In vitro toxicity of zinc oxide nanoparticles: a review

Ahamed M, Akhtar MJ, Raja M, Ahmad I, Siddiqui MK, AlSalhi MS, Alrokayan SA (2011) ZnO nanorod-induced apoptosis in human alveolar adenocarcinoma cells via p53, survivin and bax/bcl-2 pathways: role of oxidative stress. Nanomedicine UK 7(6):904–913 Amrita M, Suraj Kumar T, Rizwan W, Song-Hoon J, Inho H, You-Bing Y, Young-Soon K, Hyung-Shik S, Soon-Il Y (2011) Microbial synthesis of gold nanoparticles using the fungus Penicillium brevicompactum and their cytotoxic effects against mouse mayo blast cancer C2C12 cells. Appl Microbiol Biotechnol 92(3):617–630 Berntsen P, Park CY, Rothen-Rutishauser B, Tsuda A, Sager TM, Molina RM, Donaghey TC, Alencar AM, Kasahara DI, Ericsson T, Millet EJ, Swenson J, Tschumperlin DJ, Butler JP, Brain JD, Fredberg JJ, Gehr P, Zhou EH (2010) Biomechanical effects of environmental and engineered particles on human airway smooth muscle cells. J R Soc Interface 7(3):S331–S340 Brunner TJ, Wick P, Manser P, Spohn P, Grass RN, Limbach LK, Bruinink A, Stark WJ (2006) In vitro cytotoxicity of oxide nanoparticles: comparison to asbestos, silica, and the effect of particle solubility. Environ Sci Technol 40(14):4374–4381 Buerki-Thurnherr T, Xiao L, Diener L, Arslan O, Hirsch C, Maeder-Althaus X, Grieder K, Wampfler B, Mathur S, Wick P, Krug HF (2013) In vitro mechanistic study towards a better understanding of ZnO nanoparticle toxicity. Nanotoxicology 7(4):402–416 Cho WS, Duffin R, Poland CA, Duschl A, Oostingh GJ, Macnee W, Bradley M, Megson IL, Donaldson K (2012) Differential pro-inflammatory effects of metal oxide nanoparticles and their soluble ions in vitro and in vivo; zinc and copper nanoparticles, but not their ions, recruit eosinophils to the lungs. Nanotoxicology 6(1):22–35 De Berardis B, Civitelli G, Condello M, Lista P, Pozzi R, Arancia G, Meschini S (2010) Exposure to ZnO nanoparticles induces oxidative stress and cytotoxicity in human colon carcinoma cells. Toxicol Appl Pharmacol 246(3):116–127 Deng X, Luan Q, Chen W, Wang Y, Wu M, Zhang H, Jiao Z (2009) Nanosized zinc oxide particles induce neural stem cell apoptosis. Nanotechnology 20(11):115101 George S, Pokhrel S, Xia T, Gilbert B, Ji Z, Schowalter M, Rosenauer A, Damoiseaux R, Bradley KA, Mädler L, Nel AE (2010) Use of a rapid cytotoxicity screening approach to engineer a safer zinc oxide nanoparticle through iron doping. ACS Nano 4(1):15–29 Gerloff K, Albrecht C, Boots AW, Förster I, Schins RP (2009) Cytotoxicity and oxidative DNA damage by nanoparticles in human intestinal Caco-2 cells. Nanotoxicology 3(4):355–364 Hackenberg S, Zimmermann FZ, Scherzed A, Friehs G, Froelich K, Ginzkey C, Koehler C, Burghartz M, Hagen R, Kleinsasser N (2011) Repetitive exposure to zinc oxide nanoparticles induces DNA damage in human nasal mucosa mini organ cultures. Environ Mol Mutagen 52(7):582–589 Hanley C, Thurber A, Hanna C, Punnoose A, Zhang J, Wingett DG (2009) The influences of cell type and ZnO nanoparticle size on immune cell cytotoxicity and cytokine induction. Nanoscale Res Lett 4(12):1409–1420 Heng BC, Zhao X, Xiong S, Ng KW, Boey FY, Loo JS (2011) Cytotoxicity of zinc oxide (ZnO) nanoparticles is in influenced by cell density and culture format. Arch Toxicol 85:695–704 Hsiao IL, Huang YJ (2011a) Titanium oxide shell coatings decrease the cytotoxicity of ZnO nanoparticles. Chem Res Toxicol 24(3):303–313 Hsiao IL, Huang YJ (2011b) Effects of various physicochemical characteristics on the toxicities of ZnO and TiO(2) nanoparticles toward human lung epithelial cells. Sci Total Environ 409(7):1219–1228 Huang CC, Aronstam RS, Chen DR, Huang YW (2010) Oxidative stress, calcium homeostasis, and altered gene expression in human lung epithelial cells exposed to ZnO nanoparticles. Toxicol In Vitro 24(1):45–55 Jeng HA, Swanson J (2006) Toxicity of metal oxide nanoparticles in mammalian cells. J Environ Sci Health A Tox Hazard Subst Environ Eng 41(12):2699–2711 Kao YY, Chen YC, Cheng TJ, Chiung YM, Liu PS (2012) Zinc oxide nanoparticles interfere with zinc ion homeostasis to cause cytotoxicity. Toxicol Sci 125(2):462–472 Kermanizadeh A, Pojana G, Gaiser BK, Birkedal R, Bilanicová D, Wallin H, Jensen KA, Sellergren B, Hutchison GR, Marcomini A, Stone V (2013) In vitro assessment of engineered nanomaterials using a hepatocyte cell line: cytotoxicity, proinflammatory cytokines and functional markers. Nanotoxicology 7(3):301–313 Kim YH, Fazlollahi F, Kennedy IM, Yacobi NR, Hamm-Alvarez SF, Borok Z, Kim KJ, Crandall ED (2010) Alveolar epithelial cell injury due to zinc oxide nanoparticle exposure. Am J Respir Crit Care Med 182(11):1398–1409 Kocbek P, Teskac K, Kreft ME, Kristl J (2010) Toxicological aspects of long-term treatment of keratinocytes with ZnO and TiO2 nanoparticles. Small 6(17):1908–1917 Landsiedel R, Ma-Hock L, Van Ravenzwaay B, Schulz M, Wiench K, Champ S, Schulte S, Wohlleben W, Oesch F (2010) Gene toxicity studies on titanium dioxide and zinc oxide nanomaterials used for UV-protection in cosmetic formulations. Nanotoxicology 4:364–381 Lenz AG, Karg E, Lentner B, Dittrich V, Brandenberger C, Rothen-Rutishauser B, Schulz H, Ferron GA, Schmid O (2009) A dose-controlled system for air-liquid interface cell exposure and application to zinc oxide nanoparticles. Part Fibre Toxicol 6:32 Li JJ, Hartono D, Ong CN, Bay BH, Yung LY (2010) Autophagy and oxidative stress associated with gold nanoparticles. Biomaterials 31(23):5996–6003 Meyer K, Rajanahalli P, Ahamed M, Rowe JJ, Hong Y (2011) ZnO nanoparticles induce apoptosis in human dermal fibroblasts via p53 and p38 pathways. Toxicol In Vitro 25(8):1721–1726 Moos PJ, Chung K, Woessner D, Honeggar M, Cutler NS, Veranth JM (2010) ZnO particulate matter requires cell contact for toxicity in human colon cancer cells. Chem Res Toxicol 23(4):733–739 Moos PJ, Olszewski K, Honeggar M, Cassidy P, Leachman S, Woessner D, Cutler NS, Veranth JM (2011) Responses of human cells to ZnO nanoparticles: a gene transcription study. Metallomics 3(11):1199–1211 Müller KH, Kulkarni J, Motskin M, Goode A, Winship P, Skepper JN, Ryan MP, Porter AE (2010) pH-dependent toxicity of high aspect ratio ZnO nanowires in macrophages due to intracellular dissolution. ACS Nano 4(11):6767–6779 Muthuraman P, Ramkumar K, Kim DH (2014a) Analysis of dose-dependent effect of Zinc oxide nanoparticles on the oxidative stress and anti-oxidant enzyme activity in adipocytes. Appl Biochem Biotechnol. doi:10.1007/s12010-014-1231-5 Muthuraman P, Muthuviveganandavel V, Kim DH (2014b) Cytotoxicity of Zinc oxide nanoparticles on anti-oxidant enzyme activities and mRNA expression in the co-cultured C2C12 and 3T3-L1 Cells. Appl Biochem Biotechnol. doi:10.1007/s12010-014-1351-y Nagarajan P, Rajagopalan V (2008) Enhanced bioactivity of ZnO nanoparticles-an antimicrobial study. Sci Technol Adv Mater 9:035004 Ng KW, Khoo SP, Heng BC, Setyawati MI, Tan EC, Zhao X, Xiong S, Fang W, Leong DT, Loo JS (2011) The role of the tumor suppressor p53 pathway in the cellular DNA damage response to zinc oxide nanoparticles. Biomaterials 32(32):8218–8225 Osman IF, Baumgartner A, Cemeli E, Fletcher JN, Anderson D (2010) Genotoxicity and cytotoxicity of zinc oxide and titanium dioxide in HEp-2 cells. Nanomedicine UK 5(8):1193–1203 Osmond MJ, McCall MJ (2010) Zinc oxide nanoparticles in modern sunscreens: an analysis of potential exposure and hazard. Nanotoxicology 4(1):15–41 Palomäki J, Karisola P, Pylkkänen L, Savolainen K, Alenius H (2010) Engineered nanomaterials cause cytotoxicity and activation on mouse antigen presenting cells. Toxicology 267(1–3):125–131 Pan X, Redding JE, Wiley PA, Wen L, McConnell JS, Zhang B (2010) Mutagenicity evaluation of metal oxide nanoparticles by the bacterial reverse mutation assay. Chemosphere 79(1):113–116 Pujalté I, Passagne I, Brouillaud B, Tréguer M, Durand E, Ohayon-Courtès C, L’Azou B (2011) Cytotoxicity and oxidative stress induced by different metallic nanoparticles on human kidney cells. Part Fibre Toxicol 8:10 Qun L, Shui-Lin C, Wan-Chao J (2007) Durability of nano ZnO antibacterial cotton fabric to sweat. J Appl Polym Sci 103:412–416 Rob JV, Wim HJ (2012) A review of mammalian toxicity of ZnO nanoparticles. Nanotechnol Sci Appl 5:61–71 Shah MA, Al-Shahry M (2009) Zinc oxide nanoparticles prepared by the reaction of zinc metal with ethanol. JKAU: Sci 21(1):61–67 Sharma V, Shukla RK, Saxena N, Parmar D, Das M, Dhawan A (2009) DNA damaging potential of zinc oxide nanoparticles in human epidermal cells. Toxicol Lett 185(3):211–218 Sharma V, Singh SK, Anderson D, Tobin DJ, Dhawan A (2011) Zinc oxide nanoparticles induced genotoxicity in primary human epidermal keratinocytes. J Nanosci Nanotechnol 11(5):3782–3788 Snyder-Talkington N, Qian Y, Castranova V, Guo NL (2012) New perspectives for in vitro risk assessment of multiwalled carbon nanotubes: application of co-culture and bioinformatics. J Toxicol Environ Health B 15:468–492 Song W, Zhang J, Guo J, Zhang J, Ding F, Li L, Sun Z (2010) Role of the dissolved zinc ion and reactive oxygen species in cytotoxicity of ZnO nanoparticles. Toxicol Lett 199(3):389–397 Sun J, Wang S, Zhao D, Hun FH, Weng L, Liu H (2011) Cytotoxicity, permeability, and inflammation of metal oxide nanoparticles in human cardiac microvascular endothelial cells: cytotoxicity, permeability, and inflammation of metal oxide nanoparticles. Cell Biol Toxicol 27(5):333–342 Taccola L, Raffa V, Riggio C, Vittorio O, Iorio MC, Vanacore R, Pietrabissa A, Cuschieri A (2011) Zinc oxide nanoparticles as selective killers of proliferating cells. Int J Nanomed 6:1129–1140 Umrani DR, Paknikar KM (2014) Zinc oxide nanoparticles show antidiabetic activity in streptozotocin-induced Types-1 and 2 diabetic rats. Nanomedicine 9(1):89–104 Valdiglesias V, Costa C, Kiliç G, Costa S, Pásaro E, Laffon B, Teixeira JP (2013) Neuronal cytotoxicity and genotoxicity induced by zinc oxide nanoparticles. Environ Int 55:92–100 Wang Y, Aker WG, Hwang HM, Yedjou CG, Yu H, Tchounwou PB (2011) A study of the mechanism of in vitro cytotoxicity of metal oxide nanoparticles using catfish primary hepatocytes and human HepG2 cells. Sci Total Environ 409(22):4753–4762 Wu W, Samet JM, Peden DB, Bromberg PA (2010) Phosphorylation of p65 is required for zinc oxide nanoparticle-induced interleukin 8 expression in human bronchial epithelial cells. Environ Health Perspect 118(7):982–987 Xia T, Kovochich M, Liong M, Mädler L, Gilbert B, Shi H, Yeh JI, Zink JI, Nel AE (2008) Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2(10):2121–2134 Yang H, Liu C, Yang D, Zhang H, Xi Z (2009) Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterials: the role of particle size, shape and composition. J Appl Toxicol 29(1):69–78 Yang ST, Liu JH, Wang J, Yuan Y, Cao A, Wang H, Liu Y, Zhao Y (2010) Cytotoxicity of zinc oxide nanoparticles: importance of microenvironment. J Nanosci Nanotechnol 10(12):8638–8645 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-1α and IL-1β. Proc Natl Acad Sci USA 107(45):19449–19454 Yin H, Casey PS, McCall MJ (2010) Surface modifications of ZnO nanoparticles and their cytotoxicity. J Nanosci Nanotechnol 10(11):7565–7570 Yoshida R, Kitamura D, Maenosono S (2009) Mutagenicity of water-soluble ZnO nanoparticles in Ames test. J Toxicol Sci 34(1):119–122 Yuan JH, Chen Y, Zha HX, Song LJ, Li CY, Li JQ, Xia XH (2010) Determination, characterization and cytotoxicity on HELF cells of ZnO nanoparticles. Colloid Surf B 76(1):145–150 Zabirnyk O, Yezhelyev M, Seleverstov O (2007) Nanoparticles as a novel class of autophagy activators. Autophagy 3(3):278–281 Zhao J, Castranova V (2011) Toxicology of nanomaterials used in nanomedicine. J Toxicol Environ Health B 14:593–632