Cyto- and genotoxic effects of metallic nanoparticles in untransformed human fibroblast

Toxicology in Vitro

Volumn 29, Issue 7, 2015, Pages 1319-1331

  Franchi, Leonardo P ^a   Manshian, Bella B ^b   de Souza, Tiago A J ^a   Soenen, Stefaan J ^b   Matsubara, Elaine Y ^a   Rosolen, J Mauricio ^a   Takahashi, Catarina S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b DEPARTMENT OF IMAGING AND PATHOLOGY   (Belgium)

Author keywords

Cytotoxicity; Flow cytometry; Genotoxicity; Human fibroblasts; Metallic nanoparticles

Indexed keywords

GADD45ALPHA; GAMMA HISTONE H2AX; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; HISTONE H2AX; METAL NANOPARTICLE; MITOCHONDRIAL ENZYME; SILVER NANOPARTICLE; TITANIUM DIOXIDE NANOPARTICLE; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CERIC OXIDE; CERIUM; GADD45A PROTEIN, HUMAN; H2AFX PROTEIN, HUMAN; HISTONE; NUCLEAR PROTEIN; SILVER; TITANIUM; TITANIUM DIOXIDE;

ARTICLE; CELL ASSAY; CELL DEATH; CELL LEVEL; CELL MEMBRANE; CHEMICAL ANALYSIS; COMET ASSAY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; DNA FRAGMENTATION; ENDOSOME; ENZYME ACTIVITY; FIBROBLAST; GENOTOXICITY; HUMAN; HUMAN CELL; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; CELL CYCLE; CELL LINE; COMPARATIVE STUDY; DNA DAMAGE; DRUG EFFECTS; GENETICS; METABOLISM;

LONCHOCARPUS GLAUCIFOLIUS;

CELL CYCLE; CELL CYCLE PROTEINS; CELL DEATH; CELL LINE; CERIUM; COMET ASSAY; DNA DAMAGE; FIBROBLASTS; HISTONES; HUMANS; METAL NANOPARTICLES; NUCLEAR PROTEINS; SILVER; TITANIUM;

EID: 84936762247     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2015.05.010     Document Type: Article

References (60)

1. Ahamed M. Toxic response of nickel nanoparticles in human lung epithelial A549 cells. Toxicol. In Vitro 2011, 25:930-936.
2. Arora S., Jain J., Rajwade J.M., Paknikar K.M. Interactions of silver nanoparticles with primary mouse fibroblasts and liver cells. Toxicol. Appl. Pharmacol. 2009, 236:310-318.
3. 2 nanoparticles induce DNA damage towards human dermal fibroblasts in vitro. Nanotoxicology 2009, 3:161-171.
4. Botelho M.C., Costa C., Silva S., Costa S., Dhawan A., Oliveira P.A., Teixeira J.P. Effects of titanium dioxide nanoparticles in human gastric epithelial cells in vitro. Biomed. Pharmacother. 2014, 68:59-64.
5. Cedervall T., Lynch I., Lindman S., Berggard T., Thulin E., Nilsson H., Dawson K.A., Linse S. Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:2050-2055.
6. Chen T., Yan J., Li Y. Genotoxicity of titanium dioxide nanoparticles. J. Food Drug Anal. 2014, 22:95-104.
7. Cheng G., Guo W., Han L., Chen E., Kong L., Wang L., Ai W., Song N., Li H., Chen H. Cerium oxide nanoparticles induce cytotoxicity in human hepatoma SMMC-7721 cells via oxidative stress and the activation of MAPK signaling pathways. Toxicol. In Vitro 2013, 27:1082-1088.
8. Colman B.P., Espinasse B., Richardson C.J., Matson C.W., Lowry G.V., Hunt D.E., Wiesner M.R., Bernhardt E.S. Emerging contaminant or an old toxin in disguise? Silver nanoparticle impacts on ecosystems. Environ. Sci. Technol. 2014, 48:5229-5236.
9. 2 nanoparticles via p38-Nrf-2 signaling pathway in human bronchial epithelial cell, Beas-2B. Toxicol. Lett. 2009, 187:77-83.
10. Filho J.d.S., Matsubara E.Y., Franchi L.P., Martins I.P., Rivera L.M.R., Rosolen J.M., Grisolia C.K. Evaluation of carbon nanotubes network toxicity in zebrafish (Danio rerio) model. Environ. Res. 2014, 134:9-16.
11. Fleischer C.C., Payne C.K. Nanoparticle-cell interactions: molecular structure of the protein corona and cellular outcomes. Acc. Chem. Res. 2014, 47:2651-2659.
12. Flower N.A.L., Brabu B., Revathy M., Gopalakrishnan C., Raja S.V.K., Murugan S.S., Kumaravel T.S. Characterization of synthesized silver nanoparticles and assessment of its genotoxicity potentials using the alkaline comet assay. Mutat. Res./Genet. Toxicol. Environ. Mutagen. 2012, 742:61-65.
13. Foster K.A., Oster C.G., Mayer M.M., Avery M.L., Audus K.L. Characterization of the A549 cell line as a type II pulmonary epithelial cell model for drug metabolism. Exp. Cell Res. 1998, 243:359-366.
14. Franchi L.P., Santos R.A., Matsubara E.Y., de Lima J.C., Mauricio Rosolen J., Takahashi C.S. Cytotoxicity and genotoxicity of carbon nanotubes. Quim. Nova 2012, 35:571-580.
15. 2 rutile/anatase mixed phase nanoparticles on Caco-2 cells. Chem. Res. Toxicol. 2012, 25:646-655.
16. Guichard Y., Schmit J., Darne C., Gaté L., Goutet M., Rousset D., Rastoix O., Wrobel R., Witschger O., Martin A., Fierro V., Binet S. Cytotoxicity and genotoxicity of nanosized and microsized titanium dioxide and iron oxide particles in Syrian hamster embryo cells. Ann. Occup. Hyg. 2012, 56:631-644.
17. 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. Toxicol. Lett. 2011, 201:27-33.
18. 2) nanoparticles in Chinese hamster lung fibroblast cells. Toxicol. In Vitro 2013, 27:864-873.
19. Hosoya N., Miyagawa K. Targeting DNA damage response in cancer therapy. Cancer Sci. 2014, 105:370-388.
20. 2 nanoparticles toward human lung epithelial cells. Sci. Total Environ. 2011, 409:1219-1228.
21. Hussain S., Garantziotis S. Interplay between apoptotic and autophagy pathways after exposure to cerium dioxide nanoparticles in human monocytes. Autophagy 2013, 9:101-103.
22. Jugan M.-L., Barillet S., Simon-Deckers A., Herlin-Boime N., Sauvaigo S., Douki T., Carriere M. Titanium dioxide nanoparticles exhibit genotoxicity and impair DNA repair activity in A549 cells. Nanotoxicology 2012, 6:501-513.
23. 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. Mutat. Res. 2011, 726:129-135.
24. Lankoff A., Sandberg W.J., Wegierek-Ciuk A., Lisowska H., Refsnes M., Sartowska B., Schwarze P.E., Meczynska-Wielgosz S., Wojewodzka M., Kruszewski M. The effect of agglomeration state of silver and titanium dioxide nanoparticles on cellular response of HepG2, A549 and THP-1 cells. Toxicol. Lett. 2012, 208:197-213.
25. Lee Y.S., Kim D.W., Lee Y.H., Oh J.H., Yoon S., Choi M.S., Lee S.K., Kim J.W., Lee K., Song C.-W. Silver nanoparticles induce apoptosis and G2/M arrest via PKC zeta-dependent signaling in A549 lung cells. Arch. Toxicol. 2011, 85:1529-1540.
26. Lee Y.H., Cheng F.Y., Chiu H.W., Tsai J.C., Fang C.Y., Chen C.W., Wang Y.J. Cytotoxicity, oxidative stress, apoptosis and the autophagic effects of silver nanoparticles in mouse embryonic fibroblasts. Biomaterials 2014, 35:4706-4715.
27. Losert S., von Goetz N., Bekker C., Fransman W., Wijnhoven S.W., Delmaar C., Hungerbuhler K., Ulrich A. Human exposure to conventional and nanoparticle-containing sprays-a critical review. Environ. Sci. Technol. 2014, 48:5366-5378.
28. Magdolenova Z., Bilaničová D., Pojana G., Fjellsbø L.M., Hudecova A., Hasplova K., Marcomini A., Dusinska M. Impact of agglomeration and different dispersions of titanium dioxide nanoparticles on the human related in vitro cytotoxicity and genotoxicity. J. Environ. Monit. 2012, 14:455-464.
29. Mahmoudi M., Saeedi-Eslami S.N., Shokrgozar M.A., Azadmanesh K., Hassanlou M., Kalhor H.R., Burtea C., Rothen-Rutishauser B., Laurent S., Sheibani S., Vali H. Cell "vision": complementary factor of protein corona in nanotoxicology. Nanoscale 2012, 4:5461-5468.
30. Martinez D.S.T., Franchi L.P., Freria C.M., Ferreira O.P., Souza Filho A.G., Alves O.L., Takahashi C.S. Carbon Nanotubes: From Synthesis to Genotoxicity. Nanomedicine and Nanotoxicology 2014, 125-152. Springer, New York. fourteenth ed. N. Durán, S.S. Guterres, O.L. Alves, V. Zucolotto (Eds.).
31. Mittal S., Pandey A.K. Cerium oxide nanoparticles induced toxicity in human lung cells: role of ROS mediated DNA damage and apoptosis. Biomed. Res. Int. 2014, 2014:891934.
32. Ng K.W., Khoo S.P.K., Heng B.C., Setyawati M.I., Tan E.C., Zhao X., Xiong S., Fang W., Leong D.T., Loo J.S.C. The role of the tumor suppressor p53 pathway in the cellular DNA damage response to zinc oxide nanoparticles. Biomaterials 2011, 32:8218-8225.
33. Pagliari F., Mandoli C., Forte G., Magnani E., Pagliari S., Nardone G., Licoccia S., Minieri M., Di Nardo P., Traversa E. Cerium oxide nanoparticles protect cardiac progenitor cells from oxidative stress. ACS Nano 2012, 6:3767-3775.
34. Piao M.J., Kang K.A., Lee I.K., Kim H.S., Kim S., Choi J.Y., Choi J., Hyun J.W. Silver nanoparticles induce oxidative cell damage in human liver cells through inhibition of reduced glutathione and induction of mitochondria-involved apoptosis. Toxicol. Lett. 2011, 201:92-100.
35. Prasad R.Y., Wallace K., Daniel K.M., Tennant A.H., Zucker R.M., Strickland J., Dreher K., Kligerman A.D., Blackman C.F., Demarini D.M. Effect of treatment media on the agglomeration of titanium dioxide nanoparticles: impact on genotoxicity, cellular interaction, and cell cycle. ACS Nano 2013, 7:1929-1942.
36. Saska S., Scarel-Caminaga R.M., Teixeira L.N., Franchi L.P., dos Santos R.A., Minarelli Gaspar A.M., de Oliveira P.T., Rosa A.L., Takahashi C.S., Messaddeq Y., Lima Ribeiro S.J., Marchetto R. Characterization and in vitro evaluation of bacterial cellulose membranes functionalized with osteogenic growth peptide for bone tissue engineering. J. Mater. Sci.-Mater. Med. 2012, 23:2253-2266.
37. Setyawati M.I., Yuan X., Xie J., Leong D.T. The influence of lysosomal stability of silver nanomaterials on their toxicity to human cells. Biomaterials 2014, 35:6707-6715.
38. Shi J., Sun X., Lin Y., Zou X., Li Z., Liao Y., Du M., Zhang H. Endothelial cell injury and dysfunction induced by silver nanoparticles through oxidative stress via IKK/NF-κB pathways. Biomaterials 2014, 35:6657-6666.
39. Singh N., Manshian B., Jenkins G.J.S., Griffiths S.M., Williams P.M., Maffeis T.G.G., Wright C.J., Doak S.H. NanoGenotoxicology: the DNA damaging potential of engineered nanomaterials. Biomaterials 2009, 30:3891-3914.
40. Soenen S.J., Rivera-Gil P., Montenegro J.-M., Parak W.J., De Smedt S.C., Braeckmans K. Cellular toxicity of inorganic nanoparticles: common aspects and guidelines for improved nanotoxicity evaluation. Nano Today 2011, 6:446-465.
41. Soenen S.J., Demeester J., De Smedt S.C., Braeckmans K. The cytotoxic effects of polymer-coated quantum dots and restrictions for live cell applications. Biomaterials 2012, 33:4882-4888.
42. Soenen S.J., Demeester J., De Smedt S.C., Braeckmans K. Turning a frown upside down: exploiting nanoparticle toxicity for anticancer therapy. Nano Today 2013, 8:121-125.
43. Sur I., Altunbek M., Kahraman M., Culha M. The influence of the surface chemistry of silver nanoparticles on cell death. Nanotechnology 2012, 23:375102.
44. Svenson S. Theranostics: are we there yet?. Mol. Pharm. 2013, 10:848-856.
45. Tanaka T., Huang X., Halicka H.D., Zhao H., Traganos F., Albino A.P., Dai W., Darzynkiewicz Z. Cytometry of ATM activation and histone H2AX phosphorylation to estimate extent of DNA damage induced by exogenous agents. Cytometry Part A 2007, 71A:648-661.
46. Terreno E., Uggeri F., Aime S. Image guided therapy: the advent of theranostic agents. J. Control. Release 2012, 161:328-337.
47. Tice R.R., Agurell E., Anderson D., Burlinson B., Hartmann A., Kobayashi H., Miyamae Y., Rojas E., Ryu J.C., Sasaki Y.F. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ. Mol. Mutagen. 2000, 35:206-221.
48. Toduka Y., Toyooka T., Ibuki Y. Flow cytometric evaluation of nanoparticles using side-scattered light and reactive oxygen species-mediated fluorescence-correlation with genotoxicity. Environ. Sci. Technol. 2012, 46:7629-7636.
49. Valdiglesias V., Costa C., Sharma V., Kiliç G., Pásaro E., Teixeira J.P., Dhawan A., Laffon B. Comparative study on effects of two different types of titanium dioxide nanoparticles on human neuronal cells. Food Chem. Toxicol. 2013, 57:352-361.
50. Valodkar M., Jadeja R.N., Thounaojam M.C., Devkar R.V., Thakore S. In vitro toxicity study of plant latex capped silver nanoparticles in human lung carcinoma cells. Mater. Sci. Eng., C 2011, 31:1723-1728.
51. Vinoth K.J., Heng B.C., Poonepalli A., Banerjee B., Balakrishnan L., Lu K., Hande M.P., Cao T. Human embryonic stem cells may display higher resistance to genotoxic stress as compared to primary explanted somatic cells. Stem Cells Dev. 2008, 17:599-607.
52. Vranic S., Boggetto N., Contremoulins V., Mornet S., Reinhardt N., Marano F., Baeza-Squiban A., Boland S. Deciphering the mechanisms of cellular uptake of engineered nanoparticles by accurate evaluation of internalization using imaging flow cytometry. Particle Fibre Toxicol. 2013, 17:10.
53. Walkey C.D., Olsen J.B., Song F., Liu R., Guo H., Olsen D.W.H., Cohen Y., Emili A., Chan W.C.W. Protein corona fingerprinting predicts the cellular interaction of gold and silver nanoparticles. ACS Nano 2014, 8:2439-2455.
54. Wason M.S., Colon J., Das S., Seal S., Turkson J., Zhao J., Baker C.H. Sensitization of pancreatic cancer cells to radiation by cerium oxide nanoparticle-induced ROS production. Nanomed.: Nanotechnol., Biol. Med. 2013, 9:558-569.
55. Woodruff R.S., Li Y., Yan J., Bishop M., Jones M.Y., Watanabe F., Biris A.S., Rice P., Zhou T., Chen T. Genotoxicity evaluation of titanium dioxide nanoparticles using the Ames test and Comet assay. J. Appl. Toxicol. 2012.
56. Wu J., Sun J., Xue Y. Involvement of JNK and P53 activation in G2/M cell cycle arrest and apoptosis induced by titanium dioxide nanoparticles in neuron cells. Toxicol. Lett. 2010, 199:269-276.
57. Xia T., Rome L., Nel A. Nanobiology: particles slip cell security. Nat. Mater. 2008, 7:519-520.
58. Xiu Z.-M., Zhang Q.-B., Puppala H.L., Colvin V.L., Alvarez P.J.J. Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett. 2012, 12:4271-4275.
59. Xu C., Qu X. Cerium oxide nanoparticle: a remarkably versatile rare earth nanomaterial for biological applications. NPG Asia Mater. 2014, 6.
60. 2 nanoparticles in cells by flow cytometry. Cytometry Part A 2010, 77A.