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The Protective Effects of Vitamins A and E on Titanium Dioxide Nanoparticles (nTiO2)-Induced Oxidative Stress in the Spleen Tissues of Male Wistar Rats

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Abstract

Titanium dioxide nanoparticles (nTiO2) can accumulate in different tissues and damage them with oxidative stress induction. Different components with antioxidant capacity can protect the tissues. So in this study, the protective effects of vitamin A and E on the nTiO2-induced oxidative stress in rats’ spleen tissues were examined. Thirty-six male Wistar rats were randomly divided into 6 groups: Control 1 (received water), nTiO2, nTiO2 + vitamin E, nTiO2 + vitamin A, nTiO2 + vitamin A and E, and Control 2 (received olive oil). To investigate the status of oxidative stress, total antioxidant capacity (TAC), total oxidant status (TOS), and lipid peroxidation (LPO) were determined in spleen tissue as well as the activities of antioxidant enzymes, including glutathione peroxidase (GPx) and superoxide dismutase (SOD). Also, the gene expression of GPx, SOD, and nuclear factor-E2-related factor-2 (Nrf-2) were determined by qRT-PCR. To evaluate the spleen histopathological changes, H&E staining was carried out. nTiO2 significantly increased TOS and LPO levels, whereas it decreased TAC level, GPx and SOD activities, and gene expression of GPx, SOD, and Nrf-2 in spleen tissues of rats compared with controls (p < 0.05). In vitamin-treated rats, the levels of TOS and LPO significantly decreased, and the level of TAC, the activities of GPx and SOD, and the gene expression of GPx, SOD, and Nrf-2 increased compared to nTiO2 group (p < 0.05). These parameters are maintained near to normal levels. Histological findings confirmed the protective effects of these vitamins on tissue damage caused by nTiO2. Vitamin A and E can protect the spleen tissues from nTiO2-induced oxidative stress.

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References

  1. Smith PM (2007) In: Krebs RE (ed) The history and use of our earth’s chemical elements: a reference guide. ACS Publications

  2. Krebs RE (2006) The history and use of our earth’s chemical elements: a reference guide. Greenwood Publishing Group

  3. Lomer MC, Thompson RP, Commisso J, Keen CL, Powell JJ (2000) Determination of titanium dioxide in foods using inductively coupled plasma optical emission spectrometry. Analyst. 125(12):2339–2343

    Article  CAS  PubMed  Google Scholar 

  4. Weir A, Westerhoff P, Fabricius L, Hristovski K, Von Goetz N (2012) Titanium dioxide nanoparticles in food and personal care products. Environ Sci Technol 46(4):2242–2250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Haugen H, Will J, Köhler A, Hopfner U, Aigner J, Wintermantel E (2004) Ceramic TiO2-foams: characterisation of a potential scaffold. J Eur Ceram Soc 24(4):661–668

    Article  CAS  Google Scholar 

  6. Ackroyd R, Kelty C, Brown N, Reed M (2001) The history of photodetection and photodynamic therapy. Photochem Photobiol 74(5):656–669

    Article  CAS  PubMed  Google Scholar 

  7. Ren W, Zeng L, Shen Z, Xiang L, Gong A, Zhang J, Mao C, Li A, Paunesku T, Woloschak GE, Hosmane NS, Wu A (2013) Enhanced doxorubicin transport to multidrug resistant breast cancer cells via TiO 2 nanocarriers. RSC Adv 3(43):20855–20861

    Article  CAS  Google Scholar 

  8. Du Y, Ren W, Li Y, Zhang Q, Zeng L, Chi C et al (2015) The enhanced chemotherapeutic effects of doxorubicin loaded PEG coated TiO 2 nanocarriers in an orthotopic breast tumor bearing mouse model. J Mater Chem B 3(8):1518–1528

    Article  CAS  PubMed  Google Scholar 

  9. Cui C, Liu H, Li Y, Sun J, Wang R, Liu S, Lindsay Greer A (2005) Fabrication and biocompatibility of nano-TiO2/titanium alloys biomaterials. Mater Lett 59(24-25):3144–3148

    Article  CAS  Google Scholar 

  10. Zahin N, Anwar R, Tewari D, Kabir MT, Sajid A, Mathew B, Uddin MS, Aleya L, Abdel-Daim MM (2020) Nanoparticles and its biomedical applications in health and diseases: special focus on drug delivery. Environ Sci Pollut Res 27(16):19151–19168

    Article  CAS  Google Scholar 

  11. Peters RJ, van Bemmel G, Herrera-Rivera Z, Helsper HP, Marvin HJ, Weigel S et al (2014) Characterization of titanium dioxide nanoparticles in food products: analytical methods to define nanoparticles. J Agric Food Chem 62(27):6285–6293

    Article  CAS  PubMed  Google Scholar 

  12. Lorenz C, Tiede K, Tear S, Boxall A, Von Goetz N, Hungerbühler K (2010) Imaging and characterization of engineered nanoparticles in sunscreens by electron microscopy, under wet and dry conditions. Int J Occup Environ Health 16(4):406–428

    Article  CAS  PubMed  Google Scholar 

  13. Contado C, Pagnoni A (eds) (2010) TiO2 nano-and micro-particles in commercial foundation: field flow-fractionation techniques together with ICP-AES and SQW voltammetry for their characterization. 16th International Symposium on Separation Science. Danilo Corradini, Antonella De Rossi, Isabella Nicoletti

  14. Mahmoud WM, Rastogi T, Kümmerer K (2017) Application of titanium dioxide nanoparticles as a photocatalyst for the removal of micropollutants such as pharmaceuticals from water. Curr Opin Green Sustain Chem 6:1–10

    Article  Google Scholar 

  15. Sharma V, Anderson D, Dhawan A (2012) Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria mediated apoptosis in human liver cells (HepG2). Apoptosis. 17(8):852–870

    Article  CAS  PubMed  Google Scholar 

  16. Chen T, Yan J, Li Y (2014) Genotoxicity of titanium dioxide nanoparticles. J Food Drug Anal 22(1):95–104

    Article  CAS  PubMed  Google Scholar 

  17. Xu X-HN, Brownlow WJ, Kyriacou SV, Wan Q, Viola JJ (2004) Real-time probing of membrane transport in living microbial cells using single nanoparticle optics and living cell imaging. Biochemistry. 43(32):10400–10413

    Article  CAS  PubMed  Google Scholar 

  18. Tsai Y-C, Chen S-Y, Liaw H-W (2007) Immobilization of lactate dehydrogenase within multiwalled carbon nanotube-chitosan nanocomposite for application to lactate biosensors. Sensors Actuators B Chem 125(2):474–481

    Article  CAS  Google Scholar 

  19. Ranjan S, Dasgupta N, Sudandiradoss C, Ramalingam C, Kumar A (2018) Titanium dioxide nanoparticle–protein interaction explained by docking approach. Int J Nanomedicine 13:47–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Trouiller B, Reliene R, Westbrook A, Solaimani P, Schiestl RH (2009) Titanium dioxide nanoparticles induce DNA damage and genetic instability in vivo in mice. Cancer Res 69(22):8784–8789

    Article  CAS  PubMed  Google Scholar 

  21. Knaapen AM, Borm PJ, Albrecht C, Schins RP (2004) Inhaled particles and lung cancer. Part A: Mechanisms. Int J Cancer 109(6):799–809

    Article  CAS  PubMed  Google Scholar 

  22. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358

    Article  CAS  PubMed  Google Scholar 

  23. Manke A, Wang L, Rojanasakul Y (2013) Mechanisms of nanoparticle-induced oxidative stress and toxicity. Biomed Res Int 2013:1–15

    Article  CAS  Google Scholar 

  24. Li M, Yin J-J, Wamer WG, Lo YM (2014) Mechanistic characterization of titanium dioxide nanoparticle-induced toxicity using electron spin resonance. J Food Drug Anal 22(1):76–85

    Article  CAS  PubMed  Google Scholar 

  25. Buzea C, Pacheco II, Robbie K (2007) Nanomaterials and nanoparticles: sources and toxicity. Biointerphases. 2(4):MR17–MR71

    Article  PubMed  Google Scholar 

  26. Ighodaro O, Akinloye O (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alexandria J Med 54(4):287–293

    Article  Google Scholar 

  27. Ognjanovic B, Pavlovic S, Maletic S, Zikic R, Stajn A, Radojicic R et al (2003) Protective influence of vitamin E on antioxidant defense system in the blood of rats treated with cadmium. Physiol Res 52(5):563–570

    CAS  PubMed  Google Scholar 

  28. Zaidi SKR, Banu N (2004) Antioxidant potential of vitamins A, E and C in modulating oxidative stress in rat brain. Clin Chim Acta 340(1-2):229–233

    Article  CAS  PubMed  Google Scholar 

  29. Traber MG, Atkinson J (2007) Vitamin E, antioxidant and nothing more. Free Radic Biol Med 43(1):4–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Niki E (2014) Role of vitamin E as a lipid-soluble peroxyl radical scavenger: in vitro and in vivo evidence. Free Radic Biol Med 66:3–12

    Article  CAS  PubMed  Google Scholar 

  31. De Luca LM (1991) Retinoids and their receptors in differentiation, embryogenesis, and neoplasia. FASEB J 5(14):2924–2933

    Article  PubMed  Google Scholar 

  32. Leid M, Kastner P, Chambon P (1992) Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem Sci 17(10):427–433

    Article  CAS  PubMed  Google Scholar 

  33. Kawakami S, Suzuki S, Yamashita F, Hashida M (2006) Induction of apoptosis in A549 human lung cancer cells by all-trans retinoic acid incorporated in DOTAP/cholesterol liposomes. J Control Release 110(3):514–521

    Article  CAS  PubMed  Google Scholar 

  34. Di C, Liao S, Adamson DC, Parrett TJ, Broderick DK, Shi Q et al (2005) Identification of OTX2 as a medulloblastoma oncogene whose product can be targeted by all-trans retinoic acid. Cancer Res 65(3):919–924

    CAS  PubMed  Google Scholar 

  35. Rao J, Qian X, Wang P, Pu L, Zhai Y, Wang X et al (2013) All-trans retinoic acid preconditioning protects against liver ischemia/reperfusion injury by inhibiting the nuclear factor kappa B signaling pathway. J Surg Res 180(2):e99–e106

    Article  CAS  PubMed  Google Scholar 

  36. Rao J, Zhang C, Wang P, Lu L, Zhang F (2010) All-trans retinoic acid alleviates hepatic ischemia/reperfusion injury by enhancing manganese superoxide dismutase in rats. Biol Pharm Bull 33(5):869–875

    Article  CAS  PubMed  Google Scholar 

  37. Hisamori S, Tabata C, Kadokawa Y, Okoshi K, Tabata R, Mori A, Nagayama S, Watanabe G, Kubo H, Sakai Y (2008) All-trans-retinoic acid ameliorates carbon tetrachloride-induced liver fibrosis in mice through modulating cytokine production. Liver Int 28(9):1217–1225

    Article  CAS  PubMed  Google Scholar 

  38. Ma Q (2013) Role of nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol 53:401–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Suzuki T, Motohashi H, Yamamoto M (2013) Toward clinical application of the Keap1–Nrf2 pathway. Trends Pharmacol Sci 34(6):340–346

    Article  CAS  PubMed  Google Scholar 

  40. Abdelazim SA, Darwish HA, Ali SA, Rizk MZ, Kadry MO (2015) Potential antifibrotic and angiostatic impact of idebenone, carnosine and vitamin E in nano-sized titanium dioxide-induced liver injury. Cell Physiol Biochem 35(6):2402–2411

    Article  CAS  PubMed  Google Scholar 

  41. Orazizadeh M, Fakhredini F, Mansouri E, Khorsandi L (2014) Effect of glycyrrhizic acid on titanium dioxide nanoparticles-induced hepatotoxicity in rats. Chem Biol Interact 220:214–221

    Article  CAS  PubMed  Google Scholar 

  42. Erel O (2005) A new automated colorimetric method for measuring total oxidant status. Clin Biochem 38(12):1103–1111

    Article  CAS  PubMed  Google Scholar 

  43. Chomczynski P (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques. 15(3):532–534 6-7

    CAS  PubMed  Google Scholar 

  44. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408

    Article  CAS  Google Scholar 

  45. Papp T, Schiffmann D, Weiss D, Castranova V, Vallyathan V, Rahman Q (2008) Human health implications of nanomaterial exposure. Nanotoxicology. 2(1):9–27

    Article  CAS  Google Scholar 

  46. Xue C, Wu J, Lan F, Liu W, Yang X, Zeng F, Xu H (2010) Nano titanium dioxide induces the generation of ROS and potential damage in HaCaT cells under UVA irradiation. J Nanosci Nanotechnol 10(12):8500–8507

    Article  CAS  PubMed  Google Scholar 

  47. Sanders K, Degn LL, Mundy WR, Zucker RM, Dreher K, Zhao B, Roberts JE, Boyes WK (2012) In vitro phototoxicity and hazard identification of nano-scale titanium dioxide. Toxicol Appl Pharmacol 258(2):226–236

    Article  CAS  PubMed  Google Scholar 

  48. Palace VP, Khaper N, Qin Q, Singal PK (1999) Antioxidant potentials of vitamin A and carotenoids and their relevance to heart disease. Free Radic Biol Med 26(5-6):746–761

    Article  CAS  PubMed  Google Scholar 

  49. Mehta K, McQueen T, Tucker S, Pandita R, Aggarwal BB (1994) Inhibition by all-trans-retinoic acid of tumor necrosis factor and nitric oxide production by peritoneal macrophages. J Leukoc Biol 55(3):336–342

    Article  CAS  PubMed  Google Scholar 

  50. Shirpoor A, Norouzi L, Nemati S, Ansari MHK (2015) Protective effect of vitamin E against diabetes-induced oxidized LDL and aorta cell wall proliferation in rat. Iran Biomed J 19(2):117–123

    PubMed  PubMed Central  Google Scholar 

  51. Wang J, Zhou G, Chen C, Yu H, Wang T, Ma Y, Jia G, Gao Y, Li B, Sun J, Li Y, Jiao F, Zhao Y, Chai Z (2007) Acute toxicity and biodistribution of different sized titanium dioxide particles in mice after oral administration. Toxicol Lett 168(2):176–185

    Article  CAS  PubMed  Google Scholar 

  52. Meena R, Paulraj R (2012) Oxidative stress mediated cytotoxicity of TiO2 nano anatase in liver and kidney of Wistar rat. Toxicol Environ Chem 94(1):146–163

    Article  CAS  Google Scholar 

  53. Hong J, Zhang Y-Q (2016) Murine liver damage caused by exposure to nano-titanium dioxide. Nanotechnology. 27(11):112001

    Article  PubMed  CAS  Google Scholar 

  54. Sang X, Zheng L, Sun Q, Li N, Cui Y, Hu R, Gao G, Cheng Z, Cheng J, Gui S, Liu H, Zhang Z, Hong F (2012) The chronic spleen injury of mice following long-term exposure to titanium dioxide nanoparticles. J Biomed Mater Res A 100(4):894–902

    Article  PubMed  CAS  Google Scholar 

  55. Tassinari R, Cubadda F, Moracci G, Aureli F, D’Amato M, Valeri M, de Berardis B, Raggi A, Mantovani A, Passeri D, Rossi M, Maranghi F (2014) Oral, short-term exposure to titanium dioxide nanoparticles in Sprague-Dawley rat: focus on reproductive and endocrine systems and spleen. Nanotoxicology. 8(6):654–662

    Article  CAS  PubMed  Google Scholar 

  56. Li N, Duan Y, Hong M, Zheng L, Fei M, Zhao X, Wang J, Cui Y, Liu H, Cai J, Gong S, Wang H, Hong F (2010) Spleen injury and apoptotic pathway in mice caused by titanium dioxide nanoparticules. Toxicol Lett 195(2-3):161–168

    Article  CAS  PubMed  Google Scholar 

  57. Wang J, Li N, Zheng L, Wang S, Wang Y, Zhao X, Duan Y, Cui Y, Zhou M, Cai J, Gong S, Wang H, Hong F (2011) P38-Nrf-2 signaling pathway of oxidative stress in mice caused by nanoparticulate TiO2. Biol Trace Elem Res 140(2):186–197

    Article  CAS  PubMed  Google Scholar 

  58. Pigeolet E, Corbisier P, Houbion A, Lambert D, Michiels C, Raes M, Zachary MD, Remacle J (1990) Glutathione peroxidase, superoxide dismutase, and catalase inactivation by peroxides and oxygen derived free radicals. Mech Ageing Dev 51(3):283–297

    Article  CAS  PubMed  Google Scholar 

  59. Ahamed M, Posgai R, Gorey TJ, Nielsen M, Hussain SM, Rowe JJ (2010) Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster. Toxicol Appl Pharmacol 242(3):263–269

    Article  CAS  PubMed  Google Scholar 

  60. Kim KT, Klaine SJ, Cho J, Kim S-H, Kim SD (2010) Oxidative stress responses of Daphnia magna exposed to TiO2 nanoparticles according to size fraction. Sci Total Environ 408(10):2268–2272

    Article  CAS  PubMed  Google Scholar 

  61. Kandeil MA, Mohammed ET, Hashem KS, Aleya L, Abdel-Daim MM (2020) Moringa seed extract alleviates titanium oxide nanoparticles (TiO2-NPs)-induced cerebral oxidative damage, and increases cerebral mitochondrial viability. Environ Sci Pollut Res 27(16):19169–19184

    Article  CAS  Google Scholar 

  62. Mohammed ET, Safwat GM (2020) Grape seed proanthocyanidin extract mitigates titanium dioxide nanoparticle (TiO2-NPs)–induced hepatotoxicity through TLR-4/NF-κB signaling pathway. Biol Trace Elem Res 196(2):579–589

    Article  CAS  PubMed  Google Scholar 

  63. Abdel-Daim MM, Eissa IA, Abdeen A, Abdel-Latif HM, Ismail M, Dawood MA et al (2019) Lycopene and resveratrol ameliorate zinc oxide nanoparticles-induced oxidative stress in Nile tilapia, Oreochromis niloticus. Environ Toxicol Pharmacol 69:44–50

    Article  CAS  PubMed  Google Scholar 

  64. Sun Q, Tan D, Zhou Q, Liu X, Cheng Z, Liu G et al (2012) Oxidative damage of lung and its protective mechanism in mice caused by long-term exposure to titanium dioxide nanoparticles. J Biomed Mater Res A 100(10):2554–2562

    Article  PubMed  CAS  Google Scholar 

  65. Zhou L, Xu D-Y, Sha W-G, Shen L, Lu G-Y, Yin X et al (2015) High glucose induces renal tubular epithelial injury via Sirt1/NF-kappaB/microR-29/Keap1 signal pathway. J Transl Med 13(1):352

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Gui S, Li B, Zhao X, Sheng L, Hong J, Yu X, Sang X, Sun Q, Ze Y, Wang L, Hong F (2013) Renal injury and Nrf2 modulation in mouse kidney following chronic exposure to TiO2 nanoparticles. J Agric Food Chem 61(37):8959–8968

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank staff of Hamadan Health Center for providing assistance.

Funding

This study was financially supported by Hamadan University of Medical Sciences (Grant Number: 970128398).

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Authors and Affiliations

  1. Department of Clinical Biochemistry, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran

    Mozhgan Afshari-Kaveh, Roghayeh Abbasalipourkabir & Nasrin Ziamajidi

  2. Department of Pathobiology, Faculty of Paraveterinary Medicine, Bu-Ali Sina University, Hamedan, Iran

    Alireza Nourian

  3. Molecular Medicine Research Center, Hamadan University of Medical Sciences, Hamadan, Iran

    Nasrin Ziamajidi

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  1. Mozhgan Afshari-Kaveh
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Afshari-Kaveh, M., Abbasalipourkabir, R., Nourian, A. et al. The Protective Effects of Vitamins A and E on Titanium Dioxide Nanoparticles (nTiO2)-Induced Oxidative Stress in the Spleen Tissues of Male Wistar Rats. Biol Trace Elem Res 199, 3677–3687 (2021). https://doi.org/10.1007/s12011-020-02487-z

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