Research Article
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Nickel oxide nanoparticles induced DNA damages in human liver cells

Year 2021, Volume: 51 Issue: 2, 175 - 182, 31.08.2021

Mahmoud Abudayyak , E. Elif Güzel Gül Özhan

Abstract

Background and Aims: Nickel oxide nanoparticles (NiO-NPs) are one of the most used nanoparticles, especially as photosensitizers. Although some studies evaluate their toxicity in the liver, the information about their toxicity at the cellular and molecular levels is still controversial. In the present study, it was aimed to investigate the in vitro toxic potentials of NiO-NPs (average size 15.0 nm) in the liver (HepG2) cell line. Methods: NiO-NPs were characterized by Transmission Electron Microscopy (TEM), the cellular uptake of NPs and the morphologic changes were evaluated by TEM and Inductively Coupled Plasma-Mass Spectrometry (ICP-MS), the cytotoxicity was evaluated by MTT and neutral red uptake (NRU) tests, comet assay was used for genotoxicity, Annexin V-FITC/propidium iodide (PI) apoptosis detection kit was used for apoptosis/ necrosis evaluation and Enzyme-Linked Immune Sorbent Assays (ELISA) kits were used for the potential of oxidative damage. Results: Our results showed that cellular uptake of NiO-NPs led to morphological changes in the cells, and caused cell death (IC50 was 146.7 μg/mL by MTT) mainly by apoptosis. Genotoxicity and oxidative damage were observed to be in a dosedependent manner. Conclusion: Results confirm previous data and draw attention to the toxic effects of NiO-NPs; further in vivo and in vitro studies need to be done to clarify the safety or toxicity of NiO-NPs.

Keywords

Nickel oxide Nanoparticles Genotoxicity Oxidative stress Apoptosis

Supporting Institution

Research Fund of Istanbul University

Project Number

37785

References

  • • Abudayyak, M., Guzel, E., & Özhan, G. (2017a). Nickel oxide nanoparticles induce oxidative DNA damage and apoptosis in kidney cell line (NRK-52E). Biological Trace Element Research, 178(1), 98-104. https://doi.org/10.1007/s12011016–0892-z.
  • • Abudayyak, M., Guzel, E., & Özhan, G. (2017b). Nickel oxide nanoparticles are highly toxic to SH-SY5Y neuronal cells. Neurochemistry International, 108, 7-14. https://doi.org/10.1016/j. neuint.2017.01.017.
  • • Ahamed, M. (2011). Toxic response of nickel nanoparticles in human lung epithelial A549 cells. Toxicology in vitro, 25(4), 930-936. https://doi.org/10.1016/j.tiv.2011.02.015.
  • • Ahamed, M., Akhtar, M.J., Siddiqui, M.A., Ahmad, J., Musarrat, J., Al-Khedhairy, A.A. … Alrokayan, S.A. (2011). Oxidative stress mediated apoptosis induced by nickel ferrite nanoparticles in cultured A549 cells. Toxicology, 283(2-3), 101-108. https://doi. org/10.1016/j.tox.2011.02.010.
  • • Ahamed, M., Ali, D., Alhadlaq, H.A., & Akhtar, M.J. (2013). Nickel oxide nanoparticles exert cytotoxicity via oxidative stress and induce apoptotic response in human liver cells (HepG2). Chemosphere, 93(10), 2514-2522. https://doi.org/10.1016/j.chemosphere. 2013.09.047.
  • • Ahmad, J., Alhadlaq, H.A., Siddiqui, M.A., Saquib, Q., Al-Khedhairy, A.A., Musarrat, J., & Ahamed, M. (2013). Concentration-dependent induction of reactive oxygen species, cell cycle arrest and apoptosis in human liver cells after nickel nanoparticles exposure. Environmental Toxicology, 30, 137-148. https://doi.org/10.1002/ tox.21879.
  • • Arora, S., Rajwade, J.M., & Paknikar, K.M. (2012). Nanotoxicology and in vitro studies: the need of the hour. Toxicology and Applied Pharmacology, 258(2), 151-165. https://doi.org/10.1016/j. taap.2011.11.010.
  • • Barillet, S., Simon-Deckers, A., Herlin-Boime, N., Mayne-L’Hermite, M., Reynaud, C., Cassio, D., & Carrière, M. (2010). Toxicological consequences of TiO2, SiC nanoparticles and multi-walled carbon nanotubes exposure in several mammalian cell types: an in vitro study. Journal of Nanoparticle Research, 12(1), 61-73. https://doi. org/10.1007/s11051-009-9694-y.
  • • Boverhof, D.R., & Raymond M.D. (2010). Nanomaterial characterization: considerations and needs for hazard assessment and safety evaluation. Analytical and Bioanalytical Chemistry, 396(3), 953-961. https://doi.org/10.1007/s00216-009-3103-3.
  • • Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 7, 248-254. https://doi.org/10.1006/abio.1976.999.
  • • Brand, R.M., Hannah, T.L., Mueller, C., Cetin, Y., & Hamel, FG. (2000). A novel system to study the impact of epithelial barrierson cellular metabolism. Annals of Biomedical Engineering, 28, 1210-1217. https://doi.org/10.1114/1.1318926.
  • • Brooking, J., Davis, S.S., & Illum, L. (2001). Transport of nanoparticles across the rat nasal mucosa. Journal of Drug Targeting, 9, 267-279. https://doi.org/10.3109/10611860108997935.
  • • Capasso, L., Marina, C., & Maurizio, G. (2014). Nickel oxide nanoparticles induce inflammation and genotoxic effect in lung epithelial cells. Toxicology Letters, 226(1), 28-34. https://doi.org/10.1016/j. toxlet.2014.01.040.
  • • Chen, X, Wang, Z., Zhou, J., Fu, X., Liang, J., Qiu, Y., & Huang, Z. (2014). Renal interstitial fibrosis induced by high-dose mesoporous silica nanoparticles via the NF-ΚB signaling pathway. International Journal of Nanomedicine, 10, 1-22. https://doi.org/10.2147/ IJN.S73538.
  • • Cho, W.S., Duffin, R., Poland, C.A., Howie, S.E., MacNee, W., Bradley, M. … Donaldson, K. (2010). Metal oxide nanoparticles induce unique inflammatory footprints in the lung: important implications for nanoparticle testing. Environmental Health Perspectives, 118(12), 1699-1706. https://doi.org/10.1289/ehp.1002201.
  • • Collins, A.R. (2004). The comet assay for DNA damage and repair: principles, applications, and limitations. Applied Biochemistry and Biotechnology - Part B Molecular Biotechnology, 26(3), 249-261. https://doi.org/10.1385/MB:26:3:249.
  • • Dhawan, A., & Sharma, V. (2010). Toxicity assessment of nanomaterials: methods and challenges. Analytical and Bioanalytical Chemistry 398(2), 589-605. https://doi.org/10.1007/s00216-010- 3996-x.
  • • Duan, W.X., He, M.D., Mao, L., Qian, F.H., Li, Y.M., Pi, H.F. … Zhou, Z. (2015). NiO nanoparticles induce apoptosis through repressing SIRT1 in human bronchial epithelial cells. Toxicology and Applied Pharmacology, 286(2), 80-91. https://doi.org/10.1016/j. taap.2015.03.024.
  • • Dunnick, J.K., Benson, J.M., Hobbs, C.H., Hahn, F.F., Cheng, Y.S., & Eidson, A.F. (1988). Comparative toxicity of nickel oxide, nickel sulphate hexahydrate, and nickel subsulfide after 12 days of inhalation exposure to F344/N rats and B6C3F1 mice. Toxicology, 50, 145-156. https://doi.org/10.1016/0300-483X(88)90087-X
  • • Horev-Azaria, L., Kirkpatrick, C.J., Korenstein, R., Marche, P.N., Maimon, O., Ponti, J. … Villiers, C. (2011). Predictive toxicology of cobalt nanoparticles and ions: comparative in vitro study of different cellular models using methods of knowledge discovery from data. Journal of Toxicological Sciences, 122, 489-501. https:// doi.org/10.1093/toxsci/kfr124.
  • • Horie, M., Fukui, H., Nishio, K., Endoh, S., Kato, H., Fujita, K., Miyauchi, A. … Iwahashi, H. (2011). Evaluation of acute oxidative stress induced by NiO nanoparticles in vivo and in vitro. Journal of Occupational Health, 53, 64-74. https://doi.org/10.1539/joh.l10121
  • • Horie, M., Fukui, H., Endoh, S., Maru, J., Miyauchi, A., Shichiri, M. … Iwahashi, H. (2012). Comparison of acute oxidative stress on rat lung induced by nano and fine-scale, soluble and insoluble metal oxide particles: NiO and TiO2. Inhalation Toxicology, 24(7), 391-400. https://doi.org/10.3109/08958378.2012.682321.
  • • Horie, M., Nishio, K., Fujita, K., Kato, H., Nakamura, A., Kinugasa, S. … Nakanishi, J. (2009). Ultrafine NiO particles induce cytotoxicity in vitro by cellular uptake and subsequent Ni(II) release. Chemical Research in Toxicology, 22(8), 1415-1426. https://doi.org/10.1021/ tx900171n.
  • • International Agency for Research on Cancer (IARC). (1990). Nickel compounds group 1, IARC monographs on the evaluation of carcinogenic risks to human’s chromium, nickel and welding. IARC 49, 257-411.
  • • Jeong, J., Kim, J., Seok, S.H., & Cho, W.S. (2016). Indium oxide (In2O3) nanoparticles induce progressive lung injury distinct from lung injuries by copper oxide (CuO) and nickel oxide (NiO) nanoparticles. Archives of Toxicology, 90(4), 817-828. https://doi. org/10.1007/s00204-015-1493-x.
  • • Kang, G.S., Gillespie, P.A., Gunnison, A., Rengifo, H., Koberstein, J., & Chen, L.C. (2011). Comparative pulmonary toxicity of inhaled nickel nanoparticles; role of deposited dose and solubility. Inhalation Toxicology, 23(2), 95-103. https://doi.org/10.3109/0895837 8.2010.543440.
  • • Khatchadourian, A., & Maysinger, D. (2009). Lipid droplets: their role in nanoparticle-induced oxidative stress. Molecular Pharmaceutics, 6(4), 1125-1137. https://doi.org/10.1021/mp900098p.
  • • Kim, Y.J., Yu, M., Park, H.O., & Yang, S.I. (2010). Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by silica nanomaterials in human neuronal cell line. Molecular and Cellular Toxicology, 6(4), 337-344. https://doi.org/10.1007/s13273-010- 0045-y.
  • • Lanone, S., Rogerieux, F., Geys, J., Dupont, A., Maillot-Marechal, E., Boczkowski, J. … Hoet, P. (2009). Comparative toxicity of 24 manufactured nanoparticles in human alveolar epithelial and macrophage cell lines. Particle and Fibre Toxicology, 6, 1-12. https://doi. org/10.1186/1743-8977-6-14.
  • • Lee, J., Homma, T., Kurahashi, T., Kang, E.S., & Fujii, J. (2015). Oxidative stress triggers lipid droplet accumulation in primary cultured hepatocytes by activating fatty acid synthesis. Biochemical and Biophysical Research Communications, 464(1), 229-235. https://doi. org/10.1016/j.bbrc.2015.06.121.
  • • Marmorato, P., Ceccone, G., Gianoncelli, A., Pascolo, L., Ponti, J., Rossi, F. … Kiskinova, M. (2011). Cellular distribution and degradation of cobalt ferrite nanoparticles in balb/3T3 mouse fibroblasts. Toxicology Letters, 207(2), 128-136. https://doi.org/10.1016/j.toxlet. 2011.08.026.
  • • Martin, K.R., Failla, M.L., & Smith, J.C. (1997). Differential susceptibility of Caco-2 and HepG2 human cell lines to oxidative stress. Journal of the Elisha Mitchell Scientific Society, 113(4), 149-162. https://www.jstor.org/stable/44706114.
  • • Morimoto, Y., Ogami, A., Todoroki, M., Yamamoto, M., Murakami, M., Hirohashi, M. … Tanaka, I. (2010). Expression of inflammationrelated cytokines following intratracheal instillation of nickel oxide nanoparticles. Nanotoxicology, 4(2), 161-176. https://doi. org/10.3109/17435390903518479.
  • • Morimoto, Y., Hirohashi, M., Ogami, A., Oyabu, T., Myojo, T., Hashib, M. … Tanaka, I. (2011). Pulmonary toxicity following an intratracheal instillation of nickel oxide nanoparticle agglomerates. Journal of Occupational Health, 53(4), 293-295. https://doi. org/10.1539/joh.11-0034-BR.
  • • Napierska, D., Thomassen, L.C., Lison, D., Marten,s J.A., & Hoet, P.H. 2010. The nanosilica hazard: another variable entity. Particle and Fibre Toxicology, 7(1), 39. https://doi.org/10.1186/1743-8977-7-39.
  • • Nishi, K., Morimoto, Y., Ogami, A., Murakami, M., Myojo, T., Oyabu, T., Kadoya, C. … Tanaka, I. (2009). Expression of cytokine-induced neutrophil chemoattractant in rat lungs by intratracheal instillation of nickel oxide nanoparticles. Inhalation Toxicology, 21, 1030- 1039. https://doi.org/ 10.1080/08958370802716722.
  • • O’Brien, P.J., Irwin, W., Diaz, D., Howard-Cofield, E., Krejsa, C.M., Slaughter, M.R., Gao, B. … Hougham, C. (2006). High concordance of drug-induced human hepatotoxicity with in vitro cytotoxicity measured in a novel cell-based model using high content screening. Archives of Toxicology, 80, 580-604. https://doi.org/10.1007/ s00204-006-0091-3.
  • • Oberdorster, G. (2001). Pulmonary effects of inhaled ultrafine particles. International Archives of Occupational and Environmental Health, 74, 1-8. https://doi.org/10.1007/s004200000185.
  • • Oberdorster, G., Oberdorster, E., & Oberdorster, J. (2005). Nanotoxicology: An emerging discipline evolving from studies of ultrafine particles. Environmental Health Perspectives 113, 823-839. https:// doi.org/10.1289/ehp.7339.
  • • Ogami, A., Morimoto, Y., Myojo, T., Oyabu, T., Murakami, M., Todoroki, M. … Tanaka, I. (2009). Pathological features of different sizes of nickel oxide following intratracheal instillation in rats. Inhalation Toxicology, 21(10), 812-818. https://doi. org/10.1080/08958370802499022.
  • • Oyabu, T., Ogami, A., Morimoto, Y., Shimada, M., Lenggoro, W., Okuyama, K., & Tanaka, I. (2007). Biopersistence of inhaled nickel oxide nanoparticles in rat lung. Inhalation Toxicology, 19(1), 55-58. https://doi.org/10.1080/08958370701492995.
  • • Repetto, G., del Peso, A., & Zurita, J.L. (2008). Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nature Protocols, 3(7), 1125-1131. https://doi.org/10.1038/nprot.2008.75.
  • • Sadeghi, L., Tanwir, F., & Babadi, V.Y. (2015). In vitro toxicity of iron oxide nanoparticle: oxidative damages on HepG2 cells. Experimental and Toxicologic Pathology, 67, 197-203. https://doi. org/10.1016/j.etp.2014.11.010.
  • • Sahu, S., Njoroge, J, Bryce, S.M., Yourick, J.J., & Sprando, R.L. (2014). Comperative genotoxicity of nanosilver in human liver HepG2 and colon Caco2 cells evaluated by a flow cytometric in vitro micronucleus assay. Journal of Applied Toxicology, 34, 1226-1234. https://doi.org/10.1002/jat.3065.
  • • Schrand, A.M., Rahman, M.F., Hussain, S.M., Schlager, J.J., Smith, D.A., & Syed, A.F. (2010). Metal-based nanoparticles and their toxicity assessment. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, 2(5), 544-568. https://doi.org/10.1002/ wnan.103.
  • • Siddiqui, M.A., Ahamed, M., Ahmad, J., Majeed Khan M.A., Musarrat, J. Al-Khedhairy, A.A., & Alrokayan, S.A. (2012). Nickel oxide nanoparticles induce cytotoxicity, oxidative stress and apoptosis in cultured human cells that is abrogated by the dietary antioxidant curcumin. Food and Chemical Toxicology, 50(3-4), 641-647. https://doi.org/10.1016/j.fct.2012.01.017.
  • • Speit, G., & Hartmann, A. (1999). The comet assay (single-cell gel test). A sensitive genotoxicity test for the detection of DNA damage and repair. Methods in Molecular Biology 113, 203-212. https:// doi.org/10.1385/1-59259-675-4:203.
  • • Van Meerloo, J., Kaspers, G.J., & Cloos, J. (2011). Cell sensitivity assays: the MTT assay. Methods in Molecular Biology 731, 237-245. https://doi.org/10.1007/978-1-61779-080-5_20.
  • • Walczyk, D., Bombelli, F.B., Monopoli, M.P., Lynch, I., & Dawson, K.A. (2010). What the cell “Sees” in bionanoscience. Journal of the American Chemical Society 132(16), 5761-5768. https://doi: 10.1021/ ja910675v.
  • • Zhang, H., Ji, Z., Xia, T., Low-Kam, C., Liu, R., Pokhrel, S. … Nel, A.E. (2012). Use of metal oxide nanoparticle band gap to develop a predictive paradigm for oxidative stress and acute pulmonary inflammation. ACS Nano 6, 4349-4368. https://doi.org/ 10.1021/ nn3010087.

Year 2021, Volume: 51 Issue: 2, 175 - 182, 31.08.2021

Mahmoud Abudayyak , E. Elif Güzel Gül Özhan

Abstract

Project Number

37785

References

  • • Abudayyak, M., Guzel, E., & Özhan, G. (2017a). Nickel oxide nanoparticles induce oxidative DNA damage and apoptosis in kidney cell line (NRK-52E). Biological Trace Element Research, 178(1), 98-104. https://doi.org/10.1007/s12011016–0892-z.
  • • Abudayyak, M., Guzel, E., & Özhan, G. (2017b). Nickel oxide nanoparticles are highly toxic to SH-SY5Y neuronal cells. Neurochemistry International, 108, 7-14. https://doi.org/10.1016/j. neuint.2017.01.017.
  • • Ahamed, M. (2011). Toxic response of nickel nanoparticles in human lung epithelial A549 cells. Toxicology in vitro, 25(4), 930-936. https://doi.org/10.1016/j.tiv.2011.02.015.
  • • Ahamed, M., Akhtar, M.J., Siddiqui, M.A., Ahmad, J., Musarrat, J., Al-Khedhairy, A.A. … Alrokayan, S.A. (2011). Oxidative stress mediated apoptosis induced by nickel ferrite nanoparticles in cultured A549 cells. Toxicology, 283(2-3), 101-108. https://doi. org/10.1016/j.tox.2011.02.010.
  • • Ahamed, M., Ali, D., Alhadlaq, H.A., & Akhtar, M.J. (2013). Nickel oxide nanoparticles exert cytotoxicity via oxidative stress and induce apoptotic response in human liver cells (HepG2). Chemosphere, 93(10), 2514-2522. https://doi.org/10.1016/j.chemosphere. 2013.09.047.
  • • Ahmad, J., Alhadlaq, H.A., Siddiqui, M.A., Saquib, Q., Al-Khedhairy, A.A., Musarrat, J., & Ahamed, M. (2013). Concentration-dependent induction of reactive oxygen species, cell cycle arrest and apoptosis in human liver cells after nickel nanoparticles exposure. Environmental Toxicology, 30, 137-148. https://doi.org/10.1002/ tox.21879.
  • • Arora, S., Rajwade, J.M., & Paknikar, K.M. (2012). Nanotoxicology and in vitro studies: the need of the hour. Toxicology and Applied Pharmacology, 258(2), 151-165. https://doi.org/10.1016/j. taap.2011.11.010.
  • • Barillet, S., Simon-Deckers, A., Herlin-Boime, N., Mayne-L’Hermite, M., Reynaud, C., Cassio, D., & Carrière, M. (2010). Toxicological consequences of TiO2, SiC nanoparticles and multi-walled carbon nanotubes exposure in several mammalian cell types: an in vitro study. Journal of Nanoparticle Research, 12(1), 61-73. https://doi. org/10.1007/s11051-009-9694-y.
  • • Boverhof, D.R., & Raymond M.D. (2010). Nanomaterial characterization: considerations and needs for hazard assessment and safety evaluation. Analytical and Bioanalytical Chemistry, 396(3), 953-961. https://doi.org/10.1007/s00216-009-3103-3.
  • • Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 7, 248-254. https://doi.org/10.1006/abio.1976.999.
  • • Brand, R.M., Hannah, T.L., Mueller, C., Cetin, Y., & Hamel, FG. (2000). A novel system to study the impact of epithelial barrierson cellular metabolism. Annals of Biomedical Engineering, 28, 1210-1217. https://doi.org/10.1114/1.1318926.
  • • Brooking, J., Davis, S.S., & Illum, L. (2001). Transport of nanoparticles across the rat nasal mucosa. Journal of Drug Targeting, 9, 267-279. https://doi.org/10.3109/10611860108997935.
  • • Capasso, L., Marina, C., & Maurizio, G. (2014). Nickel oxide nanoparticles induce inflammation and genotoxic effect in lung epithelial cells. Toxicology Letters, 226(1), 28-34. https://doi.org/10.1016/j. toxlet.2014.01.040.
  • • Chen, X, Wang, Z., Zhou, J., Fu, X., Liang, J., Qiu, Y., & Huang, Z. (2014). Renal interstitial fibrosis induced by high-dose mesoporous silica nanoparticles via the NF-ΚB signaling pathway. International Journal of Nanomedicine, 10, 1-22. https://doi.org/10.2147/ IJN.S73538.
  • • Cho, W.S., Duffin, R., Poland, C.A., Howie, S.E., MacNee, W., Bradley, M. … Donaldson, K. (2010). Metal oxide nanoparticles induce unique inflammatory footprints in the lung: important implications for nanoparticle testing. Environmental Health Perspectives, 118(12), 1699-1706. https://doi.org/10.1289/ehp.1002201.
  • • Collins, A.R. (2004). The comet assay for DNA damage and repair: principles, applications, and limitations. Applied Biochemistry and Biotechnology - Part B Molecular Biotechnology, 26(3), 249-261. https://doi.org/10.1385/MB:26:3:249.
  • • Dhawan, A., & Sharma, V. (2010). Toxicity assessment of nanomaterials: methods and challenges. Analytical and Bioanalytical Chemistry 398(2), 589-605. https://doi.org/10.1007/s00216-010- 3996-x.
  • • Duan, W.X., He, M.D., Mao, L., Qian, F.H., Li, Y.M., Pi, H.F. … Zhou, Z. (2015). NiO nanoparticles induce apoptosis through repressing SIRT1 in human bronchial epithelial cells. Toxicology and Applied Pharmacology, 286(2), 80-91. https://doi.org/10.1016/j. taap.2015.03.024.
  • • Dunnick, J.K., Benson, J.M., Hobbs, C.H., Hahn, F.F., Cheng, Y.S., & Eidson, A.F. (1988). Comparative toxicity of nickel oxide, nickel sulphate hexahydrate, and nickel subsulfide after 12 days of inhalation exposure to F344/N rats and B6C3F1 mice. Toxicology, 50, 145-156. https://doi.org/10.1016/0300-483X(88)90087-X
  • • Horev-Azaria, L., Kirkpatrick, C.J., Korenstein, R., Marche, P.N., Maimon, O., Ponti, J. … Villiers, C. (2011). Predictive toxicology of cobalt nanoparticles and ions: comparative in vitro study of different cellular models using methods of knowledge discovery from data. Journal of Toxicological Sciences, 122, 489-501. https:// doi.org/10.1093/toxsci/kfr124.
  • • Horie, M., Fukui, H., Nishio, K., Endoh, S., Kato, H., Fujita, K., Miyauchi, A. … Iwahashi, H. (2011). Evaluation of acute oxidative stress induced by NiO nanoparticles in vivo and in vitro. Journal of Occupational Health, 53, 64-74. https://doi.org/10.1539/joh.l10121
  • • Horie, M., Fukui, H., Endoh, S., Maru, J., Miyauchi, A., Shichiri, M. … Iwahashi, H. (2012). Comparison of acute oxidative stress on rat lung induced by nano and fine-scale, soluble and insoluble metal oxide particles: NiO and TiO2. Inhalation Toxicology, 24(7), 391-400. https://doi.org/10.3109/08958378.2012.682321.
  • • Horie, M., Nishio, K., Fujita, K., Kato, H., Nakamura, A., Kinugasa, S. … Nakanishi, J. (2009). Ultrafine NiO particles induce cytotoxicity in vitro by cellular uptake and subsequent Ni(II) release. Chemical Research in Toxicology, 22(8), 1415-1426. https://doi.org/10.1021/ tx900171n.
  • • International Agency for Research on Cancer (IARC). (1990). Nickel compounds group 1, IARC monographs on the evaluation of carcinogenic risks to human’s chromium, nickel and welding. IARC 49, 257-411.
  • • Jeong, J., Kim, J., Seok, S.H., & Cho, W.S. (2016). Indium oxide (In2O3) nanoparticles induce progressive lung injury distinct from lung injuries by copper oxide (CuO) and nickel oxide (NiO) nanoparticles. Archives of Toxicology, 90(4), 817-828. https://doi. org/10.1007/s00204-015-1493-x.
  • • Kang, G.S., Gillespie, P.A., Gunnison, A., Rengifo, H., Koberstein, J., & Chen, L.C. (2011). Comparative pulmonary toxicity of inhaled nickel nanoparticles; role of deposited dose and solubility. Inhalation Toxicology, 23(2), 95-103. https://doi.org/10.3109/0895837 8.2010.543440.
  • • Khatchadourian, A., & Maysinger, D. (2009). Lipid droplets: their role in nanoparticle-induced oxidative stress. Molecular Pharmaceutics, 6(4), 1125-1137. https://doi.org/10.1021/mp900098p.
  • • Kim, Y.J., Yu, M., Park, H.O., & Yang, S.I. (2010). Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by silica nanomaterials in human neuronal cell line. Molecular and Cellular Toxicology, 6(4), 337-344. https://doi.org/10.1007/s13273-010- 0045-y.
  • • Lanone, S., Rogerieux, F., Geys, J., Dupont, A., Maillot-Marechal, E., Boczkowski, J. … Hoet, P. (2009). Comparative toxicity of 24 manufactured nanoparticles in human alveolar epithelial and macrophage cell lines. Particle and Fibre Toxicology, 6, 1-12. https://doi. org/10.1186/1743-8977-6-14.
  • • Lee, J., Homma, T., Kurahashi, T., Kang, E.S., & Fujii, J. (2015). Oxidative stress triggers lipid droplet accumulation in primary cultured hepatocytes by activating fatty acid synthesis. Biochemical and Biophysical Research Communications, 464(1), 229-235. https://doi. org/10.1016/j.bbrc.2015.06.121.
  • • Marmorato, P., Ceccone, G., Gianoncelli, A., Pascolo, L., Ponti, J., Rossi, F. … Kiskinova, M. (2011). Cellular distribution and degradation of cobalt ferrite nanoparticles in balb/3T3 mouse fibroblasts. Toxicology Letters, 207(2), 128-136. https://doi.org/10.1016/j.toxlet. 2011.08.026.
  • • Martin, K.R., Failla, M.L., & Smith, J.C. (1997). Differential susceptibility of Caco-2 and HepG2 human cell lines to oxidative stress. Journal of the Elisha Mitchell Scientific Society, 113(4), 149-162. https://www.jstor.org/stable/44706114.
  • • Morimoto, Y., Ogami, A., Todoroki, M., Yamamoto, M., Murakami, M., Hirohashi, M. … Tanaka, I. (2010). Expression of inflammationrelated cytokines following intratracheal instillation of nickel oxide nanoparticles. Nanotoxicology, 4(2), 161-176. https://doi. org/10.3109/17435390903518479.
  • • Morimoto, Y., Hirohashi, M., Ogami, A., Oyabu, T., Myojo, T., Hashib, M. … Tanaka, I. (2011). Pulmonary toxicity following an intratracheal instillation of nickel oxide nanoparticle agglomerates. Journal of Occupational Health, 53(4), 293-295. https://doi. org/10.1539/joh.11-0034-BR.
  • • Napierska, D., Thomassen, L.C., Lison, D., Marten,s J.A., & Hoet, P.H. 2010. The nanosilica hazard: another variable entity. Particle and Fibre Toxicology, 7(1), 39. https://doi.org/10.1186/1743-8977-7-39.
  • • Nishi, K., Morimoto, Y., Ogami, A., Murakami, M., Myojo, T., Oyabu, T., Kadoya, C. … Tanaka, I. (2009). Expression of cytokine-induced neutrophil chemoattractant in rat lungs by intratracheal instillation of nickel oxide nanoparticles. Inhalation Toxicology, 21, 1030- 1039. https://doi.org/ 10.1080/08958370802716722.
  • • O’Brien, P.J., Irwin, W., Diaz, D., Howard-Cofield, E., Krejsa, C.M., Slaughter, M.R., Gao, B. … Hougham, C. (2006). High concordance of drug-induced human hepatotoxicity with in vitro cytotoxicity measured in a novel cell-based model using high content screening. Archives of Toxicology, 80, 580-604. https://doi.org/10.1007/ s00204-006-0091-3.
  • • Oberdorster, G. (2001). Pulmonary effects of inhaled ultrafine particles. International Archives of Occupational and Environmental Health, 74, 1-8. https://doi.org/10.1007/s004200000185.
  • • Oberdorster, G., Oberdorster, E., & Oberdorster, J. (2005). Nanotoxicology: An emerging discipline evolving from studies of ultrafine particles. Environmental Health Perspectives 113, 823-839. https:// doi.org/10.1289/ehp.7339.
  • • Ogami, A., Morimoto, Y., Myojo, T., Oyabu, T., Murakami, M., Todoroki, M. … Tanaka, I. (2009). Pathological features of different sizes of nickel oxide following intratracheal instillation in rats. Inhalation Toxicology, 21(10), 812-818. https://doi. org/10.1080/08958370802499022.
  • • Oyabu, T., Ogami, A., Morimoto, Y., Shimada, M., Lenggoro, W., Okuyama, K., & Tanaka, I. (2007). Biopersistence of inhaled nickel oxide nanoparticles in rat lung. Inhalation Toxicology, 19(1), 55-58. https://doi.org/10.1080/08958370701492995.
  • • Repetto, G., del Peso, A., & Zurita, J.L. (2008). Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nature Protocols, 3(7), 1125-1131. https://doi.org/10.1038/nprot.2008.75.
  • • Sadeghi, L., Tanwir, F., & Babadi, V.Y. (2015). In vitro toxicity of iron oxide nanoparticle: oxidative damages on HepG2 cells. Experimental and Toxicologic Pathology, 67, 197-203. https://doi. org/10.1016/j.etp.2014.11.010.
  • • Sahu, S., Njoroge, J, Bryce, S.M., Yourick, J.J., & Sprando, R.L. (2014). Comperative genotoxicity of nanosilver in human liver HepG2 and colon Caco2 cells evaluated by a flow cytometric in vitro micronucleus assay. Journal of Applied Toxicology, 34, 1226-1234. https://doi.org/10.1002/jat.3065.
  • • Schrand, A.M., Rahman, M.F., Hussain, S.M., Schlager, J.J., Smith, D.A., & Syed, A.F. (2010). Metal-based nanoparticles and their toxicity assessment. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, 2(5), 544-568. https://doi.org/10.1002/ wnan.103.
  • • Siddiqui, M.A., Ahamed, M., Ahmad, J., Majeed Khan M.A., Musarrat, J. Al-Khedhairy, A.A., & Alrokayan, S.A. (2012). Nickel oxide nanoparticles induce cytotoxicity, oxidative stress and apoptosis in cultured human cells that is abrogated by the dietary antioxidant curcumin. Food and Chemical Toxicology, 50(3-4), 641-647. https://doi.org/10.1016/j.fct.2012.01.017.
  • • Speit, G., & Hartmann, A. (1999). The comet assay (single-cell gel test). A sensitive genotoxicity test for the detection of DNA damage and repair. Methods in Molecular Biology 113, 203-212. https:// doi.org/10.1385/1-59259-675-4:203.
  • • Van Meerloo, J., Kaspers, G.J., & Cloos, J. (2011). Cell sensitivity assays: the MTT assay. Methods in Molecular Biology 731, 237-245. https://doi.org/10.1007/978-1-61779-080-5_20.
  • • Walczyk, D., Bombelli, F.B., Monopoli, M.P., Lynch, I., & Dawson, K.A. (2010). What the cell “Sees” in bionanoscience. Journal of the American Chemical Society 132(16), 5761-5768. https://doi: 10.1021/ ja910675v.
  • • Zhang, H., Ji, Z., Xia, T., Low-Kam, C., Liu, R., Pokhrel, S. … Nel, A.E. (2012). Use of metal oxide nanoparticle band gap to develop a predictive paradigm for oxidative stress and acute pulmonary inflammation. ACS Nano 6, 4349-4368. https://doi.org/ 10.1021/ nn3010087.
There are 50 citations in total.

Details

Primary Language English
Subjects Pharmacology and Pharmaceutical Sciences
Journal Section Original Article
Authors

Mahmoud Abudayyak 0000-0003-2286-4777

E. Elif Güzel This is me 0000-0001-9072-3322

Gül Özhan 0000-0002-6926-5723

Project Number 37785
Publication Date August 31, 2021
Submission Date December 8, 2020
Published in Issue Year 2021 Volume: 51 Issue: 2

Cite

APA Abudayyak, M., Güzel, E. E., & Özhan, G. (2021). Nickel oxide nanoparticles induced DNA damages in human liver cells. İstanbul Journal of Pharmacy, 51(2), 175-182.
AMA Abudayyak M, Güzel EE, Özhan G. Nickel oxide nanoparticles induced DNA damages in human liver cells. iujp. August 2021;51(2):175-182.
Chicago Abudayyak, Mahmoud, E. Elif Güzel, and Gül Özhan. “Nickel Oxide Nanoparticles Induced DNA Damages in Human Liver Cells”. İstanbul Journal of Pharmacy 51, no. 2 (August 2021): 175-82.
EndNote Abudayyak M, Güzel EE, Özhan G (August 1, 2021) Nickel oxide nanoparticles induced DNA damages in human liver cells. İstanbul Journal of Pharmacy 51 2 175–182.
IEEE M. Abudayyak, E. E. Güzel, and G. Özhan, “Nickel oxide nanoparticles induced DNA damages in human liver cells”, iujp, vol. 51, no. 2, pp. 175–182, 2021.
ISNAD Abudayyak, Mahmoud et al. “Nickel Oxide Nanoparticles Induced DNA Damages in Human Liver Cells”. İstanbul Journal of Pharmacy 51/2 (August 2021), 175-182.
JAMA Abudayyak M, Güzel EE, Özhan G. Nickel oxide nanoparticles induced DNA damages in human liver cells. iujp. 2021;51:175–182.
MLA Abudayyak, Mahmoud et al. “Nickel Oxide Nanoparticles Induced DNA Damages in Human Liver Cells”. İstanbul Journal of Pharmacy, vol. 51, no. 2, 2021, pp. 175-82.
Vancouver Abudayyak M, Güzel EE, Özhan G. Nickel oxide nanoparticles induced DNA damages in human liver cells. iujp. 2021;51(2):175-82.
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