The influence of Citrate or PEG coating on silver nanoparticle toxicity to a human keratinocyte cell line

Toxicology Letters

Volumn 249, Issue , 2016, Pages 29-41

  Bastos, V ^a   Ferreira de Oliveira, J M P ^a   Brown, D ^b   Jonhston, H ^b   Malheiro, E ^c   Daniel da Silva, A L ^c   Duarte, I F ^c   Santos, C ^a,d   Oliveira, H ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b HERIOT WATT UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF AVEIRO   (Portugal)

^d UNIVERSITY OF PORTO   (Portugal)

Author keywords

Apoptosis; Cell cycle; Citrate coating; Cytokines; Nanotoxicology; PEG coating; ROS; Silver nanoparticles

Indexed keywords

CASPASE 3; CITRIC ACID; CYCLIN B1; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROGOL; MONOCYTE CHEMOTACTIC PROTEIN 1; NANOCOATING; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; SILVER NANOPARTICLE; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; LIPOCORTIN 5; MACROGOL DERIVATIVE; METAL NANOPARTICLE; SILVER;

APOPTOSIS; ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE REGULATION; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOMETRY; CYTOTOXICITY; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IN VITRO STUDY; KERATINOCYTE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; S PHASE CELL CYCLE CHECKPOINT; CELL CULTURE; CELL CYCLE; CELL SURVIVAL; DRUG EFFECTS; FLOW CYTOMETRY; METABOLISM; SECRETION (PROCESS);

ANNEXIN A5; CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CITRIC ACID; CYTOKINES; FLOW CYTOMETRY; HUMANS; KERATINOCYTES; METAL NANOPARTICLES; POLYETHYLENE GLYCOLS; REACTIVE OXYGEN SPECIES; SILVER;

EID: 84962315801     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2016.03.005     Document Type: Article

References (77)

1. Abdelhalim M.A.K., Jarrar B.M. Renal tissue alterations were size-dependent with smaller ones induced more effects and related with time exposure of gold nanoparticles. Lipids Health Dis. 2011, 2011.
2. Ahamed M., Alsalhi M., Siddiqui M. Silver nanoparticle applications and human health. Clin. Chim. Acta 2010, 411(23):1841-1848.
3. Ahlberg S., Meinke M.C., Werner L., Epple M., Diendorf J., Blume-Peytavi U., Lademann J., Vogt A., Rancan F. Comparison of silver nanoparticles stored under air or argon with respect to the induction of intracellular free radicals and toxic effects toward keratinocytes. Eur. J. Pharm. Biopharm. 2014, 88(3):651-657.
4. AshaRani P., Low Kah Mun G., Hande M., Valiyaveettil S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 2009, 3:279-290.
5. Asharani P., Sethu S., Lim H., Balaji G., Valiyaveettil S., Hande M. Differential regulation of intracellular factors mediating cell cycle, DNA repair and inflammation following exposure to silver nanoparticles in human cells. Genome Integr 2012, 3(1):2.
6. Behra R., Sigg L., Clift M., Herzog F., Minghetti M., Johnston B., Petri-Fink A., Rothen-Rutishauser B. Bioavailability of silver nanoparticles and ions: from a chemical and biochemical perspective. J. R. Soc. Interface 2013, 10:20130396.
7. Benn T., Westerhoff P. Nanoparticle silver released into water from commercially available sock fabrics. Environ. Sci. Technol. 2008, 42:4133-4139.
8. Boonkaew B., Kempf M., Kimble R., Cuttle L. Cytotoxicity testing of silver-containing burn treatments using primary and immortal skin cells. Burns 2014, 40(8):1562-1569.
9. Boukamp P., Petrussevska R., Breitkreutz D., Hornung J., Markham A., Fusenig N. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 1988, 106:761-771.
10. Brandenberger C., Mühlfeld C., Ali Z., Lenz A.-G.G., Schmid O., Parak W.J., Gehr P., Rothen-Rutishauser B. Quantitative evaluation of cellular uptake and trafficking of plain and polyethylene glycol-coated gold nanoparticles. Small 2010, 6:1669-1678.
11. Brown D.M., Dickson C., Duncan P., Al-Attili F., Stone V. Interaction between nanoparticles and cytokine proteins: impact on protein and particle functionality. Nanotechnology 2010, 21:215104.
12. Browning L., Lee K., Nallathamby P., Xu X.-H.N. Silver nanoparticles incite size- and dose-dependent developmental phenotypes and nanotoxicity in zebrafish embryos. Chem. Res. Toxicol. 2013, 26:1503-1513.
13. Brunelle J.K., Letai A. Control of mitochondrial apoptosis by the Bcl-2 family. J. Cell Sci. 2009, 122:437-441.
14. Caballero-Díaz E., Pfeiffer C., Kastl L., Gil P., Simonet B., Valcárcel M., Lamana J., Laborda F., Parak W.J. The toxicity of silver nanoparticles depends on their uptake by cells and thus on their surface chemistry. Part. Part. Syst. Char. 2013, 30:1079-1085.
15. Carrola J., Bastos V., Ferreira de Oliveira J.M., Oliveira H., Santos C., Gil A.M., Duarte I.F. Insights into the impact of silver nanoparticles on human keratinocytes metabolism through NMR metabolomics. Arch. Biochem. Biophys. 2016, 589:53-61.
16. Casals E., Pfaller T., Duschl A., Oostingh G.J., Puntes V. Time evolution of the nanoparticle protein corona. ACS Nano. 2010, 4:3623-3632.
17. Chairuangkitti P., Lawanprasert S., Roytrakul S., Aueviriyavit S., Phummiratch D., Kulthong K., Chanvorachote P., Maniratanachote R. Silver nanoparticles induce toxicity in A549 cells via ROS-dependent and ROS-independent pathways. Toxicol. In Vitro 2013, 27(1):330-338.
18. Chen X., Schluesener H. Nanosilver: a nanoproduct in medical application. Toxicol. Lett. 2008, 176:1-12.
19. Comfort K.K., Maurer E.I., Hussain S.M. Slow release of ions from internalized silver nanoparticles modifies the epidermal growth factor signaling response. Colloid Surface B. 2014, 123:136-142.
20. EPA EPA, 2010. State of the Science Literature Review: Everything Nanosilver and More. Scientific, Technical, Research, Engineering and Modeling Support Final Report.
21. Eckhardt S., Brunetto P., Gagnon J., Priebe M., Giese B., Fromm K. Nanobio silver: its interactions with peptides and bacteria, and its uses in medicine. Chem. Rev. 2013, 113:4708-4754.
22. El Badawy A.M., Scheckel K.G., Suidan M., Tolaymat T. The impact of stabilization mechanism on the aggregation kinetics of silver nanoparticles. Sci. Total Environ. 2012, 429:325-331.
23. England C., Priest T., Zhang G., Sun X., Patel D., McNally L., van Berkel V., Gobin A., Frieboes H. Enhanced penetration into 3D cell culture using two and three layered gold nanoparticles. Int. J. Nanomed. 2013, 8:3603-3617.
24. Fernández-López C., Mateo-Mateo C., Alvarez-Puebla R., Pérez-Juste J., Pastoriza-Santos I., Liz-Marzán L. Highly controlled silica coating of PEG-capped metal nanoparticles and preparation of SERS-encoded particles. Langmuir 2009, 25:13894-13899.
25. Foldbjerg R., Irving E., Hayashi Y., Sutherland D., Thorsen K., Autrup H., Beer C. Global gene expression profiling of human lung epithelial cells after exposure to nanosilver. Toxicol. Sci. 2012, 130:145-157.
26. George R., Merten S., Wang T.T., Kennedy P., Maitz P. In vivo analysis of dermal and systemic absorption of silver nanoparticles through healthy human skin. Australas. J. Dermatol. 2014, 55:185-190.
27. Gliga A., Skoglund S., Odnevall Wallinder I., Fadeel B., Karlsson H. 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):11-17.
28. Greulich C., Diendorf J., Simon T., Eggeler G., Epple M., Köller M. Uptake and intracellular distribution of silver nanoparticles in human mesenchymal stem cells. Acta Biomater. 2011, 7:347-354.
29. Grosse S., Evje L., Syversen T. Silver nanoparticle-induced cytotoxicity in rat brain endothelial cell culture. Toxicol. In Vitro 2013, 27:305-313. (1).
30. Haberl N., Hirn S., Wenk A., Diendorf J., Epple M., Johnston B., Krombach F., Kreyling W., Schleh C. Cytotoxic and proinflammatory effects of PVP-coated silver nanoparticles after intratracheal instillation in rats. Beilstein J. Nanotechnol. 2013, 4(1):933-940.
31. Hsiao I.L.L., Hsieh Y.-K.K., Wang C.-F.F., Chen I.C.C., Huang Y.-J.J. Trojan-horse mechanism in the cellular uptake of silver nanoparticles verified by direct intra- and extracellular silver speciation analysis. Environ. Sci. Technol. 2015, 49:3813-3821.
32. Jeyaraj M., Renganathan A., Sathishkumar G. Biogenic metal nanoformulations induce Bax/Bcl2 and caspase mediated mitochondrial dysfunction in human breast cancer cells (MCF 7). RSC Adv. 2015, 5(3):2159-2166.
33. Jiang X., Foldbjerg R., Miclaus T., Wang L., Singh R., Hayashi Y., Sutherland D., Chen C., Autrup H., Beer C. Multi-platform genotoxicity analysis of silver nanoparticles in the model cell line CHO-K1. Toxicol. Lett. 2013, 222:55-63.
34. Jokerst J.V., Lobovkina T., Zare R.N., Gambhir S.S. Nanoparticle PEGylation for imaging and therapy. Nanomedicine (Lond). 2011, 6:715-728.
35. Kang S., Lee Y., Lee E.-K., Kwak M.-K. Silver nanoparticles-mediated G2/M cycle arrest of renal epithelial cells is associated with NRF2-GSH signaling. Toxicol. Lett. 2012, 211:334-341.
36. 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.
37. Kim S., Choi J., Choi J., Chung K.-H., Park K., Yi J., Ryu D.-Y. Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol. In Vitro 2009, 23:1076-1084.
38. 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. Part A 2012, 100A:1033-1043.
39. Larese F.F., D'Agostin F., Crosera M., Adami G., Renzi N., Bovenzi M., Maina G. Human skin penetration of silver nanoparticles through intact and damaged skin. Toxicology 2009, 255:33-37.
40. Lee Y., Kim D., Oh J., Yoon S., Choi M., Lee S., Kim J., Lee K., Song C.-W. Silver nanoparticles induce apoptosis and G2/M arrest via PKCζ-dependent signaling in A549 lung cells. Arch. Toxicol. 2011, 85:1529-1540.
41. Li X., Lenhart J.J., Walker H.W. Aggregation kinetics and dissolution of coated silver nanoparticles. Langmuir. 2012, 28:1095-1104.
42. Li X., Xu L., Shao A., Wu G., Hanagata N. Cytotoxic and genotoxic effects of silver nanoparticles on primary Syrian hamster embryo (SHE) cells. J. Nanosci. Nanotechnol. 2013, 13:161-170.
43. Liu W., Wu Y., Wang C., Li H., Wang T., Liao C., Cui L., Zhou Q., Yan B., Jiang G. Impact of silver nanoparticles on human cells: effect of particle size. Nanotoxicology 2010, 4:319-330.
44. Lu W., Senapati D., Wang S., Tovmachenko O., Singh A., Yu H., Ray P. Effect of surface coating on the toxicity of silver nanomaterials on human skin keratinocytes. Chem. Phys. Lett. 2010, 487.
45. Maiorano G., Sabella S., Sorce B., Brunetti V., Malvindi M.A., Cingolani R., Pompa P.P. 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.
46. Michel R., Pasche S., Textor M., Castner D.G. Influence of PEG architecture on protein adsorption and conformation. Langmuir. 2005, 21:12327-12332.
47. Mukherjee S.G., O'Claonadh N., Casey A., Chambers G. Comparative in vitro cytotoxicity study of silver nanoparticle on two mammalian cell lines. Toxicol. In Vitro 2012, 26:238-251.
48. Nowack B., Bucheli T. Occurrence, behavior and effects of nanoparticles in the environment. Environ. Pollut. 2007, 150:5-22.
49. Nowack B., Krug H., Height M. 120 years of nanosilver history: implications for policy makers. Environ. Sci. Technol. 2011, 45:1177-1183.
50. Nymark P., Catalán J., Suhonen S., Järventaus H., Birkedal R., Clausen P., Jensen K., Vippola M., Savolainen K., Norppa H. Genotoxicity of polyvinylpyrrolidone-coated silver nanoparticles in BEAS 2B cells. Toxicology 2013, 313:38-48.
51. Oliveira H., Monteiro C., Pinho F., Pinho S., Ferreira de Oliveira J.M., Santos C. Cadmium-induced genotoxicity in human osteoblast-like cells. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2014, 77(775-776):38-47.
52. Orlowski P., Krzyzowska M., Zdanowski R., Winnicka A., Nowakowska J., Stankiewicz W., Tomaszewska E., Celichowski G., Grobelny J. Assessment of in vitro cellular responses of monocytes and keratinocytes to tannic acid modified silver nanoparticles. Toxicol. In Vitro 2013, 27:1798-1808.
53. Park E.-J.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.
54. Park J., Lim D.-H.H., Lim H.-J.J., Kwon T., Choi J-sS, Jeong S., Choi I.-H.H., Cheon J. Size dependent macrophage responses and toxicological effects of Ag nanoparticles. Chem. Commun. 2011, 4382-4384.
55. Pfaffl M. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45. (9).
56. 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.
57. Povoski S.P., Davis P.D., Colcher D., Martin E.W. Single molecular weight discrete PEG compounds: emerging roles in molecular diagnostics, imaging and therapeutics. Expert Rev. Mol. Diagn. 2013, 13:315-319.
58. Robert I.M. Colloidal stability of silver nanoparticles in biologically relevant conditions. J. Nanopart. Res. 2010.
59. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 2000, 132:365-386.
60. Sahu S.C., Zheng J., Graham L., Chen L., Ihrie J., Yourick J.J., Sprando R.L. Comparative cytotoxicity of nanosilver in human liver HepG2 and colon Caco2 cells in culture. J. Appl. Toxicol. 2014, 34:1155-1166.
61. Samberg M.E., Oldenburg S.J., Monteiro-Riviere N.A. Evaluation of silver nanoparticle toxicity in skin in vivo and keratinocytes in vitro. Environ. Health Perspect. 2010, 118:407-413.
62. Sharma V., Yngard R., Lin Y. Silver nanoparticles: green synthesis and their antimicrobial activities. Adv. Colloid Interface 2009, 145(1):83-96.
63. X-l Song, Li B., Xu K., Liu J., Ju W., Wang J., X-d Liu, Li J., Qi Y-f. Cytotoxicity of water-soluble mPEG-SH-coated silver nanoparticles in HL-7702 cells. Cell Biol. Toxicol. 2012, 28:225-237.
64. Suk J.S., Lai S.K., Boylan N.J., Dawson M.R., Boyle M.P., Hanes J. Rapid transport of muco-inert nanoparticles in cystic fibrosis sputum treated with N-acetyl cysteine. Nanomed.-UK 2011, 6:365-375.
65. Suliman Y.A.O., Ali D., Alarifi S., Harrath A.H., Mansour L., Alwasel S.H. Evaluation of cytotoxic, oxidative stress, proinflammatory and genotoxic effect of silver nanoparticles in human lung epithelial cells. Environ. Toxicol. 2015, 30:149-160.
66. 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.
67. Tao X., Ning Z., Heather L.N., Donglu S., Xuejun W. Modification of nanostructured materials for biomedical applications. Mater. Sci. Eng.: C 2007, 27(3):579-594.
68. Thorley A.J., Tetley T.D. New perspectives in nanomedicine. Pharmacol. Therapeut. 2013, 140:176-185.
69. Twentyman P., Luscombe M. A study of some variables in a tetrazolium dye (MTT) based assay for cell growth and chemosensitivity. Br. J. Cancer 1987, 56:279-285.
70. Wang X., Ji Z., Chang C.H., Zhang H., Wang M., Liao Y.-P.P., Lin S., Meng H., Li R., Sun B., et al. Use of coated silver nanoparticles to understand the relationship of particle dissolution and bioavailability to cell and lung toxicological potential. Small 2014, 10:385-398.
71. Wei L., Tang J., Zhang Z., Chen Y., Zhou G., Xi T. Investigation of the cytotoxicity mechanism of silver nanoparticles in vitro. Biomed. Mater. 2010, 5:44103.
72. Yang E.-J.J., Jang J., Lim D.-H.H., Choi I.-H.H. Enzyme-linked immunosorbent assay of IL-8 production in response to silver nanoparticles. Methods Mol. Biol. 2012, 926:131-139.
73. 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.
74. Zhang T., Wang L., Chen Q., Chen C. Cytotoxic potential of silver nanoparticles. Yonsei Med. J. 2014, 55:283-291.
75. Zhang X.-F.F., Choi Y.-J.J., Han J.W., Kim E., Park J.H., Gurunathan S., Kim J.-H.H. Differential nanoreprotoxicity of silver nanoparticles in male somatic cells and spermatogonial stem cells. Int. J. Nanomed. 2015, 10:1335-1357.
76. Zhao S., Fernald R. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol. 2005, 12:1047-1064.
77. Zucker R.M., Daniel K.M., Massaro E.J., Karafas S.J., Degn L.L., Boyes W.K. Detection of silver nanoparticles in cells by flow cytometry using light scatter and far-red fluorescence. Cytometry A 2013, 83(10):962-972.