Negligible particle-specific toxicity mechanism of silver nanoparticles: The role of Ag+ ion release in the cytosol

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 11, Issue 3, 2015, Pages 731-739

  De Matteis, Valeria ^a   Malvindi, Maria Ada ^a   Galeone, Antonio ^a   Brunetti, Virgilio ^a   De Luca, Elisa ^a   Kote, Sachin ^a   Kshirsagar, Prakash ^a   Sabella, Stefania ^a   Bardi, Giuseppe ^a   Pompa, Pier Paolo ^a  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

Ion release; Nanoparticles; Silver; Toxicity

Indexed keywords

CELL CULTURE; CELL DEATH; CELLS; CHELATION; CYTOLOGY; IONS; NANOCONJUGATES; NANOPARTICLES; TOXICITY;

CELL CULTURE MEDIUMS; FLUORESCENT PROBES; ION RELEASE; NANOPARTICLE INTERNALIZATIONS; REGULATORY GUIDELINES; SILVER NANOPARTICLES; SILVER NANOPARTICLES (AGNPS); TOXICITY MECHANISMS;

SILVER;

CHELATING AGENT; FLUORESCENT DYE; METALLOTHIONEIN; SILVER; SILVER NANOPARTICLE; METAL NANOPARTICLE; MONOVALENT CATION;

A549 CELL LINE; ARTICLE; CELL CYCLE; CELL DAMAGE; CELL DEATH; CONTROLLED STUDY; CULTURE MEDIUM; CYTOSOL; CYTOTOXICITY; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; INTERNALIZATION; LYSOSOME; MITOCHONDRIAL MEMBRANE POTENTIAL; TOXICITY; CHEMISTRY; METABOLISM;

CATIONS, MONOVALENT; CYTOSOL; HELA CELLS; HUMANS; LYSOSOMES; METAL NANOPARTICLES; SILVER;

EID: 84933517942     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2014.11.002     Document Type: Article

References (63)

1. Wang A., Marinakos S.M., Badireddy A.R., Powers C.M., Houck K. Characterization of physicochemical properties of nanomaterials and their immediate environments in high-throughput screening of nanomaterial biological activity. Wires Nanomed Nanobiotechnol 2013, 5:430-448.
2. Chen X., Schluesener H.J. Nanosilver: a nanoproduct in medical application. Toxicol Lett 2008, 176:1-12.
3. Rizzello L., Pompa P.P. Nanosilver-based antibacterial drugs and devices: mechanisms, methodological drawbacks, and guidelines. Chem Soc Rev 2014, 43:1501-1518.
4. Chaudhry Q., Scotter M., Blackburn J., Ross B., Boxall A., Castle L., et al. Applications and implications of nanotechnologies for the food sector. Food Addit Contam Part A 2008, 25:241-258.
5. Ahamed M., AlSalhi M.S., Siddiqui M.K.J. Silver nanoparticle applications and human health. Clin Chim Acta 2010, 411:1841-1848.
6. Benn T.M., Westerhoff P. Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 2008, 42:4133-4139.
7. Fan M., Thompson M., Andrade M.L., Brolo A.G. Silver nanoparticles on a plastic platform for localized surface plasmon resonance biosensing. Anal Chem 2010, 82:6350-6352.
8. Zhang Z.L., Zhang X.Y., Xin Z.Q., Deng M.M., Wen Y.Q., Song Y.L. Synthesis of monodisperse silver nanoparticles for ink-jet printed flexible electronics. Nanotechnology 2011, 22. 10.1088/0957-4484/22/42/425601.
9. Son Y., Yeo J., Moon H., Lim T.W., Hong S., Nam K.H., et al. Nanoscale electronics: digital fabrication by direct femtosecond laser processing of metal nanoparticles. Adv Mater 2011, 23:3176-3181.
10. Kim T.H., Kim M., Park H.S., Shin U.S., Gong M.S., Kim H.W. Size-dependent cellular toxicity of silver nanoparticles. J Biomed Mater Res A 2012, 100A:1033-1043.
11. Lim D.H., Jang J., Kim S., Kang T., Lee K., Choi I.H. The effects of sub-lethal concentrations of silver nanoparticles on inflammatory and stress genes in human macrophages using cDNA microarray analysis. Biomaterials 2012, 33:4690-4699.
12. Haase A., Rott S., Mantion A., Graf P., Plendl J., Thunemann A.F., et al. Effects of silver nanoparticles on primary mixed neural cell cultures: uptake, oxidative stress and acute calcium responses. Toxicol Sci 2012, 126:457-468.
13. Greulich C., Diendorf J., Simon T., Eggeler G., Epple M., Koller M. Uptake and intracellular distribution of silver nanoparticles in human mesenchymal stem cells. Acta Biomater 2011, 7:347-354.
14. Van der Zande M., Vandebriel R.J., Van Doren E., Kramer E., Rivera Z.H., Serrano-Rojero C.S., et al. Distribution, elimination, and toxicity of silver nanoparticles and silver ions in rats after 28-day oral exposure. ACS Nano 2012, 6:7427-7442.
15. Rahman M.F., Wang J., Patterson T.A., Saini U.T., Robinson B.L., Newport G.D., et al. Expression of genes related to oxidative stress in the mouse brain after exposure to silver-25 nanoparticles. Toxicol Lett 2009, 187:15-21.
16. Lim D., Roh J.Y., Eom H.J., Choi J.Y., Hyun J., Choi J. Oxidative stress-related PMK-1 P38 MAPK activation as a mechanism for toxicity of silver nanoparticles to reproduction in the nematode Caenorhabditis elegans. Environ Toxicol Chem 2012, 31:585-592.
17. Roh J.Y., Sim S.J., Yi J., Park K., Chung K.H., Ryu D.Y., et al. Ecotoxicity of silver nanoparticles on the soil nematode Caenorhabditis elegans using functional ecotoxicogenomics. Environ Sci Technol 2009, 43:3933-3940.
18. Choi J.E., Kim S., Ahn J.H., Youn P., Kang J.S., Park K., et al. Induction of oxidative stress and apoptosis by silver nanoparticles in the liver of adult zebrafish. Aquat Toxicol 2010, 100:151-159.
19. Bilberg K., Malte H., Wang T., Baatrup E. Silver nanoparticles and silver nitrate cause respiratory stress in Eurasian perch (Perca fluviatilis). Aquat Toxicol 2010, 96:159-165.
20. Panacek A., Prucek R., Safarova D., Dittrich M., Richtrova J., Benickova K., et al. Acute and chronic toxicity effects of silver nanoparticles (NPs) on Drosophila melanogaster. Environ Sci Technol 2011, 45:4974-4979.
21. Hansen S.F., Baun A. When enough is enough. Nat Nanotechnol 2012, 7:409-411.
22. Yen H.J., Hsu S.H., Tsai C.L. Cytotoxicity and immunological response of gold and silver nanoparticles of different sizes. Small 2009, 5:1553-1561.
23. Sur I., Altunbek M., Kahraman M., Culha M. The influence of the surface chemistry of silver nanoparticles on cell death. Nanotechnology 2012, 23. 10.1088/0957-4484/23/37/375102.
24. Wijnhoven S.W.P., Peijnenburg W.J.G.M., Herberts C.A., Hagens W.I., Oomen A.G., Heugens E.H.W., et al. Nano-silver-a review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology 2009, 3:109-138.
25. Kim S., Choi J.E., Choi J., Chung K.H., Park K., Yi J., et al. Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol in Vitro 2009, 23:1076-1084.
26. Kawata K., Osawa M., Okabe S. In vitro toxicity of silver nanoparticles at noncytotoxic doses to HepG2 human hepatoma cells. Environ Sci Technol 2009, 43:6046-6051.
27. Park E.J., Yi J., Kim Y., Choi K., Park K. Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol in Vitro 2010, 24:872-878.
28. Dadosh T. Synthesis of uniform silver nanoparticles with a controllable size. Mater Lett 2009, 63:2236-2238.
29. Malvindi M.A., Brunetti V., Vecchio G., Galeone A., Cingolani R., Pompa P.P. SiO2 nanoparticles biocompatibility and their potential for gene delivery and silencing. Nanoscale 2012, 4:486-495.
30. Brunetti V., Chibli H., Fiammengo R., Galeone A., Malvindi M.A., Vecchio G., et al. InP/ZnS as a safer alternative to CdSe/ZnS core/shell quantum dots: in vitro and in vivo toxicity assessment. Nanoscale 2013, 5:307-317.
31. Maiorano G., Sabella S., Sorce B., Brunetti V., Malvindi M.A., Cingolani R., et al. Effects of cell culture media on the dynamic formation of protein-nanoparticle complexes and influence on the cellular response. ACS Nano 2010, 4:7481-7491.
32. Malvindi M.A., De Matteis V., Galeone A., Brunetti V., Anyfantis G.C., Athanassiou A., et al. Toxicity assessment of silica coated iron oxide nanoparticles and biocompatibility improvement by surface engineering. PLoS One 2014, 9. 10.1371/journal.pone.0085835.
33. Hsin Y.H., Chena 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. Toxicol Lett 2008, 179:130-139.
34. Teodoro J.S., Simoes A.M., Duarte F.V., Rolo A.P., Murdoch R.C., Hussain S.M., et al. Assessment of the toxicity of silver nanoparticles in vitro: a mitochondrial perspective. Toxicol in Vitro 2011, 25:664-670.
35. Hackenberg S., Scherzed A., Kessler M., Hummel S., Technau A., Froelich K., et al. Silver nanoparticles: evaluation of DNA damage, toxicity and functional impairment in human mesenchymal stem cells. Toxicol Lett 2011, 201:27-33.
36. Eom H.J., Choi J. p38 MAPK activation, DNA damage, cell cycle arrest and apoptosis as mechanisms of toxicity of silver nanoparticles in Jurkat T cells. Environ Sci Technol 2010, 44:8337-8342.
37. Pellegata N.S., Antoniono R.J., Redpath J.L., Stanbridge E.J. DNA damage and p53-mediated cell cycle arrest: a reevaluation. Proc Natl Acad Sci U S A 1996, 93:15209-15214.
38. Boonstra J., Post J.A. Molecular events associated with reactive oxygen species and cell cycle progression in mammalian cells. Gene 2004, 337:1-13.
39. AshaRani P.V., Mun G.L.K., Hande M.P., Valiyaveettil S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 2009, 3:279-290.
40. Porter A.G., Janicke R.U. Emerging roles of caspase-3 in apoptosis. Cell Death Differ 1999, 6:99-104.
41. Nicholson D.W., Ali A., Thornberry N.A., Vaillancourt J.P., Ding C.K., Gallant M., et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995, 376:37-43.
42. Hu M.M., Fan J.L., Cao J.F., Song K.D., Zhang H., Sun S.G., et al. Enhanced fluorescent chemosensor for Ag+ in absolute aqueous solution and living cells: an experimental and theoretical study. Analyst 2012, 137:2107-2111.
43. Reidy B., Haase A., Luch A., Dawson K.A., Lynch I. Mechanisms of silver nanoparticle release, transformation and toxicity: a critical review of current knowledge and recommendations for future studies and applications. Materials 2013, 6:2295-2350.
44. Beer C., Foldbjerg R., Hayashi Y., Sutherland D.S., Autrup H. Toxicity of silver nanoparticles-nanoparticle or silver ion?. Toxicol Lett 2012, 208:286-292.
45. Kone B.C., Kaleta M., Gullans S.R. Silver ion (Ag+)-induced increases in cell membrane K+ and Na+ permeability in the renal proximal tubule: reversal by thiol reagents. J Membr Biol 1988, 102:11-19.
46. Sigel A., Sigel H., Sigel R.K.O. Metallothioneins and related chelators. Metal ions in life sciences 2009, vol. 5:44. Royal Society of Chemistry, Cambridge, England.
47. Nordberg M., Nordberg G.F. Metallothioneins: historical development and overview. Metal ions in life sciences 2009, 5:1-29. Royal Society of Chemistry, Cambridge, England.
48. Luther E.M., Schmidt M.M., Diendorf J., Epple M., Dringen R. Upregulation of metallothioneins after exposure of cultured primary astrocytes to silver nanoparticles. Neurochem Res 2012, 37:1639-1648.
49. Park E.J., Bae E., Yi J., Kim Y., Choi K., Lee S.H., et al. Repeated-dose toxicity and inflammatory responses in mice by oral administration of silver nanoparticles. Environ Toxicol Pharmacol 2010, 30:162-168.
50. Vecchio G., Fenech M., Pompa P.P., Voelcker N.H. Lab-on-a-chip-based high-throughput screening of the genotoxicity of engineered nanomaterials. Small 2014, 10:2721-2734. 10.1002/smll.201303359.
51. Kim S., Ryu D.Y. Silver nanoparticle-induced oxidative stress, genotoxicity and apoptosis in cultured cells and animal tissues. J Appl Toxicol 2013, 33:78-89.
52. Franco R., Sanchez-Olea R., Reyes-Reyes E.M., Panayiotidis M.I. Environmental toxicity, oxidative stress and apoptosis: menage a trois. Mutat Res 2009, 674:3-22.
53. Carlson C., Hussain S.M., Schrand A.M., Braydich-Stolle L.K., Hess K.L., Jones R.L., et al. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B 2008, 112:13608-13619.
54. Ahamed M., Karns M., Goodson M., Rowe J., Hussain S.M., Schlager J.J., et al. DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicol Appl Pharmacol 2008, 233:404-410.
55. Piao M.J., Kang K.A., Lee I.K., Kim H.S., Kim S., Choi J.Y., et al. 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.
56. Ostermeyer A.K., Mumuper C.K., Semprini L., Radniecki T. Influence of bovine serum albumin and alginate on silver nanoparticle dissolution and toxicity to Nitrosomonas europaea. Environ Sci Technol 2013, 47:14403-14410.
57. Liu J.Y., Sonshine D.A., Shervani S., Hurt R.H. Controlled release of biologically active silver from nanosilver surfaces. ACS Nano 2010, 4:6903-6913.
58. Pratsinis A., Hervella P., Leroux J.C., Pratsinis S.E., Sotiriou G.A. Toxicity of silver nanoparticles in macrophages. Small 2013, 9:2576-2584.
59. Loza K., Diendorf J., Sengstock C., Ruiz-Gonzalez L., Gonzalez-Calbet J.M., Vallet-Regi M., Köller M., Epple M. The dissolution and biological effects of silver nanoparticles in biological media. J Mater Chem B 2014, 2:1634-1643.
60. Zhang W., Yao Y., Sullivan N., Chen Y. Modeling the primary size effects of citrate-coated silver nanoparticles on their ion release kinetics. Environ Sci Technol 2011, 45:4422-4428.
61. Liu J., Hurt R.H. Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ Sci Technol 2010, 44:2169-2175.
62. Gliga A.R., Skoglund S., Wallinder I.O., Fadeel B., Karlsson H.L. Size-dependent cytotoxicity of silver nanoparticles in human lung cells: the role of cellular uptake, agglomeration and Ag release. Part Fibre Toxicol 2014, 11:11.
63. Bondarenko O., Ivask A., Käkinen A., Kurvet I., Kahru A. Particle-cell contact enhances antibacterial activity of silver nanoparticles. PLoS One 2013, 8(5):e64060.