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Research Articles

Hippocampal apoptosis of the neonates born from TiO2 nanoparticles-exposed rats is mediated by inducible nitric oxide synthase

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Pages 162-171 | Received 14 Aug 2018, Accepted 11 Jan 2019, Published online: 22 Feb 2019

References

  • Ahlawat, A., and Sharma, S., 2018. A new promising simultaneous approach for attenuating type II diabetes mellitus induced neuropathic pain in rats: iNOS inhibition and neuroregeneration. European journal of pharmacology, 818, 419–428.
  • Alipour, M., et al., 2016. Effect of sub-chronic intraperitoneal administration of aminoguanidine on the memory and hippocampal apoptosis-related genes in diabetic rats. Bratislavske lekarske listy, 117 (8), 472–479.
  • Anaeigoudari, A., et al., 2016. Inducible nitric oxide inhibitor aminoguanidine, ameliorates deleterious effects of lipopolysaccharide on memory and long term potentiation in rat. Life science, 158, 22–30.
  • Annunziato, L., et al., 2003. Apoptosis induced in neuronal cells by oxidative stress: role played by caspases and intracellular calcium ions. Toxicological letters, 139 (2–3), 125–133.
  • Asghari, A., et al., 2018. 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. The journal of maternal fetal neonatal medicine, 1–12. https://doi.org/10.1080/14767058.2018.1480602
  • Asiaei, F., et al., 2017. Neuroprotective effects of Nigella sativa extract upon the hippocampus in PTU-induced hypothyroidism juvenile rats: A stereological study. Metabolic brain disease, 32 (5), 1755–1765.
  • Baranova, L.A., Zhornik, E.V., and Volotovski, I.D., 2015. Influence of silver and titanium dioxide nanoparticles on the expression of genes of biomarkers of inflammatory responses and apoptosis. Biofizika, 60 (2), 234–241.
  • Brune, B., von Knethen, A., and Sandau, K.B., 1998. Nitric oxide and its role in apoptosis. European journal of pharmacology, 351 (3), 261–261272.
  • Cardaci, S., et al., 2008. Reactive oxygen species mediate p53 activation and apoptosis induced by sodium nitroprusside in SH-SY5Y cells. Molecular pharmacology, 74 (5), 1234–1245.
  • Chen, X., and Mao, S.S., 2007. Titanium dioxide nanomaterials: synthesis, properties, modifications, and applications. Chemical reviews, 107 (7), 2891–2959.
  • Chen, Y.F., et al., 2016. Trans-cinnamaldehyde, an essential oil in cinnamon powder, ameliorates cerebral ischemia-induced brain injury via inhibition of neuroinflammation through attenuation of iNOS, COX-2 expression and NFkappa-B signaling pathway. Neuromolecular medicine, 18 (3), 322–333.
  • Chowdhury, R., et al., 2009. Arsenic induced apoptosis in malignant melanoma cells is enhanced by menadione through ROS generation, p38 signaling and p53 activation. Apoptosis, 14 (1), 108–123.
  • Czajka, M., et al., 2015. Toxicity of titanium dioxide nanoparticles in central nervous system. Toxicology in vitro, 29 (5), 1042–1052.
  • Disdier, C., et al., 2015. Tissue biodistribution of intravenously administrated titanium dioxide nanoparticles revealed blood-brain barrier clearance and brain inflammation in rat. Part fibre toxicology, 12, 27.
  • Disdier, C., et al., 2017. Brain inflammation, blood brain barrier dysfunction and neuronal synaptophysin decrease after inhalation exposure to titanium dioxide nano-aerosol in aging rats. Science reports, 7 (1), 12196.
  • Ebrahimzadeh Bideskan, A., et al., 2017. Maternal exposure to titanium dioxide nanoparticles during pregnancy and lactation alters offspring hippocampal mRNA BAX and Bcl-2 levels, induces apoptosis and decreases neurogenesis. Experimental and toxicologic pathology, 69 (6), 329–337.
  • Ebrahimzadeh-Bideskan, A.R., et al., 2018. The effects of soy and tamoxifen on apoptosis in the hippocampus and dentate gyrus in a pentylenetetrazole-induced seizure model of ovariectomized rats. Anatomical science international, 93 (2), 218–230.
  • Elibol, B., et al., 2001. Nitric oxide is involved in ischemia-induced apoptosis in brain: a study in neuronal nitric oxide synthase null mice. Neuroscience, 105 (1), 79–86.
  • Firouzjaei, M.A., et al., 2014. Aminoguanidine changes hippocampal expression of apoptosis-related genes, improves passive avoidance learning and memory in streptozotocin-induced diabetic rats. Cellular and molecular neurobiology, 34 (3), 343–350.
  • Gahm, C., et al., 2006. Neuroprotection by selective inhibition of inducible nitric oxide synthase after experimental brain contusion. Journal of neurotrauma, 23 (9), 1343–1354.
  • Hong, F., et al., 2015. Chronic exposure to nanoparticulate TiO2 causes renal fibrosis involving activation of the Wnt pathway in mouse kidney. Journal of Agricultural and Food Chemistry, 63 (5), 1639–1647.
  • Hong, F., et al., 2016. Titanium dioxide nanoparticle-induced dysfunction of cardiac hemodynamics is involved in cardiac inflammation in mice. Journal of biomedical materials research part A, 104 (12), 2917–2927.
  • Hong, F., et al., 2017. Maternal exposure to nanosized titanium dioxide suppresses embryonic development in mice. International journal of nanomedicine, 12, 6197–6204.
  • Hu, R., et al., 2010. Neurotoxicological effects and the impairment of spatial recognition memory in mice caused by exposure to TiO2 nanoparticles. Biomaterials, 31 (31), 8043–8050.
  • Hu, R., et al., 2011. Molecular mechanism of hippocampal apoptosis of mice following exposure to titanium dioxide nanoparticles. Journal of hazard materials, 191 (1–3), 32–40.
  • Hu, Y.L., and Gao, J.Q., 2010. Potential neurotoxicity of nanoparticles. International Journal of Pharmaceutics, 394 (1-2), 115–121.
  • Huang, D., et al., 2017. Nitric oxide mediates apoptosis and mitochondrial dysfunction and plays a role in growth hormone deficiency by nivalenol in GH3 cells. Science reports, 7 (1), 17079.
  • Jia, X., et al., 2017. The potential liver, brain, and embryo toxicity of titanium dioxide nanoparticles on mice. Nanoscale research letters, 12 (1), 478.
  • Kozlov, A.V., et al., 2017. Alterations in nitric oxide homeostasis during traumatic brain injury. Biochimica et biophysica acta, 1863 (10), 2627–2632.
  • Laomettachit, T., Puri, I.K., and Liangruksa, M., 2017. A two-step model of TiO2 nanoparticle toxicity in human liver tissue. Toxicology and applied pharmacology, 334, 47–54.
  • Lee, K.P., Trochimowicz, H.J., and Reinhardt, C.F., 1985. Pulmonary response of rats exposed to titanium dioxide (TiO2) by inhalation for two years. Toxicology and applied pharmacology, 79 (2), 179–192.
  • Liao, Q., et al., 2016. Endothelial nitric oxide synthase deficiency influences normal cell cycle progression and apoptosis in trabecular meshwork cells. International journal of ophthalmology, 9 (6), 799–803.
  • Liu, D., et al., 2017. Lung inflammation caused by long-term exposure to titanium dioxide in mice involving in NF-kappaB signaling pathway. Journal of biomedical materials research A, 105 (3), 720–727.
  • Long, T.C., et al., 2006. Titanium dioxide (P25) produces reactive oxygen species in immortalized brain microglia (BV2): implications for nanoparticle neurotoxicity. Environmental science and technology, 40 (14), 4346–4352.
  • Lu, J., et al., 2003. Nitric oxide induces macrophage apoptosis following traumatic brain injury in rats. Neuroscience letters, 339 (2), 147–150.
  • Lu, N., et al., 2008. Nano titanium dioxide photocatalytic protein tyrosine nitration: a potential hazard of TiO2 on skin. Biochemical biophysical research communications, 370 (4), 675–680.
  • Ma, L., et al., 2010. Oxidative stress in the brain of mice caused by translocated nanoparticulate TiO2 delivered to the abdominal cavity. Biomaterials, 31 (1), 99–105.
  • Marquez-Ramirez, S.G., et al., 2012. Titanium dioxide nanoparticles inhibit proliferation and induce morphological changes and apoptosis in glial cells. Toxicology, 302 (2–3), 146–156.
  • Meena, R., et al., 2012. Nano-TiO2-induced apoptosis by oxidative stress-mediated DNA damage and activation of p53 in human embryonic kidney cells. Applied biochemistry and biotechnology, 167 (4), 791–808.
  • Mohammadipour, A., et al., 2014. Maternal exposure to titanium dioxide nanoparticles during pregnancy; impaired memory and decreased hippocampal cell proliferation in rat offspring. Environmental toxicology and pharmacology, 37 (2), 617–625.
  • Mohammadipour, A., et al., 2016. The effects of exposure to titanium dioxide nanoparticles during lactation period on learning and memory of rat offspring. Toxicology and industrial health, 32 (2), 221–228.
  • Nataraj, N., et al., 2014. Synthesis and anti-staphylococcal activity of TiO2 nanoparticles and nanowires in ex vivo porcine skin model. Journal of biomedical nanotechnology, 10 (5), 864–870.
  • Orman, D., et al., 2015. Aminoguanidine mitigates apoptosis, testicular seminiferous tubules damage, and oxidative stress in streptozotocin-induced diabetic rats. Tissue cell, 47 (3), 284–290.
  • Park, Y.H., et al., 2011. Analysis for the potential of polystyrene and TiO2 nanoparticles to induce skin irritation, phototoxicity, and sensitization. Toxicology in vitro, 25 (8), 1863–1869.
  • Paul, V., and Ekambaram, P., 2011. Involvement of nitric oxide in learning & memory processes. Indian journal of medical research, 133, 471–478.
  • Philippu, A., 2016. Nitric oxide: a universal modulator of brain function. Current medicinal chemistry, 23 (24), 2643–2652.
  • Popov, A.P., et al., 2005. Effect of size of TiO2 nanoparticles embedded into stratum corneum on ultraviolet-A and ultraviolet-B sun-blocking properties of the skin. Journal of biomedical optics, 10 (6), 064037.
  • Pujalte, I., et al., 2017. Toxicokinetics of titanium dioxide (TiO2) nanoparticles after inhalation in rats. Toxicology letters, 265, 77–85.
  • Ramkumar, K.M., et al., 2012. Oxidative stress-mediated cytotoxicity and apoptosis induction by TiO2 nanofibers in HeLa cells. European journal of pharmaceutica and biopharmaceutics, 81 (2), 324–333.
  • Schweighofer, H., et al., 2014. Brain function in iNOS knock out or iNOS inhibited (l-NIL) mice under endotoxic shock. Intensive care medicine experimental, 2 (1), 24.
  • Sharma, H.S., et al., 2017. Histaminergic receptors modulate spinal cord injury-induced neuronal nitric oxide synthase upregulation and cord pathology: new roles of nanowired drug delivery for neuroprotection. International review of neurobiology, 137, 65–98.
  • Sheng, L., et al., 2015. Mechanisms of TiO2 nanoparticle-induced neuronal apoptosis in rat primary cultured hippocampal neurons. Journal of biomedical materials research part A, 103 (3), 1141–1149.
  • Sheu, J.R., et al., 2018. CME-1, a novel polysaccharide, suppresses iNOS expression in lipopolysaccharide-stimulated macrophages through ceramide-initiated protein phosphatase 2A activation. Journal of cellular and molecular medicine, 22 (2), 999–1013.
  • Shrivastava, R., et al., 2014. Effects of sub-acute exposure to TiO2, ZnO and Al2O3 nanoparticles on oxidative stress and histological changes in mouse liver and brain. Drug and chemical toxicology, 37 (3), 336–347.
  • Simon, H.U., Haj-Yehia, A., and Levi-Schaffer, F., 2000. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis, 5 (5), 415–418.
  • Tzeng, H.P., et al., 2017. Benzo[a]pyrene activates interleukin-6 induction and suppresses nitric oxide-induced apoptosis in rat vascular smooth muscle cells. PLoS One, 12 (5), e0178063.
  • Uysal, A., et al., 2008. Quantitative immunohistochemical analysis of nitric oxide synthases and apoptosis regulator proteins in the fetal rat brain following maternal uterine artery ligation. International journal of neuroscience, 118 (6), 891–901.
  • Wang, Y., et al., 2014. Genotoxic effects of oral-exposed TiO2 nanoparticles on bone marrow cells in young rats. Zhonghua Yu Fang Yi Xue Za Zhi, 48 (9), 815–818.
  • Yang, F., et al., 2012. Emerging inorganic nanomaterials for pancreatic cancer diagnosis and treatment. Cancer treatment reviews, 38 (6), 566–579.
  • Ze, Y., et al., 2014. TiO2 nanoparticles induced hippocampal neuroinflammation in mice. PLoS One, 9 (3), e92230–24658543.
  • Zhao, X., et al., 2014. Mechanisms of nanosized titanium dioxide-induced testicular oxidative stress and apoptosis in male mice. Part fibre toxicology, 11, 47.
  • Zhou, Y., et al., 2018. Surfactant protein D attenuates nitric oxide-stimulated apoptosis in rat chondrocyte by suppressing p38 MAPK signaling. Biochemical and biophysical research communication, 495 (1), 526–532.

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