Cellular uptake and toxicity effects of silver nanoparticles in mammalian kidney cells

Journal of Applied Toxicology

Volumn 35, Issue 6, 2015, Pages 581-592

  Milić, Mirta ^a   Leitinger, Gerd ^b   Pavičić, Ivan ^a   Zebić Avdičević, Maja ^c   Dobrović, Slaven ^c   Goessler, Walter ^d   Vinković Vrček, Ivana ^a  

^a INSTITUTE FOR MEDICAL RESEARCH AND OCCUPATIONAL HEALTH   (Croatia)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

^c UNIVERSITY OF ZAGREB   (Croatia)

^d UNIVERSITY OF GRAZ   (Austria)

Author keywords

Absorption; Cytotoxicity; Genotoxicity; Pk15 cells; Silver nanoparticles

Indexed keywords

NANOMATERIAL; SILVER NANOPARTICLE; METAL NANOPARTICLE; SILVER DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL VIABILITY; COMET ASSAY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY TEST; ENDOCYTOSIS; GENOTOXICITY; IN VITRO STUDY; INTERNALIZATION; KIDNEY CELL; MAMMAL CELL; NONHUMAN; PIG; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CELL LINE; CELL SURVIVAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; KIDNEY;

MAMMALIA; SUS;

ANIMALS; CELL LINE; CELL SURVIVAL; COMET ASSAY; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; IN VITRO TECHNIQUES; KIDNEY; METAL NANOPARTICLES; MICROSCOPY, ELECTRON, TRANSMISSION; SILVER COMPOUNDS; SWINE;

EID: 84928171592     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.3081     Document Type: Article

References (53)

1. AshaRani PV, Kah Mun GL, Prakash Hande M, Valiyaveettil S. 2009. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3: 279-290.
2. Auffan MV, Rose J, Wiesner MR, Bottero J-Y. 2009. Chemical stability of metallic nanoparticles: a parameter controlling their potential cellular toxicity in vitro. Environ. Pollut. 157: 1127-1133.
3. Behra R, Sigg L, Clift MJD, Herzog F, Minghetti M, Johnston B, Petri-Fink A, Rothen-Rutishauser B. 2013. Bioavailability of silver nanoparticles and ions: from a chemical and biochemical perspective. J. R. Soc. Interface 10: 20130396. DOI: 10.1098/rsif.2013.0396.
4. Benn TM, Westerhoff P. 2008. Nanoparticle silver released into water from commercially available sock fabrics. Environ. Sci. Technol. 42: 4133-4139.
5. Brandenberger C, Mühlfeld C, Ali Z, Lenz A-G, Scmid O, Parak WJ, Gehr P, Rothen-Rutishauser B. 2010. Quantitative evaluation of cellular uptake and trafficking of plain and polyethylene glycol-coated gold nanoparticles. Small 6: 1669-1678.
6. + channel. Am. J. Physiol. Regul. Integr. Comp. Physiol. 277: R1385-R1391.
7. Cañamares MV, Garcia-Ramos JV, Sanchez-Cortes S, Castillejo M, Oujja M. 2008. Comparative SERS effectiveness of silver nanoparticles prepared by different methods: A study of the enhancement factor and the interfacial properties. J. Colloid Interface Sci. 326: 103-109.
8. Castellini C, Ruggeri S, Mattioli S, Bernardini G, Macchioni L, Moretti E, Collodel G. 2014. Long-term effects of silver nanoparticles on reproductive activity of rabbit buck. Syst. Biol. Reprod. Med. 60: 143-150.
9. Chithrani BD, Ghazani AA, Chan WC. 2006. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 6: 662-668.
10. Chithrani BD, Chan WCW. 2007. Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett. 7: 1542-1550.
11. Choi O, Clevenger TE, Deng B, Surampalli RY, Ross JL, Hu Z. 2009. Role of sulphide and ligand strength in controlling nanosilver toxicity. Water Res. 43: 1879-1886.
12. Christian P, Von der Kammer F, Baalousha M, Hofmann T. 2008. Nanoparticles: preparation properties and behavior in environmental media. Ecotoxicology 17: 326-343.
13. Cohen MS, Stern JM, Vanni AJ, Kelley RS, Baumgart E, Field D, Libertino JA, Summerhayes IC. 2007. In vitro analysis of a nanocrystalline silver-coated surgical mesh. Surg. Infect. (Larchmt.) 8: 397-404.
14. Collins AR, Dobson VL, Dusinska M, Kennedy G, Stetina R. 1997. The comet assay: what can it really tell us? Mutat. Res. 375: 183-193.
15. Cronholm P, Karlsson HL, Hedberg J, Lowe TA, Winnberg L, Elihn K, Wallinder IO, Moller L. 2013. Intracellular uptake and toxicity of Ag and CuO nanoparticles: a comparison between nanoparticles and their corresponding metal ions. Small 9: 970-982.
16. De Lima R, Seabra AB, Durán N. 2012. Silver nanoparticles: a brief review of cytotoxicity and genotoxicity of chemically and biogenically synthesized nanoparticles. J. Appl. Toxicol. 32: 867-869.
17. Dziendzikowska K, Gromadzka-Ostowska J, Lankoff A, Oczkowski M, Krawczyńska A, Chwastowska J, Sadowska-Bratek M, Chajduk E, Wojewódzka M, Dušinská M, Kruszewski M. 2012. Time-dependent biodistribution and excretion of silver nanoparticles in male Wistar rats. J. Appl. Toxicol. 32: 920-928.
18. Farkas J, Christian P, Gallego-Urrea JA, Roos N, Hassellov M, Tollefsen KE, Thomas KV. 2011. Uptake and effects of manufactured X nanoparticles in rainbow trout (Oncorhynchus mykiss) gill cells RID F-3693-2010. Aquat. Toxicol. 101: 117-125.
19. Fraga S, Faria H, Soares ME, Duarte JA, Soares L, Pereira E, Costa-Pereira C, Teixeira JP, De Lourdes Bastos M, Carmo H. 2013. Influence of the surface coating on the cytotoxicity, genotoxicity and uptake of gold nanoparticles in human HepG2 cells. J. Appl. Toxicol. 33: 1111-1119.
20. Gao H, Shi W, Freund LB. 2005. Mechanics of receptor-mediated endocytosis. Proc. Natl. Acad. Sci. U. S. A. 102: 9469-9474.
21. Hinderliter PM, Minard KR, Orr G, Chrisler WB, Thrall BD, Pounds JG, Teeguarden JG. 2010. ISDD: A computational model of particle sedimentation, diffusion and target cell dosimetry for in vitro toxicity studies. Part. Fibre Toxicol. 7: 36.
22. Holder AL, Goth-Goldstein R, Lucas D, Koshland CP. 2012. Particle-induced artifacts in the MTT and LDH viability assays. Chem. Res. Toxicol. 25: 1885-1892.
23. Kassie F, Parzefall W, Knasmuller S. 2000. Single cell gel electrophoresis assay: a new technique for human biomonitoring studies. Mutat. Res. 463: 13-31.
24. Kim YJ, Yang SI, Ryu JC. 2010. Cytotoxicity and genotoxicity of nano-silver in mammalian cell lines. Mol. Cell. Toxicol. 6: 119-125.
25. Kim YS, Kim JS, Cho HS, Rha DS, Kim JM, Park JD, Choi BS, Lim R, Chang HK, Chung YH, Kwon IH, Jeong J, Han BS, Yu IJ. 2008. Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Sprague-Dawley rats. Inhal. Toxicol. 20: 575-583.
26. Kumar C. 2006. Nanomaterials-Toxicity, Health and Environmental Issues. Wiley-VCH Verlag GmbH & Co.: Weinheim.
27. Lee HY, Park HK, Lee YM, Kim K, Park SB. 2007. A practical procedure for producing silver nanocoated fabric and its antibacterial evaluation for biomedical applications. Chem. Commun. (Cambridge, UK) 28: 2959-2961.
28. Lee PC, Meisel D. 1982. Adsorption and surface-enhanced Raman of dyes on silver and gold sols. J. Phys. Chem. 86: 3391-3395.
29. Lee J, Peña MM, Nose Y, Thiele DJ. 2002. Biochemical characterization of the human copper transporter Ctr1. J. Biol. Chem. 277: 4380-4387.
30. Leitinger G, Pabst MA, Kral K. 2000. Gold toning preserves integrity of silver enhanced immunogold particles during osmium tetroxide treatment for demonstration of a biogenic amine. Brain Res. Protocol. 5: 30-38.
31. Liu JY, Hurt RH. 2010. Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ. Sci. Technol. 44: 2169-2175.
32. Liu W, Wu Y, Wang C, Li HC, Wang T, Liao CY, Cui L, Zhou QF, Yan B, Jiang GB. 2010. Impact of silver nanoparticles on human cells: effect of particle size. Nanotoxicology 4: 319-330.
33. Lok CN, Ho CM, Chen R, He QY, Yu WY, Sun H, Tam PKH, Chiu JF, Che CM. 2007. Silver nanoparticles: Partial oxidation and antibacterial activities. J. Biol. Inorg. Chem. 12: 527-534.
34. McShan D, Ray PC, Yu H. 2014. Molecular toxicity mechanism of nanosilver. J. Food Drug Anal. 22: 116-127.
35. Mosmann J. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65: 55-63.
36. Nanotechnology Consumer Product Inventory Wesbsite. 2007. Woodraw Wilson International Center for Scholars http://www.nanotechproject.org/inventories/consumer/ [10 May 2014].
37. Powers CM, Badireddy AR, Ryde IT, Seidler FJ, Slotkins TA. 2011. Silver nanoparticles compromise neurodevelopment in PC12 cells: Critical contributions of silver ion, particle size, coating and composition. Environ. Health Perspect. 119: 37-44.
38. Pritz CO, Bitsche M, Salvenmoser W, Dudás J, Scrrott-Fischer A, Glueckert R. 2013. Endocytic trafficking of silica nanoparticles in a cell line derived from the organ of Corti. Nanomedicine 8: 239-252.
39. Rabolli V, Thomassen LC, Uwambayinema F, Martens JA, Lison D. 2011. The cytotoxic activity of amorphous silica nanoparticles is mainly influenced by surface area and not by aggregation. Toxicol. Lett. 206: 197-203.
40. Sahu SC, Zheng J, Graham L, Chen L, Ihrie J, Yourick JJ, Sprando RL. 2014. Comparative cytotoxicity of nanosilver in human liver HepG2 and collon Caco2 cells in culture. J. Appl. Toxicol. DOI: 10.1002/jat.2994.
41. Salmaso S, Caliceti P, Amendola V, Meneghetti M, Magnusson JP, Pasparakis G, Alexander C. 2009. Cell up-take control of gold nanoparticles functionalized with a thermoresponsive polymer. J. Mater. Chem. 19: 1608-1615.
42. Schoonen MAA, Cohn CA, Roemer E, Laffers R, Simon SR, O'Riordan T. 2006. Mineral-induced formation of reactive oxygen species. Rev. Mineral. Geochem. 64: 179-221.
43. Singh NP, Mc Coy MT, Tice RR, Schneider LL. 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 175: 184-191.
44. Suliman YAO, Ali D, Alarifi S, Harrath AH, Mansour L, Alwasel SH. 2013. Evaluation of cytotoxic, oxidative stress, proinflammatory and genotoxic effect of silver nanoparticles in human lung epithelial cells. Environ. Toxicol. 28. DOI: 10.1002/tox.21880.
45. Tice RR, Agurell E, Anderson D, Burlinson B, Hartmenn A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF. 2000. Single cell gel / comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ. Mol. Mutagen. 35: 206-221.
46. Trop M, Novak M, Rodl S, Hellbom B, Kroell W, Goessler W. 2006. Silver-coated dressing acticoat caused raised liver enzymes and argyria-like symptoms in burn patient. J. Trauma: Inj., Infect., Crit. Care 60: 648-652.
47. Verma A, Stellacci F. 2010. Effect of surface properties on nanoparticle-cell interactions. Small 6: 12-21.
48. Vigneshwaran N, Kathe AA, Varadarajan PV, Nachane RP, Balasubramanya RH. 2007. Functional finishing of cotton fabrics using silver nanoparticles. J. Nanosci. Nanotechnol. 7: 1893-1897.
49. Walker M, Parsons D. 2012. The biological fate of silver ions following the use of silver-containing wound care products - a review. Int. Wound J.. DOI: 10.1111/j.1742-481X.2012.01115.x.
50. Wang Z, Li N, Zhao J, White JC, Qu P, Xing B. 2012. CuO nanoparticle interaction with human epithelial cells: cellular uptake, location, export, and genotoxicity. Chem. Res. Toxicol. 25: 1512-1521.
51. Yang H, Liu C, Yang D, Zhang H, Xi ZJ. 2009. Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterials: the role of particle size, shape and composition. Appl. Toxicol. 29: 69-78.
52. Yu SJ., Chao JB, Sun J, Yin YG, Liu JF, Jiang GB. 2013. Quantification of the uptake of silver nanoparticles and ions to HepG2 cells. Environ. Sci. Technol. 47: 3268-3274.
53. Zhang Y, Sun J. 2007. A Study on the bio-safety for nano-silver as anti-bacterial materials. Chin. J. Med. Instrum. 31: 35-38.