Difference in the toxicity mechanism between ion and nanoparticle forms of silver in the mouse lung and in macrophages

Toxicology

Volumn 328, Issue , 2015, Pages 84-92

  Arai, Yuta ^a   Miyayama, Takamitsu ^b,c   Hirano, Seishiro ^a,b  

^a CHIBA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE FOR ENVIRONMENTAL STUDIES   (Japan)

^c TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

Author keywords

Lung; Lysosome; Macrophages; Metallothionein; Silver ion; Silver nanoparticle

Indexed keywords

ALBUMIN; INTERLEUKIN 1BETA; ION; METALLOTHIONEIN; SILVER NANOPARTICLE; SILVER NITRATE; AUTACOID; IL1B PROTEIN, MOUSE; METAL NANOPARTICLE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOTOXICITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; IN VIVO STUDY; LIVER; LUNG LAVAGE; LUNG PARENCHYMA; LYSOSOME; MACROPHAGE; MALE; MASS SPECTROMETRY; MICROSCOPY; MOLECULAR WEIGHT; MOUSE; NEUTROPHIL; NONHUMAN; SYSTEMIC CIRCULATION; TISSUE DISTRIBUTION; TOXICITY TESTING; ADVERSE EFFECTS; ANIMAL; CELL LINE; CELL SURVIVAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; EXPOSURE; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; LUNG; METABOLISM; NEUTROPHIL CHEMOTAXIS; PARTICLE SIZE; PATHOLOGY; TIME; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; BRONCHOALVEOLAR LAVAGE FLUID; CELL LINE; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; INFLAMMATION MEDIATORS; INHALATION EXPOSURE; INTERLEUKIN-1BETA; LIVER; LUNG; LYSOSOMES; MACROPHAGES; MALE; METAL NANOPARTICLES; METALLOTHIONEIN; MICE, INBRED ICR; MOLECULAR WEIGHT; NEUTROPHIL INFILTRATION; NEUTROPHILS; PARTICLE SIZE; SILVER NITRATE; TIME FACTORS;

EID: 84919897809     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2014.12.014     Document Type: Article

References (50)

1. Ahamed M., Karns M., Goodson M., Rowe J., Hussain S.M., Schlager J.J., Hong Y. DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicol. Appl. Pharmacol. 2008, 233:404-410.
2. Almofti M.R., Ichikawa T., Yamashita K., Terada H., Shinohara Y. Silver ion induces a cyclosporine a-insensitive permeability transition in rat liver mitochondria and release of apoptogenic cytochrome C. J. Biochem. 2003, 134:43-49.
3. 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.
4. Atiyeh B.S., Costagliola M., Hayek S.N., Dibo S.A. Effect of silver on burn wound infection control and healing: review of the literature. Burns 2007, 33:139-148.
5. Baldi C., Minoia C., Di Nucci A., Capodaglio E., Manzo L. Effects of silver in isolated rat hepatocytes. Toxicol. Lett. 1988, 41:261-268.
6. Berry C.C., de la Fuente J.M., Mullin M., Chu S.W., Curtis A.S. Nuclear localization of HIV-1 tat functionalized gold nanoparticles. IEEE Trans. Nanobiosci. 2007, 6:262-269.
7. Carlson C., Hussain S.M., Schrand A.M., Braydich-Stolle L.K., Hess K.L., Jones R.L., Schlager J.J. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J. Phys. Chem. B 2008, 112:13608-13619.
8. Cartiera M.S., Johnson K.M., Rajendran V., Caplan M.J., Saltzman W.M. The uptake and intracellular fate of PLGA nanoparticles in epithelial cells. Biomaterials 2009, 30:2790-2798.
9. 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.
10. Frohlich E., Samberger C., Kueznik T., Absenger M., Roblegg E., Zimmer A., Pieber T.R. Cytotoxicity of nanoparticles independent from oxidative stress. J. Toxicol. Sci. 2009, 34:363-375.
11. Fu Z., Guo J., Jing L., Li R., Zhang T., Peng S. Enhanced toxicity and ROS generation by doxorubicin in primary cultures of cardiomyocytes from neonatal metallothionein-I/II null mice. Toxicol. In Vitro 2010, 24:1584-1591.
12. 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.
13. Haq F., Mahoney M., Koropatnick J. Signaling events for metallothionein induction. Mutat. Res. 2003, 533:211-226.
14. Hayashi Y., Miclaus T., Scavenius C., Kwiatkowska K., Sobota A., Engelmann P., Scott-Fordsmand J.J., Enghild J.J., Sutherland D.S. Species differences take shape at nanoparticles: protein corona made of the native repertoire assists cellular interaction. Environ. Sci. Technol. 2013.
15. Heuchel R., Radtke F., Georgiev O., Stark G., Aguet M., Schaffner W. The transcription factor MTF-1 is essential for basal and heavy metal-induced metallothionein gene expression. EMBO J. 1994, 13:2870-2875.
16. Hidalgo E., Domínguez C. Study of cytotoxicity mechanisms of silver nitrate in human dermal fibroblasts. Toxicol. Lett. 1998, 98:169-179.
17. Hu L., Mao Z.W., Gao C.Y. Colloidal particles for cellular uptake and delivery. J. Mater. Sci. 2009, 19:3108-3115.
18. Hussain S.M., Hess K.L., Gearhart J.M., Geiss K.T., Schlager J.J. In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol. In Vitro 2005, 19:975-983.
19. Jansson G., Harms-Ringdahl M. Stimulating effects of mercuric- and silver ions on the superoxide anion production in human polymorphonuclear leukocytes. Free Radic. Res. Commun. 1993, 18:87-98.
20. Kagi J.H., Schaffer A. Biochemistry of metallothionein. Biochemistry 1988, 27:8509-8515.
21. Kim S., Choi J.E., 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.
22. Kvitek L., Panacek A., Soukupova J., Kolar M., Vecerova R., Prucek R., Holecova M., Zboril R. Effect of surfactants and polymers on stability and antibacterial activity of silver nanoparticles (NPs). J. Phys. Chem. C 2008, 112:5825-5834.
23. Lansdown A.B. Metallothioneins: potential therapeutic aids for wound healing in the skin. Wound Repair. Regen. 2002, 10:130-132.
24. Lansdown A.B. Silver in health care: antimicrobial effects and safety in use. Curr. Probl. Dermatol. 2006, 33:17-34.
25. Lansdown A.B. A pharmacological and toxicological profile of silver as an antimicrobial agent in medical devices. Adv. Pharmacol. Sci. 2010, 2010:910686.
26. Lesniak A., Salvati A., Santos-Martinez M.J., Radomski M.W., Dawson K.A., Aberg C. Nanoparticle adhesion to the cell membrane and its effect on nanoparticle uptake efficiency. J. Am. Chem. Soc. 2013, 135:1438-1444.
27. 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.
28. Maret W. The function of zinc metallothionein: a link between cellular zinc and redox state. J. Nutr. 2000, 130:1455S-1458S.
29. Miyayama T., Arai Y., Suzuki N., Hirano S. Mitochondrial electron transport is inhibited by disappearance of metallothionein in human bronchial epithelial cells following exposure to silver nitrate. Toxicology 2013, 305:20-29.
30. Miyayama T., Ogra Y., Osima Y., Suzuki K.T. Narrow-bore HPLC-ICP-MS for speciation of copper in mutant mouse neonates bearing a defect in Cu metabolism. Anal. Bioanal. Chem. 2008, 390:1799-1803.
31. Monopoli M.P., Aberg C., Salvati A., Dawson K.A. Biomolecular coronas provide the biological identity of nanosized materials. Nat. Nanotechnol. 2012, 7:779-786.
32. Moss A.P., Sugar A., Hargett N.A., Atkin A., Wolkstein M., Rosenman K.D. The ocular manifestations and functional effects of occupational argyrosis. Arch. Ophthalmol. 1979, 97:906-908.
33. Murdock R.C., Braydich-Stolle L., Schrand A.M., Schlager J.J., Hussain S.M. Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique. Toxicol. Sci. 2008, 101:239-253.
34. Nam H.Y., Kwon S.M., Chung H., Lee S.Y., Kwon S.H., Jeon H., Kim Y., Park J.H., Kim J., Her S., Oh Y.K., Kwon I.C., Kim K., Jeong S.Y. Cellular uptake mechanism and intracellular fate of hydrophobically modified glycol chitosan nanoparticles. J. Control Release 2009, 135:259-267.
35. Nordberg M., Nordberg G.F. Toxicological aspects of metallothionein. Cell. Mol. Biol. (Noisy-le-grand) 2000, 46:451-463.
36. Oberdorster G., Ferin J., Finkelstein J., Soderholm S. Thermal degradation events as health hazards: particle vs gas phase effects, mechanistic studies with particles. Acta Astronaut. 1992, 27:251-256.
37. Oostingh G.J., Casals E., Italiani P., Colognato R., Stritzinger R., Ponti J., Pfaller T., Kohl Y., Ooms D., Favilli F., Leppens H., Lucchesi D., Rossi F., Nelissen I., Thielecke H., Puntes V.F., Duschl A., Boraschi D. Problems and challenges in the development and validation of human cell-based assays to determine nanoparticle-induced immunomodulatory effects. Part. Fibre Toxicol. 2011, 8:8.
38. Park E.J., Choi K., Park K. Induction of inflammatory responses and gene expression by intratracheal instillation of silver nanoparticles in mice. Arch. Pharm. Res. 2011, 34:299-307.
39. Powers C.M., Wrench N., Ryde I.T., Smith A.M., Seidler F.J., Slotkin T.A. Silver impairs neurodevelopment: studies in PC12 cells. Environ. Health Perspect. 2010, 118:73-79.
40. Prasad R.Y., McGee J.K., Killius M.G., Suarez D.A., Blackman C.F., DeMarini D.M., Simmons S.O. Investigating oxidative stress and inflammatory responses elicited by silver nanoparticles using high-throughput reporter genes in HepG2 cells: effect of size, surface coating, and intracellular uptake. Toxicol. In Vitro 2013, 27:2013-2021.
41. Rosenman K.D., Moss A., Kon S. Argyria: clinical implications of exposure to silver nitrate and silver oxide. J. Occup. Med. 1979, 21:430-435.
42. Sandberg W.J., Lag M., Holme J.A., Friede B., Gualtieri M., Kruszewski M., Schwarze P.E., Skuland T., Refsnes M. Comparison of non-crystalline silica nanoparticles in IL-1beta release from macrophages. Part. Fibre Toxicol. 2012, 9:32.
43. Saydam N., Steiner F., Georgiev O., Schaffner W. Heat and heavy metal stress synergize to mediate transcriptional hyperactivation by metal-responsive transcription factor MTF-1. J. Biol. Chem. 2003, 278:31879-31883.
44. Scheuhammer A.M., Cherian M.G. Quantification of metallothioneins by a silver-saturation method. Toxicol. Appl. Pharmacol. 1986, 82:417-425.
45. Soto K., Garza K.M., Murr L.E. Cytotoxic effects of aggregated nanomaterials. Acta Biomater. 2007, 3:351-358.
46. Stafeeva K., Erlanger M., Velez-Montoya R., Olson J.L. Ocular argyrosis secondary to long-term ingestion of silver nitrate salts. Clin. Ophthalmol. 2012, 6:2033-2036.
47. Sung J.H., Ji J.H., Park J.D., Yoon J.U., Kim D.S., Jeon K.S., Song M.Y., Jeong J., Han B.S., Han J.H., Chung Y.H., Chang H.K., Lee J.H., Cho M.H., Kelman B.J., Yu I.J. Subchronic inhalation toxicity of silver nanoparticles. Toxicol. Sci. 2009, 108:452-461.
48. Takenaka S., Karg E., Roth C., Schulz H., Ziesenis A., Heinzmann U., Schramel P., Heyder J. Pulmonary and systemic distribution of inhaled ultrafine silver particles in rats. Environ. Health Perspect. 2001, 109(Suppl. 4):547-551.
49. Vallhov H., Qin J., Johansson S.M., Ahlborg N., Muhammed M.A., Scheynius A., Gabrielsson S. The importance of an endotoxin-free environment during the production of nanoparticles used in medical applications. Nano Lett. 2006, 6:1682-1686.
50. Wilkinson L.J., White R.J., Chipman J.K. Silver and nanoparticles of silver in wound dressings: a review of efficacy and safety. J. Wound Care 2011, 20:543-549.