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Cerium and Yttrium Oxide Nanoparticles Against Lead-Induced Oxidative Stress and Apoptosis in Rat Hippocampus

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Abstract

Due to numerous industrial applications, lead has caused widespread pollution in the environment; it seems that the central nervous system (CNS) is the main target for lead in the human body. Oxidative stress and programmed cell death in the CNS have been assumed as two mechanisms related to neurotoxicity of lead. Cerium oxide (CeO2) and yttrium oxide (Y2O3) nanoparticles have recently shown antioxidant effects, particularly when used together, through scavenging the amount of reactive oxygen species (ROS) required for cell apoptosis. We looked into the neuroprotective effects of the combinations of these nanoparticles against acute lead-induced neurotoxicity in rat hippocampus. We used five groups in this study: control, lead, CeO2 nanoparticles + lead, Y2O3 nanoparticles + lead, and CeO2 and Y2O3 nanoparticles + lead. Nanoparticles of CeO2 (1000 mg/kg) and Y2O3 (230 mg/kg) were administered intraperitoneally during 2 days prior to intraperitoneal injection of the lead (25 mg/kg for 3 days). At the end of the treatments, oxidative stress markers, antioxidant enzymes activity, and apoptosis indexes were investigated. The results demonstrated that pretreatments with CeO2 and/or Y2O3 nanoparticles recovered lead-caused oxidative stress markers (ROS, lipid peroxidation, and total thiol molecules) and apoptosis indexes (Bax/Bcl-2 and caspase-3 protein expression). Besides, these nanoparticles reduced the activities of lead-induced superoxide dismutase and catalase as well as the ADP/ATP ratio. Interestingly, the best recovery resulted from the compound of these nanoparticles. Based on these outcomes, it appears that this combination may potentially be beneficial for protection against lead-caused acute toxicity in the brain through improving the oxidative stress-mediated programmed cell death pathway.

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References

  1. Wang J, Wu J, Zhang Z (2006) Oxidative stress in mouse brain exposed to lead. Ann Occup Hyg 50:405–409

    Article  CAS  PubMed  Google Scholar 

  2. Kermanian F, Mehdizadeh M, Nourmohammadi I (2010) Effects of vitamin C supplementation on lead-induced apoptosis in adult rat hippocampus. Neural Regener Res 5:364–367

    CAS  Google Scholar 

  3. Eren I, Naziroğlu M, Demirdaş A (2007) Protective effects of lamotrigine, aripiprazole and escitalopram on depression-induced oxidative stress in rat brain. Neurochem Res 32:1188–1195

    Article  CAS  PubMed  Google Scholar 

  4. Nazıroğlu M, Senol N, Ghazizadeh V, Yürüker V (2014) Neuroprotection induced by N-acetylcysteine and selenium against traumatic brain injury-induced apoptosis and calcium entry in hippocampus of rat. Cell Mol Neurobiol 34:895–903

    Article  PubMed  Google Scholar 

  5. Dilek M, Naziroğlu M, Baha Oral H et al (2010) Melatonin modulates hippocampus NMDA receptors, blood and brain oxidative stress levels in ovariectomized rats. J Membr Biol 233:135–142

    Article  CAS  PubMed  Google Scholar 

  6. Nazıroğlu M (2011) TRPM2 cation channels, oxidative stress and neurological diseases: where are we now? Neurochem Res 36:355–366

    Article  PubMed  Google Scholar 

  7. Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2:647–656

    Article  CAS  PubMed  Google Scholar 

  8. Lu X, Jin C, Yang J et al (2013) Prenatal and lactational lead exposure enhanced oxidative stress and altered apoptosis status in offspring rats’ hippocampus. Biol Trace Elem Res 151:75–84

    Article  CAS  PubMed  Google Scholar 

  9. Bokara KK, Brown E, McCormick R, Yallapragada PR, Rajanna S, Bettaiya R (2008) Lead-induced increase in antioxidant enzymes and lipid peroxidation products in developing rat brain. Biometals 21:9–16

    Article  CAS  PubMed  Google Scholar 

  10. Sharifi AM, Baniasadi S, Jorjani M, Rahimi F, Bakhshayesh M (2002) Investigation of acute lead poisoning on apoptosis in rat hippocampus in vivo. Neurosci Lett 329:45–48

    Article  CAS  PubMed  Google Scholar 

  11. Sharifi AM, Mousavi SH, Jorjani M (2010) Effect of chronic lead exposure on pro-apoptotic Bax and anti-apoptotic Bcl-2 protein expression in rat hippocampus in vivo. Cell Mol Neurobiol 30:769–774

    Article  CAS  PubMed  Google Scholar 

  12. Chung D (2003) Nanoparticles have health benefits too. New Scientist 179:2410–2416

    Google Scholar 

  13. Schubert D, Dargusch R, Raitano J, Chan SW (2006) Cerium and yttrium oxide nanoparticles are neuroprotective. Biochem Biophys Res Commun 342:86–91

    Article  CAS  PubMed  Google Scholar 

  14. Hosseini A, Baeeri M, Rahimifar M et al (2013) Antiapoptotic effects of cerium oxide and yttrium oxide nanoparticles in isolated rat pancreatic islets. Hum ExpToxicol 32:544–553

    Article  CAS  Google Scholar 

  15. Hosseini A, Abdollahi M (2012) Through a mechanism-based approach, nanoparticles of cerium and yttrium may improve the outcome of pancreatic islet isolation. J Med Hypotheses Ideas 6:4–6

    Article  CAS  Google Scholar 

  16. Struzyñska L, Bubko I, Walski M, Rafałowska U (2001) Astroglial reaction during the early phase of acute lead toxicity in the adult rat brain. Toxicology 165:121–131

    Article  PubMed  Google Scholar 

  17. Abdel Moneim AE (2012) Flaxseed oil as a neuroprotective agent on lead acetate-induced monoamineric alterations and neurotoxicity in rats. Biol Trace Elem Res 148:363–370

    Article  CAS  PubMed  Google Scholar 

  18. Bernardi C, Tramontina AC, Nardin P et al. (2013) Treadmill exercise induces hippocampal astroglial alterations in rats. Neural Plast 2013:709732.Epub 2013 Jan 17

  19. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  PubMed  Google Scholar 

  20. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  PubMed  Google Scholar 

  21. Flora SJ, Gautam P, Kushwaha P (2012) Lead and ethanol co-exposure lead to blood oxidative stress and subsequent neuronal apoptosis in rats. Alcohol Alcohol 47:92–101

    Article  CAS  PubMed  Google Scholar 

  22. Hosseini A, Sharifzadeh M, Rezayat SM et al (2010) Benefit of magnesium-25 carrying porphyrinfullerene nanoparticles in experimental diabetic neuropathy. Int J Nanomedicine 5:517–523

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Struzyńska L (2000) The protective role of astroglia in the early period of experimental lead toxicity in the rat. Acta Neurobiol Exp (Wars) 60:167–173

    Google Scholar 

  24. Han JM, Chang BJ, Li TZ et al (2007) Protective effects of ascorbic acid against lead-induced apoptotic neurodegeneration in the developing rat hippocampus in vivo. Brain Res 1185:68–74

    Article  CAS  PubMed  Google Scholar 

  25. Korsvik C, Patil S, Seal S, Self WT (2007) Superoxide dismutase mimetic properties exhibited by vacancy engineered ceria nanoparticles. Chem Commun 10:1056–1058

    Article  Google Scholar 

  26. Rzigalinski BA, Meehan K, Davis RM, Xu Y, Miles WC, Cohen CA (2006) Radical nanomedicine. Nanomedicine (Lond) 1:399–412

    Article  CAS  Google Scholar 

  27. Pourkhalili N, Hosseini A, Nili-Ahmadabadi A et al (2011) Biochemical and cellular evidence of the benefit of a combination of cerium oxide nanoparticles and selenium to diabetic rats. World J Diabetes 2:204–210

    PubMed Central  PubMed  Google Scholar 

  28. Das M, Patil S, Bhargava N et al (2007) Auto-catalytic ceria nanoparticles offer neuroprotection to adult rat spinal cord neurons. Biomaterials 28:1918–1925

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Niu J, Azfer A, Rogers LM, Wang X, Kolattukudy PE (2007) Cardioprotective effects of cerium oxide nanoparticles in a transgenic murine model of cardiomyopathy. Cardiovasc Res 73:549–559

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Colon J, Hsieh N, Ferguson A et al (2010) Cerium oxide nanoparticles protect gastrointestinal epithelium from radiation-induced damage by reduction of reactive oxygen species and upregulation of superoxide dismutase 2. Nanomedicine 6:698–705

    Article  CAS  PubMed  Google Scholar 

  31. Colon J, Herrera L, Smith J et al (2009) Protection from radiation-induced pneumonitis using cerium oxide nanoparticles. Nanomedicine 5:225–231

    Article  CAS  PubMed  Google Scholar 

  32. Tarnuzzer RW, Colon J, Patil S, Seal S (2005) Vacancy engineered ceria nanostructures for protection from radiation-induced cellular damage. Nano Lett 5:2573–2577

    Article  CAS  PubMed  Google Scholar 

  33. Chen J, Patil S, Seal S, McGinnis JF (2006) Rare earth nanoparticles prevent retinal degeneration induced by intracellular peroxides. Nat Nanotechnol 1:142–150

    Article  CAS  PubMed  Google Scholar 

  34. Celardo I, De Nicola M, Mandoli C, Pedersen JZ, Traversa E, Ghibelli L (2011) Ce3+ ions determine redox-dependent anti-apoptotic effect of cerium oxide nanoparticles. ACS Nano 5:4537–4549

    Article  CAS  PubMed  Google Scholar 

  35. She JQ, Wang M, Zhu DM et al (2009) Monosialoanglioside (GM1) prevents lead-induced neurotoxicity on long-term potentiation, SOD activity, MDA levels, and intracellular calcium levels of hippocampus in rats. Naunyn Schmiedebergs Arch Pharmacol 379:517–524

    Article  CAS  PubMed  Google Scholar 

  36. Nazıroğlu M (2012) Molecular role of catalase on oxidative stress-induced Ca(2+) signaling and TRP cation channel activation in nervous system. J Recept Signal Transduct Res 32:134–141

    Article  PubMed  Google Scholar 

  37. Becker S, Soukup JM, Gallagher JE (2002) Differential particulate air pollution induced oxidant stress in human granulocytes, monocytes and alveolar macrophages. Toxicol In Vitro 16:209–218

    Article  CAS  PubMed  Google Scholar 

  38. Soltaninejad K, Kebriaeezadeh A, Minaiee B et al (2003) Biochemical and ultrastructural evidences for toxicity of lead through free radicals in rat brain. Hum ExpToxicol 22:417–423

    CAS  Google Scholar 

  39. Dribben WH, Creeley CE, Farber N (2011) Low-level lead exposure triggers neuronal apoptosis in the developing mouse brain. Neurotoxicol Teratol 33:473–480

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Kiran Kumar B, PrabhakaraRao Y, Noble T et al (2009) Lead-induced alteration of apoptotic proteins in different regions of adult rat brain. Toxicol Lett 184:56–60

    Article  CAS  PubMed  Google Scholar 

  41. Flora SJ, Saxena G, Mehta A (2007) Reversal of lead-induced neuronal apoptosis by chelation treatment in rats: role of reactive oxygen species and intracellular Ca(2+). J Pharmacol Exp Ther 322:108–116

    Article  CAS  PubMed  Google Scholar 

  42. Al-Majed AA (2011) Probucol attenuates oxidative stress, energy starvation, and nitric acid production following transient forebrain ischemia in the rat hippocampus. Oxid Med Cell Longev 2011:471590

    Article  PubMed Central  PubMed  Google Scholar 

  43. Ghazizadeh V, Nazıroğlu M (2014) Electromagnetic radiation (Wi-Fi) and epilepsy induce calcium entry and apoptosis through activation of TRPV1 channel in hippocampus and dorsal root ganglion of rats. Metab Brain Dis 29:787–799

    Article  CAS  PubMed  Google Scholar 

  44. Bennet C, Bettaiya R, Rajanna S et al (2007) Region specific increase in the antioxidant enzymes and lipid peroxidation products in the brain of rats exposed to lead. Free Radic Res 41:267–273

    Article  CAS  PubMed  Google Scholar 

  45. Adewole SO, Ayoka AO (2009) Beneficial role of Quercetin on developmental brain of rats against oxidative stress-induced poisoning. Pharmacol Online 2:1171–1184

    Google Scholar 

  46. Bagchi D, Vuchetich PJ, Bagchi M et al (1997) Induction of oxidative stress by chronic administration of sodium dichromate [chromium VI] and cadmium chloride [cadmium II] to rats. Fre Radic Biol Med 22:471–478

    Article  CAS  Google Scholar 

  47. Xu J, Ji LD, Xu LH (2006) Lead-induced apoptosis in PC 12 cells: involvement of p53, Bcl-2 family and caspase-3. Toxicol Lett 166:160–167

    Article  CAS  PubMed  Google Scholar 

  48. Clark A, Zhu A, Sun K, Petty HR (2011) Cerium oxide and platinum nanoparticles protect cells from oxidant-mediated apoptosis. J Nanopart Res 13:5547–5555

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Rafałowska U, Struzyńska L, Dabrowska-Bouta B, Lenkiewicz A (1996) Is lead toxicosis a reflection of altered energy metabolism in brain synaptosomes? Acta Neurobiol Exp (Wars) 56:611–617

    Google Scholar 

  50. Prins JM, Park S, Lurie DI (2010) Decreased expression of the voltage-dependent anion channel in differentiated PC-12 and SH-SY5Y cells following low-level Pb exposure. Toxicol Sci 113:169–176

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  51. Pourkhalili N, Hosseini A, Nili-Ahmadabadi A (2012) Improvement of isolated rat pancreatic islets function by combination of cerium oxide nanoparticles/sodium selenite through reduction of oxidative stress. Toxicol Mech Methods 22:476–482

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by a grant from IUMS.

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The authors declare no potential conflicts of interest with respect to research, authorship, and/or publication of this manuscript.

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Correspondence to Asieh Hosseini.

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Hosseini, A., Sharifi, A., Abdollahi, M. et al. Cerium and Yttrium Oxide Nanoparticles Against Lead-Induced Oxidative Stress and Apoptosis in Rat Hippocampus. Biol Trace Elem Res 164, 80–89 (2015). https://doi.org/10.1007/s12011-014-0197-z

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  • DOI: https://doi.org/10.1007/s12011-014-0197-z

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