Pooling and analysis of published in vitro data: A proof of concept study for the grouping of nanoparticles

International Journal of Molecular Sciences

Volumn 16, Issue 11, 2015, Pages 26211-26236

  Simkó, Myrtill ^a   Tischler, Sonja ^a   Mattsson, Mats Olof ^a  

^a AIT AUSTRIAN INSTITUTE OF TECHNOLOGY   (Austria)

Author keywords

Cell viability; CNT; Intracellular ROS; Nanoparticles; Phagocytic and non phagocytic cells; Toxicity

Indexed keywords

CARBON NANOTUBE; CERIUM OXIDE; CUPRIC OXIDE; LACTATE DEHYDROGENASE; NANOPARTICLE; REACTIVE OXYGEN METABOLITE; SILICON DIOXIDE; TITANIUM DIOXIDE; ZINC OXIDE; METAL NANOPARTICLE;

ARTICLE; CELL VIABILITY; CYTOTOXICITY; HUMAN; MTT ASSAY; NONHUMAN; OXIDATIVE STRESS; PARTICLE SIZE; PHAGOCYTOSIS; VALIDATION PROCESS; CELL SURVIVAL; CHEMISTRY; META ANALYSIS; METABOLISM;

CELL SURVIVAL; METAL NANOPARTICLES; NANOPARTICLES; REACTIVE OXYGEN SPECIES;

EID: 84946606116     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms161125954     Document Type: Article

References (101)

1. Krug, H.F. Nanosafety research—Are we on the right track? Angew. Chem. 2014, 53, 12304–12319. [CrossRef] [PubMed]
2. Organisation for Economic Co-operation and Development (OECD). Guidance on grouping of chemicals. Series on testing and assessment. In ENV/JM/MONO(2014), 2nd ed.; OECD: Paris, France, 2014; Volume 194.
3. Arts, J.H.; Hadi, M.; Keene, A.M.; Kreiling, R.; Lyon, D.; Maier, M.; Michel, K.; Petry, T.; Sauer, U.G.; Warheit, D.; et al. A critical appraisal of existing concepts for the grouping of nanomaterials. Regul. Toxicol. Pharmacol. 2014, 70, 492–506. [CrossRef] [PubMed]
4. Walser, T.; Studer, C. Sameness: The regulatory crux with nanomaterial identity and grouping schemes for hazard assessment. Regul. Toxicol. Pharmacol. 2015, 72, 569–571. [CrossRef] [PubMed]
5. Oomen, A.G.; Bos, P.M.; Fernandes, T.F.; Hund-Rinke, K.; Boraschi, D.; Byrne, H.J.; Aschberger, K.; Gottardo, S.; von der Kammer, F.; Kuhnel, D.; et al. Concern-driven integrated approaches to nanomaterial testing and assessment—Report of the nanosafety cluster working group 10. Nanotoxicology 2014, 8, 334–348. [CrossRef] [PubMed]
6. Stone, V.; Pozzi-Mucelli, S.; Tran, L.; Aschberger, K.; Sabella, S.; Vogel, U.; Poland, C.; Balharry, D.; Fernandes, T.; Gottardo, S.; et al. ITS-NANO—Prioritising nanosafety research to develop a stakeholder driven intelligent testing strategy. Part. Fibre Toxicol. 2014, 11, 9. [CrossRef] [PubMed]
7. Lord, M.S.; Jung, M.; Teoh, W.Y.; Gunawan, C.; Vassie, J.A.; Amal, R.; Whitelock, J.M. Cellular uptake and reactive oxygen species modulation of cerium oxide nanoparticles in human monocyte cell line U937. Biomaterials 2012, 33, 7915–7924. [CrossRef] [PubMed]
8. Aranda, A.; Sequedo, L.; Tolosa, L.; Quintas, G.; Burello, E.; Castell, J.V.; Gombau, L. Dichloro-dihydro-fluorescein diacetate (DCFH-DA) assay: A quantitative method for oxidative stress assessment of nanoparticle-treated cells. Toxicol. In Vitro 2013, 27, 954–963. [CrossRef] [PubMed]
9. Gong, C.; Tao, G.; Yang, L.; Liu, J.; He, H.; Zhuang, Z. The role of reactive oxygen species in silicon dioxide nanoparticle-induced cytotoxicity and DNA damage in hacat cells. Mol. Biol. Rep. 2012, 39, 4915–4925. [CrossRef] [PubMed]
10. Li, Y.; Sun, L.; Jin, M.; Du, Z.; Liu, X.; Guo, C.; Li, Y.; Huang, P.; Sun, Z. Size-dependent cytotoxicity of amorphous silica nanoparticles in human hepatoma hepg2 cells. Toxicol. Vitro 2011, 25, 1343–1352. [CrossRef] [PubMed]
11. Zhang, J.; Song, W.; Guo, J.; Zhang, J.; Sun, Z.; Li, L.; Ding, F.; Gao, M. Cytotoxicity of different sized TiO2 nanoparticles in mouse macrophages. Toxicol. Ind. Health 2013, 29, 523–533. [CrossRef] [PubMed]
12. Jana, N.R. Design and development of quantum dots and other nanoparticles based cellular imaging probe. Phys. Chem. Chem. Phys. 2011, 13, 385–396. [CrossRef] [PubMed]
13. Rejman, J.; Oberle, V.; Zuhorn, I.; Hoekstra, D. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem. J. 2004, 377, 159–169. [CrossRef] [PubMed]
14. Sahay, G.; Alakhova, D.Y.; Kabanov, A.V. Endocytosis of nanomedicines. J. Control. Release 2010, 145, 182–195. [CrossRef] [PubMed]
15. Iversen, T.-G.; Skotland, T.; Sandvig, K. Endocytosis and intracellular transport of nanoparticles: Present knowledge and need for future studies. Nano Today 2011, 6, 176–185. [CrossRef]
16. Mao, Z.; Zhou, X.; Gao, C. Influence of structure and properties of colloidal biomaterials on cellular uptake and cell functions. Biomater. Sci. 2013, 1, 896–911. [CrossRef]
17. Shang, L.; Nienhaus, K.; Nienhaus, G.U. Engineered nanoparticles interacting with cells: Size matters. J. Nanobiotechnol. 2014, 12, 5. [CrossRef] [PubMed]
18. Kato, H.; Nakamura, A.; Takahashi, K.; Kinugasa, S. Accurate size and size-distribution determination of polystyrene latex nanoparticles in aqueous medium using dynamic light scattering and asymmetrical flow field flow fractionation with multi-angle light scattering. Nanomaterials 2012, 2, 15–30.
19. Gratton, S.E.; Ropp, P.A.; Pohlhaus, P.D.; Luft, J.C.; Madden, V.J.; Napier, M.E.; DeSimone, J.M. The effect of particle design on cellular internalization pathways. Proc. Natl. Acad. Sci. USA 2008, 105, 11613–11618. [CrossRef] [PubMed]
20. Oh, N.; Park, J.H. Endocytosis and exocytosis of nanoparticles in mammalian cells. Int. J. Nanomed. 2014, 9, 51–63.
21. Murphy, F.A.; Schinwald, A.; Poland, C.A.; Donaldson, K. The mechanism of pleural inflammation by long carbon nanotubes: Interaction of long fibres with macrophages stimulates them to amplify pro-inflammatory responses in mesothelial cells. Part. Fibre Toxicol. 2012, 9, 8. [CrossRef] [PubMed]
22. Landsiedel, R.; Sauer, U.G.; Ma-Hock, L.; Schneckenburger, J.; Wiemann, M. Pulmonary toxicity of nanomaterials—A critical comparison of published in vitro assays and in vivo inhalation or instillation studies. Nanomedicine 2014, 9, 2557–2585. [CrossRef] [PubMed]
23. Comfort, K.K.; Braydich-Stolle, L.K.; Maurer, E.I.; Hussain, S.M. Less is more: Long-term in vitro exposure to low levels of silver nanoparticles provides new insights for nanomaterial evaluation. ACS Nano 2014, 8, 3260–3271. [CrossRef] [PubMed]
24. Nel, A.E.; Madler, L.; Velegol, D.; Xia, T.; Hoek, E.M.; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding biophysicochemical interactions at the nano-bio interface. Nat. Mater. 2009, 8, 543–557. [CrossRef] [PubMed]
25. Wörle-Knirsch, J.M.; Pulskamp, K.; Krug, H.F. Oops they did it again! Carbon nanotubes hoax scientists in viability assays. Nano Lett. 2006, 6, 1261–1268. [CrossRef] [PubMed]
26. Jiang, X.; Weise, S.; Hafner, M.; Rocker, C.; Zhang, F.; Parak, W.J.; Nienhaus, G.U. Quantitative analysis of the protein corona on FePt nanoparticles formed by transferrin binding. J. R. Soc. Interface 2010, 7, 5–13.
27. Constantini, L.; Gilberti, R.; Knecht, D. The phagocytosis and toxicity of amorphous silica. PLoS ONE 2011, 6, 14647. [CrossRef] [PubMed]
28. Park, E.J.; Park, K. Oxidative stress and pro-inflammatory responses induced by silica nanoparticles in vivo and in vitro. Toxicol. Lett. 2009, 184, 18–25. [CrossRef] [PubMed]
29. Ye, Y.; Liu, J.; Chen, M.; Sun, L.; Lan, M. In vitro toxicity of silica nanoparticles in myocardial cells. Environ. Toxicol. Pharmacol. 2010, 29, 131–137. [CrossRef] [PubMed]
30. Passagne, I.; Morille, M.; Rousset, M.; Pujalte, I.; L’Azou, B. Implication of oxidative stress in size-dependent toxicity of silica nanoparticles in kidney cells. Toxicology 2012, 299, 112–124. [CrossRef] [PubMed]
31. Wang, F.; Gao, F.; Lan, M.; Yuan, H.; Huang, Y.; Liu, J. Oxidative stress contributes to silica nanoparticle-induced cytotoxicity in human embryonic kidney cells. Toxicol. Vitro 2009, 23, 808–815. [CrossRef] [PubMed]
32. Wang, F.; Jiao, C.; Liu, J.; Yuan, H.; Lan, M.; Gao, F. Oxidative mechanisms contribute to nanosize silican dioxide-induced developmental neurotoxicity in PC12 cells. Toxicol. Vitr. 2011, 25, 1548–1556. [CrossRef] [PubMed]
33. Akhtar, M.J.; Ahamed, M.; Kumar, S.; Siddiqui, H.; Patil, G.; Ashquin, M.; Ahmad, I. Nanotoxicity of pure silica mediated through oxidant generation rather than glutathione depletion in human lung epithelial cells. Toxicology 2010, 276, 95–102. [CrossRef] [PubMed]
34. Foldbjerg, R.; Wang, J.; Beer, C.; Thorsen, K.; Sutherland, D.S.; Autrup, H. Biological effects induced by BSA-stabilized silica nanoparticles in mammalian cell lines. Chem. Biol. Interact. 2013, 204, 28–38. [CrossRef] [PubMed]
35. Lin, W.; Huang, Y.W.; Zhou, X.D.; Ma, Y. In vitro toxicity of silica nanoparticles in human lung cancer cells. Toxicol. Appl. Pharmacol. 2006, 217, 252–259. [CrossRef] [PubMed]
36. Sun, L.; Li, Y.; Liu, X.; Jin, M.; Zhang, L.; Du, Z.; Guo, C.; Huang, P.; Sun, Z. Cytotoxicity and mitochondrial damage caused by silica nanoparticles. Toxicol. Vitr. 2011, 25, 1619–1629. [CrossRef] [PubMed]
37. Yu, Y.; Duan, J.; Yu, Y.; Li, Y.; Liu, X.; Zhou, X.; Ho, K.F.; Tian, L.; Sun, Z. Silica nanoparticles induce autophagy and autophagic cell death in hepg2 cells triggered by reactive oxygen species. J. Hazard. Mater. 2014, 270, 176–186. [CrossRef] [PubMed]
38. Lison, D.; Thomassen, L.C.; Rabolli, V.; Gonzalez, L.; Napierska, D.; Seo, J.W.; Kirsch-Volders, M.; Hoet, P.; Kirschhock, C.E.; Martens, J.A. Nominal and effective dosimetry of silica nanoparticles in cytotoxicity assays. Toxicol. Sci. 2008, 104, 155–162. [CrossRef] [PubMed]
39. 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, 172–177. [CrossRef] [PubMed]
40. Park, E.J.; Yi, J.; Chung, K.H.; Ryu, D.Y.; Choi, J.; Park, K. Oxidative stress and apoptosis induced by titanium dioxide nanoparticles in cultured BEAS-2B cells. Toxicol. Lett. 2008, 180, 222–229. [CrossRef] [PubMed]
41. Saquib, Q.; Al-Khedhairy, A.A.; Siddiqui, M.A.; Abou-Tarboush, F.M.; Azam, A.; Musarrat, J. Titanium dioxide nanoparticles induced cytotoxicity, oxidative stress and DNA damage in human amnion epithelial (wish) cells. Toxicol. Vitr. 2012, 26, 351–361. [CrossRef] [PubMed]
42. Shukla, R.K.; Sharma, V.; Pandey, A.K.; Singh, S.; Sultana, S.; Dhawan, A. Ros-mediated genotoxicity induced by titanium dioxide nanoparticles in human epidermal cells. Toxicol. Vitr. 2011, 25, 231–241. [CrossRef] [PubMed]
43. Long, T.C.; Tajuba, J.; Sama, P.; Saleh, N.; Swartz, C.; Parker, J.; Hester, S.; Lowry, G.V.; Veronesi, B. Nanosize titanium dioxide stimulates reactive oxygen species in brain microglia and damages neurons in vitro. Environ. Health Perspect. 2007, 115, 1631–1637. [CrossRef] [PubMed]
44. Sund, J.; Palomaki, J.; Ahonen, N.; Savolainen, K.; Alenius, H.; Puustinen, A. Phagocytosis of nano-sized titanium dioxide triggers changes in protein acetylation. J. Proteom. 2014, 108, 469–483. [CrossRef] [PubMed]
45. Karlsson, H.; Cronholm, P.; Gustafsson, J.; Mo, L. CuO NPs are highly toxic—A comparison between metal oxide NPs and CNTs. Chem. Res. Toxicol. 2008, 21, 1726–1732. [CrossRef] [PubMed]
46. Yu, M.; Mo, Y.; Wan, R.; Chien, S.; Zhang, X.; Zhang, Q. Regulation of plasminogen activator inhibitor-1 expression in endothelial cells with exposure to metal nanoparticles. Toxicol. Lett. 2010, 195, 82–89. [CrossRef] [PubMed]
47. Xia, T.; Kovochich, M.; Liong, M.; Madler, L.; Gilbert, B.; Shi, H.; Yeh, J.I.; Zink, J.I.; Nel, A.E. Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2008, 2, 2121–2134. [CrossRef] [PubMed]
48. Rothe, G.; Valet, G. Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 21,71-dichlorofluorescin. J. Leukoc. Biol. 1990, 47, 440–448. [PubMed]
49. Bellavite, P. The superoxide-forming enzymatic system of phagocytes. Free Radic. Biol. Med. 1988, 4, 225–261. [CrossRef]
50. Song, W.; Zhang, J.; Guo, J.; Zhang, J.; Ding, F.; Li, L.; Sun, Z. Role of the dissolved zinc ion and reactive oxygen species in cytotoxicity of ZnO nanoparticles. Toxicol. Lett. 2010, 199, 389–397. [CrossRef] [PubMed]
51. Ahamed, M.; Akhtar, M.J.; Raja, M.; Ahmad, I.; Siddiqui, M.K.; AlSalhi, M.S.; Alrokayan, S.A. ZnO nanorod-induced apoptosis in human alveolar adenocarcinoma cells via p53, survivin and bax/bcl-2 pathways: Role of oxidative stress. Nanomedicine 2011, 7, 904–913. [CrossRef] [PubMed]
52. Alarifi, S.; Ali, D.; Alkahtani, S.; Verma, A.; Ahamed, M.; Ahmed, M.; Alhadlaq, H.A. Induction of oxidative stress, DNA damage, and apoptosis in a malignant human skin melanoma cell line after exposure to zinc oxide nanoparticles. Int. J. Nanomed. 2013, 8, 983–993.
53. Wang, J.; Deng, X.; Zhang, F. ZnO nanoparticle-induced oxidative stress triggers apoptosis by activating JNK signaling pathway in cultured primary astrocytes. Nanoscale Res. Lett. 2014, 9, 117. [CrossRef] [PubMed]
54. Huang, C.C.; Aronstam, R.S.; Chen, D.R.; Huang, Y.W. Oxidative stress, calcium homeostasis, and altered gene expression in human lung epithelial cells exposed to ZnO nanoparticles. Toxicol. Vitr. 2010, 24, 45–55. [CrossRef] [PubMed]
55. Fahmy, B.; Cormier, S.A. Copper oxide nanoparticles induce oxidative stress and cytotoxicity in airway epithelial cells. Toxicol. Vitr. 2009, 23, 1365–1371. [CrossRef] [PubMed]
56. Wang, Z.; von dem Bussche, A.; Kabadi, P.K.; Kane, A.B.; Hurt, R.H. Biological and environmental transformations of copper based nanomaterials. ACS Nano 2013, 7, 8715–8727. [CrossRef] [PubMed]
57. Mittal, S.; Pandey, A.K. Cerium oxide nanoparticles induced toxicity in human lung cells: Role of ros mediated DNA damage and apoptosis. BioMed Res. Int. 2014, 2014, 891934. [CrossRef] [PubMed]
58. Horie, M.; Nishio, K.; Kato, H.; Fujita, K.; Endoh, S.; Nakamura, A.; Miyauchi, A.; Kinugasa, S.; Yamamoto, K.; Niki, E.; et al. Cellular responses induced by cerium oxide nanoparticles: Induction of intracellular calcium level and oxidative stress on culture cells. J. Biochem. 2011, 150, 461–471. [CrossRef] [PubMed]
59. Park, E.J.; Choi, J.; Park, Y.K.; Park, K. Oxidative stress induced by cerium oxide nanoparticles in cultured BEAS-2B cells. Toxicology 2008, 245, 90–100. [CrossRef] [PubMed]
60. Ting, S.R.; Whitelock, J.M.; Tomic, R.; Gunawan, C.; Teoh, W.Y.; Amal, R.; Lord, M.S. Cellular uptake and activity of heparin functionalised cerium oxide nanoparticles in monocytes. Biomaterials 2013, 34, 4377–4386. [CrossRef] [PubMed]
61. Karakoti, A.S.; Monteiro-Riviere, N.A.; Aggarwal, R.; Davis, J.P.; Narayan, R.J.; Self, W.T.; McGinnis, J.; Seal, S. Nanoceria as antioxidant: Synthesis and biomedical applications. JOM 2008, 60, 33–37. [CrossRef] [PubMed]
62. Herzog, E.; Byrne, H.J.; Davoren, M.; Casey, A.; Duschl, A.; Oostingh, G.J. Dispersion medium modulates oxidative stress response of human lung epithelial cells upon exposure to carbon nanomaterial samples. Toxicol. Appl. Pharmacol. 2009, 236, 276–281. [CrossRef] [PubMed]
63. Pulskamp, K.; Diabate, S.; Krug, H.F. Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol. Lett. 2007, 168, 58–74. [CrossRef] [PubMed]
64. Yang, H.; Liu, C.; Yang, D.; Zhang, H.; Xi, Z. Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterials: The role of particle size, shape and composition. J. Appl. Toxicol. 2009, 29, 69–78. [CrossRef] [PubMed]
65. Chen, B.; Liu, Y.; Song, W.M.; Hayashi, Y.; Ding, X.C.; Li, W.H. In vitro evaluation of cytotoxicity and oxidative stress induced by multiwalled carbon nanotubes in murine RAW264.7 macrophages and human A549 lung cells. Biomed. Environ. Sci. 2011, 24, 593–601. [PubMed]
66. Zhao, X.; Liu, R. Recent progress and perspectives on the toxicity of carbon nanotubes at organism, organ, cell, and biomacromolecule levels. Environ. Int. 2012, 40, 244–255. [CrossRef] [PubMed]
67. Cheng, W.W.; Lin, Z.Q.; Wei, B.F.; Zeng, Q.; Han, B.; Wei, C.X.; Fan, X.J.; Hu, C.L.; Liu, L.H.; Huang, J.H.; Single-walled carbon nanotube induction of rat aortic endothelial cell apoptosis: Reactive oxygen species are involved in the mitochondrial pathway. Int. J. Biochem. Cell. Biol. 2011, 43, 564–572. [CrossRef] [PubMed]
68. Wang, J.; Sun, P.; Bao, Y.; Dou, B.; Song, D.; Li, Y. Vitamin e renders protection to PC12 cells against oxidative damage and apoptosis induced by single-walled carbon nanotubes. Toxicol. Vitr. 2012, 26, 32–41. [CrossRef] [PubMed]
69. Piccinno, F.; Gottschalk, F.; Seeger, S.; Nowack, B. Industrial production quantities and uses of ten engineered nanomaterials in europe and the world. J. Nanopart. Res. 2012, 14, 1109. [CrossRef]
70. Hendren, C.O.; Mesnard, X.; Droge, J.; Wiesner, M.R. Estimating production data for five engineered nanomaterials as a basis for exposure assessment. Environ. Sci. Technol. 2011, 45, 2562–2569. [CrossRef] [PubMed]
71. Wang, Y.; Aker, W.G.; Hwang, H.M.; Yedjou, C.G.; Yu, H.; Tchounwou, P.B. A study of the mechanism of in vitro cytotoxicity of metal oxide nanoparticles using catfish primary hepatocytes and human HepG2 cells. Sci. Total Environ. 2011, 409, 4753–4762. [CrossRef] [PubMed]
72. De Volder, M.F.; Tawfick, S.H.; Baughman, R.H.; Hart, A.J. Carbon nanotubes: Present and future commercial applications. Science 2013, 339, 535–539. [CrossRef] [PubMed]
73. NCBI Pubmed. Available online: http://www.ncbi.nlm.nih.gov/pubmed (accessed on 10 January 2015).
74. Sciencedirect Sciencedirect. Available online: http://www.sciencedirect.com/ (accessed on 10 January 2015).
75. Simko, M.; Nosske, D.; Kreyling, W.G. Metrics, dose, and dose concept: The need for a proper dose concept in the risk assessment of nanoparticles. Int. J. Environ. Res. Public Health 2014, 11, 4026–4048. [CrossRef] [PubMed]
76. Teeguarden, J.G.; Hinderliter, P.M.; Orr, G.; Thrall, B.D.; Pounds, J.G. Particokinetics in vitro: Dosimetry considerations for in vitro nanoparticle toxicity assessments. Toxicol. Sci. 2007, 95, 300–312. [CrossRef] [PubMed]
77. Liu, X.; Sun, J. Endothelial cells dysfunction induced by silica nanoparticles through oxidative stress via JNK/P53 and NF-kappaB pathways. Biomaterials 2010, 31, 8198–8209. [CrossRef] [PubMed]
78. Fernandez, D.; Garcia-Gomez, C.; Babin, M. In vitro evaluation of cellular responses induced by ZnO nanoparticles, zinc ions and bulk ZnO in fish cells. Sci. Total Environ. 2013, 452, 262–274. [CrossRef] [PubMed]
79. Buerki-Thurnherr, T.; Xiao, L.; Diener, L.; Arslan, O.; Hirsch, C.; Maeder-Althaus, X.; Grieder, K.; Wampfler, B.; Mathur, S.; Wick, P. In vitro mechanistic study towards a better understanding of zno nanoparticle toxicity. Nanotoxicology 2013, 7, 402–416. [CrossRef] [PubMed]
80. Seker, S.; Elcin, A.E.; Yumak, T.; Sinag, A.; Elcin, Y.M. In vitro cytotoxicity of hydrothermally synthesized ZnO nanoparticles on human periodontal ligament fibroblast and mouse dermal fibroblast cells. Toxicol. Vitr. 2014, 28, 1349–1358. [CrossRef] [PubMed]
81. Setyawati, M.I.; Tay, C.Y.; Leong, D.T. Effect of zinc oxide nanomaterials-induced oxidative stress on the p53 pathway. Biomaterials 2013, 34, 10133–10142. [CrossRef] [PubMed]
82. Sun, J.; Wang, S.; Zhao, D.; Hun, F.H.; Weng, L.; Liu, H. 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. 2011, 27, 333–342. [CrossRef] [PubMed]
83. Sharma, V.; Anderson, D.; Dhawan, A. Zinc oxide nanoparticles induce oxidative DNA damage and ros-triggered mitochondria mediated apoptosis in human liver cells (HepG2). Apoptosis 2012, 17, 852–870. [CrossRef] [PubMed]
84. Song, Y.; Guan, R.; Lyu, F.; Kang, T.; Wu, Y.; Chen, X. In vitro cytotoxicity of silver nanoparticles and zinc oxide nanoparticles to human epithelial colorectal adenocarcinoma (Caco-2) cells. Mutat. Res. 2014, 769, 113–118. [CrossRef] [PubMed]
85. Akhtar, M.J.; Ahamed, M.; Kumar, S.; Khan, M.M.; Ahmad, J.; Alrokayan, S.A. Zinc oxide nanoparticles selectively induce apoptosis in human cancer cells through reactive oxygen species. Int. J. Nanomed. 2012, 7, 845–857. [PubMed]
86. Muthuraman, P.; Ramkumar, K.; Kim, D.H. Analysis of dose-dependent effect of zinc oxide nanoparticles on the oxidative stress and antioxidant enzyme activity in adipocytes. Appl. Biochem. Biotechnol. 2014, 174, 2851–2863. [CrossRef] [PubMed]
87. Akhtar, M.J.; Ahamed, M. Protective effect of sulphoraphene against oxidative stress mediated toxicity induced by CuO nps in mouse embryonic fibroblasts BALB 3T3. J. Toxicol. Sci. 2012, 37, 139–148. [CrossRef] [PubMed]
88. Kumbicak, U.; Cavas, T.; Cinkilic, N.; Kumbicak, Z.; Vatan, O.; Yilmaz, D. Evaluation of in vitro cytotoxicity and genotoxicity of copper-zinc alloy nanoparticles in human lung epithelial cells. Food Chem. Toxicol. 2014, 73, 105–112. [CrossRef] [PubMed]
89. Xu, P.; Xu, J.; Liu, S.; Yang, Z. Nano copper induced apoptosis in podocytes via increasing oxidative stress. J. Hazard. Mater. 2012, 241, 279–286. [CrossRef] [PubMed]
90. Schubert, D.; Dargusch, R.; Raitano, J.; Chan, S.W. Cerium and yttrium oxide nanoparticles are neuroprotective. Biochem. Biophys. Res. Commun. 2006, 342, 86–91. [CrossRef] [PubMed]
91. Celardo, I.; de Nicola, M.; Mandoli, C.; Pedersen, J.Z.; Traversa, E.; Ghibelli, L. Ce3+ ions determine redox-dependent anti-apoptotic effect of cerium oxide nps. ACS Nano 2011, 5, 4537–4549. [CrossRef] [PubMed]
92. Choi, S.J.; Oh, J.M.; Choy, J.H. Toxicological effects of inorganic nanoparticles on human lung cancer A549 cells. J. Inorg. Biochem. 2009, 103, 463–471. [CrossRef] [PubMed]
93. Cicchetti, R.; Divizia, M.; Valentini, F.; Argentin, G. Effects of single-wall carbon nanotubes in human cells of the oral cavity: Geno-cytotoxic risk. Toxicol. Vitr. 2011, 25, 1811–1819. [CrossRef] [PubMed]
94. Guo, Y.Y.; Zhang, J.; Zheng, Y.F.; Yang, J.; Zhu, X.Q. Cytotoxic and genotoxic effects of multi-wall carbon nanotubes on human umbilical vein endothelial cells in vitro. Mutat. Res. 2011, 721, 184–191. [CrossRef] [PubMed]
95. Kaiser, J.P.; Buerki-Thurnherr, T.; Wick, P. Influence of single walled carbon nanotubes at subtoxical concentrations on cell adhesion and other cell parameters of human epithelial cells. J. King Saud Univ. Sci. 2012, 25, 15–27. [CrossRef]
96. Pichardo, S.; Gutierrez-Praena, D.; Puerto, M.; Sanchez, E.; Grilo, A.; Camean, A.M.; Jos, A. Oxidative stress responses to carboxylic acid functionalized single wall carbon nanotubes on the human intestinal cell line Caco-2. Toxicol. Vitr. 2012, 26, 672–677. [CrossRef] [PubMed]
97. Song, M.; Zeng, L.; Yuan, S.; Yin, J.; Wang, H.; Jiang, G. Study of cytotoxic effects of single-walled carbon nanotubes functionalized with different chemical groups on human MCF7 cells. Chemosphere 2013, 92, 576–582. [CrossRef] [PubMed]
98. Thurnherr, T.; Brandenberger, C.; Fischer, K.; Diener, L.; Manser, P.; Maeder-Althaus, X.; Kaiser, J.P.; Krug, H.F.; Rothen-Rutishauser, B.; Wick, P. A comparison of acute and long-term effects of industrial multiwalled carbon nanotubes on human lung and immune cells in vitro. Toxicol. Lett. 2011, 200, 176–186. [CrossRef] [PubMed]
99. Thurnherr, T.; Su, D.S.; Diener, L.; Weinberg, G.; Manser, P.; Pfänder, N.; Arrigo, R.; Schuster, M.E.; Wick, P.; Krug, H.F. Comprehensive evaluation ofin vitrotoxicity of three large-scale produced carbon nanotubes on human jurkat t cells and a comparison to crocidolite asbestos. Nanotoxicology 2009, 3, 319–338. [CrossRef]
100. Wang, J.; Sun, P.; Bao, Y.; Liu, J.; An, L. Cytotoxicity of single-walled carbon nanotubes on PC12 cells. Toxicol. Vitro 2011, 25, 242–250. [CrossRef] [PubMed]
101. Ye, S.F.; Wu, Y.H.; Hou, Z.Q.; Zhang, Q.Q. Ros and NF-kappaB are involved in upregulation of IL-8 in A549 cells exposed to multi-walled carbon nanotubes. Biochem. Biophys. Res. Commun. 2009, 379, 643–648. [CrossRef] [PubMed]