The neurotoxicity induced by engineered nanomaterials

References

• Morris JE. Nanoparticle properties In: Morris JE, editor. Nanopackaging: Nanotechnologies and Electronics Packaging. Boston, MA: Springer US; 2008:93–107.
   Google Scholar
• Shakeel M, Jabeen F, Shabbir S, Asghar MS, Khan MS, Chaudhry AS. Toxicity of nano-titanium dioxide (TiO2-NP) through various routes of exposure: a review. Biol Trace Elem Res. 2016;172(1):1–36. doi:10.1007/s12011-015-0550-x26554951
   PubMed Web of Science ®Google Scholar
• Song B, Liu J, Feng X, Wei L, Shao L. A review on potential neurotoxicity of titanium dioxide nanoparticles. Nanoscale Res Lett. 2015;10(1):342. doi:10.1186/s11671-015-1042-9
   PubMedGoogle Scholar
• Bakand S, Hayes A. Toxicological considerations, toxicity assessment, and risk management of inhaled nanoparticles. Int J Mol Sci. 2016;17(6):929. doi:10.3390/ijms17060929
   PubMed Web of Science ®Google Scholar
• Feng X, Chen A, Zhang Y, Wang J, Shao L, Wei L. Application of dental nanomaterials: potential toxicity to the central nervous system. Int J Nanomed. 2015;10:3547–3565.
   PubMed Web of Science ®Google Scholar
• Recordati C, De Maglie M, Bianchessi S, et al. Tissue distribution and acute toxicity of silver after single intravenous administration in mice: nano-specific and size-dependent effects. Part Fibre Toxicol. 2016;13:12. doi:10.1186/s12989-016-0124-x26926244
   PubMed Web of Science ®Google Scholar
• Kafa H, Wang JT, Rubio N, et al. The interaction of carbon nanotubes with an in vitro blood-brain barrier model and mouse brain in vivo. Biomaterials. 2015;53:437–452. doi:10.1016/j.biomaterials.2015.02.08325890741
   PubMed Web of Science ®Google Scholar
• Feng XL, Chen A, Zhang Y, Wang J, Shao L, Wei L. Central nervous system toxicity of metallic nanoparticles. Int J Nanomed. 2015;10:4321–4340.
   PubMed Web of Science ®Google Scholar
• Cupaioli FA, Zucca FA, Boraschi D, Zecca L. Engineered nanoparticles. How brain friendly is this new guest? Prog Neurobiol. 2014;119–120:20–38. doi:10.1016/j.pneurobio.2014.05.002
   PubMed Web of Science ®Google Scholar
• Win-Shwe T, Fujimaki H. Nanoparticles and neurotoxicity. Int J Mol Sci. 2011;12(9):6267–6280. doi:10.3390/ijms1209626722016657
   PubMed Web of Science ®Google Scholar
• Hu Y, Gao J. Potential neurotoxicity of nanoparticles. Int J Pharmaceut. 2010;394(1–2):115–121. doi:10.1016/j.ijpharm.2010.04.026
   PubMed Web of Science ®Google Scholar
• Wang Y, Xiong L, Tang M. Toxicity of inhaled particulate matter on the central nervous system: neuroinflammation, neuropsychological effects and neurodegenerative disease. J Appl Toxicol. 2017;37(6):644–667. doi:10.1002/jat.345128299803
   PubMedGoogle Scholar
• Ou L, Song B, Liang H, et al. Toxicity of graphene-family nanoparticles: a general review of the origins and mechanisms. Part Fibre Toxicol. 2016;13(1):57. doi:10.1186/s12989-016-0168-y27799056
   PubMed Web of Science ®Google Scholar
• Cardoso FL, Brites D, Brito MA. Looking at the blood–brain barrier: molecular anatomy and possible investigation approaches. Brain Res Rev. 2010;64(2):328–363. doi:10.1016/j.brainresrev.2010.05.00320685221
   PubMed Web of Science ®Google Scholar
• Saraiva C, Praça C, Ferreira R, Santos T, Ferreira L, Bernardino L. Nanoparticle-mediated brain drug delivery: overcoming blood–brain barrier to treat neurodegenerative diseases. J Control Release. 2016;235:34–47. doi:10.1016/j.jconrel.2016.05.04427208862
   PubMed Web of Science ®Google Scholar
• Wong HL, Wu XY, Bendayan R. Nanotechnological advances for the delivery of CNS therapeutics. Adv Drug Deliv Rev. 2012;64(7):686–700. doi:10.1016/j.addr.2011.10.00722100125
   PubMed Web of Science ®Google Scholar
• Yang Z, Liu ZW, Allaker RP, et al. A review of nanoparticle functionality and toxicity on the central nervous system. J R Soc Interface. 2010;7(Suppl_4):S411–S422. doi:10.1098/rsif.2010.0158.focus20519209
   PubMedGoogle Scholar
• Adams DH, Joyce G, Richardson VJ, Ryman BE, Wiśniewski HM. Liposome toxicity in the mouse central nervous system. J Neurol Sci. 1977;31(2):173–179.839231
   PubMed Web of Science ®Google Scholar
• Trickler WJ, Lantz SM, Murdock RC, et al. Silver nanoparticle induced blood-brain barrier inflammation and increased permeability in primary rat brain microvessel endothelial cells. Toxicol Sci. 2010;118(1):160–170. doi:10.1093/toxsci/kfq24420713472
   PubMed Web of Science ®Google Scholar
• Yin Y, Qiang L, Sun H, et al. Cytotoxic effects of ZnO hierarchical architectures on RSC96 Schwann cells. Nanoscale Res Lett. 2012;7(1):439. doi:10.1186/1556-276X-7-43922873432
   PubMedGoogle Scholar
• Zeng Y, Kurokawa Y, Win-Shwe TT, et al. Effects of PAMAM dendrimers with various surface functional groups and multiple generations on cytotoxicity and neuronal differentiation using human neural progenitor cells. J Toxicol Sci. 2016;41(3):351. doi:10.2131/jts.41.1327193728
   PubMed Web of Science ®Google Scholar
• Knudsen KB, Northeved H, Pramod Kumar EK, et al. Differential toxicological response to positively and negatively charged nanoparticles in the rat brain. Nanotoxicology. 2014;8(7):764–774. doi:10.3109/17435390.2013.82958923889261
   PubMed Web of Science ®Google Scholar
• Calienni MN, Feas DA, Igartúa DE, Chiaramoni NS, Sdv A, Prieto MJ. Nanotoxicological and teratogenic effects: A linkage between dendrimer surface charge and zebrafish developmental stages. Toxicol Appl Pharmacol. 2017;337:1. doi:10.1016/j.taap.2017.10.00328993268
   PubMed Web of Science ®Google Scholar
• Phenrat T, Long TC, Lowry GV, Veronesi B. Partial oxidation (“Aging”) and surface modification decrease the toxicity of nanosized zerovalent iron. Environ Sci Technol. 2009;43(1):195–200.19209606
   PubMed Web of Science ®Google Scholar
• Karmakar A, Zhang Q, Zhang Y. Neurotoxicity of nanoscale materials. J Food Drug Anal. 2014;22(1):147–160. doi:10.1016/j.jfda.2014.01.01224673911
   PubMed Web of Science ®Google Scholar
• Zhang L, Bai R, Li B, et al. Rutile TiO2 particles exert size and surface coating dependent retention and lesions on the murine brain. Toxicol Lett. 2011;207(1):73–81. doi:10.1016/j.toxlet.2011.08.00121855616
   PubMed Web of Science ®Google Scholar
• Wu J, Wang C, Sun J, Xue Y. Neurotoxicity of silica nanoparticles: brain localization and dopaminergic neurons damage pathways. ACS Nano. 2011;5(6):4476–4489. doi:10.1021/nn103530b21526751
   PubMed Web of Science ®Google Scholar
• Neves AR, Queiroz JF, Lima SAC, Reis S. Apo E-functionalization of solid lipid nanoparticles enhances brain drug delivery: uptake mechanism and transport pathways. Bioconjugate Chem. 2017;28(4):995–1004. doi:10.1021/acs.bioconjchem.6b00705
   PubMed Web of Science ®Google Scholar
• Mendonca MCP, Soares ES, de Jesus MB, et al. Reduced graphene oxide induces transient blood-brain barrier opening: an in vivo study. J Nanobiotechnol. 2015;13(1):78. doi:10.1186/s12951-015-0143-z
   PubMedGoogle Scholar
• Liu X, Sui B, Sun J. Blood-brain barrier dysfunction induced by silica NPs in vitro and in vivo: involvement of oxidative stress and Rho-kinase/JNK signaling pathways. Biomaterials. 2017;121:64–82. doi:10.1016/j.biomaterials.2017.01.00628081460
   PubMed Web of Science ®Google Scholar
• Kafa H, Wang JT, Rubio N, et al. Translocation of LRP1 targeted carbon nanotubes of different diameters across the blood–brain barrier in vitro and in vivo. J Control Release. 2016;225:217–229. doi:10.1016/j.jconrel.2016.01.03126809004
   PubMed Web of Science ®Google Scholar
• Lu W, Sun Q, Wan J, She Z, Jiang XG. Cationic albumin-conjugated pegylated nanoparticles allow gene delivery into brain tumors via intravenous administration. Cancer Res. 2006;66(24):11878–11887. doi:10.1158/0008-5472.CAN-06-235417178885
   PubMed Web of Science ®Google Scholar
• Huang R, Ke W, Han L, et al. Brain-targeting mechanisms of lactoferrin-modified DNA-loaded nanoparticles. J Cereb Blood Flow Metab. 2009;29(12):1914–1923. doi:10.1038/jcbfm.2009.10419654588
   PubMed Web of Science ®Google Scholar
• Kreyling WG. Discovery of unique and ENM—specific pathophysiologic pathways: comparison of the translocation of inhaled iridium nanoparticles from nasal epithelium versus alveolar epithelium towards the brain of rats. Toxicol Appl Pharm. 2016;299:41–46. doi:10.1016/j.taap.2016.02.004
   PubMed Web of Science ®Google Scholar
• Elder A, Gelein R, Silva V, et al. Translocation of inhaled ultrafine manganese oxide particles to the central nervous system. Environ Health Persp. 2006;114(8):1172–1178. doi:10.1289/ehp.9030
   PubMed Web of Science ®Google Scholar
• Oberdorster G, Elder A, Rinderknecht A. Nanoparticles and the brain: cause for concern? J Nanosci Nanotechnol. 2009;9(8):4996–5007.19928180
   PubMed Web of Science ®Google Scholar
• Mistry A, Stolnik S, Illum L. Nanoparticles for direct nose-to-brain delivery of drugs. Int J Pharmaceut. 2009;379(1):146–157. doi:10.1016/j.ijpharm.2009.06.019
   PubMed Web of Science ®Google Scholar
• Kohei Y, Yasuo Y, Kazuma H, et al. Silica and titanium dioxide nanoparticles cause pregnancy complications in mice. Nat Nanotechnol. 2011;6(5):321. doi:10.1038/nnano.2011.4121460826
   PubMedGoogle Scholar
• Webster TJ, Waid MC, McKenzie JL, Price RL, Ejiofor JU. Nano-biotechnology: carbon nanofibres as improved neural and orthopaedic implants. Nanotechnology. 2004;15(1):48–54. doi:10.1088/0957-4484/15/1/009
   Web of Science ®Google Scholar
• Koch F, Möller A, Frenz M, Pieles U, Kuehni-Boghenbor K, Mevissen M. An in vitro toxicity evaluation of gold-, PLLA- and PCL-coated silica nanoparticles in neuronal cells for nanoparticle-assisted laser-tissue soldering. Toxicol In Vitro. 2014;28(5):990–998. doi:10.1016/j.tiv.2014.04.01024768613
   PubMedGoogle Scholar
• Wei X, Luan L, Zhao Z, et al. Nanofabricated ultraflexible electrode arrays for high-density intracortical recording. Adv Sci. 2018;5(6):1700625. doi:10.1002/advs.201700625
   Web of Science ®Google Scholar
• Biran R, Martin DC, Tresco PA. Neuronal cell loss accompanies the brain tissue response to chronically implanted silicon microelectrode arrays. Exp Neurol. 2005;195(1):115–126. doi:10.1016/j.expneurol.2005.04.02016045910
   PubMed Web of Science ®Google Scholar
• Zhang S, Yen S, Xiang Z, Liao L, Kwong D, Lee C. Development of silicon probe with acute study on in vivo neural recording and implantation behavior monitored by integrated Si-nanowire strain sensors. J Microelectromech Syst. 2015;24(5):1303–1313. doi:10.1109/JMEMS.2015.2417678
   Web of Science ®Google Scholar
• Droge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82(1):47. doi:10.1152/physrev.00018.200111773609
   PubMed Web of Science ®Google Scholar
• Cui K, Luo X, Xu K, Ven Murthy MR. Role of oxidative stress in neurodegeneration: recent developments in assay methods for oxidative stress and nutraceutical antioxidants. Prog Neuropsychopharmacol Biol Psychiatry. 2004;28(5):771–799. doi:10.1016/j.pnpbp.2004.05.02315363603
   PubMed Web of Science ®Google Scholar
• Ze Y, Zheng L, Zhao X, et al. Molecular mechanism of titanium dioxide nanoparticles-induced oxidative injury in the brain of mice. Chemosphere. 2013;92(9):1183–1189. doi:10.1016/j.chemosphere.2013.01.09423466083
   PubMed Web of Science ®Google Scholar
• Shrivastava R, Raza S, Yadav A, Kushwaha P, Flora SJS. Effects of sub-acute exposure to TiO2, ZnO and Al2O3 nanoparticles on oxidative stress and histological changes in mouse liver and brain. Drug Chem Toxicol. 2013;37(3):336–347. doi:10.3109/01480545.2013.86613424344737
   PubMedGoogle Scholar
• Long TC, Saleh N, Tilton RD, Lowry GV, Veronesi B. Titanium dioxide (P25) produces reactive oxygen species in immortalized brain microglia (BV2): implications for nanoparticle neurotoxicity†. Environ Sci Technol. 2006;40(14):4346–4352.16903269
   PubMed Web of Science ®Google Scholar
• Long TC, Tajuba J, Sama P, et al. Nanosize titanium dioxide stimulates reactive oxygen species in brain microglia and damages neurons in vitro. Environ Health Perspect. 2007;115(11):1631–1637. doi:10.1289/ehp.1021618007996
   PubMed Web of Science ®Google Scholar
• Sharma AK, Singh V, Gera R, Purohit MP, Ghosh D. Zinc oxide nanoparticle induces microglial death by NADPH-oxidase-independent reactive oxygen species as well as energy depletion. Mol Neurobiol. 2017;54(8):6273–6286. doi:10.1007/s12035-016-0133-727714634
   PubMedGoogle Scholar
• Yin N, Liu Q, Liu J, et al. Silver nanoparticle exposure attenuates the viability of rat cerebellum granule cells through apoptosis coupled to oxidative stress. Small. 2013;9(9–10):1831–1841. doi:10.1002/smll.20120273223427069
   PubMedGoogle Scholar
• Geppert M, Hohnholt MC, Nürnberger S, Dringen R. Ferritin up-regulation and transient ROS production in cultured brain astrocytes after loading with iron oxide nanoparticles. Acta Biomater. 2012;8(10):3832–3839. doi:10.1016/j.actbio.2012.06.02922750736
   PubMedGoogle Scholar
• Chen Z, Yin J, Zhou Y, et al. Dual enzyme-like activities of iron oxide nanoparticles and their implication for diminishing cytotoxicity. ACS Nano. 2012;6(5):4001–4012. doi:10.1021/nn300291r22533614
   PubMed Web of Science ®Google Scholar
• Ren C, Hu X, Zhou Q. graphene oxide quantum dots reduce oxidative stress and inhibit neurotoxicity in vitro and in vivo through catalase-like activity and metabolic regulation. Adv Sci. 2018;5(5):1700595. doi:10.1002/advs.v5.5
   Web of Science ®Google Scholar
• Stern ST, Adiseshaiah PP, Crist RM. Autophagy and lysosomal dysfunction as emerging mechanisms of nanomaterial toxicity. Part Fibre Toxicol. 2012;9:20. doi:10.1186/1743-8977-9-2022697169
   PubMed Web of Science ®Google Scholar
• Yang M, Zhang M, Tahara Y, et al. Lysosomal membrane permeabilization: carbon nanohorn-induced reactive oxygen species generation and toxicity by this neglected mechanism. Toxicol Appl Pharm. 2014;280(1):117–126. doi:10.1016/j.taap.2014.07.022
   PubMed Web of Science ®Google Scholar
• Hsiao I, Chang C, Wu C, et al. Indirect effects of TiO2 nanoparticle on neuron-glial cell interactions. Chem-Biol Interact. 2016;254(C):34–44. doi:10.1016/j.cbi.2016.05.02427216632
   PubMedGoogle Scholar
• Hsiao I, Hsieh Y, Chuang C, Wang C, Huang Y. Effects of silver nanoparticles on the interactions of neuron- and glia-like cells: toxicity, uptake mechanisms, and lysosomal tracking. Environ Toxicol. 2017;32(6):1742–1753. doi:10.1002/tox.2239728181394
   PubMedGoogle Scholar
• Weiss U. Inflammation. Nature. 2002;420(6917):845. doi:10.1038/nature01131
   Web of Science ®Google Scholar
• Li X, Zheng H, Zhang Z, et al. Glia activation induced by peripheral administration of aluminum oxide nanoparticles in rat brains. Nanomedicine. 2009;5(4):473–479. doi:10.1016/j.nano.2009.01.01319523415
   PubMed Web of Science ®Google Scholar
• Stansley B, Post J, Hensley K. A comparative review of cell culture systems for the study of microglial biology in Alzheimer‘s disease. J Neuroinflamm. 2012;9:115. doi:10.1186/1742-2094-9-115
   PubMed Web of Science ®Google Scholar
• Ze Y, Sheng L, Zhao X, et al. TiO2 nanoparticles induced hippocampal neuroinflammation in mice. PLoS One. 2014;9(3):e92230. doi:10.1371/journal.pone.009223024658543
   PubMed Web of Science ®Google Scholar
• Hutter E, Boridy S, Labrecque S, et al. Microglial response to gold nanoparticles. ACS Nano. 2010;4(5):2595–2606. doi:10.1021/nn901869f20329742
   PubMed Web of Science ®Google Scholar
• Sun B, Wang X, Ji Z, Li R, Xia T. NLRP3 inflammasome activation induced by engineered nanomaterials. Small. 2013;9(9–10):1595–1607. doi:10.1002/smll.20120196223180683
   PubMedGoogle Scholar
• Moquin A, Hutter E, Choi AO, et al. Caspase-1 activity in microglia stimulated by pro-inflammagen nanocrystals. ACS Nano. 2013;7(11):9585–9598. doi:10.1021/nn404473g24107183
   PubMedGoogle Scholar
• Luther EM, Petters C, Bulcke F, et al. Endocytotic uptake of iron oxide nanoparticles by cultured brain microglial cells. Acta Biomater. 2013;9(9):8454–8465. doi:10.1016/j.actbio.2013.05.02223727247
   PubMedGoogle Scholar
• Ye D, Raghnaill MN, Bramini M, Mahon E. Nanoparticle accumulation and transcytosis in brain endothelial cell layers. Nanoscale. 2013;5(22):11153–11156. doi:10.1039/c3nr02905k24077327
   PubMed Web of Science ®Google Scholar
• Xue Y, Wu J, Sun J. Four types of inorganic nanoparticles stimulate the inflammatory reaction in brain microglia and damage neurons in vitro. Toxicol Lett. 2012;214(2):91–98. doi:10.1016/j.toxlet.2012.08.00922939914
   PubMedGoogle Scholar
• Choi J, Zheng Q, Katz HE, Guilarte TR. Silica-based nanoparticle uptake and cellular response by primary microglia. Environ Health Perspect. 2010;118(5):589–595. doi:10.1289/ehp.090153420439179
   PubMed Web of Science ®Google Scholar
• Chen I, Hsiao I, Lin H, Wu C, Chuang C, Huang Y. Influence of silver and titanium dioxide nanoparticles on in vitro blood-brain barrier permeability. Environ Toxicol Pharm. 2016;47:108–118. doi:10.1016/j.etap.2016.09.009
   PubMed Web of Science ®Google Scholar
• Trickler WJ, Lantz SM, Schrand AM, et al. Effects of copper nanoparticles on rat cerebral microvessel endothelial cells. (Report). Nanomedicine-Uk. 2012;7(6):835. doi:10.2217/nnm.11.154
   PubMed Web of Science ®Google Scholar
• Xu L, Dan M, Shao A, et al. Silver nanoparticles induce tight junction disruption and astrocyte neurotoxicity in a rat blood-brain barrier primary triple coculture model. Int J Nanomedicine. 2015;10:6105.26491287
   PubMed Web of Science ®Google Scholar
• Trickler WJ, Lantz-McPeak SM, Robinson BL, et al. Porcine brain microvessel endothelial cells show pro-inflammatory response to the size and composition of metallic nanoparticles. Drug Metab Rev. 2014;46(2):224–231. doi:10.3109/03602532.2013.87345024378227
   PubMed Web of Science ®Google Scholar
• Brun E, Carrière M, Mabondzo A. In vitro evidence of dysregulation of blood–brain barrier function after acute and repeated/long-term exposure to TiO2 nanoparticles. Biomaterials. 2012;33(3):886–896. doi:10.1016/j.biomaterials.2011.10.02522027597
   PubMed Web of Science ®Google Scholar
• Raghnaill MN, Bramini M, Ye D, et al. Paracrine signalling of inflammatory cytokines from an in vitro blood brain barrier model upon exposure to polymeric nanoparticles. Analyst. 2014;139(5):923–930. doi:10.1039/c3an01621h24195103
   PubMedGoogle Scholar
• Song B, Zhang Y, Liu J, Zhou T. Unraveling the neurotoxicity of titanium dioxide nanoparticles: focusing on molecular mechanisms. Beilstein J Nanotech. 2016;7(1):645–654. doi:10.3762/bjnano.7.57
   PubMedGoogle Scholar
• Singh N, Nelson B, Scanlan L, Coskun E, Jaruga P, Doak S. Exposure to engineered nanomaterials: impact on DNA repair pathways. Int J Mol Sci. 2017;18(7):1515. doi:10.3390/ijms18071515
   PubMed Web of Science ®Google Scholar
• Golbamaki N, Rasulev B, Cassano A, et al. Genotoxicity of metal oxide nanomaterials: review of recent data and discussion of possible mechanisms. Nanoscale. 2015;7(6):2154–2198. doi:10.1039/c4nr06670g25580680
   PubMedGoogle Scholar
• Ren C, Hu X, Li X, Zhou Q. Ultra-trace graphene oxide in a water environment triggers Parkinson‘s disease-like symptoms and metabolic disturbance in zebrafish larvae. Biomaterials. 2016;93:83–94. doi:10.1016/j.biomaterials.2016.03.03627085073
   PubMedGoogle Scholar
• Shah SA, Yoon GH, Ahmad A, Ullah F, Amin FU, Kim MO. Nanoscale-alumina induces oxidative stress and accelerates amyloid beta (Aβ) production in ICR female mice. Nanoscale. 2015;7(37):15225–15237. doi:10.1039/c5nr03598h26315713
   PubMedGoogle Scholar
• Valdiglesias V, Costa C, Kiliç G, et al. Neuronal cytotoxicity and genotoxicity induced by zinc oxide nanoparticles. Environ Int. 2013;55(C):92–100. doi:10.1016/j.envint.2013.02.01323535050
   PubMedGoogle Scholar
• El-Ghor A, Noshy MM, Galal A, Mohamed HRH. Normalization of nano-sized TiO2-induced clastogenicity, genotoxicity and mutagenicity by chlorophyllin administration in mice brain, liver, and bone marrow cells. Toxicol Sci. 2014;142(1):21–32. doi:10.1093/toxsci/kfu15725129858
   PubMedGoogle Scholar
• Hawkins SJ, Crompton LA, Sood A, et al. Nanoparticle-induced neuronal toxicity across placental barriers is mediated by autophagy and dependent on astrocytes. Nat Nanotechnol. 2018;13(5):427–433. doi:10.1038/s41565-018-0085-329610530
   PubMed Web of Science ®Google Scholar
• Singh N, Manshian B, Jenkins GJS, et al. NanoGenotoxicology: the DNA damaging potential of engineered nanomaterials. Biomaterials. 2009;30(23–24):3891–3914. doi:10.1016/j.biomaterials.2009.04.00919427031
   PubMed Web of Science ®Google Scholar
• Kang Y, Liu J, Wu J, et al. Graphene oxide and reduced graphene oxide induced neural pheochromocytoma-derived PC12 cell lines apoptosis and cell cycle alterations via the ERK signaling pathways. Int J Nanomed. 2017;12:5501–5510. doi:10.2147/IJN.S141032
   PubMed Web of Science ®Google Scholar
• Valdiglesias V, Costa C, Sharma V, et al. Comparative study on effects of two different types of titanium dioxide nanoparticles on human neuronal cells. Food Chem Toxicol. 2013;57(C):352–361. doi:10.1016/j.fct.2013.04.01023597443
   PubMedGoogle Scholar
• Ganguly P, Breen A, Pillai SC. Toxicity of nanomaterials: exposure, pathways, assessment, and recent advances. Acs Biomater Sci Eng. 2018;4(7):2237–2275. doi:10.1021/acsbiomaterials.8b00068
   PubMed Web of Science ®Google Scholar
• Márquez-Ramírez SG, Delgado-Buenrostro NL, Chirino YI, Iglesias GG, López-Marure R. Titanium dioxide nanoparticles inhibit proliferation and induce morphological changes and apoptosis in glial cells. Toxicology. 2012;302(2–3):146–156. doi:10.1016/j.tox.2012.09.00523044362
   PubMed Web of Science ®Google Scholar
• Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem-Biol Interact. 2006;160(1):1–40. doi:10.1016/j.cbi.2005.12.00916430879
   PubMed Web of Science ®Google Scholar
• Wang J, Deng X, Zhang F, Chen D, Ding W. ZnO nanoparticle-induced oxidative stress triggers apoptosis by activating JNK signaling pathway in cultured primary astrocytes. Nanoscale Res Lett. 2014;9(1):117. doi:10.1186/1556-276X-9-11724624962
   PubMedGoogle Scholar
• Wu J, Sun J, Xue Y. Involvement of JNK and P53 activation in G2/M cell cycle arrest and apoptosis induced by titanium dioxide nanoparticles in neuron cells. Toxicol Lett. 2010;199(3):269–276. doi:10.1016/j.toxlet.2010.09.00920863874
   PubMed Web of Science ®Google Scholar
• Zhao X, Ren X, Zhu R, Luo Z, Ren B. Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria-mediated apoptosis in zebrafish embryos. Aquat Toxicol. 2016;180:56–70. doi:10.1016/j.aquatox.2016.09.01327658222
   PubMed Web of Science ®Google Scholar
• Hadrup N, Loeschner K, Mortensen A, et al. The similar neurotoxic effects of nanoparticulate and ionic silver in vivo and in vitro. Neurotoxicology. 2012;33(3):416–423. doi:10.1016/j.neuro.2012.04.00822531227
   PubMed Web of Science ®Google Scholar
• Rao RV, Ellerby HM, Bredesen DE. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ. 2004;11(4):372–380. doi:10.1038/sj.cdd.440137814765132
   PubMed Web of Science ®Google Scholar
• Ducray AD, Stojiljkovic A, Möller A, et al. Uptake of silica nanoparticles in the brain and effects on neuronal differentiation using different in vitro models. Nanomedicine. 2017;13(3):1195–1204. doi:10.1016/j.nano.2016.11.00127871963
   PubMedGoogle Scholar
• Parveen A, Rizvi S, Mahdi F, et al. Silica nanoparticles mediated neuronal cell death in corpus striatum of rat brain: implication of mitochondrial, endoplasmic reticulum and oxidative stress. J Nanopart Res. 2014;16(11):1–15. doi:10.1007/s11051-014-2664-z
   Web of Science ®Google Scholar
• Majno G, Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol. 1995;146(1):3–15.7856735
   PubMed Web of Science ®Google Scholar
• Zhang QL, Li MQ, Ji JW, et al. In vivo toxicity of nano-alumina on mice neurobehavioral profiles and the potential mechanisms. Int J Immunopath Ph. 2011;24(1 Suppl):23S.
   PubMed Web of Science ®Google Scholar
• Halamoda Kenzaoui B, Chapuis Bernasconi C, Guney-Ayra S, Juillerat-Jeanneret L. Induction of oxidative stress, lysosome activation and autophagy by nanoparticles in human brain-derived endothelial cells. Biochem J. 2012;441(3):813. doi:10.1042/BJ2011125222026563
   PubMedGoogle Scholar
• Xie H, Wu J. Silica nanoparticles induce alpha-synuclein induction and aggregation in PC12-cells. Chem-Biol Interact. 2016;258:197–204. doi:10.1016/j.cbi.2016.09.00627613482
   PubMed Web of Science ®Google Scholar
• Wang S, Li Y, Fan J, et al. The role of autophagy in the neurotoxicity of cationic PAMAM dendrimers. Biomaterials. 2014;35(26):7588–7597. doi:10.1016/j.biomaterials.2014.05.02924906346
   PubMed Web of Science ®Google Scholar
• Wei L, Wang J, Chen A, Liu J, Feng X, Shao L. Involvement of PINK1/parkin-mediated mitophagy in ZnO nanoparticle-induced toxicity in BV-2 cells. Int J Nanomed. 2017;12:1891–1903.
   PubMed Web of Science ®Google Scholar
• Hu X, Wei Z, Mu L. Graphene oxide nanosheets at trace concentrations elicit neurotoxicity in the offspring of zebrafish. Carbon. 2017;117:182–191. doi:10.1016/j.carbon.2017.02.092
   Web of Science ®Google Scholar
• Zhong W, Lü M, Liu L, et al. Autophagy as new emerging cellular effect of nanomaterials. Chin Sci Bull. 2013;58(33):4031–4038. doi:10.1007/s11434-013-6058-x
   Google Scholar
• Zhou Y, Hong F, Tian Y, et al. Nanoparticulate titanium dioxide-inhibited dendritic development is involved in apoptosis and autophagy of hippocampal neurons in offspring mice. Toxicol Res-Uk. 2017;6(6):889–901. doi:10.1039/C7TX00153C
   PubMed Web of Science ®Google Scholar
• Li Y, Zhu H, Wang S, et al. Interplay of oxidative stress and autophagy in PAMAM dendrimers-induced neuronal cell death. Theranostics. 2015;5(12):1363–1377. doi:10.7150/thno.1318126516373
   PubMedGoogle Scholar
• Haiyuan Z, Zhaoxia J, Tian X, et al. Use of metal oxide nanoparticle band gap to develop a predictive paradigm for oxidative stress and acute pulmonary inflammation. ACS Nano. 2012;6(5):4349. doi:10.1021/nn301008722502734
   PubMedGoogle Scholar
• Tomasz P, Bakhtiyor R, Agnieszka G, et al. Using nano-QSAR to predict the cytotoxicity of metal oxide nanoparticles. Nat Nanotechnol. 2011;6(3):175–178. doi:10.1038/nnano.2011.1021317892
   PubMedGoogle Scholar
• Oksel C, Cai YM, Jing JL, Wilkins T, Xue ZW. (Q)SAR modelling of nanomaterial toxicity: acritical review. Particuology. 2015;21(4):1–19. doi:10.1016/j.partic.2014.12.001
   Google Scholar
• Vidal F, Vásquez P, Cayumán F, et al. Prevention of synaptic alterations and neurotoxic effects of PAMAM dendrimers by surface functionalization. Nanomaterials-Basel. 2018;8(1):7. doi:10.3390/nano8010007
   Web of Science ®Google Scholar
• Tianyao H, Barth RF, Weilian Y, et al. Preparation, biodistribution and neurotoxicity of liposomal cisplatin following convection enhanced delivery in normal and F98 glioma bearing rats. PLoS One. 2012;7(11):e48752. doi:10.1371/journal.pone.004875223152799
   PubMedGoogle Scholar
• Zeng Y, Kurokawa Y, Zeng Q, et al. Effects of polyamidoamine dendrimers on a 3-D neurosphere system using human neural progenitor cells. Toxicol Sci. 2016;152(1):w68. doi:10.1093/toxsci/kfw068
   Web of Science ®Google Scholar
• Imam SZ, Lantz-McPeak SM, Cuevas E, et al. Iron oxide nanoparticles induce dopaminergic damage: in vitro pathways and in vivo imaging reveals mechanism of neuronal damage. Mol Neurobiol. 2015;52(2):913–926. doi:10.1007/s12035-015-9259-226099304
   PubMedGoogle Scholar
• Yang X, Liu X, Zhang Y, et al. Cognitive deficits and decreased locomotor activity induced by single-walled carbon nanotubes and neuroprotective effects of ascorbic acid. Int J Nanomed;2014:823. doi:10.2147/IJN.S56339.
   PubMed Web of Science ®Google Scholar
• Park E, Bae E, Yi J, et al. Repeated-dose toxicity and inflammatory responses in mice by oral administration of silver nanoparticles. Environ Toxicol Pharm. 2010;30(2):162–168. doi:10.1016/j.etap.2010.05.004
   PubMed Web of Science ®Google Scholar
• Cui Y, Chen X, Zhou Z, et al. Prenatal exposure to nanoparticulate titanium dioxide enhances depressive-like behaviors in adult rats. Chemosphere. 2014;96:99–104. doi:10.1016/j.chemosphere.2013.07.05123972732
   PubMed Web of Science ®Google Scholar
• Miao W, Zhu B, Xiao X, et al. Effects of titanium dioxide nanoparticles on lead bioconcentration and toxicity on thyroid endocrine system and neuronal development in zebrafish larvae. Aquat Toxicol. 2015;161:117–126. doi:10.1016/j.aquatox.2015.02.00225703175
   PubMed Web of Science ®Google Scholar
• Oliveira GMTD, Kist LW, Pereira TCB, et al. Transient modulation of acetylcholinesterase activity caused by exposure to dextran-coated iron oxide nanoparticles in brain of adult zebrafish. Comp Biochem Physiol C Toxicol Pharmacol. 2014;162(1):77–84. doi:10.1016/j.cbpc.2014.03.01024704546
   PubMedGoogle Scholar
• Oberdorster E. Manufactured nanomaterials (fullerenes, C60) induce oxidative stress in the brain of juvenile largemouth bass. Environ Health Perspect. 2004;112(10):1058–1062. doi:10.1289/ehp.702115238277
   PubMed Web of Science ®Google Scholar
• Bulcke F, Thiel K, Dringen R. Uptake and toxicity of copper oxide nanoparticles in cultured primary brain astrocytes. Nanotoxicology. 2014;8(7):775–785. doi:10.3109/17435390.2013.82959123889294
   PubMed Web of Science ®Google Scholar
• Huang CL, Hsiao IL, Lin HC, Wang CF, Huang YJ, Chuang CY. Silver nanoparticles affect on gene expression of inflammatory and neurodegenerative responses in mouse brain neural cells. Environ Res. 2015;136:253–263. doi:10.1016/j.envres.2014.11.00625460644
   PubMed Web of Science ®Google Scholar
• Huerta-García E, Pérez-Arizti JA, Márquez-Ramírez SG, et al. Titanium dioxide nanoparticles induce strong oxidative stress and mitochondrial damage in glial cells. Free Radical Bio Med. 2014;73:84–94. doi:10.1016/j.freeradbiomed.2014.04.02624824983
   PubMed Web of Science ®Google Scholar
• Wilson CL, Natarajan V, Hayward SL, Khalimonchuk O, Kidambi S. Mitochondrial dysfunction and loss of glutamate uptake in primary astrocytes exposed to titanium dioxide nanoparticles. Nanoscale. 2015;7(44):18477–18488. doi:10.1039/c5nr03646a26274697
   PubMedGoogle Scholar
• Coccini T, Grandi S, Lonati D, Locatelli C, De Simone U. Comparative cellular toxicity of titanium dioxide nanoparticles on human astrocyte and neuronal cells after acute and prolonged exposure. Neurotoxicology. 2015;48:77–89. doi:10.1016/j.neuro.2015.03.00625783503
   PubMedGoogle Scholar
• Xu P, Xu J, Liu S, Ren G, Yang Z. In vitro toxicity of nanosized copper particles in PC12 cells induced by oxidative stress. J Nanopart Res. 2012;14(6):1–9. doi:10.1007/s11051-011-0686-322448125
   PubMedGoogle Scholar
• Zhang Y, Ali SF, Dervishi E, et al. Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived PC12 cells. ACS Nano. 2010;4(6):3181–3186. doi:10.1021/nn100717620481456
   PubMed Web of Science ®Google Scholar
• Hussain SM, Javorina AK, Schrand AM, Duhart HM, Ali SF, Schlager JJ. The interaction of manganese nanoparticles with PC-12 cells induces dopamine depletion. Toxicol Sci. 2006;92(2):456–463. doi:10.1093/toxsci/kfl02016714391
   PubMedGoogle Scholar
• Yang X, He CE, Li J, et al. Uptake of silica nanoparticles: neurotoxicity and Alzheimer-like pathology in human SK-N-SH and mouse neuro2a neuroblastoma cells. Toxicol Lett. 2014;229(1):240–249. doi:10.1016/j.toxlet.2014.05.00924831964
   PubMed Web of Science ®Google Scholar
• Chorley B, Ward W, Simmons SO, Vallanat B, Veronesi B. The cellular and genomic response of rat dopaminergic neurons (N27) to coated nanosilver. Neurotoxicology. 2014;45:12–21. doi:10.1016/j.neuro.2014.08.01025194297
   PubMed Web of Science ®Google Scholar
• Bonaventura G, Cognata V, Iemmolo R, et al. Ag-NPs induce apoptosis, mitochondrial damages and MT3/OSGIN2 expression changes in an in vitro model of human dental-pulp-stem-cells-derived neurons. Neurotoxicology. 2018. doi:10.1016/j.neuro.2018.04.014
   PubMed Web of Science ®Google Scholar
• Zhang Y, Xu Y, Li Z, et al. Mechanistic toxicity evaluation of uncoated and PEGylated single-walled carbon nanotubes in neuronal PC12 cells. ACS Nano. 2011;5(9):7020–7033. doi:10.1021/nn201625921866971
   PubMedGoogle Scholar
• Hu Q, Guo F, Zhao F, Fu Z. Effects of titanium dioxide nanoparticles exposure on parkinsonism in zebrafish larvae and PC12. Chemosphere. 2017;173:373–379. doi:10.1016/j.chemosphere.2017.01.06328129614
   PubMedGoogle Scholar
• Liu S, Xu L, Zhang T, Ren G, Yang Z. Oxidative stress and apoptosis induced by nanosized titanium dioxide in PC12 cells. Toxicology. 2010;267(1–3):172–177. doi:10.1016/j.tox.2009.11.01219922763
   PubMedGoogle Scholar
• Liu J, Kang Y, Yin S, et al. Zinc oxide nanoparticles induce toxic responses in human neuroblastoma SHSY5Y cells in a size-dependent manner. Int J Nanomed. 2017;12:8085–8099. doi:10.2147/IJN.S149070.
   Google Scholar