508
Views
40
CrossRef citations to date
0
Altmetric
Original Article

Acute systemic exposure to silver-based nanoparticles induces hepatotoxicity and NLRP3-dependent inflammation

, , , , , , , , , , , & show all
Pages 1061-1074 | Received 07 May 2015, Accepted 02 Mar 2016, Published online: 14 Apr 2016

References

  • al-Ramadi BK, Fernandez-Cabezudo MJ, Ullah A, El-Hasasna H, Flavell RA. 2006. CD154 is essential for protective immunity in experimental salmonella infection: evidence for a dual role in innate and adaptive immune responses. J Immunol 176:496–506
  • al-Ramadi BK, Fernandez-Cabezudo MJ, El-Hasasna H, Al-Salam S, Bashir G, Chouaib S. 2009. Potent anti-tumor activity of systemically-administered IL2-expressing Salmonella correlates with decreased angiogenesis and enhanced tumor apoptosis. Clin Immunol 130:89–97
  • Arai Y, Miyayama T, Hirano S. 2014. Difference in the toxicity mechanism between ion and nanoparticle forms of silver in the mouse lung and in macrophages. Toxicology 328:84–92
  • Bergin IL, Wilding LA, Morishita M, Walacavage K, Ault AP, Axson JL, et al. 2016. Effects of particle size and coating on toxicologic parameters, fecal elimination kinetics and tissue distribution of acutely ingested silver nanoparticles in a mouse model. Nanotoxicology 10:352–60
  • Borm PJ. 2002. Particle toxicology: from coal mining to nanotechnology. Inhal Toxicol 14:311–24
  • Bugge A, Feng D, Everett LJ, Briggs ER, Mullican SE, Wang F, et al. 2012. Rev-erbα and Rev-erbβ coordinately protect the circadian clock and normal metabolic function. Genes Dev 26:657–67
  • Cabrero A, Laguna JC, Vazquez M. 2002. Peroxisome proliferator-activated receptors and the control of inflammation. Curr Drug Targets Inflamm Allergy 1:243–8
  • Carlson C, Hussain SM, Schrand AM, Braydich-Stolle LK, Hess KL, Jones RL, Schlager JJ. 2008. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B 112:13608–19
  • Cha K, Hong HW, Choi YG, Lee MJ, Park JH, Chae HK, et al. 2008. Comparison of acute responses of mice livers to short-term exposure to nano-sized or micro-sized silver particles. Biotechnol Lett 30:1893–9
  • Chen M, von Mikecz A. 2005. Formation of nucleoplasmic protein aggregates impairs nuclear function in response to SiO2 nanoparticles. Exp Cell Res 305:51–62
  • Coll RC, Robertson AA, Chae JJ, Higgins SC, Munoz-Planillo R, Inserra MC, et al. 2015. A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. Nat Med 21:248–55
  • Dos Santos CA, Seckler MM, Ingle AP, Gupta I, Galdiero S, Galdiero M, et al. 2014. Silver nanoparticles: therapeutical uses, toxicity, and safety issues. J Pharm Sci 103:1931–44
  • 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
  • Ehrchen JM, Sunderkotter C, Foell D, Vogl T, Roth J. 2009. The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J Leukocyte Biol 86:557–66
  • Fernandez-Cabezudo MJ, El-Kharrag R, Torab F, Bashir G, George JA, El-Taji H, al-Ramadi BK. 2013. Intravenous administration of manuka honey inhibits tumor growth and improves host survival when used in combination with chemotherapy in a melanoma mouse model. PLoS One 8:e55993
  • Fernandez-Cabezudo MJ, Ali SA, Ullah A, Hasan MY, Kosanovic M, Fahim MA, et al. 2007. Pronounced susceptibility to infection by Salmonella enterica serovar Typhimurium in mice chronically exposed to lead correlates with a shift to Th2-type immune responses. Toxicol Appl Pharmacol 218:215–26
  • 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
  • Gabizon A, Isacson R, Libson E, Kaufman B, Uziely B, Catane R, et al. 1994. Clinical studies of liposome-encapsulated doxorubicin. Acta Oncol 33:779–86
  • Getts DR, Terry RL, Getts MT, Deffrasnes C, Muller M, van Vreden C, et al. 2014. Therapeutic inflammatory monocyte modulation using immune-modifying microparticles. Sci Transl Med 6:219–17
  • Golan T, Grenader T, Ohana P, Amitay Y, Shmeeda H, La-Beck NM, et al. 2015. Pegylated liposomal mitomycin C prodrug enhances tolerance of mitomycin C: a phase 1 study in advanced solid tumor patients. Cancer Med 4:1472–83
  • Issac JM, Sarawathiamma D, Al-Ketbi MI, Azimullah S, Al-Ojali SM, Mohamed YA, et al. 2013. Differential outcome of infection with attenuated Salmonella in MyD88-deficient mice is dependent on the route of administration. Immunobiology 218:52–63
  • Johnston H, Pojana G, Zuin S, Jacobsen NR, Moller P, Loft S, et al. 2013. Engineered nanomaterial risk. Lessons learnt from completed nanotoxicology studies: potential solutions to current and future challenges. Crit Rev Toxicol 43:1–20
  • Jung HJ, Pak PJ, Park SH, Ju JE, Kim JS, Lee HS, Chung N. 2014. Silver wire amplifies the signaling mechanism for IL-1beta production more than silver submicroparticles in human monocytic THP-1 cells. PLoS One 9:e112256
  • Kaimala S, Mohamed YA, Nader N, Issac J, Elkord E, Chouaib S, et al. 2014. Salmonella-mediated tumor regression involves targeting of tumor myeloid suppressor cells causing a shift to M1-like phenotype and reduction in suppressive capacity. Cancer Immunol Immunother: CII 63:587–99
  • Kermanizadeh A, Pojana G, Gaiser BK, Birkedal R, Bilanicova D, Wallin H, et al. 2013. In vitro assessment of engineered nanomaterials using a hepatocyte cell line: cytotoxicity, pro-inflammatory cytokines and functional markers. Nanotoxicology 7:301–13
  • Kim JS, Kuk E, Yu KN, Kim JH, Park SJ, Lee HJ, et al. 2007. Antimicrobial effects of silver nanoparticles. Nanomedicine 3:95–101
  • Kim YS, Song MY, Park JD, Song KS, Ryu HR, Chung YH, et al. 2010. Subchronic oral toxicity of silver nanoparticles. Particle Fibre Toxicol 7:20
  • Korani M, Rezayat SM, Arbabi Bidgoli S. 2013. Sub-chronic dermal toxicity of silver nanoparticles in guinea pig: special emphasis to heart, bone and kidney toxicities. Iran J Pharm Res 12:511–19
  • Lamacchia C, Rodriguez E, Palmer G, Gabay C. 2013. Endogenous IL-1α is a chromatin-associated protein in mouse macrophages. Cytokine 63:135–44
  • Li Y, Bhalli JA, Ding W, Yan J, Pearce MG, Sadiq R, et al. 2014. Cytotoxicity and genotoxicity assessment of silver nanoparticles in mouse. Nanotoxicology 8:36–45
  • Markowitz J, Carson WE 3rd. 2013. Review of S100A9 biology and its role in cancer. Biochim Biophys Acta 1835:100–9
  • Mendez-Enriquez E, Melendez Y, Martinez F, Baay G, Huerta-Yepez S, Gonzalez-Bonilla C, et al. 2008. CDIP-2, a synthetic peptide derived from chemokine (C-C motif) ligand 13 (CCL13), ameliorates allergic airway inflammation. Clin Exp Immunol 152:354–63
  • Nel A, Xia T, Madler L, Li N. 2006. Toxic potential of materials at the nanolevel. Science 311:622–7
  • Nemmar A, Albarwani S, Beegam S, Yuvaraju P, Yasin J, Attoub S, Ali BH. 2014. Amorphous silica nanoparticles impair vascular homeostasis and induce systemic inflammation. Int J Nanomed 9:2779–89
  • Palecanda A, Kobzik L. 2001. Receptors for unopsonized particles: the role of alveolar macrophage scavenger receptors. Curr Mol Med 1:589–95
  • Park EJ, Choi K, Park K. 2011. Induction of inflammatory responses and gene expression by intratracheal instillation of silver nanoparticles in mice. Arch Pharm Res 34:299–307
  • Peeters PM, Perkins TN, Wouters EF, Mossman BT, Reynaert NL. 2013. Silica induces NLRP3 inflammasome activation in human lung epithelial cells. Particle Fibre Toxicol 10:3
  • Reisetter AC, Stebounova LV, Baltrusaitis J, Powers L, Gupta A, Grassian VH, Monick MM. 2011. Induction of inflammasome-dependent pyroptosis by carbon black nanoparticles. J Biol Chem 286:21844–52
  • Sadauskas E, Danscher G, Stoltenberg M, Vogel U, Larsen A, Wallin H. 2009. Protracted elimination of gold nanoparticles from mouse liver. Nanomedicine 5:162–9
  • Sadauskas E, Wallin H, Stoltenberg M, Vogel U, Doering P, Larsen A, Danscher G. 2007. Kupffer cells are central in the removal of nanoparticles from the organism. Particle Fibre Toxicol 4:10
  • Sarhan OM, Hussein RM. 2014. Effects of intraperitoneally injected silver nanoparticles on histological structures and blood parameters in the albino rat. Int J Nanomed 9:1505–17
  • Simard JC, Vallieres F, de Liz R, Lavastre V, Girard D. 2015. Silver nanoparticles induce degradation of the endoplasmic reticulum stress sensor activating transcription factor-6 leading to activation of the NLRP-3 inflammasome. J Biol Chem 290:5926–39
  • Simard JC, Cesaro A, Chapeton-Montes J, Tardif M, Antoine F, Girard D, Tessier PA. 2013. S100A8 and S100A9 induce cytokine expression and regulate the NLRP3 inflammasome via ROS-dependent activation of NF-κB(1.). PLoS One 8:e72138
  • Smulders S, Luyts K, Brabants G, Landuyt KV, Kirschhock C, Smolders E, et al. 2014. Toxicity of nanoparticles embedded in paints compared with pristine nanoparticles in mice. Toxicol Sci 141:132–40
  • Sun B, Wang X, Ji Z, Li R, Xia T. 2013. NLRP3 inflammasome activation induced by engineered nanomaterials. Small 9:1595–607
  • Sung JH, Ji JH, Park JD, Yoon JU, Kim DS, Jeon KS, et al. 2009. Subchronic inhalation toxicity of silver nanoparticles. Toxicol Sci 108:452–61
  • Sutterwala FS, Ogura Y, Szczepanik M, Lara-Tejero M, Lichtenberger GS, Grant EP, et al. 2006. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24:317–27
  • Trop M, Novak M, Rodl S, Hellbom B, Kroell W, Goessler W. 2006. Silver-coated dressing acticoat caused raised liver enzymes and argyria-like symptoms in burn patient. J Trauma 60:648–52
  • Valsami-Jones E, Lynch I. 2015. NANOSAFETY. How safe are nanomaterials? Science 350:388–9
  • Vogl T, Tenbrock K, Ludwig S, Leukert N, Ehrhardt C, van Zoelen MA, et al. 2007. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 13:1042–9
  • Wang X, Xia T, Duch MC, Ji Z, Zhang H, Li R, et al. 2012. Pluronic F108 coating decreases the lung fibrosis potential of multiwall carbon nanotubes by reducing lysosomal injury. Nano Lett 12:3050–61
  • Winter M, Beer HD, Hornung V, Kramer U, Schins RP, Forster I. 2011. Activation of the inflammasome by amorphous silica and TiO2 nanoparticles in murine dendritic cells. Nanotoxicology 5:326–40
  • Yang EJ, Kim S, Kim JS, Choi IH. 2012. Inflammasome formation and IL-1β release by human blood monocytes in response to silver nanoparticles. Biomaterials 33:6858–67
  • Yazdi AS, Guarda G, Riteau N, Drexler SK, Tardivel A, Couillin I, Tschopp J. 2010. Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1alpha and IL-1beta. Proc Natl Acad Sci USA 107:19449–54
  • Yimlamai D, Christodoulou C, Galli GG, Yanger K, Pepe-Mooney B, Gurung B, et al. 2014. Hippo pathway activity influences liver cell fate. Cell 157:1324–38
  • Youm YH, Nguyen KY, Grant RW, Goldberg EL, Bodogai M, Kim D, et al. 2015. The ketone metabolite β-hydroxybutyrate blocks NLRP3 inflammasome-mediated inflammatory disease. Nat Med 21:263–9

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.