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Biochemical, Toxicological, and Histopathological outcome in rat brain following treatment with NiO and NiO nanoparticles

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Abstract

Nickel oxide nanoparticle (NiO NPs) has been widely used in various fields such as catalysts, radiotherapy, and nanomedicine. The aim of this study was to compare the effects of nickel oxide (NiO) and NiO NPs on oxidative stress biomarkers and histopathological changes in brain tissue of rats. In this study, 49 male rats were randomly divided into one control group and 6 experimental groups (n = 7). The control group received normal saline and the treatment groups received NiO and NiO NPs at doses of 10, 25, and 50 mg/kg intraperitoneally for 8 days. After 8 days, animal was sacrificed, brain excised, homogenized, centrifuged, and then supernatant was collected for antioxidant assays. The results showed that activity of GST in NiO NPs groups with doses of 10, 25, and 50 mg/kg (79.42 ± 4.24, p = 0.035; 78.77 ± 8.49, p = 0.041; 81.38 ± 12.39, p = 0.042 to 47.26 ± 7.17) and catalase in NiO NPs groups with concentrations of 25 and 50 mg/kg (69.95 ± 8.65 to 39.75 ± 5.11, p = 0.02) and (68.80 ± 4.18 to 39.75 ± 5.11 p = 0.027) were significantly increased compared with the control, respectively. Total antioxidant capacity in NiONPs group with doses of 50 mg/kg was significantly decreased (345.00 ± 23.62, p = 0.015 to 496.66 ± 25.77) compared with control. The GSH level in all doses NiO and NiONPs was significantly decreased compared with the control (p = 0.002). MDA level in NiONPs and NiO groups with doses of 50 mg/kg was significantly increased (13.03 ± 1.29, p = < 0.01; 15.61 ± 1.08, p = < 0.001 to 7.32 ± 0.51) compared with the control, respectively. Our results revealed a range of histopathological changes, including necrosis, hyperemia, gliosis, and spongy changes in brain tissue. Thus, increasing level of MDA, GST, and CAT enzymes and decreasing GSH and TAC and also histopathological changes confirmed NiONPs and NiO toxicity.

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References

  1. Grazyna AP, Joanna C, Ibrahim MB (2014) Biosurfactant mediated biosynthesis of selected metallic nanoparticles. Int J Mol Sci 15(8):13720–13737

    Article  CAS  Google Scholar 

  2. Klaine SJ, Alvarez PJJ, Batley GE (2008) Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27(9):1825–1851

    Article  CAS  PubMed  Google Scholar 

  3. Lin D, Xing B (2007) Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ Pollut 150:243–250

    Article  CAS  PubMed  Google Scholar 

  4. Flora S, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J Med Res 128(4):501–523

    CAS  PubMed  Google Scholar 

  5. Grandjean P (1984) Human exposure to nickel. Nickel in the human environment. IARC Sci Publ 53:469–485

    CAS  Google Scholar 

  6. Zhao J, Shi X, Castranova V, Ding M (2009) occupational toxicology of nickel and nickel compounds. J Environ Pathol Toxicol Oncol 28(3):177–208

    Article  PubMed  Google Scholar 

  7. El-Kemaryn M, Nagy N, El-Mehasseb I (2013) Nickel oxide nanoparticles: synthesis and spectral studies of interactions with glucose. Mater Sci Semicond Process 16:1747–1752

    Article  CAS  Google Scholar 

  8. Magaye R, Zhao J (2012) Recent progress in studies of metallic nickel and nickel-based nanoparticles’ genotoxicity and carcinogenicity. Environ Toxicol Chem 34(3):644–650

    CAS  Google Scholar 

  9. Rao KV, Sunandana CS (2008) Effect of fuel to oxidizer ratio on the structure, micro structure and EPR of combustion synthesized NiO nanoparticles. J Nanosci Nanotechnol 8:4247–4253

    Article  CAS  PubMed  Google Scholar 

  10. Svenes KB, Andersen I (1998) Distribution of nickel in lungs from former nickel workers. Int Arch Occup Environ Health 71:424–428

    Article  CAS  PubMed  Google Scholar 

  11. Hsieh TH, Yu CP, Oberdörster G (1999b) Modeling of deposition and clearance of inhaled Ni compounds in the human lung. Regul Toxicol Pharmacol 30:18–28

    Article  CAS  PubMed  Google Scholar 

  12. Baek YW, An YJ (2011) Microbial toxicity of metal oxide nanoparticles (CuO, NiO, ZnO, and Sb2O3) to Escherichia coli, Bacillus subtilis, and Streptococcus aureus. SciTotal Environ 409:1603–1608

    CAS  Google Scholar 

  13. Horie M, Fukui H, Nishio K, Endoh S, Kato H, Fujita K (2011) Evaluation of acute oxidative stress induced by NiO nanoparticles in vivo and in vitro. J Occup Health 53(2):64–74

    Article  CAS  PubMed  Google Scholar 

  14. Bouayed J, Rammal H, Soulimani R (2009) Oxidative stress and anxiety: relationship and cellular pathways. Oxidative Med Cell Longev 2(2):63–67

    Article  Google Scholar 

  15. Halliwell B (2006) Oxidative stress and neurodegeneration: where are we now? JNC 97:1634–1658

    CAS  PubMed  Google Scholar 

  16. Nel A, Xia T, Madler L, Li N (2006) Toxic potential of materials at the nano level. Nature 311:622–627

    CAS  Google Scholar 

  17. Aebi H (1984) Catalase. In: Packer, L. (Ed.). In: Methods in enzymology, 105. Academic Press, Orlando, pp. 121–126

  18. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 105:302–310

    Article  Google Scholar 

  19. Sedlak J, Lindsay RH (1986) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25(1):192–205

    Google Scholar 

  20. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferase the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    Article  CAS  PubMed  Google Scholar 

  21. Benzie IFF, Strain J (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1):70–76

    Article  CAS  PubMed  Google Scholar 

  22. Afifi M, Saddick S, Abu Zinada O (2016) Toxicity of silver nanoparticles on the brain of Oreochromis niloticus and Tilapia zillii. Saudi J Biol Sci 23:754–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Evans PH (1999) Free radicals in brain metabolism and pathology. Br Med Bull 49:577–587

    Article  Google Scholar 

  24. Somani SM (1996) Exercise, drugs, and tissue specific antioxidant system. Pharmacology in sport and exercise:57–95

  25. Bhattacharjee R, Sil PC (2006) The protein fraction of Phyllanthus niruri plays a protective role against acetaminophen induced hepatic disorder via its antioxidant properties. Phytother Res 20(7):595–601

    Article  PubMed  Google Scholar 

  26. Kong L, Gao X, Zhu J, Cheng K, Tang M (2016) Mechanisms involved in reproductive toxicity caused by nickel nanoparticle in female rats. Environ Toxicol 31(11):1674–1683

    Article  CAS  PubMed  Google Scholar 

  27. Krezel A, Szczepanik W, Sokołowska M, Jezowska-Bojczuk M, Bal W (2003) Correlations between complexation modes and redox activities of Ni (II)-GSH complexes. Chem Res Toxicol 16(7):855–864

    Article  CAS  PubMed  Google Scholar 

  28. Kanti Das T, Rina Wati M, Fatima-Shad K (2014) Oxidative stress gated by Fenton and Haber Weiss reactions and its association with Alzheimer’s disease. Arch Neurosci 2(3):e20078

    Article  Google Scholar 

  29. Kasprzak KS, Bare RM (1989) In vitro polymerization of histones by carcinogenic nickel compounds. Carcinogenesis 10(3):621–624

    Article  CAS  PubMed  Google Scholar 

  30. Siddiqui MA, Ahamed M, Ahmad J, Majeed Khan MA, Musarrat J, Al-Khedhairy AA, Alrokayan SA (2012) Nickel oxide nanoparticles induce cytotoxicity, oxidative stress and apoptosis in cultured human cells that is abrogated by the dietary antioxidant curcumin. Food Chem Toxicol 50(3–4):641–647

    Article  CAS  PubMed  Google Scholar 

  31. Dumala N, Mangalampalli B, Kalyan Kamal SS, Grover P (2018) Biochemical alterations induced by nickel oxide nanoparticles in female Wistar albino rats after acute oral exposure. Biomarkers 23(1):33–43

    Article  CAS  PubMed  Google Scholar 

  32. Minigalieva IA, Katsnelson BA, Privalova LI, Sutunkova MP, Gurvich VB, Shur VY, Shishkina EV, Valamina IE, Makeyev OH, Panov VG, Varaksin AN, Grigoryeva EV, Meshtcheryakova EY (2015) Attenuation of combined nickel (II) oxide and manganese(II, III) oxide nanoparticles’ adverse effects with a complex of bioprotectors. Int J Mol Sci 16(9):22555–22583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Madrigal JL, Olivenza R, Moro MA, Lizasoain I, Lorenzo P, Rodrigo J, Leza JC (2001) Glutathione depletion, lipid peroxidation and mitochondrial dysfunction are induced by chronic stress in rat brain. Neuropsychopharmacology 24(4):420–429

    Article  CAS  PubMed  Google Scholar 

  34. Chen CY, Huang YL, Lin TH (1998) Lipid peroxidation in liver of mice administrated with nickel chloride: with special reference to trace elements and antioxidants. Biol Trace Elem Res 61(2):193–205

    Article  CAS  PubMed  Google Scholar 

  35. Ajdari M, Ghahnavieh MZ (2014) Histopathology effects of nickel nanoparticles on lungs, liver, and spleen tissues in male mice. Int Nano Lett 4(3):113

    Article  CAS  Google Scholar 

  36. Topal A, Atamanalp M, Oruç E, Halıcı MB, Şişecioğlu M, Erol HS, Gergit A, Yilmaz B (2015) Neurotoxic effects of nickel chloride in the rainbow trout brain: assessment of c-Fos activity, antioxidant responses, acetylcholinesterase activity, and histopathological changes. Fish Physiol Biochem 41(3):625–634

    Article  CAS  PubMed  Google Scholar 

  37. Haber LT, Erdreicht L, Diamond GL, Maier AM, Ratney R, Zhao Q, Dourson ML (2000) Hazard identification and dose response of inhaled nickel-soluble salts. Regul Toxicol Pharmacol 31:210–230

    Article  CAS  PubMed  Google Scholar 

  38. Henriksson J, Tallkvist J, Tjdve H (1997) Uptake of nickel into the brain via olfactory neurons in rats. Toxicol Lett 91:153–162

    Article  CAS  PubMed  Google Scholar 

  39. Bharadwaj VN, Nguyen DT, Kodibagkar VD, Stabenfeldt SE (2018) Nanoparticle-based therapeutics for brain injury. Adv Healthc Mater 7(1)

  40. Oman P, Lien CF, Ahmad Z, Dietrich S, Smith JR, An Q (2015) Nanoparticles of alkylglyceryl-dextran-graft-poly (lactic acid) for drug delivery to the brain: preparation and in vitro investigation. Acta Biomater 23:250–262

    Article  CAS  Google Scholar 

  41. Ku S, Yan F, Wang Y, Sun Y, Yang N, Ye L (2010) The blood-brain barrier penetration and distribution of PEGylated fluorescein-doped magnetic silica nanoparticles in rat brain. Biochem Biophys Res Commun 16:394(4)

    Google Scholar 

  42. Liu D, Lin B, Shao W, Zhu Z, Ji T, Yang C (2014) In vitro and in vivo studies on the transport of PEGylated silica nanoparticles across the blood-brain barrier. ACS Appl Mater Interfaces 6(3):2131–2136

    Article  CAS  PubMed  Google Scholar 

  43. Chen Y, Liu L (2012) Modern methods for delivery of drugs across the blood-brain barrier. Adv Drug Deliv Rev 64(7):640–665

    Article  CAS  PubMed  Google Scholar 

  44. Voigt N, Henrich-Noack P, Kockentiedt S, Hintz W, Tomas J, Sabel BA (2014) Surfactants, not size or zeta-potential influence blood-brain barrier passage of polymeric nanoparticles. Eur J Pharm Biopharm 87(1):19–29

    Article  CAS  PubMed  Google Scholar 

  45. Ada K, Turk M, Oguztuzun S, Kilic M, Demirel M, Tandogan N et al (2010) Cytotoxicity and apoptotic effects of nickel oxide nanoparticles in cultured HeLa cells. Folia Histochem Cytobiol 48(4):524–529

    PubMed  Google Scholar 

  46. Muñoz A, Costa M (2012) Elucidating the mechanisms of nickel compound uptake: a review of particulate and nano-nickel endocytosis and toxicity. Toxicol Appl Pharmacol 260(1):1–16

    Article  PubMed  CAS  Google Scholar 

  47. Oller AR (2002) Respiratory carcinogenicity assessment of soluble nickel compounds. Environ Health Perspect 110(Suppl 5):841–844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Horie M, Nishio K, Fujita K, Kato H, Nakamura A, Kinugasa S (2009) Ultrafine NiO particles induce cytotoxicity in vitro by cellular uptake and subsequent Ni(II) release. Chem Res Toxicol 22(8):1415–1426

    Article  CAS  PubMed  Google Scholar 

  49. Schwerdtle T, Hartwig A (2006) Bioavailability and genotoxicity of soluble and particulate nickel compounds in cultured human lung cells Mat.-wiss. u. Werkstofftech 37(6):521–525

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Funding

This work is supported by the University of Mazandaran, Grant No. 1384.10.14.

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Authors and Affiliations

  1. Department of Molecular and Cell Biology, Faculty of Basic Sciences, University of Mazandaran, Babolsar, Iran

    Aidin Marzban, Bagher Seyedalipour & Ali Taravati

  2. Department of Cell and Molecular Biology, Faculty of Basic Science, University of Golestan, Gorgan, Iran

    Aidin Marzban & Manigheh Mianabady

  3. Department of Veterinary Pathobiology, Faculty of Veterinary Medicine, Islamic Azad University, Babol branch, Babol, Iran

    Seyed Mohammad Hoseini

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  1. Aidin Marzban
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Correspondence to Bagher Seyedalipour.

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This study was carried out in agreement with the Guide of Care and was approved by the ethics committee on animal experimentation of the University of Mazandaran.

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Marzban, A., Seyedalipour, B., Mianabady, M. et al. Biochemical, Toxicological, and Histopathological outcome in rat brain following treatment with NiO and NiO nanoparticles. Biol Trace Elem Res 196, 528–536 (2020). https://doi.org/10.1007/s12011-019-01941-x

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