Effects of silver nanoparticles on the liver and hepatocytes in vitro

Toxicological Sciences

Volumn 131, Issue 2, 2013, Pages 537-547

  Gaiser, Birgit K ^a   Hirn, Stephanie ^b   Kermanizadeh, Ali ^a   Kanase, Nilesh ^a   Fytianos, Kleanthis ^a   Wenk, Alexander ^b   Haberl, Nadine ^b   Brunelli, Andrea ^c   Kreyling, Wolfgang G ^b   Stone, Vicki ^a  

^a HERIOT WATT UNIVERSITY   (United Kingdom)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c CA' FOSCARI UNIVERSITY OF VENICE   (Italy)

Author keywords

Hepatocytes; In vitro alternatives; Liver toxicology; Metals; Nanoparticles

Indexed keywords

ALBUMIN; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 8; LACTATE DEHYDROGENASE; MACROPHAGE INFLAMMATORY PROTEIN 2; SILVER NANOPARTICLE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; BLOOD FLOW; CELL LINE; CELL NUCLEUS; CELL STRUCTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOPLASM; CYTOTOXICITY; ENVIRONMENTAL EXPOSURE; FEMALE; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INGESTION; INJECTION; LIVER; LIVER CELL; LIVER TOXICITY; LOW DRUG DOSE; MEDIATOR; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT;

ANIMALS; APOPTOSIS; CELL LINE; FEMALE; FLOW CYTOMETRY; GLUTATHIONE; HEPATOCYTES; INFLAMMATION MEDIATORS; LIVER; METAL NANOPARTICLES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SILVER;

EID: 84873857913     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs306     Document Type: Article

References (39)

1. Alkilany, A. M., and Murphy, C. J. (2010). Toxicity and cellular uptake of gold nanoparticles: What we have learned so far? J. Nanopart. Res. 12, 2313-2333.
2. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
3. Brown, D. M., Wilson, M. R., MacNee, W., Stone, V., and Donaldson, K. (2001). Size-dependent proinflammatory effects of ultrafine polystyrene particles: A role for surface area and oxidative stress in the enhanced activity of ultrafines. Toxicol. Appl. Pharmacol. 175, 191-199.
4. Carlson, C., Hussain, S. M., Schrand, A. M., Braydich-Stolle, L. K., Hess, K. L., Jones, R. L., and Schlager, J. J. (2008). Unique cellular interaction of silver nanoparticles: Size-dependent generation of reactive oxygen species. J. Phys. Chem. B 112, 13608-13619.
5. Chao, J. B., Liu, J. F., Yu, S. J., Feng, Y. D., Tan, Z. Q., Liu, R., and Yin, Y. G. (2011). Speciation analysis of silver nanoparticles and silver ions in antibacterial products and environmental waters via cloud point extraction-based separation. Anal. Chem. 83, 6875-6882.
6. Cheng, C., Yun, K.-Y., Ressom, H. W., Mohanty, B., Bajic, V. B., Jia, Y., Yun, S. J., and de los Reyes, B. G. (2007). An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chillingtolerant japonica rice. BMC Genomics 8, 175.
7. dos Santos, S. A., de Andrade Júnior, D. R., and de Andrade, D. R. (2011). TNF-α production and apoptosis in hepatocytes after Listeria monocytogenes and Salmonella Typhimurium invasion. Rev. Inst. Med. Trop. Sao Paulo 53, 107-112.
8. Gaiser, B. K., Fernandes, T. F., Jepson, M. A., Lead, J. R., Tyler, C. R., Baalousha, M., Biswas, A., Britton, G. J., Cole, P. A., Johnston, B. D., et al. (2012). Interspecies comparisons on the uptake and toxicity of silver and cerium dioxide nanoparticles. Environ. Toxicol. Chem. 31, 144-154.
9. Gearing, A. J., Hemingway, I., Pigott, R., Hughes, J., Rees, A. J., and Cashman, S. J. (1992). Soluble forms of vascular adhesion molecules, E-selectin, ICAM-1, and VCAM-1: Pathological significance. Ann. N. Y. Acad. Sci. 667, 324-331.
10. Gonçalves, D. M., and Girard, D. (2011). Titanium dioxide (TiO2) nanoparticles induce neutrophil influx and local production of several pro-inflammatory mediators in vivo. Int. Immunopharmacol. 11, 1109-1115.
11. Hasch, E., Jarnum, S., and Tygstrup, N. (1967). Albumin synthesis rate as a measure of liver function in patient with cirrhosis. Acta Med. Scand. 182, 83-92.
12. Hirn, S., Semmler-Behnke, M., Schleh, C., Wenk, A., Lipka, J., Schäffler, M., Takenaka, S., Möller, W., Schmid, G., Simon, U., et al. (2011). Particle size-dependent and surface charge-dependent biodistribution of gold nanoparticles after intravenous administration. Eur. J. Pharm. Biopharm. 77, 407-416.
13. Johnston, H. J., Hutchison, G., Christensen, F. M., Peters, S., Hankin, S., and Stone, V. (2010). A review of the in vivo and in vitro toxicity of silver and gold particulates: Particle attributes and biological mechanisms responsible for the observed toxicity. Crit. Rev. Toxicol. 40, 328-346.
14. Kasper, J., Hermanns, M. I., Bantz, C., Maskos, M., Stauber, R., Pohl, C., Unger, R. E., and Kirkpatrick, J. C. (2011). Inflammatory and cytotoxic responses of an alveolar-capillary coculture model to silica nanoparticles: Comparison with conventional monocultures. Part. Fibre Toxicol. 8, 6.
15. Kermanizadeh, A., Pojana, G., Gaiser, B. K., Birkedal, R., Bilanicova, D., Wallin, H., Jensen, K. A., Sellergren, B., Hutchison, G. R., Marcomini, A., et al. (2012). In vitro assessment of engineered nanomaterials using a hepatocyte cell line: Cytotoxicity, pro-inflammatory cytokines and functional markers. Nanotoxicology. Advance access published January 20, 2012. doi:10.3109/ 17435390.2011.653416.
16. Kim, H. R., Kim, M. J., Lee, S. Y., Oh, S. M., and Chung, K. H. (2011). Genotoxic effects of silver nanoparticles stimulated by oxidative stress in human normal bronchial epithelial (BEAS-2B) cells. Mutat. Res. 726, 129-135.
17. Klein, C., Comero, S., Stahlmecke, B., Romazanov, J., Kuhlbusch, T., van Doren, E., Wick, P., Locoro, G., Koerdel, W., Gawlik, B., et al. (2011). NM-300 silver characterisation, stability, homogeneity. EUR - Scientific and Technical Research Reports, JRC Publication No. JRC60709, EUR 24693 EN, Publications Office of the European Union. Doi:10.2788/23079.
18. Korani, M., Rezayat, S. M., Gilani, K., Arbabi Bidgoli, S., and Adeli, S. (2011). Acute and subchronic dermal toxicity of nanosilver in guinea pig. Int. J. Nanomedicine 6, 855-862.
19. Kulthong, K., Srisung, S., Boonpavanitchakul, K., Kangwansupamonkon, W., and Maniratanachote, R. (2010). Determination of silver nanoparticle release from antibacterial fabrics into artificial sweat. Part. Fibre Toxicol. 7, 8.
20. Mühlfeld, C., Gehr, P., and Rothen-Rutishauser, B. (2008). Translocation and cellular entering mechanisms of nanoparticles in the respiratory tract. Swiss Med. Wkly. 138, 387-391.
21. Nishanth, R. P., Jyotsna, R. G., Schlager, J. J., Hussain, S. M., and Reddanna, P. (2011). Inflammatory responses of RAW 264.7 macrophages upon exposure to nanoparticles: Role of ROS-NFκB signaling pathway. Nanotoxicology 5, 502-516.
22. Nowack, B., Krug, H. F., and Height, M. (2011). 120 years of nanosilver history: Implications for policy makers. Environ. Sci. Technol. Advance access published January 10, 2011. doi:10.1021/es103316q.
23. Oberdörster, G. (2012). Nanotoxicology: In vitro-in vivo dosimetry. Environ. Health Perspect. 120, A13.
24. Piao, M. J., Kang, K. A., Lee, I. K., Kim, H. S., Kim, S., Choi, J. Y., Choi, J., and Hyun, J. W. (2011). Silver nanoparticles induce oxidative cell damage in human liver cells through inhibition of reduced glutathione and induction of mitochondria-involved apoptosis. Toxicol. Lett. 201, 92-100.
25. Powers, C. M., Badireddy, A. R., Ryde, I. T., Seidler, F. J., and Slotkin, T. A. (2011). Silver nanoparticles compromise neurodevelopment in PC12 cells: Critical contributions of silver ion, particle size, coating, and composition. Environ. Health Perspect. 119, 37-44.
26. Rimkunas, V. M., Graham, M. J., Crooke, R. M., and Liscum, L. (2009). TNF-{alpha} plays a role in hepatocyte apoptosis in Niemann-Pick type C liver disease. J. Lipid Res. 50, 327-333.
27. Ryou, S. M., Kim, J. M., Yeom, J. H., Hyun, S., Kim, S., Han, M. S., Kim, S. W., Bae, J., Rhee, S., and Lee, K. (2011). Gold nanoparticle-assisted delivery of small, highly structured RNA into the nuclei of human cells. Biochem. Biophys. Res. Commun. 416, 178-183.
28. Sadauskas, E., Wallin, H., Stoltenberg, M., Vogel, U., Doering, P., Larsen, A., and Danscher, G. (2007). Kupffer cells are central in the removal of nanoparticles from the organism. Part. Fibre Toxicol. 4, 10.
29. Salvi, S. S., Nordenhall, C., Blomberg, A., Rudell, B., Pourazar, J., Kelly, F. J., Wilson, S., Sandström, T., Holgate, S. T., and Frew, A. J. (2000). Acute exposure to diesel exhaust increases IL-8 and GRO-alpha production in healthy human airways. Am. J. Respir. Crit. Care Med. 161(2 Pt 1), 550-557.
30. Schleh, C., Semmler-Behnke, M., Lipka, J., Wenk, A., Hirn, S., Schäffler, M., Schmid, G., Simon, U., and Kreyling, W. G. (2012). Size and surface charge of gold nanoparticles determine absorption across intestinal barriers and accumulation in secondary target organs after oral administration. Nanotoxicology 6, 36-46.
31. Senft, A. P., Dalton, T. P., and Shertzer, H. G. (2000). Determining glutathione and glutathione disulfide using the fluorescence probe o-phthalaldehyde. Anal. Biochem. 280, 80-86.
32. Sharma, R. J., Macallan, D. C., Sedgwick, P., Remick, D. G., and Griffin, G. E. (1992). Kinetics of endotoxin-induced acute-phase protein gene expression and its modulation by TNF-alpha monoclonal antibody. Am. J. Physiol. 262(5 Pt 2), R786-R793.
33. Silver, S., Phung, le. T., and Silver, G. (2006). Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds. J. Ind. Microbiol. Biotechnol. 33, 627-634.
34. Stern, A., Rotem, D., Popov, I., and Porath, D. (2012). Quasi 3D imaging of DNA-gold nanoparticle tetrahedral structures. J. Phys. Condens. Matter 24, 164203.
35. Stone, V., Johnston, H., and Schins, R. P. (2009). Development of in vitro systems for nanotoxicology: Methodological considerations. Crit. Rev. Toxicol. 39, 613-626.
36. Tekamp-Olson, P., Gallegos, C., Bauer, D., McClain, J., Sherry, B., Fabre, M., van Deventer, S., and Cerami, A. (1990). Cloning and characterization of cDNAs for murine macrophage inflammatory protein 2 and its human homologues. J. Exp. Med. 172, 911-919.
37. Trickler, W. J., Lantz, S. M., Murdock, R. C., Schrand, A. M., Robinson, B. L., Newport, G. D., Schlager, J. J., Oldenburg, S. J., Paule, M. G., Slikker, W., Jr, et al. (2010). Silver nanoparticle induced blood-brain barrier inflammation and increased permeability in primary rat brain microvessel endothelial cells. Toxicol. Sci. 118, 160-170.
38. Wong, K. K., Cheung, S. O., Huang, L., Niu, J., Tao, C., Ho, C. M., Che, C. M., and Tam, P. K. (2009). Further evidence of the anti-inflammatory effects of silver nanoparticles. ChemMedChem 4, 1129-1135.
39. Yazdi, A. S., Guarda, G., Riteau, N., Drexler, S. K., Tardivel, A., Couillin, I., and Tschopp, J. (2010). Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1α and IL-1β. Proc. Natl. Acad. Sci. U.S.A. 107, 19449-19454.