Res. 1997, 394:125-132.
36. 2 and Ag nanoparticles on reproduction and development of Drosophila melanogaster and CD-1 mice. Toxicol. Appl. Pharmacol. 2011, 257:429-436.
37. Pompa P.P., Vecchio G., Galeone A., Brunetti V., Sabella S., Maiorano G., Falqui A., Bertoni G., Cingolani R. In vivo toxicity assessment of gold nanoparticles in Drosophila melanogaster. Nano Res. 2011, 4:405-413.
38. Posgai R., Cipolla-McCulloch C.B., Murphy K.R., Hussain S.M., Rowe J.J., Nielsen M.G. Differential toxicity of silver and titanium dioxide nanoparticles on Drosophila melanogaster development, reproductive effort, and viability: size, coatings and antioxidants matter. Chemosphere 2011, 85:34-42.
39. Rahman Q., Narwood J., Hatch G. Evidence that exposure of particulate air pollutants to human and rat alveolar macrophages leads to different oxidative stress. Biochem. Biophys. Res. Commun. 2002, 240:669-672.
40. 2) nanoparticle-induced cytotoxicity and oxidative DNA damage in fish cells. Mutat. Res. 2008, 640:113-122.
41. Reiter L.T., Potocki L., Chien S., Gribskov M., Bier E. A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res. 2001, 11:1114-1125.
42. Ribeiro D.A., Carlin V., Fracalossi A.C.C., Oyama L.M. Radiopacifiers do not induce genetic damage in murine fibroblasts: an in vitro study. Int. Endod. J. 2009, 42:987-991.
43. Silver Key S.C., Reaves D., Turner F., Bangn J.J. Impacts of silver nanoparticle ingestion on pigmentation and developmental progression in Drosophila. ATLAS J. Biol. 2011, 1:52-56.
44. Singh N., Manshian B., Jenkins G.J., Griffiths S.M., Williams P.M., Maffeis T.G., Wright C.J., Doak S.H. NanoGenotoxicology: the DNA damaging potential of engineered nanomaterials. Biomaterials 2009, 30:3891-3914.
45. Soto K., Garza K.M., Murr L.E. Cytotoxic effects of aggregated nanomaterials. Acta Biomater. 2007, 3:351-358.
46. Theogaraj E., Riley S., Hughes L., Maier M., Kirkland D. An investigation of the photo-clastogenic potential of ultrafine titanium dioxide particles. Mutat. Res. 2007, 634:205-219.
47. Tripathy N.K., Würgler F.E., Frei H. Genetic toxicity of six carcinogens and six non-carcinogens in the Drosophila wing spot test. Mutat. Res. 1990, 242:169-180.
48. Trouiller B., Reliene R., Westbrook A., Solaimani P., Schiesti R.H. Titanium dioxide nanoparticles induce DNA damage and genetic instability in vivo in mice. Cancer Res. 2009, 69:8784-8789.
49. Tsaousi A., Jones E., Case C.P. The in vitro genotoxicity of orthopaedic ceramic (Al2O3) and metal (CoCr alloy) particles. Mutat. Res. 2010, 697:1-9.
50. Vales G., Demir E., Kaya B., Creus A., Marcos R. Genotoxicity of cobalt nanoparticles and ions in Drosophila. Nanotoxicology 2013, 7:462-468.
51. Vecchio G., Galeone A., Brunetti V., Maiorano G., Rizzello L., Sabella S., Cingolani R., Pompa P.P. Mutagenic effects of gold nanoparticles induce aberrant phenotypes in Drosophila melanogaster. Nanomedicine 2012, 8:1-7.
52. 2 particles in cultured human lymphoblastoid cells. Mutat. Res. 2007, 628:99-106.
53. Wua Z., Dua Y., Xuea H., Wua Y., Zhoua B. Aluminum induces neurodegeneration and its toxicity arises from increased iron accumulation and reactive oxygen species (ROS) production. Neurobiol. Aging 2012, 33:199.e1-199.e12.
54. Yadav J.S., Lavanya M.P., Das P.P., Bag I., Krishnan A., Leary R., Bagchi A., Jagannadh B., Mohapatra D.K., Bhadra M.P., Bhadra U. 4-N-pyridin-2-yl-benzamide nanotubes compatible with mouse stem cell and oral delivery in Drosophila. Nanotechnology 2010, 21:155102.
55. Yadav J.S., Das P.P., Reddy T.L., Bag I., Lavanya P.M., Jagannadh B., Mohapatra D.K., Bhadra M.P., Bhadra U. Sub-cellular internalization and organ specific oral delivery of PABA nanoparticles by side chain variation. J. Nanobiotechnol. 2011, 9:10.