Interaction of titanium dioxide and zinc oxide nanoparticles induced cytogenotoxicity in Allium cepa

Abstract

The extensive production and utilisation of titanium dioxide (TiO2) and zinc oxide (ZnO) nanoparticles (NPs) in consumable items may enhance significant increase in fauna and flora exposure. Studies showing the interactive effect of NPs in biological systems are limited. Herein, we showed the cytogenotoxic effects of TiO2 and ZnO NPs, and their mixture (1:1) using the Allium cepa assay. Mitotic index (MI) and chromosomal aberrations (CAs) were assessed in A. cepa L. bulbs exposed to each NP and their mixture at concentrations of 5, 10, 20, 40 and 80 mg L−1, respectively. The recovery effect of the root tip cells from the cytogenotoxic effects of the nanoparticles was also investigated. TiO2, ZnO NPs and their mixture significantly (p < 0.05) induced increase in CA and reduction in MI in A. cepa root cells, but the mixture induced the highest frequency of CA and reduction in MI. When the treated meristematic cells were placed in water for recovery, there were reduction in the number of aberrant cells in A. cepa exposed to TiO2 and the mixture. Interactive factor analysis of the effects of the mixture showed antagonism. The aberrations induced by TiO2 NPs appeared to be transient while those induced by ZnO NPs may be transmissible due to the increase in frequency of aberrations in the recovery test. This finding showed the potential of tested NPs to induce mutation in somatic cells, and is of public and environmental health significance.

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References

  1. 1.

    Amer SM, Ali EM. Cytological effects of pesticides V. Effects of some herbicides on Vicia faba. Cytologia. 1974;39:633.

    CAS  Google Scholar 

  2. 2.

    Asztemborska M, Steborowski R, Kowalska J, Bystrzejewska-Piotrowska G. Accumulation of aluminium by plants exposed to nano-and microsized particles of Al. Int J Environ Res. 2015;9(1):109–16.

    CAS  Google Scholar 

  3. 3.

    Atoyebi SM, Oyeyemi IT, Dauda BA, Bakare AA. Genotoxicity and anti- genotoxicity of aqueous extracts of herbal recipes containing Luffa cylindrica (L), Nymphaea lotus (L) and Spondias mombin (L) using the Allium cepa (L) assay. African Journal of Pharmacy and Pharmacology. 2015;9(15):492–9.

    Google Scholar 

  4. 4.

    Bakare AA, Okunola AA, Adetunji OA, Jenmi HB. Genotoxicity assessment of a pharmaceutical effluent using four bioassays. Genet Mol Biol. 2009;32(2):373–81.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Bakare AA, Adeyemi AO, Adeyemi A, Alabi OA, Osibanjo O. Cytogenotoxic effects of electronic waste leachate in Allium cepa. Caryologia. 2012;65(2):94–100.

    Google Scholar 

  6. 6.

    Bakare AA, Alabi OA, Gbadebo AM, Ogunsuyi OI, Alimba CG. In vivo cytogenotoxicity and oxidative stress induced by electronic waste leachate and contaminated groundwater. Challenges. 2013;4:169–87.

    Google Scholar 

  7. 7.

    Balasubramanyam A, Sailaja N, Mahboob M, Rahman MF, Hussain SM, Grover P. In vivo genotoxicity assessment of aluminum oxide nanomaterials in rat peripheral blood cells using the Comet assay and micronucleus test. Mutagenesis. 2009;24(3):245–51.

    CAS  Google Scholar 

  8. 8.

    Bundschuh M, Filser J, Lüderwald S, McKee MS, Metreveli G, Schaumann GE, Schulz R, Wagner S. Nanoparticles in the environment: where do we come from, where do we go to? Environ Sci Eur. 2018;30:6. https://doi.org/10.1186/s12302-018-0132-6.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Choi J, Lee JK, Jeong J, Choy J. Toxicity evaluation of inorganic nanoparticles: considerations and challenges. Mol Cell Toxicol. 2013;9:205–10.

    CAS  Google Scholar 

  10. 10.

    Darlington CD, Mc LL. Action of maleic hydrazide on the cell. Nature. 1951;167:407–8.

    CAS  PubMed  Google Scholar 

  11. 11.

    Di Virgilio AL, Regiosa M, Arnal PM, Lorenzo F, de Mele M. Comparative study of the cytotoxic and genotoxic effects of titanium dioxide and aluminum oxide nanoparticles in Chinese hamster ovary (CHO-K1) cells. J Hazard Mater. 2010;177:711–8.

    PubMed  Google Scholar 

  12. 12.

    Drost W, Matzke M, Backhaus T. Heavy metal toxicity to Lemna minor: studies on the time dependence of growth inhibition and the recovery after exposure. Chemosphere. 2007;67:36–433.

    CAS  PubMed  Google Scholar 

  13. 13.

    Dutta J, Ahmad A, Singh J. Study of industrial effluents induced genotoxicity on Allium cepa. Caryologia. 2018;71(2):139–45.

    Google Scholar 

  14. 14.

    Fadoju OM, Ogunsuyi OI, Akanni O, Alabi O, Alimba C, Adaramoye O, Cambier S, Eswara S, Gutleb AC, Bakare AA. Evaluation of cytogenotoxicity and oxidative stress parameters in male Swiss mice co-exposed to titanium dioxide and zinc oxide nanoparticles. Environ Toxicol Pharmacol. 2019;70:103204.

    PubMed  Google Scholar 

  15. 15.

    Fang J, Shijirbaatar A, Lin DH, Wang DJ, Shen B, Sun PD, Zhou ZQ. Stability of co-existing ZnO and TiO2 nanomaterials in natural water: aggregation and sedimentation mechanisms. Chemosphere. 2017;184:1125–33.

    CAS  PubMed  Google Scholar 

  16. 16.

    Filho RDS, Vicari T, Santos SA, Felisbino K, Mattoso N, Anna-Santos BFS, Cestari MM, Leme DM. Genotoxicity of titanium dioxide nanoparticles and triggering of defense mechanisms in Allium cepa. Genet Mol Biol. 2019;42(2):425–35.

    Google Scholar 

  17. 17.

    Fiskesjo G. The Allium test as standard in environmental monitoring. Hereditas. 1985;102:99–112.

    CAS  PubMed  Google Scholar 

  18. 18.

    Fiskesjo G. Allium test for screening chemicals; evaluation of cytological parameters. In: Wuncheng W, Gorsuch JW, Hughes JS, editors. Plants for environmental studies. Boca Raton: CRC Lewis Publishers; 1997. p. 307–333.

    Google Scholar 

  19. 19.

    Ghodake G, Seo YD, Lee DS. Hazardous phytotoxic nature of cobalt and zinc oxide nanoparticles assesses using Allium cepa. J Hazard Mater. 2011;186:952–5.

    CAS  PubMed  Google Scholar 

  20. 20.

    Ghosh M, Bandyopadhyay M, Mukherjee A. Genotoxicity of titanium dioxide (TiO2) nanoparticles at two trophic levels: plant and human lymphocytes. Chemosphere. 2010;81:1253–62.

    CAS  PubMed  Google Scholar 

  21. 21.

    Ghosh M, Jana A, Sinha S, Jothiramajayam M, Nag A, Chakraborty A, Mukherjee A, Mukherjee A. Effects of ZnO nanoparticles in plants: cytotoxicity, genotoxicity, deregulation of antioxidant defenses, and cell-cycle arrest. Mutat Res. 2016;807:25–322.

    CAS  Google Scholar 

  22. 22.

    Gichner T, Patkova Z, Szakova J, Demnerova K. Cadmium induces DNA damage in tobacco roots, but no DNA damage, somatic mutations or homologous recombinations in tobacco leaves. Mutat Res. 2004;559:49–57.

    CAS  PubMed  Google Scholar 

  23. 23.

    Grover IS, Kaur S. Genotoxicity of wastewater samples from sewage and industrial effluent detected by the Allium root anaphase aberration and micronucleus assays. Mutat Res. 1999;426:183–8.

    CAS  PubMed  Google Scholar 

  24. 24.

    Hashimoto M, Imazato S. Cytotoxic and genotoxic characterization of aluminum and silicon oxide nanoparticles in macrophages. Dent Mater. 2015;31(5):556–64.

    CAS  PubMed  Google Scholar 

  25. 25.

    Jia F, Sun Z, Yan X, Zhou B, Wang J. Effect of pubertal nano-TiO2 exposure on testosterone synthesis and spermatogenesis in mice. Arch Toxicol. 2013;88(3):781–8.

    PubMed  Google Scholar 

  26. 26.

    Jiang Y, Sun Y, Liu H, Zhu F, Yin H. Solar photocatalytic decolorisation of C.I. Basic Blue 41 in an aqueous suspension of TiO2-ZnO. Dyes and Pigment. 2008;78(1):77–83.

    CAS  Google Scholar 

  27. 27.

    Katsifis SP, Kinney PL, Hosselet S, Burns FJ, Christie NT. Interaction of nickel with in the induction of sister chromatid exchanges in human lymphocytes. Mutation. 1996;359(1):7–15.

    Google Scholar 

  28. 28.

    Kaufman BP. Cytochemical studies of changes induced in cellular material by ionization radiations. Ann N Y Acad Sci. 1958;59:553.

    Google Scholar 

  29. 29.

    Khan M, Naqvi AH, Ahmad M. Comparative study of the cytotoxic and genotoxic potentials of zinc oxide and titanium dioxide nanoparticles. Toxicology Report. 2015;2:765–74.

    CAS  Google Scholar 

  30. 30.

    Kim K, Song J, Kim M, Chung A, Jeong J, Yang J, Choi A, Choi H, Oh J. Physicochemical analysis methods for nanomaterials considering their toxicological evaluations. Mol Cell Toxicol. 2014;10:342–60.

    Google Scholar 

  31. 31.

    Klancnik K, Drobne D, Valant J, DolencKoce J. Use of a modified Allium test with nanoTiO2. Ecotoxicol Environ Saf. 2011;74:85–92.

    CAS  PubMed  Google Scholar 

  32. 32.

    Ko K, Koh D, Kong I. Toxicity evaluation of individual and mixtures of nanoparticles based on algal chlorophyll content and cell count. Materials (Basel). 2018;11(1):121.

    Google Scholar 

  33. 33.

    Kocaman AY, Kilic E. Evaluation of the genotoxicity of commercial formulations of ethephon and ethephon+cyclanilide on Allium cepa L. root meristematic cells. Caryologia. 2017;70(3):229–37.

    Google Scholar 

  34. 34.

    Kumar A, Najafzadeh M, Jacob BK, Dhawan A, Anderson D. Zinc oxide nanoparticles affect the expression of p53, Ras p21 and JNKs: an ex vivo/in vitro exposure study in respiratory disease patients. Mutagenesis. 2015;30(2):237–45.

    CAS  PubMed  Google Scholar 

  35. 35.

    Kumar A, Dhawan A. Genotoxic and carcinogenic potential of engineered nanoparticles: an update. Arch Toxicol. 2013;87:1883–900.

    CAS  PubMed  Google Scholar 

  36. 36.

    Kumari M, Khan SS, Pakrashi S, Mukherjee A, Chandrasekaran N. Cytogenetic and genotoxic effects of zinc oxide nanoparticles on root cells of Allium cepa. J Hazard Mater. 2011;190:613–21.

    CAS  PubMed  Google Scholar 

  37. 37.

    Larue C, Laurette J, Herlin-Boime N, Khodja H, Favard B, Flank A, Brisset F, Carriere M. Accumulation, trans location and impact of TiO2 nanoparticles in wheat: influence of diameter and crystal phase. Sci Total Environ. 2012;431:197–208.

    CAS  PubMed  Google Scholar 

  38. 38.

    Lee CW, Mahendra S, Zodrow K, Li D, Tsai YC, Braam J. Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environ Toxicol Chem. 2010;29:669–75.

    CAS  PubMed  Google Scholar 

  39. 39.

    Lee S, Chung H, Kim S, Lee I. The genotoxic effect of ZnO and CuO nanoparticles on early growth of Buckwheat, Fagopyrum esculentum. Water, Air, Soil Pollut. 2013;224:1668.

    Google Scholar 

  40. 40.

    Leme DM, Marin-Morales MA. Allium cepa test in environmental monitoring: a review on its application. Mutat Res. 2009;682:71–81.

    CAS  PubMed  Google Scholar 

  41. 41.

    Lin D, Xing B. Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ Pollut. 2008;150(2):243–50.

    Google Scholar 

  42. 42.

    Magdolenova Z, Collins A, Kumar A, Dhawan A, Stone V, Dusinska M. Mechanisms of genotoxicity: a review of in vitro and in vivo studies with engineered nanoparticles. Nanotoxicology. 2014;8(3):233–78.

    CAS  PubMed  Google Scholar 

  43. 43.

    Mesi A, Kopliku D. Cytotoxic and genotoxic potency screening of two pesticides on Allium cepa. Procedia Technol. 2013;8:19–26.

    Google Scholar 

  44. 44.

    Nam D, Lee B, Eom I, Kim P, Yeo M. Uptake and bioaccumulation of titanium- and silver- nanoaparticles in aquatic ecosystems. Mol Cell Toxicol. 2014;10:9–17.

    CAS  Google Scholar 

  45. 45.

    Ogunsuyi OI, Fadoju OM, Coker MM, Akinrinade SO, Oyeyemi IT, Alabi OA, Alimba CG, Bakare AA. Nano-genotoxicity evaluation: a review. In: Kumar VN, Ranjan S, editors. Nanotoxicology: toxicity, risk assessment and management. Boca Raton: CRC Press Taylor and Francis Group; 2018. p. 463–504.

    Google Scholar 

  46. 46.

    Oyeyemi IT, Bakare AA. Genotoxic and anti-genotoxic effect of aqueous extracts of Spondias mombin L., Nymphea lotus L. and Luffa cylindrica L. on Allium cepa root tip cells. Caryologia. 2013;66(4):360–7.

    Google Scholar 

  47. 47.

    Pakrashi S, Jain N, Dalai S, Jayakumar J, Chandrasekaran PT, Raichur AM, Chandrasekaran N, Mukherjee A. In vivo genotoxicity assessment of titanium dioxide nanoparticles by Allium cepa root tip assay at high exposure concentrations. PLoS ONE. 2014;9(2):e87789.

    PubMed  PubMed Central  Google Scholar 

  48. 48.

    Park C, Jung J, Baek M, Sung B, Park J, Seol Y, Yeom D, Park J, Kin Y. Mixture toxicity of metal oxide nanoparticles and silver ions on Daphnia magna. J Nanopart Res. 2019;21:166.

    Google Scholar 

  49. 49.

    Ramesh M, Palanisamy K, Babu K, Sharma NK. Effects of bulk and nano-titanium dioxide and zinc oxide on physio-morphological changes in Triticum aestivum Linn. J Glob Biosci. 2014;3(2):415–22.

    Google Scholar 

  50. 50.

    Sharma V, Singh P, Pandey A, Dhawan A. Induction of oxidative stress, DNA damage and apoptosis in mouse liver after sub-acute oral exposure to zinc oxide nanoparticles. Mutat Res. 2012;745:84–91.

    CAS  PubMed  Google Scholar 

  51. 51.

    Shaymurat T, Gu J, Xu C, Yang Z, Zhao Q, Liu Y, Liu Y. Phytotoxic and genotoxic effects of ZnO nanoparticles on garlic (Allium sativum L.): a morphological study. Nanotechnology. 2012;6(3):241–8.

    CAS  Google Scholar 

  52. 52.

    Shukla RK, Sharma V, Pandey AK, Singh S, Sultana S, Dhawan A. ROS-mediated genotoxicity induced by titanium dioxide nanoparticles in human epidermal cells. Toxicol In Vitro. 2011;25:231–41.

    CAS  PubMed  Google Scholar 

  53. 53.

    Singh S. Nanomaterials as non-viral siRNA delivery agents for cancer therapy. Bioimpacts. 2013;3(2):53–655.

    PubMed  PubMed Central  Google Scholar 

  54. 54.

    Sun Z, Xiong T, Zhang T, Wang N, Chen D, Li S. Influences of zinc oxide nanoparticles on Allium cepa root cells and the primary cause of phytotoxicity. Ecotoxicology. 2019;28(2):175–88.

    CAS  PubMed  Google Scholar 

  55. 55.

    Yah CS, Simate GS, Iyuke SE. Nanoparticles toxicity and their routes of exposures. J Pharm Sci. 2012;25(2):477–91.

    CAS  Google Scholar 

  56. 56.

    Zhang H, Jiang Y, He Z, Ma M. Cadmium accumulation and oxidative burst in garlic (Allium sativum). J Plant Physiol. 2005;162:977–84.

    CAS  PubMed  Google Scholar 

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Correspondence to Adekunle A. Bakare.

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Fadoju, O.M., Osinowo, O.A., Ogunsuyi, O.I. et al. Interaction of titanium dioxide and zinc oxide nanoparticles induced cytogenotoxicity in Allium cepa. Nucleus 63, 159–166 (2020). https://doi.org/10.1007/s13237-020-00308-1

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Keywords

  • Allium cepa
  • Chromosome aberration
  • Titanium dioxide nanoparticle
  • Zinc oxide
  • Nanoparticle
  • Mitotic index