Abstract
Nowadays, different kinds of nanoparticles (NPs) are produced around the world and used in many fields and products. NPs can enter the body and aggregate in the various organs including brain. They can damage neurons, in particular dopaminergic neurons in the substantia nigra (SN) and striatal neurons which their lesion is associated with Parkinson’s disease (PD). So, NPs can have a role in PD induction along with other agents and factors. PD is the second most common neurodegenerative disease in the world, and in patients, its symptoms progressively worsen day by day through different pathways including oxidative stress, neuroinflammation, mitochondrial dysfunction, α-synuclein increasing and aggregation, apoptosis and reduction of tyrosine hydroxylase positive cells. Unfortunately, there is no effective treatment for PD. So, prevention of this disease is very important. On the other hand, without having sufficient information about PD inducers, prevention of this disease would not be possible. Therefore, we need to have sufficient information about things we contact with them in daily life. Since, NPs are widely used in different products especially in consumer products, and they can enter to the brain easily, in this review the toxicity effects of metal and metal oxide NPs have been evaluated in molecular and cellular levels to determine potential of different kinds of NPs in development of PD.
Funding source: Mashhad University of Medical Sciences
Research funding: We express our sincere gratitude for the support and funding provided by the Vice Chancellor for Research, Mashhad University of Medical Sciences, Mashhad, Iran.
Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
Competing interests: The authors declare no conflict of interest regarding the publication of this review.
Informed consent: Not applicable.
Ethical approval: Not applicable.
References
1. Ebrahimzadeh Bideskan, A, Mohammadipour, A, Fazel, A, Haghir, H, Rafatpanah, H, Hosseini, M, Rajabzadeh, A. Maternal exposure to titanium dioxide nanoparticles during pregnancy and lactation alters offspring hippocampal mRNA BAX and Bcl-2 levels, induces apoptosis and decreases neurogenesis. Exp Toxicol Pathol 2017;69:329–37. https://doi.org/10.1016/j.etp.2017.02.006.Search in Google Scholar
2. Heidari, Z, Mohammadipour, A, Haeri, P, Ebrahimzadeh-bideskan, A. The effect of titanium dioxide nanoparticles on mice midbrain substantia nigra. Iran J Basic Med Sci 2019;22:745–51. https://doi.org/10.22038/ijbms.2019.33611.8018.Search in Google Scholar
3. Valentini, X, Deneufbourg, P, Paci, P, Rugira, P, Laurent, S, Frau, A, Stanicki, D, Ris, L, Nonclercq, D. Morphological alterations induced by the exposure to TiO2 nanoparticles in primary cortical neuron cultures and in the brain of rats. Toxicol Rep 2018;5:878–89. https://doi.org/10.1016/j.toxrep.2018.08.006.Search in Google Scholar
4. Haeri, P, Mohammadipour, A, Heidari, Z, Ebrahimzadeh-Bideskan, A. Neuroprotective effect of crocin on substantia nigra in MPTP-induced Parkinson’s disease model of mice. Anat Sci Int 2019;94:119–27. https://doi.org/10.1007/s12565-018-0457-7.Search in Google Scholar
5. Hauser, DN, Hastings, TG. Mitochondrial dysfunction and oxidative stress in Parkinson’s disease and monogenic Parkinsonism. Neurobiol Dis 2013;51:35–42. https://doi.org/10.1016/j.nbd.2012.10.011.Search in Google Scholar
6. Phillipson, OT. Alpha-synuclein, epigenetics, mitochondria, metabolism, calcium traffic, & circadian dysfunction in Parkinson’s disease. an integrated strategy for management. Ageing Res Rev 2018;40:149–67. https://doi.org/10.1016/j.arr.2017.09.006.Search in Google Scholar
7. Cacabelos, R. Parkinson’s disease: from pathogenesis to pharmacogenomics. Int J Mol Sci 2017;18:551. https://doi.org/10.3390/ijms18030551.Search in Google Scholar
8. Bobori, D, Dimitriadi, A, Karasiali, S, Tsoumaki-Tsouroufli, P, Mastora, M, Kastrinaki, G, et al. Common mechanisms activated in the tissues of aquatic and terrestrial animal models after TiO2 nanoparticles exposure. Environ Int 2020;138:105611. https://doi.org/10.1016/j.envint.2020.105611.Search in Google Scholar
9. Dreno, B, Alexis, A, Chuberre, B, Marinovich, M. Safety of titanium dioxide nanoparticles in cosmetics. J Eur Acad Dermatol Venereol 2019;33:34–46. https://doi.org/10.1111/jdv.15943.Search in Google Scholar
10. 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;7:18477–88. https://doi.org/10.1039/c5nr03646a.Search in Google Scholar
11. Mamelak, M. Parkinson’s disease, the dopaminergic neuron and gammahydroxybutyrate. Neurology 2018;7:5–11. https://doi.org/10.1007/s40120-018-0091-2.Search in Google Scholar
12. Natarajan, V, Wilson, CL, Hayward, SL, Kidambi, S. Titanium dioxide nanoparticles trigger loss of function and perturbation of mitochondrial dynamics in primary hepatocytes. Plos One 2015;10:e0134541. https://doi.org/10.1371/journal.pone.0134541.Search in Google Scholar
13. Pereira, LC, Pazin, M, Franco-Bernardes, MF, Martins, ADCJr, Barcelos, GRM, Pereira, MC, et al. A perspective of mitochondrial dysfunction in rats treated with silver and titanium nanoparticles (AgNPs and TiNPs). J Trace Elem Med Biol 2018;47:63–9. https://doi.org/10.1016/j.jtemb.2018.01.007.Search in Google Scholar
14. Ze, Y, Sheng, L, Zhao, X, Hong, J, Ze, X, Yu, X, et al. TiO2 nanoparticles induced hippocampal neuroinflammation in mice. Plos One 2014;9:e92230. https://doi.org/10.1371/journal.pone.0092230.Search in Google Scholar
15. Wu, J, Xie, H. Effects of titanium dioxide nanoparticles on α-synuclein aggregation and the ubiquitin-proteasome system in dopaminergic neurons. Artif Cells Nanomed Biotechnol 2016;44:690–4. https://doi.org/10.3109/21691401.2014.980507.Search in Google Scholar
16. Hu, Q, Guo, F, Zhao, F, Fu, Z. Effects of titanium dioxide nanoparticles exposure on Parkinsonism in zebrafish larvae and PC12. Chemosphere 2017;173:373–9. https://doi.org/10.1016/j.chemosphere.2017.01.063.Search in Google Scholar
17. Asghari, A, Hosseini, M, Beheshti, F, Shafei, MN, Mehri, S. Inducible nitric oxide inhibitor aminoguanidine, ameliorated oxidative stress, interleukin-6 concentration and improved brain-derived neurotrophic factor in the brain tissues of neonates born from titanium dioxide nanoparticles exposed rats. J Matern Fetal Neonatal Med 2019;32:3962–73. https://doi.org/10.1080/14767058.2018.1480602.Search in Google Scholar
18. Rahmani, F, Saghazadeh, A, Rahmani, M, Teixeira, AL, Rezaei, N, Aghamollaii, V, et al. Plasma levels of brain-derived neurotrophic factor in patients with Parkinson disease: a systematic review and meta-analysis. Brain Res 2019;1704:127–36. https://doi.org/10.1016/j.brainres.2018.10.006.Search in Google Scholar
19. da Silva Germanos, S, Vieira, B, da Silva, IRV, da Cunha, JJ, Nique, S, Striebel, V, et al. The impact of an aquatic exercise program on BDNF levels in Parkinson’s disease patients: short-and long-term outcomes. Funct Neurol 2019;34:65–70. 31556385.Search in Google Scholar
20. Hong, F, Sheng, L, Ze, Y, Hong, J, Zhou, Y, Wang, L, et al. Suppression of neurite outgrowth of primary cultured hippocampal neurons is involved in impairment of glutamate metabolism and NMDA receptor function caused by nanoparticulate TiO2. Biomaterials 2015;53:76–85. https://doi.org/10.1016/j.biomaterials.2015.02.067.Search in Google Scholar
21. Bagheri-Abassi, F, Alavi, H, Mohammadipour, A, Motejaded, F, Ebrahimzadeh-Bideskan, A. The effect of silver nanoparticles on apoptosis and dark neuron production in rat hippocampus. Iran J Basic Med Sci 2015;18:644–8. 26351553.Search in Google Scholar
22. Mao, BH, Chen, ZY, Wang, YJ, Yan, SJ. Silver nanoparticles have lethal and sublethal adverse effects on development and longevity by inducing ROS-mediated stress responses. Sci Rep 2018;8:2445. https://doi.org/10.1038/s41598-018-20728-z.Search in Google Scholar
23. Li, J, Zhang, B, Chang, X, Gan, J, Li, W, Niu, S, et al. Silver nanoparticles modulate mitochondrial dynamics and biogenesis in HepG2 cells. Environ Pollut 2020;256:113430. https://doi.org/10.1016/j.envpol.2019.113430.Search in Google Scholar
24. Dong, P, Li, JH, Xu, SP, Wu, XJ, Xiang, X, Yang, QQ, et al. Mitochondrial dysfunction induced by ultra-small silver nanoclusters with a distinct toxic mechanism. J Hazard Mater 2016;308:139–48. https://doi.org/10.1016/j.jhazmat.2016.01.017.Search in Google Scholar
25. Abd El-Maksoud, EM, Lebda, MA, Hashem, AE, Taha, NM, Kamel, MA. Ginkgo biloba mitigates silver nanoparticles-induced hepatotoxicity in Wistar rats via improvement of mitochondrial biogenesis and antioxidant status. Environ Sci Pollut Res 2019;26:25844–54. https://doi.org/10.1007/s11356-019-05835-2.Search in Google Scholar
26. Ebabe Elle, R, Gaillet, S, Vidé, J, Romain, C, Lauret, C, Rugani, N, et al. Dietary exposure to silver nanoparticles in Sprague-Dawley rats: effects on oxidative stress and inflammation. Food Chem Toxicol 2013;60:297–301. https://doi.org/10.1016/j.fct.2013.07.071.Search in Google Scholar
27. Ziemińska, E, Stafiej, A, Strużyńska, L. The role of the glutamatergic NMDA receptor in nanosilver-evoked neurotoxicity in primary cultures of cerebellar granule cells. Toxicology 2014;315:38–48. https://doi.org/10.1016/j.tox.2013.11.008.Search in Google Scholar
28. Van der Zande, M, Vandebriel, RJ, Groot, MJ, Kramer, E, Herrera Rivera, ZE, Rasmussen, K, et al. Sub-chronic toxicity study in rats orally exposed to nanostructured silica. Part Fibre Toxicol 2014;11:8. https://doi.org/10.1186/1743-8977-11-8.Search in Google Scholar
29. Zhu, B, He, W, Hu, S, Kong, R, Yang, L. The fate and oxidative stress of different sized SiO2 nanoparticles in zebrafish (Danio rerio) larvae. Chemosphere 2019;225:705–12. https://doi.org/10.1016/j.chemosphere.2019.03.091.Search in Google Scholar
30. Li, X, Ji, X, Wang, R, Zhao, J, Dang, J, Gao, Y, et al. Zebrafish behavioral phenomics employed for characterizing behavioral neurotoxicity caused by silica nanoparticles. Chemosphere 2020;240:124937. https://doi.org/10.1016/j.chemosphere.2019.124937.Search in Google Scholar
31. Guo, C, Wang, J, Jing, L, Ma, R, Liu, X, Gao, L, et al. Mitochondrial dysfunction, perturbations of mitochondrial dynamics and biogenesis involved in endothelial injury induced by silica nanoparticles. Environ Pollut 2018;236:926–36. https://doi.org/10.1016/j.envpol.2017.10.060.Search in Google Scholar
32. Xie, H, Wu, J. Silica nanoparticles induce alpha-synuclein induction and aggregation in PC12-cells. Chem-Biol Interact 2016;258:197–204. https://doi.org/10.1016/j.cbi.2016.09.006.Search in Google Scholar
33. Wu, J, Wang, C, Sun, J, Xue, Y. Neurotoxicity of silica nanoparticles: brain localization and dopaminergic neurons damage pathways. ACS Nano 2011;5:4476–89. https://doi.org/10.1021/nn103530b.Search in Google Scholar
34. Duan, J, Liang, S, Feng, L, Yu, Y, Sun, Z. Silica nanoparticles trigger hepatic lipid-metabolism disorder in vivo and in vitro. Int J Nanomed 2018;13:7303–18. https://doi.org/10.2147/ijn.s185348.Search in Google Scholar
35. Badie Bostan, H, Rezaee, R, Gorji Valokala, M, Tsarouhas, K, Kirill Golokhvast, K, Tsatsakis, AM, et al. Cardiotoxicity of nano-particles. Life Sci 2016;165:91–99. https://doi.org/10.1016/j.lfs.2016.09.017.Search in Google Scholar
36. Khanna, P, Ong, C, Bay, BH, Baeg, GH. Nanotoxicity: an interplay of oxidative stress, inflammation and cell death. Nanomaterials 2015;5:1163–80. https://doi.org/10.3390/nano5031163.Search in Google Scholar
37. Liu, X, Sun, J. Endothelial cells dysfunction induced by silica nanoparticles through oxidative stress via jnk/p53 and NF-κB pathways. Biomaterials 2010;2010:8198–209. https://doi.org/10.1016/j.biomaterials.2010.07.069.Search in Google Scholar
38. Yu, KN, Yoon, TJ, Minai-Tehrani, A, Kim, JE, Park, SJ, Jeong, MS, et al. Zinc oxide nanoparticle induced autophagic cell death and mitochondrial damage via reactive oxygen species generation. Toxicol In Vitro 2013;27:1187–95. https://doi.org/10.1016/j.tiv.2013.02.010.Search in Google Scholar
39. Yaqub, A, Faheem, I, Anjum, KM, Ditta, SA, Yousaf, MZ, Tanvir, F, et al. Neurotoxicity of ZnO nanoparticles and associated motor function deficits in mice. Appl Nanosci 2019;10:177–85. https://doi.org/10.1007/s13204-019-01093-3.Search in Google Scholar
40. Liang, H, Chen, A, Lai, X, Liu, J, Wu, J, Kang, Y, et al. Neuroinflammation is induced by tongue-instilled ZnO nanoparticles via the Ca2+-dependent NF-κB and MAPK pathways. Part Fiber Toxicol 2018;15:39. https://doi.org/10.1186/s12989-018-0274-0.Search in Google Scholar
41. Chevallet, M, Gallet, B, Fuchs, A, Jouneau, PH, Um, K, Mintz, E, et al. Metal homeostasis disruption and mitochondrial dysfunction in hepatocytes exposed to sub-toxic doses of zinc oxide nanoparticles. Nanoscale 2016;8:18495–506. https://doi.org/10.1039/c6nr05306h.Search in Google Scholar
42. Liu, H, Yang, H, Fang, Y, Li, K, Tian, L, Liu, X, et al. Neurotoxicity and biomarkers of zinc oxide nanoparticles in main functional brain regions and dopaminergic neurons. Sci Total Environ 2020;705:135809. https://doi.org/10.1016/j.scitotenv.2019.135809.Search in Google Scholar
43. Manickam, V, Dhakshinamoorthy, V, Perumal, E. Iron oxide nanoparticles affects behaviour and monoamine levels in mice. Neurochem Res 2019;44:1533–48. https://doi.org/10.1007/s11064-019-02774-9.Search in Google Scholar
44. Yarjanli, Z, Ghaedi, K, Esmaeili, A, Rahgozar, S, Zarrabi, A. Iron oxide nanoparticles may damage to the neural tissue through iron accumulation, oxidative stress, and protein aggregation. BMC Neurosci 2017;18:51. https://doi.org/10.1186/s12868-017-0369-9.Search in Google Scholar
45. Imam, SZ, Lantz-McPeak, SM, Cuevas, E, Rosas-Hernandez, H, Liachenko, S, Zhang, Y, et al. Iron oxide nanoparticles induce dopaminergic damage: in vitro pathways and in vivo imaging reveals mechanism of neuronal damage. Mol Neurobiol 2015;52:913–26. https://doi.org/10.1007/s12035-015-9259-2.Search in Google Scholar
46. Liu, Y, Harding, M, Pittman, A, Dore, J, Striessnig, J, Rajadhyaksha, A, et al. Cav1.2 and Cav1.3 L-type calcium channels regulate dopaminergic firing activity in the mouse ventral tegmental area. J Neurophysiol 2014;112:1119–30. https://doi.org/10.1152/jn.00757.2013.Search in Google Scholar
47. Ludtmann, MHR, Abramov, AY. Mitochondrial calcium imbalance in Parkinson’s disease. Neurosci Lett 2018;663:86–90. https://doi.org/10.1016/j.neulet.2017.08.044.Search in Google Scholar
48. M1, T, Arotcarena, ML, Faggiani, E, Laferriere, F, Bezard, E, Dehay, B. Targeting α-synuclein for PD therapeutics: a pursuit on all fronts. Biomolecules 2020;10:E391. https://doi.org/10.3390/biom10030391.Search in Google Scholar
49. Manickam, V, Dhakshinamoorthy, V, Perumal, E. Iron oxide nanoparticles induces cell cycle-dependent neuronal apoptosis in mice. Mol Neurosci 2018;64:352–62. https://doi.org/10.1007/s12031-018-1030-5.Search in Google Scholar
50. Chen, H, He, J. Facile synthesis of monodisperse manganese oxide nanostructures and their application in water treatment. J Phys Chem C 2008;112:17540–5. https://doi.org/10.1021/jp806160g.Search in Google Scholar
51. Sadeghi, L, Babadi, VY, Tanwir, F. Manganese dioxide nanoparticle induces Parkinson like neurobehavioral abnormalities in rats. Bratisl Lek Listy 2018;119:379–84. https://doi.org/10.4149/bll_2018_070.Search in Google Scholar
52. Hafez, AA, Naserzadeh, P, Ashtari, K, Mortazavian, AM, Salimi, A. Protection of manganese oxide nanoparticles-induced liver and kidney damage by vitamin D. Regul Toxicol Pharmacol 2018;98:240–4. https://doi.org/10.1016/j.yrtph.2018.08.005.Search in Google Scholar
53. 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;92:456–63. https://doi.org/10.1093/toxsci/kfl020.Search in Google Scholar
54. Li, T, Shi, T, Li, X, Zeng, S, Yin, L, Pu, Y. Effects of Nano-MnO2 on dopaminergic neurons and the spatial learning capability of rats. Int J Environ Res Public Health 2015;11:7918–30. https://doi.org/10.3390/ijerph110807918.Search in Google Scholar
55. Bondarenko, O, Juganson, K, Ivask, A, Kasemets, K, Mortimer, M, Kahru, A. Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review. Arch Toxicol 2013;87:1181–200. https://doi.org/10.1007/s00204-013-1079-4.Search in Google Scholar
56. Akhtar, MJ, Kumar, S, Alhadlaq, HA, Alrokayan, SA, Abu-Salah, KM, Ahamed, M. Dose-dependent genotoxicity of copper oxide nanoparticles stimulated by reactive oxygen species in human lung epithelial cells. Toxicology 2016;32:809–21. https://doi.org/10.1177/0748233713511512.Search in Google Scholar
57. Zhang, CH, Wang, Y, Sun, QQ, Xia, LL, Hu, JJ, Cheng, K, et al. Copper nanoparticles show obvious in vitro and in vivo reproductive toxicity via ERK mediated signaling pathway in female mice. Int J Biol Sci 2018;14:1834–44. https://doi.org/10.7150/ijbs.27640.Search in Google Scholar
58. Ko, JW, Shin, NR, Park, JW, Park, SH, Lee, IC, Kim, JS, et al. Copper oxide nanoparticles induce collagen deposition via TGF-beta1/Smad3 signaling in human airway epithelial cells. Nanotoxicology 2018;12:239–50. https://doi.org/10.1080/17435390.2018.1432778.Search in Google Scholar
59. Baeg, E, Sooklert, K, Sereemaspun, A. Copper oxide nanoparticles cause a dose-dependent toxicity via inducing reactive oxygen species in Drosophila. Nanomaterials 2018;8:824. https://doi.org/10.3390/nano8100824.Search in Google Scholar
60. Li, X, Zhang, C, Zhang, X, Wang, S, Meng, Q, Wu, S, et al. An acetyl-L-carnitine switch on mitochondrial dysfunction and rescue in the metabolomics study on aluminum oxide nanoparticles. Part Fibre Toxicol 2016;13:4. https://doi.org/10.1186/s12989-016-0115-y.Search in Google Scholar
61. Liu, H, Zhang, W, Fang, Y, Yang, H, Tian, L, Li, K, et al. Neurotoxicity of aluminum oxide nanoparticles and their mechanistic role in dopaminergic neuron injury involving p53-related pathways. J Hazard Mater 2020;392:122312. https://doi.org/10.1016/j.jhazmat.2020.122312.Search in Google Scholar
62. Whitton, P. Inflammation as a causative factor in the aetiology of Parkinson’s disease. Br J Pharmacol 2007;150:963–76. https://doi.org/10.1038/sj.bjp.0707167.Search in Google Scholar
63. Ahmed, M, Akhtar, MJ, Khan, MAM, Alhadlaq, HA, Aldalbahi, A. Nanocubes of indium oxide induce cytotoxicity and apoptosis through oxidative stress in human lung epithelial cells. Colloid Surface B 2017;156:157–64. https://doi.org/10.1016/j.colsurfb.2017.05.020.Search in Google Scholar
64. Bomhard, EM. The toxicology of indium oxide. Environ Toxicol Pharmacol 2018;58:250–8. https://doi.org/10.1016/j.etap.2018.02.003.Search in Google Scholar
65. Kim, SH, Jeon, S, Lee, DK, Lee, S, Jeong, J, Kim, JS, et al. The early onset and persistent worsening pulmonary alveolar proteinosis in rats by indium oxide nanoparticles. Nanotoxicology 2019;27:1–11. https://doi.org/10.1080/17435390.2019.1694184.Search in Google Scholar
66. Horie, M, Nishio, K, Fujita, K, Kato, H, Nakamura, A, Kinugasa, S, et al. Ultrafine NiO particles induce cytotoxicity in vitro by cellular uptake and subsequent Ni(II) release. Chem Res Toxicol 2009;22:1415–26. https://doi.org/10.1021/tx900171n.Search in Google Scholar
67. Schrand, AM, Rahman, MF, Hussain, SM, Schlager, JJ, Smith, DA, Syed, AF, et al. Metal-based nanoparticles and their toxicity assessment. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2010;2:544–68. https://doi.org/10.1002/wnan.103.Search in Google Scholar
68. Capasso, L, Camatini, M, Gualtieri, M. Nickel oxide nanoparticles induce inflammation and genotoxic effect in lung epithelial cells. Toxicol Lett 2014;7:28–34. https://doi.org/10.1016/j.toxlet.2014.01.040.Search in Google Scholar
69. Minigalieva, IA, Katsnelson, BA, Privalova, LI. Attenuation of combined nickel (II) oxide and manganese (II, III) oxide nanoparticles’ adverse effects with a complex bioprotectors. Int J Mol Sci 2015;16:22555–83. https://doi.org/10.3390/ijms160922555.Search in Google Scholar
70. Abudayyak, M, Guzel, E, Özhan, G. Nickel oxide nanoparticles are highly toxic to SH-SY5Y neuronal cells. Neurochem Int 2017;108:7–14. https://doi.org/10.1016/j.neuint.2017.01.017.Search in Google Scholar
71. Morimoto, Y, Ogami, A, Todoroki, M, Yamamoto, M, Murakami, M, Hirohashi, M, et al. Expression of inflammation-related cytokines following intratracheal instillation of nickel oxide nanoparticles. Nanotoxicology 2010;4:161–76. https://doi.org/0.3109/17435390903518479.10.3109/17435390903518479Search in Google Scholar PubMed
72. Bai, KJ, Chuang, KJ, Chen, JK, Hua, HE, Shen, YL, Liao, WN, et al. Investigation into the pulmonary inflammopathology of exposure to nickel oxide nanoparticles in mice. Nanomed: Nanotechnol 2018;14:2329–39. https://doi.org/10.1016/j.nano.2017.10.003.Search in Google Scholar
73. Akerlund, E, Islam, MS, McCarrick, S, Alfaro-Moreno, E, Karlsson, HL. Inflammation and (secondary) genotoxicity of Ni and NiO nanoparticles. Nanotoxicology 2019;13:1060–72. https://doi.org/10.1080/17435390.2019.1640908.Search in Google Scholar
74. Saquib, Q, Attia, SM, Ansari, SM, Al-Salim, A, Faisal, M, Alatar, AA, et al. p53, MAPKAPK-2 and caspases regulate nickel oxide nanoparticles induce cell death and cytogenetic anomalies in rats. Int J Biol Macromol 2017;105:228–37. https://doi.org/10.1016/j.ijbiomac.2017.07.032.Search in Google Scholar
75. Saquib, Q, Xia, P, Siddiqui, MA, Zhang, J, Xie, Y, Faisal, M, et al. High-throughput transcriptomics: an insight on the pathways affected in HepG2 cells exposed to nickel oxide nanoparticles. Chemosphere 2020;244:125488. https://doi.org/10.1016/j.chemosphere.2019.125488.Search in Google Scholar
76. Bandoli, G, Barreca, D, Brescacin, E, Rizzi, GA, Tondello, E. Pure and mixed phase Bi2O3 thin films obtained by metal organic chemical vapor deposition. Chem Vap Depos 1996;2:238–42. https://doi.org/10.1002/cvde.19960020605.Search in Google Scholar
77. Hyodo, T, Kanazawa, E, Takao, Y, Shimizu, Y, Egashira, M. H2 sensing properties and mechanism of Nb2O5-Bi2O3 varistor-type gas sensors. Electrochem 2000;68:24–31. https://doi.org/10.5796/electrochemistry.68.24.Search in Google Scholar
78. Schuisky, M, Harsta, A. Epitaxial growth of Bi2O2.33 by halide Cvd. Chem Vap Depos 1996;2:235–8. https://doi.org/10.1002/cvde.19960020604.Search in Google Scholar
79. Pan, A, Ghosh, A. A new family of lead-bismuthate glass with a large transmitting window. J Non-Cryst Solids 2000;27:157–61. https://doi.org/10.1016/s0022-3093(00)00111-3.Search in Google Scholar
80. Pauliukaite, R, Metelka, R, Svancara, I, Królicka, A, Bobrowski, A, Vytras, K, et al. Carbon paste electrodes modified with Bi2O3 as sensors for the determination of Cd and Pb. Anal Bioanal Chem 2002;374:1155–8. https://doi.org/10.1007/s00216-002-1569-3.Search in Google Scholar
81. Periasamy, AP, Yang, S, Chen, SM. Preparation and characterization of bismuth oxide nanoparticles-multiwalled carbon nanotube composite for the development of horseradish peroxidase based H2O2 biosensor. Talanta 2011;87:15–23. https://doi.org/10.1016/j.talanta.2011.09.021.Search in Google Scholar
82. Abudayyak, M, Öztaş, E, Arici, M, Özhan, G. Investigation of the toxicity of bismuth oxide nanoparticles in various cell lines. Chemosphere 2017;169:117–23. https://doi.org/10.1016/j.chemosphere.2016.11.018.Search in Google Scholar
83. Alinovi, R, Goldoni, M, Pinelli, S, Campanini, M, Aliatis, I, Bersani, D, et al. Oxidative and pro-inflammatory effects of cobalt and titanium oxide nanoparticles on aortic and venous endothelial cells. Toxicol in Vitro 2015;29:426–37. https://doi.org/10.1016/j.tiv.2014.12.007.Search in Google Scholar
84. Wang, H, Ren, T, Zhu, N, Yu, Q, Li, M. Co3O4 nanoparticles at sublethal concentrations inhibit cell growth by impairing mitochondrial function. Biochem Biophys Res Commun 2018;505:775–80. https://doi.org/10.1016/j.bbrc.2018.10.002.Search in Google Scholar
85. Nouri, M, Esfahanizadeh, N, Shahpar, MG, Attar, F, Sartipnia, N, Akhtari, K, et al. Cobalt oxide nanoparticles mediate tau denaturation and cytotoxicity against PC-12 cell line. Int J Biol Macromol 2018;118:1763–72. https://doi.org/10.1016/j.ijbiomac.2018.07.024.Search in Google Scholar
86. Xue, Y, Chen, Q, Sun, J. Hydroxyapatite nanoparticle-induced mitochondrial energy metabolism impairment in liver cells: in vitro and in vivo studies. J Appl Toxicol 2017;37:1004–16. https://doi.org/10.1002/jat.3450.Search in Google Scholar
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