486
Views
43
CrossRef citations to date
0
Altmetric
Original Article

Oral subchronic exposure to silver nanoparticles causes renal damage through apoptotic impairment and necrotic cell death

, , , , , , , , , & show all
Pages 671-686 | Received 23 Jan 2017, Accepted 11 Jun 2017, Published online: 04 Jul 2017

References

  • Arora S, Jain J, Rajwade JM, Paknikar KM. 2009. Interactions of silver nanoparticles with primary mouse fibroblasts and liver cells. Toxicol Appl Pharmacol 236:310–18.
  • Asharani PV, Low Kah Mun G, Hande MP, Valiyaveettil S. 2009. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3:279–90.
  • Basak S, Hoffmann A. 2008. Crosstalk via the NF-kappaB signaling system. Cytokine Growth Factor Rev 19:187–97.
  • Benn T, Cavanagh B, Hristovski K, Posner JD, Westerhoff P. 2010. The release of nanosilver from consumer products used in the home. J Environ Qual 39:1875–82.
  • Braydich-Stolle L, Hussain S, Schlager JJ, Hofmann MC. 2005. In vitro cytotoxicity of nanoparticles in mammalian germline stem cells. Toxicol Sci 88:412–19.
  • Burrell RE. 2003. A scientific perspective on the use of topical silver preparations. Ostomy Wound Manage 49:19–24.
  • Chen X, Schluesener HJ. 2008. Nanosilver: a nanoproduct in medical application. Toxicol Lett 176:1–12.
  • Choi J, Reipa V, Hitchins VM, Goering PL, Malinauskas RA. 2011. Physicochemical characterization and in vitro hemolysis evaluation of silver nanoparticles. Toxicol Sci 123:133–43.
  • Chromek M, Tullus K, Hertting O, Jaremko G, Khalil A, Li YH, Brauner A. 2003. Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinases-1 in acute pyelonephritis and renal scarring. Pediatr Res 53:698–705.
  • Comfort KK, Braydich-Stolle LK, Maurer EI, Hussain SM. 2014. Less is more: long-term in vitro exposure to low levels of silver nanoparticles provides new insights for nanomaterial evaluation. ACS Nano 8:3260–71.
  • Dziendzikowska K, Gromadzka-Ostrowska J, Lankoff A, Oczkowski M, Krawczynska A, Chwastowska J, et al. 2012. Time-dependent biodistribution and excretion of silver nanoparticles in male Wistar rats. J Appl Toxicol 32:920–8.
  • Ebabe Elle R, Gaillet S, Vide J, Romain C, Lauret C, Rugani N, et al. 2013. Dietary exposure to silver nanoparticles in Sprague-Dawley rats: effects on oxidative stress and inflammation. Food Chem Toxicol 60:297–301.
  • Ellman GL. 1959. Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–7.
  • Eom HJ, Choi J. 2010. p38 MAPK activation, DNA damage, cell cycle arrest and apoptosis as mechanisms of toxicity of silver nanoparticles in Jurkat T cells. Environ Sci Technol 44:8337–42.
  • Faedmaleki F, F HS, Salarian AA, Ahmadi Ashtiani H, Rastegar H. 2014. Toxicity effect of silver nanoparticles on mice liver primary cell culture and HepG2 cell line. Iran J Pharm Res 13:235–42.
  • Foldbjerg R, Olesen P, Hougaard M, Dang DA, Hoffmann HJ, Autrup H. 2009. PVP-coated silver nanoparticles and silver ions induce reactive oxygen species, apoptosis and necrosis in THP-1 monocytes. Toxicol Lett 190:156–62.
  • Fu PP, Xia Q, Hwang HM, Ray PC, Yu H. 2014. Mechanisms of nanotoxicity: generation of reactive oxygen species. J Food Drug Anal 22:64–75.
  • Gao J, Mahapatra CT, Mapes CD, Khlebnikova M, Wei A, Sepulveda MS. 2016. Vascular toxicity of silver nanoparticles to developing zebrafish (Danio rerio). Nanotoxicology 10:1363–72.
  • Garcia T, Lafuente D, Blanco J, Sanchez DJ, Sirvent JJ, Domingo JL, Gomez M. 2016. Oral subchronic exposure to silver nanoparticles in rats. Food Chem Toxicol 92:177–87.
  • Gopinath P, Gogoi SK, Sanpui P, Paul A, Chattopadhyay A, Ghosh SS. 2010. Signaling gene cascade in silver nanoparticle induced apoptosis. Colloids Surf B Biointerf 77:240–5.
  • Guo H, Zhang J, Boudreau M, Meng J, Yin JJ, Liu J, Xu H. 2016. Intravenous administration of silver nanoparticles causes organ toxicity through intracellular ROS-related loss of inter-endothelial junction. Part Fibre Toxicol 13:21.
  • Hamilton EI, Minski MJ. 1973. Abundance of the chemical elements in man’s diet and possible relations with environmental factors. Sci Total Environ 1:375–94.
  • Heydrnejad MS, Samani RJ, Aghaeivanda S. 2015. Toxic effects of silver nanoparticles on liver and some hematological parameters in male and female mice (Mus musculus). Biol Trace Elem Res 165:153–8.
  • Hissin PJ, Hilf R. 1976. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 74:214–26.
  • Hsin YH, Chen CF, Huang S, Shih TS, Lai PS, Chueh PJ. 2008. The apoptotic effect of nanosilver is mediated by a ROS- and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicol Lett 179:130–9.
  • Huang Y, Chen S, Bing X, Gao C, Wang T, Yuan B. 2011. Nanosilver migrated into food†simulating solutions from commercially available food fresh containers. Packag Technol Sci 24:291–7.
  • Jiang X, Miclaus T, Wang L, Foldbjerg R, Sutherland DS, Autrup H, et al. 2015. Fast intracellular dissolution and persistent cellular uptake of silver nanoparticles in CHO-K1 cells: implication for cytotoxicity. Nanotoxicology 9:181–9.
  • Jimenez-Lamana J, Laborda F, Bolea E, Abad-Alvaro I, Castillo JR, Bianga J, et al. 2014. An insight into silver nanoparticles bioavailability in rats. Metallomics 6:2242–9.
  • Khosho FK, Kaufmann RC, Amankwah KS. 1985. A simple and efficient method for obtaining urine samples from rats. Lab Anim Sci 35:513–4.
  • Kim NH, Kim KB, Kim DL, Kim SG, Choi KM, Baik SH, et al. 2004. Plasma and urinary vascular endothelial growth factor and diabetic nephropathy in Type 2 diabetes mellitus. Diabet Med 21:545–51.
  • Kim TH, Kim M, Park HS, Shin US, Gong MS, Kim HW. 2012. Size-dependent cellular toxicity of silver nanoparticles. J Biomed Mater Res A 100:1033–43.
  • Kim WY, Kim J, Park JD, Ryu HY, Yu IJ. 2009. Histological study of gender differences in accumulation of silver nanoparticles in kidneys of Fischer 344 rats. J Toxicol Environ Health A 72:1279–84.
  • Kim YS, Kim JS, Cho HS, Rha DS, Kim JM, Park JD, et al. 2008. Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Sprague–Dawley rats. Inhal Toxicol 20:575–83.
  • Kim YS, Song MY, Park JD, Song KS, Ryu HR, Chung YH, et al. 2010. Subchronic oral toxicity of silver nanoparticles. Part Fibre Toxicol 7:20.
  • Kovvuru P, Mancilla PE, Shirode AB, Murray TM, Begley TJ, Reliene R. 2015. Oral ingestion of silver nanoparticles induces genomic instability and DNA damage in multiple tissues. Nanotoxicology 9:162–71.
  • Kroemer G, El-Deiry WS, Golstein P, Peter ME, Vaux D, Vandenabeele P, et al. 2005. Classification of cell death: recommendations of the nomenclature committee on cell death. Cell Death Differ 12:1463–7.
  • Kurien BT, Scofield RH. 1999. Mouse urine collection using clear plastic wrap. Lab Anim 33:83–6.
  • Kwok KW, Dong W, Marinakos SM, Liu J, Chilkoti A, Wiesner MR, et al. 2016. Silver nanoparticle toxicity is related to coating materials and disruption of sodium concentration regulation. Nanotoxicology 10:1306–17.
  • Lankveld DP, Oomen AG, Krystek P, Neigh A, Troost-De Jong A, Noorlander CW, et al. 2010. The kinetics of the tissue distribution of silver nanoparticles of different sizes. Biomaterials 31:8350–61.
  • Li L, Wu H, Peijnenburg WJ, Van Gestel CA. 2015. Both released silver ions and particulate Ag contribute to the toxicity of AgNPs to earthworm Eisenia fetida. Nanotoxicology 9:792–801.
  • Liu Q, Qiu J, Liang M, Golinski J, Van Leyen K, Jung JE, et al. 2014. Akt and mTOR mediate programmed necrosis in neurons. Cell Death Dis 5:e1084.
  • Loeschner K, Hadrup N, Qvortrup K, Larsen A, Gao X, Vogel U, et al. 2011. Distribution of silver in rats following 28 days of repeated oral exposure to silver nanoparticles or silver acetate. Part Fibre Toxicol 8:18
  • Mcnamara CR, Ahuja R, Osafo-Addo AD, Barrows D, Kettenbach A, Skidan I, et al. 2013. Akt Regulates TNFalpha synthesis downstream of RIP1 kinase activation during necroptosis. PLoS One 8:e56576.
  • Meng J, Ji Y, Liu J, Cheng X, Guo H, Zhang W, et al. 2014. Using gold nanorods core/silver shell nanostructures as model material to probe biodistribution and toxic effects of silver nanoparticles in mice. Nanotoxicology 8:686–96.
  • Munger MA, Radwanski P, Hadlock GC, Stoddard G, Shaaban A, Falconer J, et al. 2014. In vivo human time-exposure study of orally dosed commercial silver nanoparticles. Nanomedicine 10:1–9.
  • Panacek A, Kolar M, Vecerova R, Prucek R, Soukupova J, Krystof V, et al. 2009. Antifungal activity of silver nanoparticles against Candida spp. Biomaterials 30:6333–40.
  • Park EJ, Bae E, Yi J, Kim Y, Choi K, Lee SH, et al. 2010. Repeated-dose toxicity and inflammatory responses in mice by oral administration of silver nanoparticles. Environ Toxicol Pharmacol 30:162–8.
  • Park K, Park EJ, Chun IK, Choi K, Lee SH, Yoon J, Lee BC. 2011. Bioavailability and toxicokinetics of citrate-coated silver nanoparticles in rats. Arch Pharm Res 34:153–8.
  • Peng W, Chen J, Jiang Y, Shou Z, Chen Y, Wang H. 2007. Non-invasive detection of acute renal allograft rejection by measurement of vascular endothelial growth factor in urine. J Int Med Res 35:442–9.
  • Rached E, Hoffmann D, Blumbach K, Weber K, Dekant W, Mally A. 2008. Evaluation of putative biomarkers of nephrotoxicity after exposure to ochratoxin a in vivo and in vitro. Toxicol Sci 103:371–81.
  • Recordati C, De Maglie M, Bianchessi S, Argentiere S, Cella C, Mattiello S, et al. 2016. Tissue distribution and acute toxicity of silver after single intravenous administration in mice: nano-specific and size-dependent effects. Part Fibre Toxicol 13:12.
  • Rinna A, Magdolenova Z, Hudecova A, Kruszewski M, Refsnes M, Dusinska M. 2015. Effect of silver nanoparticles on mitogen-activated protein kinases activation: role of reactive oxygen species and implication in DNA damage. Mutagenesis 30:59–66.
  • Rush JW, Quadrilatero J, Levy AS, Ford RJ. 2007. Chronic resveratrol enhances endothelium-dependent relaxation but does not alter eNOS levels in aorta of spontaneously hypertensive rats. Exp Biol Med (Maywood) 232:814–22.
  • Segerer S, Nelson PJ, Schlondorff D. 2000. Chemokines, chemokine receptors, and renal disease: from basic science to pathophysiologic and therapeutic studies. J Am Soc Nephrol 11:152–76.
  • Shibutani ST, Yoshimori T. 2014. A current perspective of autophagosome biogenesis. Cell Res 24:58–68.
  • Sondi I, Salopek-Sondi B. 2004. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for gram-negative bacteria. J Colloid Interface Sci 275:177–82.
  • Stensberg MC, Madangopal R, Yale G, Wei Q, Ochoa-Acuna H, Wei A, et al. 2014. Silver nanoparticle-specific mitotoxicity in Daphnia magna. Nanotoxicology 8:833–42.
  • Sun RW, Chen R, Chung NP, Ho CM, Lin CL, Che CM. 2005. Silver nanoparticles fabricated in Hepes buffer exhibit cytoprotective activities toward HIV-1 infected cells. Chem Commun (Camb) 40:5059–61.
  • Teodoro JS, Simoes AM, Duarte FV, Rolo AP, Murdoch RC, Hussain SM, Palmeira CM. 2011. Assessment of the toxicity of silver nanoparticles in vitro: a mitochondrial perspective. Toxicol in Vitro 25:664–70.
  • Toh HS, Batchelor-Mcauley C, Tschulik K, Compton RG. 2014. Chemical interactions between silver nanoparticles and thiols: a comparison of mercaptohexanol against cysteine. Sci China Chem 57:1199–210.
  • Toora BD, Rajagopal G. 2002. Measurement of creatinine by Jaffe’s reaction–determination of concentration of sodium hydroxide required for maximum color development in standard, urine and protein free filtrate of serum. Indian J Exp Biol 40:352–4.
  • Van Der Zande M, Vandebriel RJ, Van Doren E, Kramer E, Herrera Rivera Z, Serrano-Rojero CS, et al. 2012. Distribution, elimination, and toxicity of silver nanoparticles and silver ions in rats after 28-day oral exposure. ACS Nano 6:7427–42.
  • Vance ME, Kuiken T, Vejerano EP, Mcginnis SP, Hochella MF Jr, Rejeski D, Hull MS. 2015. Nanotechnology in the real world: Redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol 6:1769–80.
  • Vivarelli M, Massella L, Ruggiero B, Emma F. 2016. Minimal change disease. Clin J Am Soc Nephrol 12:332–45.
  • Von Goetz N, Fabricius L, Glaus R, Weitbrecht V, Gunther D, Hungerbuhler K. 2013. Migration of silver from commercial plastic food containers and implications for consumer exposure assessment. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 30:612–20.
  • Wu YT, Tan HL, Huang Q, Ong CN, Shen HM. 2009. Activation of the PI3K-Akt-mTOR signaling pathway promotes necrotic cell death via suppression of autophagy. Autophagy 5:824–34.
  • Xie L, Zheng X, Qin J, Chen Z, Jin Y, Ding W. 2006. Role of PI3-kinase/Akt signalling pathway in renal function and cell proliferation after renal ischaemia/reperfusion injury in mice. Nephrology (Carlton) 11:207–12.
  • Xie Y, Sakatsume M, Nishi S, Narita I, Arakawa M, Gejyo F. 2001. Expression, roles, receptors, and regulation of osteopontin in the kidney. Kidney Int 60:1645–57.
  • Xu L, Shi C, Shao A, Li X, Cheng X, Ding R, et al. 2015. Toxic responses in rat embryonic cells to silver nanoparticles and released silver ions as analyzed via gene expression profiles and transmission electron microscopy. Nanotoxicology 9:513–22.
  • Xu Y, Tang H, Liu JH, Wang H, Liu Y. 2013. Evaluation of the adjuvant effect of silver nanoparticles both in vitro and in vivo. Toxicol Lett 219:42–8.
  • 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 47:3268–74.
  • Zhou Y, Vaidya VS, Brown RP, Zhang J, Rosenzweig BA, Thompson KL, et al. 2008. Comparison of kidney injury molecule-1 and other nephrotoxicity biomarkers in urine and kidney following acute exposure to gentamicin, mercury, and chromium. Toxicol Sci 101:159–70.
  • Zong WX, Thompson CB. 2006. Necrotic death as a cell fate. Genes Dev 20:1–15.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.