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Research Articles

Antioxidant thymoquinone and eugenol alleviate TiO2 nanoparticle-induced toxicity in human blood cells in vitro

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Pages 619-629 | Received 28 Apr 2021, Accepted 23 Jun 2021, Published online: 19 Jul 2021

References

  • Aebi H. 1984. Catalase in vitro. Methods Enzymol. 105:121–126.
  • Afaq F, Abidi P, Matin R, Rahman Q. 1998. Cytotoxicity, pro-oxidant effects and antioxidant depletion in rat lung alveolar macrophages exposed to ultrafine titanium dioxide. J Appl Toxicol. 18(5):307–312.
  • Ali BH, Blunden G. 2003. Pharmacological and toxicological properties of Nigella sativa. Phytother Res. 17(4):299–305.
  • Andrés MT, Fierro JF. 2010. Antimicrobial mechanism of action of transferrins: selective inhibition of H+-ATPase. Antimicrob Agents Chemother. 54(10):4335–4342.
  • Badary OA, Taha RA, Gamal el-Din AM, Abdel-Wahab MH. 2003. Thymoquinone is a potent superoxide anion scavenger. Drug Chem Toxicol. 26(2):87–98.
  • Bal S, Yadav A, Verma N, Aggarwal NK, Gupta R. 2017. Ameliorative effect of eugenol and anethole on arsenic induced oxidative DNA damage in cultured human peripheral blood lymphocytes. IJPSDR. 9 (3):134–138.
  • Banerjee D, Kumar PA, Kumar B, Madhusoodanan UK, Nayak S, Jacob J. 2002. Determination of absolute hydrogen peroxide concentration by spectrophotometric method. Curr Sci. 83(10):1193–1194.
  • Baranowska-Wójcik E, Szwajgier D, Oleszczuk P, Winiarska-Mieczan A. 2020. Effects of titanium dioxide nanoparticles exposure on human health: a review. Biol Trace Elem Res. 193(1):118–129.
  • Behnam MA, Emami F, Sobhani Z, Dehghanian AR. 2018. The application of titanium dioxide (TiO2) nanoparticles in the photo-thermal therapy of melanoma cancer model. Iran J Basic Med Sci. 21(11):1133–1139.
  • Beutler E. 1984. Red cell metabolism: a manual of biochemical methods. 3rd ed. New York (NY): Grune and Stratton.
  • Buege JA, Aust SD. 1978. Microsomal lipid peroxidation. In: Methods in enzymeology. Academic Press, USA; p. 302–310.
  • Burd JF, Usategui-Gomez M. 1973. A colorimetric assay for serum lactate dehydrogenase. Clin Chim Acta. 46(3):223–227.
  • Burits M, Bucar F. 2000. Antioxidant activity of Nigella sativa essential oil. Phytother Res. 14(5):323–328.
  • Canli EG, Canli, M. 2019. Nanoparticles (Al2O3, CuO, TiO2) decrease ATPase activity in the osmoregulatory organs of freshwater fish (Oreochromis niloticus): Histopathological investigations of tissues by transmission electron microscope. SSRN Electron J. 7(9):909–924.
  • Catalá A, Díaz M. 2016. Editorial: Impact of lipid peroxidation on the physiology and pathophysiology of cell membranes. Front Physiol. 7:423.
  • Chan FK-M, Moriwaki K, De Rosa MJ. 2013. Detection of necrosis by release of lactate dehydrogenase activity. Methods Mol Biol. 979:65–70.
  • Chen C, Bu W, Ding H, Li Q, Wang D, Bi H, Guo D. 2017. Cytotoxic effect of zinc oxide nanoparticles on murine photoreceptor cells via potassium channel block and Na+/K+ -ATPase inhibition. Cell Prolif. 50(3):e12339.
  • Chen T, Yan J, Li Y. 2014. Genotoxicity of titanium dioxide nanoparticles. J Food Drug Anal. 22(1):95–104.
  • Chniguir A, Pintard C, Liu D, Dang PM-C, El-Benna J, Bachoual R. 2019. Eugenol prevents fMLF-induced superoxide anion production in human neutrophils by inhibiting ERK1/2 signaling pathway and p47phox phosphorylation. Sci Rep. 9(1):18540.
  • Cho EC, Au L, Zhang Q, Xia Y. 2010. The effects of size, shape, and surface functional group of gold nanostructures on their adsorption and internalization by cells. Small. 6(4):517–522.
  • Dobrzyńska MM, Gajowik A, Radzikowska J, Lankoff A, Dušinská M, Kruszewski M. 2014. Genotoxicity of silver and titanium dioxide nanoparticles in bone marrow cells of rats in vivo. Toxicology. 315:86–91.
  • Duan Y, Liu J, Ma L, Li N, Liu H, Wang J, Zheng L, Liu C, Wang X, Zhao X, et al. 2010. Toxicological characteristics of nanoparticulate anatase titanium dioxide in mice. Biomaterials. 31(5):894–899.
  • Dubey K, Anand BG, Shekhawat DS, Kar K. 2017. Eugenol prevents amyloid formation of proteins and inhibits amyloid-induced hemolysis. Sci Rep. 7:40744.
  • Duchnowicz P, Koter M, Duda W. 2002. Damage of erythrocyte by phenoxyacetic herbicides and their metabolites. Pestic Biochem Physiol. 74(1):1–7.
  • EFSA Panel on Food Additives and Nutrient Sources added to Food (ANS). 2016. Re‐evaluation of titanium dioxide (E 171) as a food additive. EFSA J. 14(9):e04545.
  • Elbahy DA, Madkour HI, Abdel-Raheem MH. 2015. Evaluation of antihyperlipidemic activity of eugenol in triton induced hyperlipidemia in rats. International Journal of Research Studies in Biosciences. 10(3):19–26.
  • Gatoo MA, Naseem S, Arfat MY, Dar AM, Qasim K, Zubair S. 2014. Physicochemical properties of nanomaterials: implication in associated toxic manifestations. Biomed Res Int. 2014:498420.
  • Ghosh M, Chakraborty A, Mukherjee A. 2013. Cytotoxic, genotoxic and the hemolytic effect of titanium dioxide (TiO2 ) nanoparticles on human erythrocyte and lymphocyte cells in vitro. J Appl Toxicol. 33(10):1097–1110.
  • Halliwell B. 2006. Reactive species and antioxidants: Redox biology is a fundamental theme of aerobic life. Plant Physiol. 141(2):312–322.
  • Hamida RS, Albasher G, Bin-Meferij MM. 2020. Oxidative stress and apoptotic responses elicited by nostoc-synthesized silver nanoparticles against different cancer cell lines. Cancers. 12(8):2099.
  • Hamida RS, Ali MA, Redhwan AMO, Bin-Meferij MM. 2020. Cyanobacteria: a promising platform in green nanotechnology: a review on nanoparticles fabrication and their prospective applications. Int J Nanomed. 15:6033–6066.
  • Hassanein KMA, El-Amir YO. 2017. Protective effects of thymoquinone and avenanthramides on titanium dioxide nanoparticles induced toxicity in Sprague-Dawley rats. Pathol Res Pract. 213(1):13–22.
  • Hauck TS, Ghazani AA, Chan WCW. 2008. Assessing the effect of surface chemistry on gold nanorod uptake, toxicity, and gene expression in mammalian cells. Small. 4(1):153–159.
  • Hebbel RP, Leung A, Mohandas N. 1990. Oxidation-induced changes in microrheologic properties of the red blood cell membrane. Blood. 76(5):1015–1020.
  • Hu R, Gong X, Duan Y, Li N, Che Y, Cui Y, Zhou M, Liu C, Wang H, Hong F. 2010. Neurotoxicological effects and the impairment of spatial recognition memory in mice caused by exposure to TiO2 nanoparticles. Biomaterials. 31(31):8043–8050.
  • Huang X, Liu Y, Lu Y, Ma C. 2015. Anti-inflammatory effects of eugenol on lipopolysaccharide-induced inflammatory reaction in acute lung injury via regulating inflammation and redox status. Int Immunopharmacol. 26(1):265–271.
  • Jawaid P, Rehman MU, Zhao Q-L, Misawa M, Ishikawa K, Hori M, Shimizu T, Saitoh J-I, Noguchi K, Kondo T. 2020. Small size gold nanoparticles enhance apoptosis-induced by cold atmospheric plasma via depletion of intracellular GSH and modification of oxidative stress. Cell Death Discov. 6:83.
  • Jin C, Tang Y, Yang FG, Li XL, Xu S, Fan XY, Huang YY, Yang YJ. 2011. Cellular toxicity of TiO2 nanoparticles in anatase and rutile crystal phase. Biol Trace Elem Res. 141(1–3):3–15.
  • Jugan M-L, Barillet S, Simon-Deckers A, Herlin-Boime N, Sauvaigo S, Douki T, Carriere M. 2012. Titanium dioxide nanoparticles exhibit genotoxicity and impair DNA repair activity in A549 cells. Nanotoxicology. 6(5):501–513.
  • Kandil EI, El-Sonbaty SM, Moawed FS, Khedr OM. 2018. Anticancer redox activity of gallium nanoparticles accompanied with low dose of gamma radiation in female mice. Tumour Biol. 40(3):1010428317749676.
  • Kaur P, Purewal SS, Sandhu KS, Kaur M. 2019. DNA damage protection: an excellent application of bioactive compounds. Bioresour Bioprocess. 6(1):2.
  • Khazdair MR. 2015. The protective effects of Nigella sativa and its constituents on induced neurotoxicity. J Toxicol. 2015:841823–841827.
  • Kim D-Y, Won K-J, Hwang DI, Park SM, Kim B, Lee HM. 2018. Chemical composition, antioxidant and anti-melanogenic activities of essential oils from Chrysanthemum boreale Makino at different harvesting stages. Chem Biodiversity. 15(2):e1700506.
  • Lee K-G, Shibamoto T. 2001. Antioxidant property of aroma extract isolated from clove buds [Syzygium aromaticum (L.) Merr. et Perry]. Food Chem. 74(4):443–448.
  • Lee SR, Yang KS, Kwon J, Lee C, Jeong W, Rhee SG. 2002. Reversible inactivation of the tumor suppressor PTEN by H2O2. J Biol Chem. 277(23):20336–20342.
  • Leroux MM, Doumandji Z, Chézeau L, Gaté L, Nahle S, Hocquel R, Zhernovkov V, Migot S, Ghanbaja J, Bonnet C, et al. 2020. Toxicity of TiO2 nanoparticles: Validation of alternative models. IJMS. 21(14):4855.
  • Li L, Du J, Lian Y, Zhang Y, Li X, Liu Y, Zou L, Wu T. 2016. Protective effects of coenzyme Q10 against hydrogen peroxide-induced oxidative stress in PC12 Cell: The role of Nrf2 and antioxidant enzymes. Cell Mol Neurobiol. 36(1):103–111.
  • Li S-Q, Zhu R-R, Zhu H, Xue M, Sun X-Y, Yao S-D, Wang S-L. 2008. Nanotoxicity of TiO(2) nanoparticles to erythrocyte in vitro. Food Chem Toxicol. 46(12):3626–3631.
  • Liochev SI, Chen LL, Hallewell RA, Fridovich I. 1998. The familial amyotrophic lateral sclerosis-associated amino acid substitutions E100G, G93A, and G93R do not influence the rate of inactivation of copper- and zinc-containing superoxide dismutase by H2O2. Arch Biochem Biophys. 352(2):237–239.
  • Liu H, Ma L, Liu J, Zhao J, Yan J, Hong F. 2010. Toxicity of nano-anatase TiO2 to mice: liver injury, oxidative stress. Toxicol Environ Chem. 92(1):175–186.
  • Liu H, Ma L, Zhao J, Liu J, Yan J, Ruan J, Hong F. 2009. Biochemical toxicity of nano-anatase TiO2 particles in mice. Biol Trace Elem Res. 129(1–3):170–180.
  • Madhubala V, Pugazhendhi A, Thirunavukarasu K. 2019. Cytotoxic and immunomodulatory effects of the low concentration of titanium dioxide nanoparticles (TiO2 NPs) on human cell lines – an in vitro study. Process Biochem. 86:186–195.
  • Maheshwari N, Mahmood R. 2020a. 3,4-Dihydroxybenzaldehyde attenuates pentachlorophenol-induced cytotoxicity, DNA damage and collapse of mitochondrial membrane potential in isolated human blood cells. Drug Chem Toxicol. 1–18. doi: https://doi.org/10.1080/01480545.2020.1811722
  • Maheshwari N, Mahmood R. 2020b. Protective effect of catechin on pentachlorophenol-induced cytotoxicity and genotoxicity in isolated human blood cells. Environ Sci Pollut Res Int. 27(12):13826–13843.
  • Mahmoud SS, Torchilin VP. 2013. Hormetic/cytotoxic effects of Nigella sativa seed alcoholic and aqueous extracts on MCF-7 breast cancer cells alone or in combination with doxorubicin. Cell Biochem Biophys. 66(3):451–460.
  • Mahmoud YK, Abdelrazek HMA. 2019. Cancer: Thymoquinone antioxidant/pro-oxidant effect as potential anticancer remedy. Biomed Pharmacother. 115:108783.
  • Marano F, Hussain S, Rodrigues-Lima F, Baeza-Squiban A, Boland S. 2011. Nanoparticles: molecular targets and cell signalling. Arch Toxicol. 85(7):733–741.
  • Marklund S, Marklund G. 1974. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem. 47(3):469–474.
  • 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.
  • 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.
  • Morsi NM. 2000. Antimicrobial effect of crude extracts of Nigella sativa on multiple antibiotics-resistant bacteria. Acta Microbiol Pol. 49(1):63–74.
  • Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 65(1–2):55–63.
  • MubarakAli D, Arunkumar J, Nag KH, SheikSyedIshack KA, Baldev E, Pandiaraj D, Thajuddin N. 2013. Gold nanoparticles from pro and eukaryotic photosynthetic microorganisms-comparative studies on synthesis and its application on biolabelling. Colloids Surf B Biointerfaces. 103:166–173.
  • Nagashima K. 1989. Inhibitory effect of eugenol on Cu2+-catalyzed lipid peroxidation in human erythrocyte membranes. Int J Biochem. 21(7):745–749.
  • Nel A, Xia T, Mädler L, Li N. 2006. Toxic potential of materials at the nanolevel. Science. 311(5761):622–627.
  • Ortlieb M. 2010. White giant or white dwarf?: Particle size distribution measurements of TiO2. GIT Laboratory Journal Europe. 14:42–43.
  • Pourahmad J, Amirmostofian M, Kobarfard F, Shahraki J. 2009. Biological reactive intermediates that mediate dacarbazine cytotoxicity. Cancer Chemother Pharmacol. 65 (1):89–96.
  • Pramod K, Ansari SH, Ali J. 2010. Eugenol: A natural compound with versatile pharmacological actions. Nat Prod Commun. 5 (12):1934578X1000501.
  • R Core Team 2018. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
  • Rahman A, Shahabuddin n, Hadi SM, Parish JH. 1990. Complexes involving quercetin, DNA and Cu(II). Carcinogenesis. 11 (11):2001–2003.
  • Rao PV, Gan SH. 2014. Cinnamon: a multifaceted medicinal plant. Evid Based Complement Alternat Med. 2014:642912–642942.
  • Raza M, Alghasham AA, Alorainy MS, El-Hadiyah TM. 2008. Potentiation of valproate-induced anticonvulsant response by Nigella sativa seed constituents: the role of GABA receptors. Int J Health Sci. 2(1):15–25.
  • Scott MD, van den Berg JJ, Repka T, Rouyer-Fessard P, Hebbel RP, Beuzard Y, Lubin BH. 1993. Effect of excess alpha-hemoglobin chains on cellular and membrane oxidation in model beta-thalassemic erythrocytes. J Clin Invest. 91(4):1706–1712.
  • Shukla RK, Sharma V, Pandey AK, Singh S, Sultana S, Dhawan A. 2011. ROS-mediated genotoxicity induced by titanium dioxide nanoparticles in human epidermal cells. Toxicol Vitro. 25 (1):231–241.
  • Sies H. 2000. What is oxidative stress?. In: Keaney JF, Jr, editor. Oxidative stress and vascular disease. Boston (MA): Kluwer Academic Publishers; p. 1–8.
  • Sundaresan M, Yu Z, Ferrans V, Irani K, Finkel T. 1995. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science. 270(5234):296–299.
  • Sycheva LP, Zhurkov VS, Iurchenko VV, Daugel-Dauge NO, Kovalenko MA, Krivtsova EK, Durnev AD. 2011. Investigation of genotoxic and cytotoxic effects of micro- and nanosized titanium dioxide in six organs of mice in vivo. Mutat Res. 726 (1):8–14.
  • Tiku AB, Abraham SK, Kale RK. 2004. Eugenol as an in vivo radioprotective agent. J Radiat Res. 45 (3):435–440.
  • USFDA 2020. Listing of color additives exempt from certification. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?CFRPart=73
  • Valdiglesias V, Costa C, Sharma V, Kiliç G, Pásaro E, Teixeira JP, Dhawan A, Laffon B. 2013. Comparative study on effects of two different types of titanium dioxide nanoparticles on human neuronal cells. Food Chem Toxicol. 57:352–361.
  • Venkadeswaran K, Muralidharan AR, Annadurai T, Ruban VV, Sundararajan M, Anandhi R, Thomas PA, Geraldine P. 2014. 2014. Antihypercholesterolemic and antioxidative potential of an extract of the plant, Piper betle, and its active constituent, eugenol, in triton WR-1339-induced hypercholesterolemia in experimental rats. Evid Based Complement Alternat Med. 2014:478911–478973.
  • Venkatachallam TSK, Pattekhan H, Divakar S, Kadimi US. 2010. Chemical composition of Nigella sativa L. seed extracts obtained by supercritical carbon dioxide. J Food Sci Technol. 47(6):598–605.
  • Wang C, Hu X, Gao Y, Ji Y. 2015. ZnO Nanoparticles treatment induces apoptosis by increasing intracellular ROS levels in LTEP-a-2 cells. BioMed Res Int. 2015:1–9.
  • Wang H, Joseph JA. 1999. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Rad Biol Med. 27(5–6):612–616.
  • Wani MR, Shadab G. 2020. Titanium dioxide nanoparticle genotoxicity: a review of recent in vivo and in vitro studies. Toxicol Ind Health. 36(7):514–530.
  • Wani MR, Shadab GGHA. 2021. Low doses of thymoquinone protect isolated human blood cells from TiO2 nanoparticles induced oxidative stress, hemolysis, cytotoxicity, DNA damage and collapse of mitochondrial activity. Phytomedicine Plus. 1(4):100056.
  • Wani MR, Maheshwari N, Shadab G. 2021. Eugenol attenuates TiO2 nanoparticles-induced oxidative damage, biochemical toxicity and DNA damage in Wistar rats: an in vivo study. Environ Sci Pollut Res. 28(18):22664–22678.
  • Xia Z, He J, Li B, He K, Yang W, Chen X, Zhang J, Xiang G. 2018. Titanium dioxide nanoparticles induce mitochondria-associated apoptosis in HepG2 cells. RSC Adv. 8(55):31764–31776.
  • Xie G, Wang C, Sun J, Zhong G. 2011. Tissue distribution and excretion of intravenously administered titanium dioxide nanoparticles. Toxicol Lett. 205(1):55–61.
  • Xu Y, Hadjiargyrou M, Rafailovich M, Mironava T. 2017. Cell-based cytotoxicity assays for engineered nanomaterials safety screening: exposure of adipose derived stromal cells to titanium dioxide nanoparticles. J Nanobiotechnology. 15 (1):50.
  • Yogalakshmi B, Viswanathan P, Anuradha CV. 2010. Investigation of antioxidant, anti-inflammatory and DNA-protective properties of eugenol in thioacetamide-induced liver injury in rats. Toxicology. 268(3):204–212.
  • Yu Z, Li Q, Wang J, Yu Y, Wang Y, Zhou Q, Li P. 2020. Reactive oxygen species-related nanoparticle toxicity in the biomedical field. Nanoscale Res Lett. 15(1):115.
  • Zhao H, Chen L, Zhong G, Huang Y, Zhang X, Chu C, Chen L, Wang M. 2019. Titanium dioxide nanoparticles induce mitochondrial dynamic imbalance and damage in HT22 cells. J Nanomater. 2019:1–16.
  • Zhu QY, Schramm DD, Gross HB, Holt RR, Kim SH, Yamaguchi T, Kwik-Uribe CL, Keen CL. 2005. Influence of cocoa flavanols and procyanidins on free radical-induced human erythrocyte hemolysis. Clin Develop Immunol. 12(1):27–34.

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