Advertisement

Endoplasmic Reticulum (ER) Stress as a Mechanism for NP-Induced Toxicity

  • Loutfy H. MadkourEmail author
Chapter
Part of the Nanomedicine and Nanotoxicology book series (NANOMED)

Abstract

Understanding the mechanism of nanoparticle (NP)-induced toxicity is important for nanotoxicological and nanomedicinal studies. Endoplasmic reticulum (ER) is a crucial organelle involved in proper protein folding. High levels of misfolded proteins in the ER could lead to a condition termed as ER stress, which may ultimately influence the fate of cells and development of human diseases. In this chapter, we summarized studies about the effects of NP exposure on ER stress. A variety of NPs, especially metal-based NPs, could induce morphological changes of ER and activate ER stress pathway both in vivo and in vitro. In addition, modulation of ER stress by chemicals has been shown to alter the toxicity of NPs. These studies in combination suggested that ER stress could be the mechanism responsible for NP-induced toxicity. Meanwhile, nanomedicinal studies also used ER stress-inducing NPs or NPs loaded with ER stress inducer to selectively induce ER stress-mediated apoptosis in cancer cells for cancer therapy. In contrast, the alleviation of ER stress by NPs has also been shown as a strategy to cure metabolic diseases. In conclusion, exposure to NPs may modulate ER stress, which could be a target for future nanotoxicological and nanomedicinal studies. In summary, preliminary assessment of NPs-induced toxicity by monitoring the ER stress-signaling pathway gives novel assumptions toward empathizing the effects of NPs at the cellular level. The adverse effects associated with the exposure to NPs can be avoided by sensibly using these minerals within the safe dose. Therefore, the relationship between NP-induced ER stress and inflammation may still need further studies.

Keywords

Nanoparticle (NP) Endoplasmic reticulum (ER) stress Mechanism Nanotoxicology 

References

  1. Ahamed M, Karns M, Goodson M, Rowe J, Hussain SM, Schlager JJ et al (2008) DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicol Appl Pharmacol 233:404–410CrossRefGoogle Scholar
  2. Ahamed M, Alsalhi MS, Siddiqui MK (2010a) Silver nanoparticle applications and human health. Clin Chim Acta 411:1841–1848CrossRefGoogle Scholar
  3. Ahamed M, Posgai R, Gorey TJ, Nielsen M, Hussain SM, Rowe JJ (2010b) Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster. Toxicol Appl Pharmacol 242:263–269CrossRefGoogle Scholar
  4. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124:783–801CrossRefGoogle Scholar
  5. Anding AL, Chapman JS, Barnett DW, Curley RW Jr, Clagett-Dame M (2007) The unhydrolyzable fenretinide analogue 4-hydroxybenzylretinone induces the proapoptotic genes GADD153 (CHOP) and Bcl-2-binding component 3 (PUMA) and apoptosis that is caspase dependent and independent of the retinoic acid receptor. Cancer Res 67:6270–6277CrossRefGoogle Scholar
  6. Anspach L, Unger RE, Brochhausen C, Gibson MI, Klok HA, Kirkpatrick CJ, Freese C (2016) Impact of polymer-modified gold nanoparticles on brain endothelial cells: exclusion of endoplasmic reticulum stress as a potential risk factor. Nanotoxicology 10:1341–1350CrossRefGoogle Scholar
  7. Arami H, Khandhar A, Liggitt D, Krishnan KM (2015) In vivo delivery, pharmacokinetics, biodistribution and toxicity of iron oxide nanoparticles. Chem Soc Rev 44:8576–8607CrossRefGoogle Scholar
  8. Arora S, Jain J, Rajwade JM, Paknikar KM (2008) Cellular responses induced by silver nanoparticles: in vitro studies. Toxicol Lett 179:93–100CrossRefGoogle Scholar
  9. AshaRani PV, Low Kah Mun G, Hande MP, Valiyaveettil S (2009a) Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3:279–290CrossRefGoogle Scholar
  10. Asharani PV, Hande MP, Valiyaveettil S (2009b) Anti-proliferative activity of silver nanoparticles. BMC Cell Biol. 10:65CrossRefGoogle Scholar
  11. Asharani P, Sethu S, Lim HK, Balaji G, Valiyaveettil S, Hande MP (2012) Differential regulation of intracellular factors mediating cell cycle, DNA repair and inflammation following exposure to silver nanoparticles in human cells. Genome Integr 3:2CrossRefGoogle Scholar
  12. Barone MV, Crozat A, Tabaee A, Philipson L, Ron D (1994) CHOP (GADD153) and its oncogenic variant, TLS-CHOP, have opposing effects on the induction of G1/S arrest. Genes Dev 8:453–464CrossRefGoogle Scholar
  13. Bidgoli SA, Mahdavi M, Rezayat SM, Korani M, Amani A, Ziarati P (2013) Toxicity assessment of nanosilver wound dressing in wistar rat. Acta Med Iran 51:203–208Google Scholar
  14. Blaser SA, Scheringer M, Macleod M, Hungerbuhler K (2008) Estimation of cumulative aquatic exposure and risk due to silver: contribution of nano-functionalized plastics and textiles. Sci Total Environ 390:396–409CrossRefGoogle Scholar
  15. Boonstra J, Post JA (2004) Molecular events associated with reactive oxygen species and cell cycle progression in mammalian cells. Gene 337:1–13CrossRefGoogle Scholar
  16. Braydich-Stolle L, Hussain S, Schlager JJ, Hofmann MC (2005) In vitro cytotoxicity of nanoparticles in mammalian germline stem cells. Toxicol Sci 88:412–419CrossRefGoogle Scholar
  17. Bryant CD, Peck, DL (eds) (2006) 21st century sociology: a reference handbook. Sage Publications. https://books.google.com.sa
  18. Buzea C, Pacheco II, Robbie K (2007) Nanomaterials and nanoparticles: sources and toxicity. Biointerphases 2(4):MR17–MR71CrossRefGoogle Scholar
  19. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP et al (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92–96CrossRefGoogle Scholar
  20. Cao SS, Kaufman RJ (2014) Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid Redox Signal 21:396–413CrossRefGoogle Scholar
  21. Cao Y, Gong Y, Liu L, Zhou Y, Fang X, Zhang C, Li Y, Li J (2017) The use of human umbilical vein endothelial cells (HUVECs) as an in vitro model to assess the toxicity of nanoparticles to endothelium: a review. J Appl Toxicol 37(12):1359–1369.  https://doi.org/10.1002/jat.3470 Epub 2017 Apr 6CrossRefGoogle Scholar
  22. Carlson C, Hussain SM, Schrand AM, Hess KL, Jones RL, Schlager JJ (2008) Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B 112:13608–13619CrossRefGoogle Scholar
  23. Caron WP, Morgan KP, Zamboni BA, Zamboni WC (2013) A review of study designs and outcomes of phase I clinical studies of nanoparticle agents compared with small-molecule anticancer agents. Clin Cancer Res 19:3309–3315CrossRefGoogle Scholar
  24. Chen X, Schluesener HJ (2008) Nanosilver: a nanoproduct in medical application. Toxicol Lett 176:1–12CrossRefGoogle Scholar
  25. Chen R, Huo L, Shi X, Bai R, Zhang Z, Zhao Y, Chang Y, Chen C (2014) Endoplasmic reticulum stress induced by zinc oxide nanoparticles is an earlier biomarker for nanotoxicological evaluation. ACS Nano 8:2562–2574CrossRefGoogle Scholar
  26. Chen R, Ling D, Zhao L, Wang S, Liu Y, Bai R, Baik S, Zhao Y, Chen C, Hyeon T (2015) Parallel comparative studies on mouse toxicity of oxide nanoparticle- and gadolinium-based T1 MRI contrast agents. ACS Nano 9:12425–12435CrossRefGoogle Scholar
  27. Chen G, Shen Y, Li X, Jiang Q, Cheng S, Gu Y, Liu L, Cao Y (2017) The endoplasmic reticulum stress inducer thapsigargin enhances the toxicity of ZnO nanoparticles to macrophages and macrophage-endothelial co-culture. Environ Toxicol Pharmacol 50:103–110CrossRefGoogle Scholar
  28. Chistiakov DA, Sobenin IA, Orekhov AN, Bobryshev YV (2014) Role of endoplasmic reticulum stress in atherosclerosis and diabetic macrovascular complications. Biomed Res Int 2014:610140Google Scholar
  29. Chiu HW, Xia T, Lee YH, Chen CW, Tsai JC, Wang YJ (2015) Cationic polystyrene nanospheres induce autophagic cell death through the induction of endoplasmic reticulum stress. NANO 7:736–746Google Scholar
  30. Choi JE, Kim S, Ahn JH, Youn P, Kang JS, Park K, Yi J, Ryu DY (2010) Induction of oxidative stress and apoptosis by silver nanoparticles in the liver of adult zebrafish. Aquat Toxicol 100(2):151–159CrossRefGoogle Scholar
  31. Choi YJ, Gurunathan S, Kim D, Jang HS, Park WJ, Cho SG, Park C, Song H, Seo HG, Kim JH (2016) Rapamycin ameliorates chitosan nanoparticle-induced developmental defects of preimplantation embryos in mice. Oncotarget 7:74658–74677Google Scholar
  32. Chopra I (2007) The increasing use of silver-based products as antimicrobial agents: a useful development or a cause for concern? J Antimicrob Chemother 59:587–590CrossRefGoogle Scholar
  33. Christen V, Fent K (2012) Silica nanoparticles and silver-doped silica nanoparticles induce endoplasmatic reticulum stress response and alter cytochrome P4501A activity. Chemosphere 87:423–434CrossRefGoogle Scholar
  34. Christen V, Treves S, Duong FH, Heim MH (2007) Activation of endoplasmic reticulum stress response by hepatitis viruses up-regulates protein phosphatase 2A. Hepatology 46:558–565CrossRefGoogle Scholar
  35. Christen V, Capelle M, Fent K (2013) Silver nanoparticles induce endoplasmatic reticulum stress response in zebrafish. Toxicol Appl Pharmacol 272:519–528CrossRefGoogle Scholar
  36. Cohen MS, Stern JM, Vanni AJ, Kelley RS, Baumgart E, Field D et al (2007) In vitro analysis of a nanocrystalline silver-coated surgical mesh. Surg Infect (Larchmt) 8:397–403CrossRefGoogle Scholar
  37. Cullinan SB, Diehl JA (2006) Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol 38:317–332CrossRefGoogle Scholar
  38. Dabbaghi M, Kazemi OR, Hashemi K, Afkhami GA (2018) evaluating polyethyleneimine/DNA nanoparticles-mediated damage to cellular organelles using endoplasmic reticulum stress profile. Artif Cells Nanomed Biotechnol 46(1):192–199.  https://doi.org/10.1080/21691401.2017.1304406CrossRefGoogle Scholar
  39. Dara L, Ji C, Kaplowitz N (2011) The contribution of endoplasmic reticulum stress to liver disease. Hepatology 53:1752–1763CrossRefGoogle Scholar
  40. de Lima R, Seabra AB, Duran N (2012) Silver nanoparticles: a brief review of cytotoxicity and genotoxicity of chemically and biogenically synthesized nanoparticles. J Appl Toxicol 32:867–879CrossRefGoogle Scholar
  41. de Virgilio M, Kitzmuller C, Schwaiger E, Klein M, Kreibich G, Ivessa NE (1999) Degradation of a short-lived glycoprotein from the lumen of the endoplasmic reticulum: the role of N-linked glycans and the unfolded protein response. Mol Biol Cell 10:4059–4073CrossRefGoogle Scholar
  42. De Volder MF, Tawfick SH, Baughman RH, Hart AJ (2013) Carbon nanotubes: present and future commercial applications. Science 339:535–539CrossRefGoogle Scholar
  43. Dhawan A, Sharma V (2010) Toxicity assessment of nanomaterials: methods and challenges. Anal Bioanal Chem 398:589–605CrossRefGoogle Scholar
  44. Dhawan A, Pandey A, Sharma V (2011) Toxicity assessment of engineered nanomaterials: resolving the challenges. J Biomed Nanotechnol 7:6–7CrossRefGoogle Scholar
  45. 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 44:8337–8342CrossRefGoogle Scholar
  46. Erbis S, Ok Z, Isaacs JA, Benneyan JC, Kamarthi S (2016) Review of research trends and methods in nano environmental, health, and safety risk analysis. Risk Anal 36:1644–1665CrossRefGoogle Scholar
  47. Fadeel B, Kagan VE (2003) Apoptosis and macrophage clearance of neutrophils: regulation by reactive oxygen species. Redox Rep 8(3):143–150CrossRefGoogle Scholar
  48. Farkas J, Christian P, Urrea JA, Roos N, Hassellöv M, Tollefsen KE, Thomas KV (2010) Effects of silver and gold nanoparticles on rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat Toxicol 96(1):44–52CrossRefGoogle Scholar
  49. 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 190:156–162CrossRefGoogle Scholar
  50. Foldbjerg R, Dang DA, Autrup H (2011) Cytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549. Arch Toxicol 85:743–750CrossRefGoogle Scholar
  51. Friedman AD (1996) GADD153/CHOP a DNA damage-inducible protein, reduced CAAT/enhancer binding protein activities and increased apoptosis in 32D c13 myeloid cells. Cancer Res 56:3250–3256Google Scholar
  52. Fubini B, Hubbard A (2003) Reactive oxygen species (ROS) and reactive nitrogen species (RNS) generation by silica in inflammation and fibrosis. Free Radic Biol Med 34(12):1507–1516CrossRefGoogle Scholar
  53. Gagné F, André C, Skirrow R, Gélinas M, Auclair J, van Aggelen G, Turcotte P, Gagnon C (2012) Toxicity of silver nanoparticles to rainbow trout: a toxicogenomic approach. Chemosphere 89(5):615–622CrossRefGoogle Scholar
  54. Gaiser BK, Hirn S, Kermanizadeh A, Kanase N, Fytianos K, Wenk A, Haberl N, Brunelli A, Kreyling WG, Stone V (2013) Effects of silver nanoparticles on the liver and hepatocytes in vitro. Toxicol Sci 131(2):537–547CrossRefGoogle Scholar
  55. George S, Lin S, Ji Z, Thomas CR, Li L, Mecklenburg M, Meng H, Wang X, Zhang H, Xia T, Hohman JN, Lin S, Zink JI, Weiss PS, Nel AE (2012) Surface defects on plate-shaped silver nanoparticles contribute to its hazard potential in a fish gill cell line and zebrafish embryos. ACS Nano 6(5):3745–3759CrossRefGoogle Scholar
  56. Gopinath P, Gogoi SK, Sanpui P, Paul A, Chattopadhyay A, Ghosh SS (2010) Signaling gene cascade in silver nanoparticle induced apoptosis. Colloids Surf B Biointerfaces 77:240–245CrossRefGoogle Scholar
  57. Gotoh T, Oyadomari S, Mori K, Mori M (2002) Nitric oxide-induced apoptosis in RAW 264.7 macrophages are mediated by endoplasmic reticulum stress pathway involving ATF6 and CHOP. J Biol Chem 277:12343–12350CrossRefGoogle Scholar
  58. Greulich C, Diendorf J, Gessmann J, Simon T, Habijan T, Eggeler G, Schildhauer TA, Epple M, Koller M (2011a) Cell type-specific responses of peripheral blood mononuclear cells to silver nanoparticles. Acta Biomater 7:3505–3514CrossRefGoogle Scholar
  59. Greulich C, Diendorf J, Simon T, Eggeler G, Epple M, Koller M (2011b) Uptake and intracellular distribution of silver nanoparticles in human mesenchymal stem cells. Acta Biomater 7:347–354CrossRefGoogle Scholar
  60. Griffitt RJ, Luo J, Gao J, Bonzongo JC, Barber DS (2008) Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 9:1972–1978CrossRefGoogle Scholar
  61. Griffitt RJ, Hyndman K, Denslow ND, Barber DS (2009) Comparison of molecular and histological changes in zebrafish gills exposed to metallic nanoparticles. Toxicol Sci 107(2):404–415CrossRefGoogle Scholar
  62. Gu Y, Cheng S, Chen G, Shen Y, Li X, Jiang Q, Li J, Cao Y (2017) The effects of endoplasmic reticulum stress inducer thapsigargin on the toxicity of ZnO or TiO2 nanoparticles to human endothelial cells. Toxicol Mech Methods 27:191–200CrossRefGoogle Scholar
  63. Gunduz N, Ceylan H, Guler MO, Tekinay AB (2017) Intracellular accumulation of gold nanoparticles leads to inhibition of macropinocytosis to reduce the endoplasmic reticulum stress. Sci Rep 7:40493CrossRefGoogle Scholar
  64. Hackenberg S, Scherzed A, Kessler M, Hummel S, Technau A, Froelich K, Ginzkey C, Koehler C, Hagen R, Kleinsasser N (2011) Silver nanoparticles: Evaluation of DNA damage, toxicity and functional impairment in human mesenchymal stem cells. Toxicol Lett 201:27–33CrossRefGoogle Scholar
  65. Harding HP, Calfon M, Urano F, Novoa I, Ron D (2002) Transcriptional and translational control in the Mammalian unfolded protein response. Annu Rev Cell Dev Biol 18:575–599CrossRefGoogle Scholar
  66. He X, Young S, Schwegler-Berry D, Chisholm WP, Fernback JE, Ma Q (2011) Multiwalled carbon nanotubes induce a fibrogenic response by stimulating reactive oxygen species production, activating NF-κB signaling, and promoting fibroblastto-myofibroblast transformation. Chem Res Toxicol 24(12):2237–2248CrossRefGoogle Scholar
  67. Hetz C (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13:89–102CrossRefGoogle Scholar
  68. Hetz C, Bernasconi P, Fisher J, Lee AH, Bassik MC, Antonsson B et al (2006) Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 312:572–576CrossRefGoogle Scholar
  69. Hirsch I, Weiwad M, Prell E, Ferrari DM (2014) ERp29 deficiency affects sensitivity to apoptosis via impairment of the ATF6-CHOP pathway of stress response. Apoptosis 19:801–815CrossRefGoogle Scholar
  70. Hoseinzadeh E, Makhdoumi P, Taha P, Stelling J, Hossini H, Kamal MA, Ashraf GM (2017) A Review on nano-antimicrobials: metal nanoparticles. Methods Mech Curr Drug Metab 18(2):120–128.  https://doi.org/10.2174/1389200217666161201111146CrossRefGoogle Scholar
  71. Hou CC, Tsai TL, Su WP, Hsieh HP, Yeh CS, Shieh DB, Su WC (2013) Pronounced induction of endoplasmic reticulum stress and tumor suppression by surfactant-free poly (lactic-co-glycolic acid) nanoparticles via modulation of the PI3K signaling pathway. Int J Nanomedicine 8:2689–2707CrossRefGoogle Scholar
  72. Hsin YH, Chen CF, Huang S, Shih TS, Lai PS, Chueh PJ (2008a) The apoptotic effect of nanosilver is mediated by a ROS- and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicol Lett 179:130–139CrossRefGoogle Scholar
  73. Hsin Y, Chen C, Huang S, Shih T, Lai P, Chueh PJ (2008b) The apoptotic effect of nanosilver is mediated by a ROS- and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicol Lett 179(3):130–139CrossRefGoogle Scholar
  74. Hu Y, Mao K, Zeng Y, Chen S, Tao Z, Yang C, Sun S, Wu X, Meng G, Sun B (2010) Tripartite-motif protein 30 negatively regulates NLRP3 inflammasome activation by modulating reactive oxygen species production. J Immunol 185(12):7699–7705CrossRefGoogle Scholar
  75. Hudecova A, Kusznierewicz B, Runden-Pran E, Magdolenova Z, Hasplova K, Rinna A et al (2012a) Silver nanoparticles induce premutagenic DNA oxidation that can be prevented by phytochemicals from Gentiana asclepiadea. Mutagenesis 27:759–769CrossRefGoogle Scholar
  76. Hudecova A, Kusznierewicz B, Hašplova K, Huk A, Magdolenova Z, Miadokova E, Galova E, Dušinska M (2012b) Gentiana asclepiadea exerts antioxidant activity and enhances DNA repair of hydrogen peroxide and silver nanoparticles-induced DNA damage. Food Chem Toxicol 50:3352–3359CrossRefGoogle Scholar
  77. Huo L, Chen R, Zhao L, Shi X, Bai R, Long D, Chen F, Zhao Y, Chang YZ, Chen C (2015) Silver nanoparticles activate endoplasmic reticulum stress signaling pathway in cell and mouse models: the role in toxicity evaluation. Biomaterials 61:307–315CrossRefGoogle Scholar
  78. Hussain SM, Hess KL, Gearhart JM, Geiss KT, Schlager JJ (2005) In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol Vitr 19:975–983CrossRefGoogle Scholar
  79. Hussain SM, Javorina AK, Schrand AM, Duhart HM, Ali SF, Schlager JJ (2006) The interaction of manganese nanoparticles with PC-12 cells induces dopamine depletion. Toxicol Sci 92:456–463CrossRefGoogle Scholar
  80. Jena P, Mohanty S, Mallick R, Jacob B, Sonawane A (2012) Toxicity and antibacterial assessment of chitosan-coated silver nanoparticles on human pathogens and macrophage cells. Int J Nanomed 7:1805–1818Google Scholar
  81. Jeng HA, Swanson J (2006) Toxicity of metal oxide nanoparticles in mammalian cells. J Environ Sci Health A 41(12):2699–2711CrossRefGoogle Scholar
  82. Jiang HY, Wek RC (2005) Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J Biol Chem 280:14189–14202CrossRefGoogle Scholar
  83. Jiang X, Foldbjerg R, Miclaus T, Wang L, Singh R, Hayashi Y et al (2013) Multiplatform genotoxicity analysis of silver nanoparticles in the model cell line CHO-K1. Toxicol Lett 222:55–63CrossRefGoogle Scholar
  84. 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(2):181–189CrossRefGoogle Scholar
  85. Ju-Nam Y, Lead JR (2008) Manufactured nanoparticles: an overview of their chemistry, interactions and potential environmental implications. Sci Total Environ 400:396–414CrossRefGoogle Scholar
  86. Jung WK, Kim SH, Koo HC, Shin S, Kim JM, Park YK, Hwang SY, Yang H, Park YH (2007) Antifungal activity of the silver ion against contaminated fabric. Mycoses 50:265–269CrossRefGoogle Scholar
  87. Jung WK, Koo HC, Kim KW, Shin S, Kim SH, Park YH (2008) Antibacterial activity and mechanism of action of the silver ion in staphylococcus aureus and Escherichia coli. Appl Environ Microbiol 74:2171–2178CrossRefGoogle Scholar
  88. Kägi RA, Voegelin B, Sinnet S, Zuleeg H, Hagendorfer BM, Siegrist HR (2011) Behaviour of metallic silver nanoparticles in a pilot wastewater treatment plant. Environ Sci Technol 45:3902–3908CrossRefGoogle Scholar
  89. Kang JS, Yum YN, Kim JH, Song H, Jeong J, Lim YT et al (2009) Induction of DNA damage in L5178 cells treated with gold nanoparticle. Biomol Ther 17:92–97CrossRefGoogle Scholar
  90. Karthikeyan B, Arun A, Harini L, Sundar K, Kathiresan T (2016) Role of ZnS nanoparticles on endoplasmic reticulum stress-mediated apoptosis in retinal pigment epithelial cells. Biol Trace Elem Res 170:390–400CrossRefGoogle Scholar
  91. Kaufman RJ, Scheuner D, Schroder M, Shen X, Lee K, Liu CY et al (2002) The unfolded protein response in nutrient sensing and differentiation. Nat Rev Mol Cell Biol 3:411–421CrossRefGoogle Scholar
  92. Kawata K, Osawa M, Okabe S (2009) In vitro toxicity of silver nanoparticles at noncytotoxic doses to HepG2 human hepatoma cells. Environ Sci Technol 43:6046–6051CrossRefGoogle Scholar
  93. Kim HJ, Yum KS, Sung JH, Rhie DJ, Kim MJ, Min DS et al (2004) Epigallocatechin-3-gallate increases intracellular [Ca2+] in U87 cells mainly by influx of extracellular Ca2+ and partly by release of intracellular stores. Naunyn Schmiedebergs Arch Pharmacol 369:260–267CrossRefGoogle Scholar
  94. Kim JS, Kuk E, Yu KN, Kim JH, Park SJ, Lee HJ et al (2007) Antimicrobial effects of silver nanoparticles. Nanomed Nanotechnol Biol Med 3:95–101CrossRefGoogle Scholar
  95. Kim I, Xu W, Reed JC (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7:1013–1030CrossRefGoogle Scholar
  96. Kim S, Choi JE, Choi J, Chung KH, Park K, Yi J, Ryu DY (2009) Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol Vitr 23:1076–1084CrossRefGoogle Scholar
  97. Kim HR, Kim MJ, Lee SY, Oh SM, Chung KH (2011) Genotoxic effects of silver nanoparticles stimulated by oxidative stress in human normal bronchial epithelial (BEAS-2B) cells. Mutat Res 726(2):129–135CrossRefGoogle Scholar
  98. 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(4):1033–1043CrossRefGoogle Scholar
  99. Kim KT, Truong L, Wehmas L, Tanguay RL (2013) Silver nanoparticle toxicity in the embryonic zebrafish is governed by particle dispersion and ionic environment. Nanotechnology 24(11):115101CrossRefGoogle Scholar
  100. King A, Gottlieb E, Brooks DG, Murphy MP, Dunaief JL (2004) Mitochondria-derived reactive oxygen species mediate blue light-induced death of retinal pigment epithelial cells. Photochem Photobiol 79:470–475CrossRefGoogle Scholar
  101. Kittler S, Greulich C, Diendorf J, Koller M, Epple M (2010) Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions. Chem Mater 22:4548–4554CrossRefGoogle Scholar
  102. Kozuka C, Shimizu-Okabe C, Takayama C, Nakano K, Morinaga H, Kinjo A, Fukuda K, Kamei A, Yasuoka A, Kondo T, Abe K, Egashira K, Masuzaki H (2017) Marked augmentation of PLGA nanoparticle-induced metabolically beneficial impact of gamma-oryzanol on fuel dyshomeostasis in genetically obese-diabetic ob/ob mice. Drug Deliv 24:558–568CrossRefGoogle Scholar
  103. Kruszewski M, Brzoska K, Brunborg G, Asare N, Dobrzyńska H, Dusinska M et al (2011) Toxicity of silver nanomaterials in higher eukaryotes. Adv Mol Toxicol 5:179–218CrossRefGoogle Scholar
  104. Kuang H, Yang P, Yang L, Aguilar ZP, Xu H (2016) Size dependent effect of ZnO nanoparticles on endoplasmic reticulum stress signaling pathway in murine liver. J Hazard Mater 317:119–126CrossRefGoogle Scholar
  105. Kulthong K, Maniratanachote R, Kobayashi Y, Fukami T, Yokoi T (2012) Effects of silver nanoparticles on rat hepatic cytochrome P450 enzyme activity. Xenobiotica 42(9):854–862CrossRefGoogle Scholar
  106. Kwok KW, Auffan M, Badireddy AR, Nelson CM, Wiesner MR, Chilkoti A, Liu J, Marinakos SM, Hinton DE (2012) Uptake of silver nanoparticles and toxicity to early life stages of Japanese medaka (Oryzias latipes): effect of coating materials. Aquat Toxicol 120–121:59–66CrossRefGoogle Scholar
  107. Kwon JT, Hwang SK, Jin H, Kim DS, Minai-Tehrani A, Yoon HJ, Choi M, Yoon TJ, Han DY, Kang YW, Yoon BI, Lee JK, Cho MH (2008) Body distribution of inhaled fluorescent magnetic nanoparticles in the mice. J Occup Health 50:1–6CrossRefGoogle Scholar
  108. Lankoff A, Sandberg WJ, Wegierek-Ciuk A, Lisowska H, Refsnes M, Sartowska B, Schwarze PE, Meczynska-Wielgosz S, Wojewodzka M, Kruszewski M (2012) The effect of agglomeration state of silver and titanium dioxide nanoparticles on cellular response of Hep G2, A549 and THP-1 cells. Toxicol Lett 208:197–213CrossRefGoogle Scholar
  109. Lee HY, Park HK, Lee YM, Kim K, Park SB (2007) A practical procedure for producing silver nanocoated fabric and its antibacterial evaluation for biomedical applications. Chem Commun (Camb) 28:2959–2961CrossRefGoogle Scholar
  110. Lewinski N, Colvin V, Drezek R (2008) Cytotoxicity of nanoparticles. Small 4:26–49CrossRefGoogle Scholar
  111. Li J, Zhu JJ (2013) Quantum dots for fluorescent biosensing and bio-imaging applications. Analyst 138:2506–2515CrossRefGoogle Scholar
  112. Li N, Xia T, Nel AE (2008) The role of oxidative stress in ambient particulate matter-induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radic Biol Med 44(9):1689–1699CrossRefGoogle Scholar
  113. Li JJ, Muralikrishnan S, Ng CT, Yung LY, Bay BH (2010) Nanoparticle-induced pulmonary toxicity. Exp Biol Med 235(9):1025–1033CrossRefGoogle Scholar
  114. Li J, Zhou Y, Zhang W, Bao C, Xie Z (2017) Relief of oxidative stress and cardiomyocyte apoptosis by using curcumin nanoparticles. Colloids Surf B Biointerfaces 153:174–182CrossRefGoogle Scholar
  115. Lim JH, Park JW, Kim SH, Choi YH, Choi KS, Kwon TK (2008) Rottlerin induces pro-apoptotic endoplasmic reticulum stress through the protein kinase C-delta-independent pathway in human colon cancer cells. Apoptosis 13:1378–1385CrossRefGoogle Scholar
  116. Lim ZZ, Li JE, Ng CT, Yung LY, Bay BH (2011) Gold nanoparticles in cancer therapy. Acta Pharmacol Sin 32:983–990CrossRefGoogle Scholar
  117. Lin WC, Chuang YC, Chang YS, Lai MD, Teng YN, Su IJ (2012) Endoplasmic reticulum stress stimulates p53 expression through NF-κB activation. PLoS One 7:e39120CrossRefGoogle Scholar
  118. Liu J, Sonshine DA, Shervani S, Hurt RH (2010) Controlled release of biologically active silver from nanosilver surfaces. ACS Nano 4:6903–6913CrossRefGoogle Scholar
  119. Liu Z, Lv Y, Zhao N, Guan G, Wang J (2015) Protein kinase R-like ER kinase and its role in endoplasmic reticulum stress-decided cell fate. Cell Death Dis 6:e1822CrossRefGoogle Scholar
  120. Locker N, Easton LE, Lukavsky PJ (2007) HCV and CSFV IRES domain II mediate eIF2 release during 80S ribosome assembly. EMBO J 26:795–805CrossRefGoogle Scholar
  121. Logue SE, Cleary P, Saveljeva S, Samali A (2013) New directions in ER stress-induced cell death. Apoptosis 18:537–546CrossRefGoogle Scholar
  122. Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, Dawson KA (2008) Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. Proc Natl Acad Sci USA 105:14265–14270CrossRefGoogle Scholar
  123. Luo YH, Wu SB, Wei YH, Chen YC, Tsai MH, Ho CC, Lin SY, Yang CS, Lin P (2013) Cadmium-based quantum dot induced autophagy formation for cell survival via oxidative stress. Chem Res Toxicol 26:662–673CrossRefGoogle Scholar
  124. Luo YH, Chang LW, Lin P (2015) Metal-based nanoparticles and the immune system: activation, inflammation, and potential applications. Biomed Res Int 2015:143720Google Scholar
  125. Malysheva A, Lombi E, Voelcker NH (2015) Bridging the divide between human and environmental nanotoxicology. Nat Nanotechnol 10:835–844CrossRefGoogle Scholar
  126. Manna P, Ghosh M, Ghosh J, Das J, Sil PC (2012) Contribution of nano-copper particles to in vivo liver dysfunction and cellular damage: role of IB/NF-κB, MAPKs and mitochondrial signal. Nanotoxicology 6(1):1–21CrossRefGoogle Scholar
  127. Marano F, Hussain S, Rodrigues-Lima F, Baeza-Squiban A, Boland S (2011) Nanoparticles: molecular targets and cell signalling. Arch Toxicol 85(7):733–741CrossRefGoogle Scholar
  128. Martincic M, Tobias G (2015) Filled carbon nanotubes in biomedical imaging and drug delivery. Expert Opin Drug Deliv 12:563–581CrossRefGoogle Scholar
  129. Matsumoto M, Minami M, Takeda K, Sakao Y, Akira S (1996) Ectopic expression of CHOP (GADD153) induces apoptosis in M1 myeloblastic leukemia cells. FEBS Lett 395:143–147CrossRefGoogle Scholar
  130. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21:1249–1259CrossRefGoogle Scholar
  131. Mei N, Zhang Y, Chen Y, Guo X, Ding W, Ali SF, Biris AS, Rice P, Moore MM, Chen T (2012) Silver nanoparticle-induced mutations and oxidative stress in mouse lymphoma cells. Environ Mol Mutagen 53(6):409–419CrossRefGoogle Scholar
  132. Menu P, Mayor A, Zhou R, Tardivel A, Ichijo H, Mori K, Tschopp J (2012) ER stress activates the NLRP3 inflammasome via an UPR-independent pathway. Cell Death Dis 3:e261CrossRefGoogle Scholar
  133. Mishra AR, Zheng J, Tang X, Goering PL (2016) Silver nanoparticle-induced autophagic-lysosomal disruption and NLRP3-inflammasome activation in HepG2 cells is size-dependent. Toxicol Sci 150:473–487CrossRefGoogle Scholar
  134. Mitrano DM, Rimmele E, Wichser A, Erni R, Height M, Nowack B (2014) Presence of nanoparticles in wash water from conventional silver and nano-silver textiles. ACS Nano 8:7208–7219CrossRefGoogle Scholar
  135. Miura N, Shinohara Y (2009) Cytotoxic effect and apoptosis induction by silver nanoparticles in HeLa cells. Biochem Biophys Res Commun 390(3):733–737CrossRefGoogle Scholar
  136. Moenner M, Pluquet O, Bouchecareilh M, Chevet E (2007) Integrated endoplasmic reticulum stress responses in cancer. Cancer Res 67:10631–10634CrossRefGoogle Scholar
  137. Mohamud R, Xiang SD, Selomulya C, Rolland JM, O’Hehir RE, Hardy CL, Plebanski M (2014) The effects of engineered nanoparticles on pulmonary immune homeostasis. Drug Metab Rev 46:176–190CrossRefGoogle Scholar
  138. Monopoli MP, Bombelli FB, Dawson KA (2011a) Nanobiotechnology: nanoparticle coronas take shape. Nat Nanotechnol 6:11–12CrossRefGoogle Scholar
  139. Monopoli MP, Walczyk D, Campbell A, Elia G, Lynch I, Baldelli BF, Dawson KA (2011b) Physical chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. J Am Chem Soc 133(8):2525–2534CrossRefGoogle Scholar
  140. Mori K (2000) Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 101:451–454CrossRefGoogle Scholar
  141. Naqvi S, Samim M, Abdin MZ et al (2010) Concentrationdependent toxicity of iron oxide nanoparticles mediated by increased oxidative stress. Int J Nanomed 5(1):983–989CrossRefGoogle Scholar
  142. Nel A, Xia T, Madler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627CrossRefGoogle Scholar
  143. Ng CT, Yong LQ, Hande MP, Ong CN, Yu LE, Bay BH, Baeg GH (2017) Zinc oxide nanoparticles exhibit cytotoxicity and genotoxicity through oxidative stress responses in human lung fibroblasts and drosophila Melanogaster. Int J Nanomedicine 12:1621–1637CrossRefGoogle Scholar
  144. Niu J, Azfer A, Rogers M, Wang X, Kolattukudy PE (2007) Cardioprotective effects of cerium oxide nanoparticles in a transgenic murine model of cardiomyopathy. Cardiovasc Res 73:549–559CrossRefGoogle Scholar
  145. Noel C, Simard JC, Girard D (2016) Gold nanoparticles induce apoptosis, endoplasmic reticulum stress events and cleavage of cytoskeletal proteins in human neutrophils. Toxicol Vitr 31:12–22CrossRefGoogle Scholar
  146. Nohynek GJ, Dufour EK (2012) Nano-sized cosmetic formulations or solid nanoparticles in sunscreens: a risk to human health? Arch Toxicol 86:1063–1075CrossRefGoogle Scholar
  147. Nowack B, Krug HF, Height M (2011) 120 years of nanosilver history: implications for policy makers. Environ Sci Technol 45:1177–11783CrossRefGoogle Scholar
  148. Oakes SA, Papa FR (2015) The role of endoplasmic reticulum stress in human pathology. Annu Rev Pathol 10:173–194CrossRefGoogle Scholar
  149. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12:913–922CrossRefGoogle Scholar
  150. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11:381–389CrossRefGoogle Scholar
  151. Oyadomari S, Takeda K, Takiguchi M, Gotoh T, Matsumoto M, Wada I et al (2001) Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci USA 98:10845–10850CrossRefGoogle Scholar
  152. Oyadomari S, Araki E, Mori M (2002a) Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells. Apoptosis 7:335–345CrossRefGoogle Scholar
  153. Oyadomari S, Koizumi A, Takeda K, Gotoh T, Akira S, Araki E et al (2002b) Targeted disruption of the chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 109:525–532CrossRefGoogle Scholar
  154. Ozcan L, Tabas I (2012) Role of endoplasmic reticulum stress in metabolic disease and other disorders. Annu Rev Med 63:317–328CrossRefGoogle Scholar
  155. Panda KK, Achary VM, Krishnaveni R, Padhi BK, Sarangi SN, Sahu SN et al (2011) In vitro biosynthesis and genotoxicity bioassay of silver nanoparticles using plants. Toxicol Vitr 25:1097–1105CrossRefGoogle Scholar
  156. Park EJ, Yi J, Kim Y, Choi K, Park K (2010) Silver nanoparticles induce cytotoxicity by a trojan-horse type mechanism. Toxicol Vitr 24:872–878CrossRefGoogle Scholar
  157. Park EJ, Choi DH, Kim Y, Lee EW, Song J, Cho MH, Kim JH, Kim SW (2014) Magnetic iron oxide nanoparticles induce autophagy preceding apoptosis through mitochondrial damage and ER stress in RAW264.7 cells. Toxicol Vitr 28:1402–1412CrossRefGoogle Scholar
  158. Peynshaert K, Manshian BB, Joris F, Braeckmans K, De Smedt SC, Demeester J, Soenen SJ (2014) Exploiting intrinsic nanoparticle toxicity: the pros and cons of nanoparticle- induced autophagy in biomedical research. Chem Rev 114:7581–7609CrossRefGoogle Scholar
  159. Piao MJ, Kang KA, Lee IK, Kim HS, Kim S, Choi JY et al (2011) Silver nanoparticles induce oxidative cell damage in human liver cells through inhibition of reduced glutathione and induction of mitochondria-involved apoptosis. Toxicol Lett 201:92–100CrossRefGoogle Scholar
  160. Pillai S (2005) Birth pangs: the stressful origins of lymphocytes. J Clin Invest 115:224–227CrossRefGoogle Scholar
  161. Pino SC, O‘Sullivan-Murphy B, Lidstone EA, Yang C, Lipson KL, Jurczyk A et al (2009) CHOP mediates endoplasmic reticulum stress-induced apoptosis in Gimap5-deficient T cells. PLoS One 4:e5468CrossRefGoogle Scholar
  162. Poljak-Blazi M, Jaganjac M, Mustapic M, Pivac N, Muck-Seler D (2009) Acute immunomodulatory effects of iron polyisomaltosate in rats. Immunobiology 214(2):121–128CrossRefGoogle Scholar
  163. Pryor WA, Stone K, Cross CE, Machlin L, Packer L (1993) Oxidants in cigarette smoke: radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann N Y Acad Sci 686:12–28CrossRefGoogle Scholar
  164. Puckett MC, Goldman EH, Cockrell LM, Huang B, Kasinski AL, Du Y, Wang CY, Lin A, Ichijo H, Khuri F, Fu H (2013) Integration of apoptosis signal-regulating kinase 1-mediated stress signaling with the Akt/protein kinase B-IkappaB kinase cascade. Mol Cell Biol 33:2252–2259CrossRefGoogle Scholar
  165. Pujalté I, Passagne I, Brouillaud B et al (2011) Cytotoxicity and oxidative stress induced by different metallic nanoparticles on human kidney cells. Part Fibre Toxicol 8 (article 10)CrossRefGoogle Scholar
  166. Rashid HO, Yadav RK, Kim HR, Chae HJ (2015) ER stress: autophagy induction, inhibition and selection. Autophagy 11:1956–1977CrossRefGoogle Scholar
  167. Risom L, Møller P, Loft S (2005) Oxidative stress-induced DNA damage by particulate air pollution. Mutat Res 592(1–2):119–137CrossRefGoogle Scholar
  168. Rosas-Hernandez H, Jimenez-Badillo S, Martinez-Cuevas PP, Gracia- Espino E, Terrones H, Terrones M, Hussain SM, Ali SF, Gonzalez C (2009) Effects of 45-nm silver nanoparticles on coronary endothelial cells and isolated rat aortic rings. Toxicol Lett 191:305–313CrossRefGoogle Scholar
  169. Saha S, Xiong X, Chakraborty PK, Shameer K, Arvizo RR, Kudgus RA, Dwivedi SK, Hossen MN, Gillies EM, Robertson JD, Dudley JT, Urrutia RA, Postier RG, Bhattacharya R, Mukherjee P (2016) Gold nanoparticle reprograms pancreatic tumor microenvironment and inhibits tumor growth. ACS Nano 10:10636–10651CrossRefGoogle Scholar
  170. Sanges D, Marigo V (2006) Cross-talk between two apoptotic pathways activated by endoplasmic reticulum stress: differential contribution of caspase-12 and AIF. Apoptosis 11:1629–1641CrossRefGoogle Scholar
  171. Sano R, Reed JC (1833) ER stress-induced cell death mechanisms. Biochim Biophys Acta 2013:3460–3470Google Scholar
  172. Schrand AM, Rahman MF, Hussain SM, Schlager JJ, Smith DA, Syed AF (2010) Metal-based nanoparticles and their toxicity assessment. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2:544–568CrossRefGoogle Scholar
  173. Schrand AM, Dai L, Schlager JJ, Hussain SM (2012) Toxicity testing of nanomaterials. Adv Exp Med Biol 745:58–75CrossRefGoogle Scholar
  174. Schroder M, Kaufman RJ (2005) The mammalian unfolded protein response. Annu Rev Biochem 74:739–789CrossRefGoogle Scholar
  175. Shi Y, Wang F, He J, Yadav S, Wang H (2010) Titaniumdioxide nanoparticles cause apoptosis in BEAS-2B cells through the caspase 8/t-Bid-independent mitochondrial pathway. Toxicol Lett 196(1):21–27CrossRefGoogle Scholar
  176. Shvedova AA, Pietroiusti A, Fadeel B, Kagan VE (2012a) Mechanisms of carbon nanotube- induced toxicity: focus on oxidative stress. Toxicol Appl Pharmacol 261:121–133CrossRefGoogle Scholar
  177. Shvedova AA, Pietroiusti A, Fadeel B, Kagan VE (2012b) Mechanisms of carbon nanotube-induced toxicity: focus on oxidative stress. Toxicol Appl Pharmacol 261(2):121–133CrossRefGoogle Scholar
  178. Simard JC, de Liz R, Vallieres F, 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 290:5926–5939CrossRefGoogle Scholar
  179. Simard JC, Durocher I, Girard D (2016) Silver nanoparticles induce irremediable endoplasmic reticulum stress leading to unfolded protein response dependent apoptosis in breast cancer cells. Apoptosis 21:1279–1290CrossRefGoogle Scholar
  180. Simon M, Saez G, Muggiolu G, Lavenas M, Le TQ, Michelet C, Deves G, Barberet P, Chevet E, Dupuy D, Delville MH, Seznec H (2017) In situ quantification of diverse titanium dioxide nanoparticles unveils selective endoplasmic reticulum stress-dependent toxicity. Nanotoxicology 11:134–145CrossRefGoogle Scholar
  181. Singh N, Manshian B, Jenkins GJ, Griffiths SM, Williams PM, Maffeis TG, Wright CJ, Doak SH (2009) Nanogenotoxicology: the DNA damaging potential of engineered nanomaterials. Biomaterials 30:3891–3914CrossRefGoogle Scholar
  182. Smita S, Gupta SK, Bartonova A, Dusinska M, Gutleb AC, Rahman Q (2012) Nanoparticles in the environment: assessment using the causal diagram approach. Environ Health 11(Suppl 1):S13CrossRefGoogle Scholar
  183. Snopczynski T, Goralczyk K, Czaja K, Strucinski P, Hernik A, Korcz W, Ludwicki JK (2009) Nanotechnology—possibilities and hazards. Rocz Panstw Zakl Hig 60:101–111 (in Polish)Google Scholar
  184. Soenen SJ, Parak WJ, Rejman J, Manshian B (2015) (Intra) cellular stability of inorganic nanoparticles: effects on cytotoxicity, particle functionality, and biomedical applications. Chem Rev 115:2109–2135CrossRefGoogle Scholar
  185. Sohaebuddin SK, Thevenot PT, Baker D, Eaton JW, Tang L (2010) Nanomaterial cytotoxicity is composition, size, and cell type dependent. Part Fibre Toxicol 7 (article 22)CrossRefGoogle Scholar
  186. Sovolyova N, Healy S, Samali A, Logue SE (2014) Stressed to death—mechanisms of ER stress-induced cell death. Biol Chem 395:1–13CrossRefGoogle Scholar
  187. Srivastava M, Singh S, Self WT (2012) Exposure to silver nanoparticles inhibits selenoprotein synthesis and the activity of thioredoxin reductase. Environ Health Persp 120:56–61CrossRefGoogle Scholar
  188. Stensberg MC, Wei Q, McLamore ES, Porterfield DM, Wei A, Sepulveda MS (2011) Toxicological studies on silver nanoparticles: challenges and opportunities in assessment, monitoring and imaging. Nanomedicine (Lond) 6:879–898CrossRefGoogle Scholar
  189. Stern ST, Adiseshaiah PP, Crist RM (2012) Autophagy and lysosomal dysfunction as emerging mechanisms of nanomaterial toxicity. Part Fibre Toxicol 9:20CrossRefGoogle Scholar
  190. Talekar M, Kendall J, Denny W, Garg S (2011) Targeting of nanoparticles in cancer: drug delivery and diagnostics. Anticancer Drugs 22(10):949–962CrossRefGoogle Scholar
  191. Tee JK, Ong CN, Bay BH, Ho HK, Leong DT (2016) Oxidative stress by inorganic nanoparticles. Wiley Interdiscip Rev Nanomed Nanobiotechnol 8:414–438CrossRefGoogle Scholar
  192. Tsai YY, Huang YH, Chao YL, Hu KY, Chin LT, Chou SH, Hour AL, Yao YD, Tu CS, Liang YJ, Tsai CY, Wu HY, Tan SW, Chen HM (2011) Identification of the nanogold particle-induced endoplasmic reticulum stress by omic techniques and systems biology analysis. ACS Nano 5:9354–9369CrossRefGoogle Scholar
  193. Tschopp J (2011) Mitochondria: Sovereign of inflammation? Eur J Immunol 41(5):1196–1202CrossRefGoogle Scholar
  194. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664–666CrossRefGoogle Scholar
  195. van der Valk FM, Schulte DM, Meiler S, Tang J, Zheng KH, Van den Bossche J, Seijkens T, Laudes M, de Winter M, Lutgens E, Alaarg A, Metselaar JM, Dallinga-Thie M, Mulder WJ, Stroes ES, Hamers AA (2016) Liposomal prednisolone promotes macrophage lipotoxicity in experimental atherosclerosis. Nanomedicine 12:1463–1470CrossRefGoogle Scholar
  196. van Montfort RL, Congreve M, Tisi D, Carr R, Jhoti H (2003) Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423(6941):773–777CrossRefGoogle Scholar
  197. van Schadewijk A, van’t Wout EF, Stolk J, Hiemstra PS (2012) A quantitative method for detection of spliced X-box binding protein-1 (XBP1) mRNA as a measure of endoplasmic reticulum (ER) stress. Cell Stress Chaperones 17:275–279CrossRefGoogle Scholar
  198. 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 6:1769–1780CrossRefGoogle Scholar
  199. Vandebriel RJ, Tonk EC, de la Fonteyne-Blankestijn LJ, Gremmer ER, Verharen HW, van der Ven LT et al (2014) Immunotoxicity of silver nanoparticles in an intravenous 28-day repeated-dose toxicity study in rats. Part Fibre Toxicol 11:21CrossRefGoogle Scholar
  200. Vanwinkle BA, de Mesy Bentley KL, Malecki JM, Gunter KK, Evans IM, Elder A, Finkelstein JN, Oberdorster G, Gunter TE (2009) Nanoparticle (NP) uptake by type I alveolar epithelial cells and their oxidant stress response. Nanotoxicology 3:307–318CrossRefGoogle Scholar
  201. Vigneshwaran N, Kathe AA, Varadarajan PV, Nachane RP, Balasubramanya RH (2007) Functional finishing of cotton fabrics using silver nanoparticles. J Nanosci Nanotechnol 7:1893–1897CrossRefGoogle Scholar
  202. Walczyk D, Bombelli FB, Monopoli MP, Lynch I, Dawson KA (2010) What the cell “sees” in bionanoscience. J Am Chem Soc 132:5761–5768CrossRefGoogle Scholar
  203. Walter L, Hajnoczky G (2005) Mitochondria and endoplasmic reticulum: the lethal interorganelle cross-talk. J Bioenerg Biomembr 37:191–206CrossRefGoogle Scholar
  204. Wang XZ, Lawson B, Brewer JW, Zinszner H, Sanjay A, Mi LJ et al (1996) Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol Cell Biol 16:4273–4280CrossRefGoogle Scholar
  205. Wang L, Bowman L, Lu Y et al (2005) Essential role of p53 in silica-induced apoptosis. Am J Physiol 288(3):L488–L496Google Scholar
  206. Wang X, Wang B, Fan Z, Shi X, Ke ZJ, Luo J (2007) Thiamine deficiency induces endoplasmic reticulum stress in neurons. Neuroscience 144:1045–1056CrossRefGoogle Scholar
  207. Wang L, Mercer RR, Rojanasakul Y et al (2010) Direct fibrogenic effects of dispersed single-walled carbon nanotubes on human lung fibroblasts. J Toxicol Environ Health A 73(5–6):410–422CrossRefGoogle Scholar
  208. Wang J, Fang X, Liang W (2012) Pegylated phospholipid micelles induce endoplasmic reticulum-dependent apoptosis of cancer cells but not normal cells. ACS Nano 6:5018–5030CrossRefGoogle Scholar
  209. Wang L, Meng J, Cao W, Li Q, Qiu Y, Sun B, Li LM (2014) Induction of apoptosis through ER stress and TP53 in MCF-7 cells by the nanoparticle [Gd@C82 (OH) 22]n: a systems biology study. Methods 67:394–406CrossRefGoogle Scholar
  210. Wang Y, Zhao Q, Han N, Bai L, Li J, Liu J, Che E, Hu L, Zhang Q, Jiang T, Wang S (2015a) Mesoporous silica nanoparticles in drug delivery and biomedical applications. Nanomedicine 11:313–327CrossRefGoogle Scholar
  211. Wang Y, Kaur G, Zysk A, Liapis V, Hay S, Santos A, Losic D, Evdokiou A (2015b) Systematic in vitro nanotoxicity study on anodic alumina nanotubes with engineered aspect ratio: understanding nanotoxicity by a nanomaterial model. Biomaterials 46:117–130CrossRefGoogle Scholar
  212. Wang H, Liu Z, Gou Y, Qin Y, Xu Y, Liu J, Wu JZ (2015c) Apoptosis and necrosis induced by novel realgar quantum dots in human endometrial cancer cells via endoplasmic reticulum stress signaling pathway. Int J Nanomedicine 10:5505–5512CrossRefGoogle Scholar
  213. Wang Y, Kaur G, Chen Y, Santos A, Losic D, Evdokiou A (2015d) Bioinert anodic alumina nanotubes for targeting of endoplasmic reticulum stress and autophagic signaling: a combinatorial nanotube-based drug delivery system for enhancing cancer therapy. ACS Appl Mater Interfaces 7:27140–27151CrossRefGoogle Scholar
  214. Wiechers JW, Musee N (2010) Engineered inorganic nanoparticles and cosmetics: facts, issues, knowledge gaps and challenges. J Biomed Nanotechnol 6:408–431CrossRefGoogle Scholar
  215. Wolfram J, Zhu M, Yang Y, Shen J, Gentile E, Paolino D, Fresta M, Nie G, Chen C, Shen H, Ferrari M, Zhao Y (2015) Safety of nanoparticles in medicine. Curr Drug Targets 16:1671–1681CrossRefGoogle Scholar
  216. Wu J, Kaufman RJ (2006a) from acute ER stress to physiological roles of the unfolded protein response, cell death. Differentiation 13:374–384CrossRefGoogle Scholar
  217. Wu J, Kaufman RJ (2006b) From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ 13:374–384CrossRefGoogle Scholar
  218. Wu Y, Zhou Q (2012) Dose- and time-related changes in aerobic metabolism, chorionic disruption, and oxidative stress in embryonic medaka (Oryzias latipes): underlying mechanisms for silver nanoparticle developmental toxicity. Aquat Toxicol 124–125:238–246CrossRefGoogle Scholar
  219. Wu Y, Zhou Q (2013) Silver nanoparticles cause oxidative damage and histological changes in medaka (Oryzias latipes) after 14 days of exposure. Environ Toxicol Chem 32(1):165–173CrossRefGoogle Scholar
  220. Xia T, Kovochich M, Brant J et al (2006) Comparison of the abilities of ambient and manufactured nanoparticles to induce cellular toxicity according to an oxidative stress paradigm. Nano Lett 6(8):1794–1807CrossRefGoogle Scholar
  221. Yamada M, Foote M, Prow TW (2015) Therapeutic gold, silver, and platinum nanoparticles. Wiley Interdiscip Rev Nanomed Nanobiotechnol 7:428–445CrossRefGoogle Scholar
  222. Yan M, Zhang Y, Qin H, Liu K, Guo M, Ge Y, Xu M, Sun Y, Zheng X (2016) Cytotoxicity of CdTe quantum dots in human umbilical vein endothelial cells: the involvement of cellular uptake and induction of pro-apoptotic endoplasmic reticulum stress. Int J Nanomedicine 11:529–542Google Scholar
  223. Yang X, Shao H, Liu W, Gu W, Shu X, Mo Y, Chen X, Zhang Q, Jiang M (2015) Endoplasmic reticulum stress and oxidative stress are involved in ZnO nanoparticle-induced hepatotoxicity. Toxicol Lett 234:40–49CrossRefGoogle Scholar
  224. Yasui H, Takeuchi R, Nagane M, Meike S, Nakamura Y, Yamamori T, Ikenaka Y, Kon Y, Murotani H, Oishi M, Nagasaki Y, Inanami O (2014) Radiosensitization of tumor cells through endoplasmic reticulum stress induced by PEGylated nanogel containing gold nanoparticles. Cancer Lett 347:151–158CrossRefGoogle Scholar
  225. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R, Brown MS, Goldstein JL (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6:1355–1364CrossRefGoogle Scholar
  226. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881–891CrossRefGoogle Scholar
  227. Younce CW, Wang K, Kolattukudy PE (2010) Hyperglycaemia-induced cardiomyocyte death is mediated via MCP-1 production and induction of a novel zinc-finger protein MCPIP. Cardiovasc Res 87:665–674CrossRefGoogle Scholar
  228. Yu KN, Sung JH, Lee S, Kim JE, Kim S, Cho WY, Lee AY, Park SJ, Lim J, Park C, Chae C, Lee JK, Lee J, Kim JS, Cho MH (2015a) Inhalation of titanium dioxide induces endoplasmic reticulum stress-mediated autophagy and inflammation in mice. Food Chem Toxicol 85:106–113CrossRefGoogle Scholar
  229. Yu KN, Chang SH, Park SJ, Lim J, Lee J, Yoon TJ, Kim JS, Cho MH (2015b) Titanium dioxide nanoparticles induce endoplasmic reticulum stress-mediated autophagic cell death via mitochondria-associated endoplasmic reticulum membrane disruption in normal lung cells. PLoS One 10:e0131208CrossRefGoogle Scholar
  230. Zhang K, Kaufman RJ (2004) Signaling the unfolded protein response from the endoplasmic reticulum. J Biol Chem 279:25935–25938CrossRefGoogle Scholar
  231. Zhang R, Piao MJ, Kim KC, Kim AD, Choi JY, Choi J, Hyun JW (2011a) Endoplasmic reticulum stress signaling is involved in silver nanoparticles-induced apoptosis. Int J Biochem Cell Biol 44(1):224–232CrossRefGoogle Scholar
  232. Zhang XQ, Yin LH, Tang M, Pu YP (2011b) ZnO, TiO2, SiO2, and Al2O3 nanoparticles-induced toxic effects on human fetal lung fibroblasts. Biomed Environ Sci 24(6):661–669Google Scholar
  233. Zhang R, Piao MJ, Kim KC, Kim AD, Choi JY, Choi J, Hyun JW (2012) Endoplasmic reticulum stress signaling is involved in silver nanoparticles-induced apoptosis. Int J Biochem Cell Biol 44:224–232CrossRefGoogle Scholar
  234. Zhang X, Zhang H, Liang X, Zhang J, Tao W, Zhu X, Chang D, Zeng X, Liu G, Mei L (2016) Iron oxide nanoparticles induce autophagosome accumulation through multiple mechanisms: lysosome impairment, mitochondrial damage, and ER stress. Mol Pharm 13:2578–2587CrossRefGoogle Scholar
  235. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H et al (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12:982–995CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Physical Chemistry and Nanoscience, Department of Chemistry, Faculty of ScienceAl Baha UniversityBaljurashiSaudi Arabia

Personalised recommendations