Advertisement

The Nucleus

, Volume 62, Issue 3, pp 211–219 | Cite as

Genotoxicity of nanoscale zerovalent iron particles in tobacco BY-2 cells

  • Ilika Ghosh
  • Abhisek Sadhu
  • Yuji Moriyasu
  • Maumita Bandyopadhyay
  • Anita MukherjeeEmail author
Original Article

Abstract

Nanoremediation by direct injection of nZVI into contaminated water or soil has engendered their liberation into the environment facilitating interaction with plant systems. Available reports display a scarcity of information on the genotoxicity of nZVI in plants. In this study, the cyto-genotoxic potential of nZVI was evaluated in tobacco BY-2 cells treated for 24 h. A wide range of concentrations from 5 to 500 µg/mL of nZVI were tested for cytotoxicity and for other assays a maximum concentration of 20 µg/mL was used. Cytotoxicity assessed by TTC and Evans Blue tests showed maximum cell death in cells treated with the lowest concentration of nZVI (5 µg/mL). Comet assay confirmed high DNA damage at low concentrations, which corroborated with high accumulation of nZVI as observed by Prussian blue staining. Qualitative and quantitative estimation of ROS confirmed the accumulation of superoxide anions, hydroxyl, peroxyl radicals and hydrogen peroxide upon treatment with low concentrations of nZVI. Taken together, this study confirmed ROS mediated cytotoxicity and genotoxicity of nZVI and unravels further prospects in the safety evaluation of nZVI as well as the toxicity testing of other nanomaterials of ecotoxicological relevance.

Keywords

Zerovalent iron particles ROS Tobacco bright yellow2 cell line DNA damage Dynamic light scattering 

Notes

References

  1. 1.
    Auffan M, Achouak W, Rose J, Roncato MA, Chanéac C, Waite DT, Masion A, Woicik JC, Wiesner MR, Bottero JY. Relation between the redox state of iron-based nanoparticles and their cytotoxicity toward Escherichia coli. Environ Sci Technol. 2008;42:6730–5.CrossRefGoogle Scholar
  2. 2.
    Barzan E, Mehrabian S, Irian S. Antimicrobial and genotoxicity effects of zero-valent iron nanoparticles. Jundishapur J Microbiol. 2014;7:e10054.CrossRefGoogle Scholar
  3. 3.
    Boutry S, Forge D, Burtea C, Mahieu I, Murariu O, Laurent S, Vander Elst L, Muller RN. How to quantify iron in an aqueous or biological matrix: a technical note. Contrast Media Mol Imaging. 2009;4:299–304.CrossRefGoogle Scholar
  4. 4.
    Diao M, Yao M. Use of zero-valent iron nanoparticles in inactivating microbes. Water Res. 2009;43:5243–51.CrossRefGoogle Scholar
  5. 5.
    El-Temsah YS, Joner EJ. Impact of Fe and Ag nanoparticles on seed germination and differences in bioavailability during exposure in aqueous suspension and soil. Environ Toxicol. 2012;27:42–9.CrossRefGoogle Scholar
  6. 6.
    El-Temsah YS, Joner EJ. Effects of nano-sized zero-valent iron (nZVI) on DDT degradation in soil and its toxicity to collembola and ostracods. Chemosphere. 2013;92:131–7.CrossRefGoogle Scholar
  7. 8.
    Ghosh M, Chakraborty A, Mukherjee A. Cytotoxic, genotoxic and the hemolytic effect of titanium dioxide (TiO2) nanoparticles on human erythrocyte and lymphocyte cells in vitro. J Appl Toxicol. 2013;33:1097–110.CrossRefGoogle Scholar
  8. 10.
    Ghosh M, Sinha S, Jothiramajayam M, Jana A, Nag A, Mukherjee A. Cyto-genotoxicity and oxidative stress induced by zinc oxide nanoparticle in human lymphocyte cells in vitro and Swiss albino male mice in vivo. Food Chem Toxicol. 2016;97:286–96.CrossRefGoogle Scholar
  9. 7.
    Ghosh I, Mukherjee A, Mukherjee A. Inplantagenotoxicity of nZVI: influence of colloidal stability on uptake, DNA damage, oxidative stress and cell death. Mutagenesis. 2017;32:371–87.CrossRefGoogle Scholar
  10. 9.
    Ghosh M, Ghosh I, Godderis L, Hoet P, Mukherjee A. Genotoxicity of engineered nanoparticles in higher plants. Mutat Res, Genet Toxicol Environ Mutagen. 2019;842:135–45.Google Scholar
  11. 11.
    Gil-Díaz M, Pinilla P, Alonso J, Lobo MC. Viability of a nanoremediation process in single or multi-metal (loid) contaminated soils. J Hazard Mater. 2017;321:812–9.CrossRefGoogle Scholar
  12. 12.
    Gonzalo S, Llaneza V, Pulido-Reyes G, Fernández-Piñas F, Bonzongo JC, Leganes F, Rosal R, García-Calvo E, Rodea-Palomares I. A colloidal singularity reveals the crucial role of colloidal stability for nanomaterials in-vitro toxicity testing: nZVI-microalgae colloidal system as a case study. PLoS ONE. 2014;9:e109645.CrossRefGoogle Scholar
  13. 13.
    Huang W, Xing W, LiD Liu Y. Microcystin-RR induced apoptosis in tobacco BY-2 suspension cells is mediated by reactive oxygen species and mitochondrial permeability transition pore status. Toxicol Vitro. 2008;22:328–37.CrossRefGoogle Scholar
  14. 14.
    Jiang J, Oberdörster G, Biswas P. Characterization of size, surface charge, and agglomeration state of nanoparticle dispersions for toxicological studies. J Nanopart Res. 2009;11:77–89.CrossRefGoogle Scholar
  15. 15.
    Kadar E, Tarran GA, Jha AN, Al-Subiai SN. Stabilization of engineered zero-valentnanoiron with Na-acrylic copolymer enhances spermiotoxicity. Environ Sci Technol. 2011;45:3245–51.CrossRefGoogle Scholar
  16. 16.
    Karn B, Kuiken T, Otto M. Nanotechnology and in situ remediation: a review of the benefits and potential risks. Environ Health Perspect. 2009;117:1813–31.CrossRefGoogle Scholar
  17. 17.
    Keenan CR, Goth-Goldstein R, Lucas D, Sedlak DL. Oxidative stress induced by zero-valent iron nanoparticles and Fe (II) in human bronchial epithelial cells. Environ Sci Technol. 2009;43:4555–60.CrossRefGoogle Scholar
  18. 18.
    Kim JH, Lee Y, Kim EJ, Gu S, Sohn EJ, Seo YS, An HJ, Chang YS. Exposure of iron nanoparticles to Arabidopsis thaliana enhances root elongation by triggering cell wall loosening. Environ Sci Technol. 2014;48:3477–85.CrossRefGoogle Scholar
  19. 19.
    Kumaravel TS, Jha AN. Reliable Comet assay measurements for detecting DNA damage induced by ionising radiation and chemicals. Mutat Res, Genet Toxicol Environ Mutagen. 2006;605:7–16.CrossRefGoogle Scholar
  20. 20.
    Iavicoli I, Fontana L, Leso V, Calabrese EJ. Hormetic dose–responses in nanotechnology studies. Sci Total Environ. 2014;487:361–74.CrossRefGoogle Scholar
  21. 21.
    Li X, Yang Y, Gao B, Zhang M. Stimulation of peanut seedling development and growth by zero-valent iron nanoparticles at low concentrations. PLoS ONE. 2015;10:e0122884.CrossRefGoogle Scholar
  22. 22.
    Libralato G, Devoti AC, Zanella M, Sabbioni E, Mičetić I, Manodori L, Pigozzo A, Manenti S, Groppi F, Ghirardini AV. Phytotoxicity of ionic, micro-and nano-sized iron in three plant species. Ecotoxicol Environ Saf. 2016;123:81–8.CrossRefGoogle Scholar
  23. 23.
    Ma X, Gurung A, Deng Y. Phytotoxicity and uptake of nanoscale zero-valent iron (nZVI) by two plant species. Sci Total Environ. 2013;443:844–9.CrossRefGoogle Scholar
  24. 24.
    Ma Y, Elankumaran S, Marr LC, Vejerano EP, Pruden A. Toxicity of engineered nanomaterials and their transformation products following wastewater treatment on A549 human lung epithelial cells. Toxicol Rep. 2014;1:871–6.CrossRefGoogle Scholar
  25. 25.
    Marsalek B, Jancula D, Marsalkova E, Mashlan M, Safarova K, Tucek J, Zboril R. Multimodal action and selective toxicity of zerovalent iron nanoparticles against cyanobacteria. Environ Sci Technol. 2012;46:2316–23.CrossRefGoogle Scholar
  26. 26.
    Menke M, Chen IP, Angelis KJ, Schubert I. DNA damage and repair in Arabidopsis thaliana as measured by the comet assay after treatment with different classes of genotoxins. Mutat Res, Genet Toxicol Environ Mutagen. 2001;493:87–93.CrossRefGoogle Scholar
  27. 27.
    Moriyasu Y, Ohsumi Y. Autophagy in tobacco suspension-cultured cells in response to sucrose starvation. Plant Physiol. 1996;111:1233–41.CrossRefGoogle Scholar
  28. 28.
    Namvar F, Rahman HS, Mohamad R, Baharara J, Mahdavi M, Amini E, Chartrand MS, Yeap SK. Cytotoxic effect of magnetic iron oxide nanoparticles synthesized via seaweed aqueous extract. Int J Nanomed. 2014;9:2479–88.CrossRefGoogle Scholar
  29. 29.
    Ohno R, Kadota Y, Fujii S, Sekine M, Umeda M, Kuchitsu K. Cryptogein-induced cell cycle arrest at G2 phase is associated with inhibition of cyclin-dependent kinases, suppression of expression of cell cycle-related genes and protein degradation in synchronized tobacco BY-2 cells. Plant Cell Physiol. 2011;52:922–32.CrossRefGoogle Scholar
  30. 30.
    Phenrat T, Long TC, Lowry GV, Veronesi B. Partial oxidation (“aging”) and surface modification decrease the toxicity of nanosized zerovalent iron. Environ Sci Technol. 2008;43:195–200.CrossRefGoogle Scholar
  31. 31.
    Ravikumar KVG, Kumar D, Rajeshwari A, Madhu GM, Mrudula P, Chandrasekaran N, Mukherjee A. A comparative study with biologically and chemically synthesized nZVI: applications in Cr (VI) removal and ecotoxicity assessment using indigenous microorganisms from chromium-contaminated site. Environ Sci Pollut Res. 2016;23:2613–27.CrossRefGoogle Scholar
  32. 32.
    Sadhu A, Ghosh I, Moriyasu Y, Mukherjee A, Bandyopadhyay M. Role of cerium oxide nanoparticle-induced autophagy as a safeguard to exogenous H2O2-mediated DNA damage in tobacco BY-2 cells. Mutagenesis. 2018;33:161–77.CrossRefGoogle Scholar
  33. 33.
    Sun Z, Yang L, Chen KF, Chen GW, Peng YP, Chen JK, Suo G, Yu J, Wang WC, Lin CH. Nano zerovalent iron particles induce pulmonary and cardiovascular toxicity in an in vitro human co-culture model. Nanotoxicology. 2016;10:881–90.CrossRefGoogle Scholar
  34. 34.
    Towill LE, Mazur P. Studies on the reduction of 2,3,5-triphenyltetrazolium chloride as a viability assay for plant tissue cultures. Can J Bot. 1975;53:1097–102.CrossRefGoogle Scholar
  35. 35.
    U.S. EPA. Office of Solid Waste and Emergency Response. Nanotechnology for Site Remediation Fact Sheet; 2008. Report number: EPA 542F-08-009. http://www.epa.gov/tio/download/remed/542-f-08-009.pdf. Accessed 5 May 2019.
  36. 36.
    U.S. EPA. Technical fact sheet-Nanomaterials. Solid waste and emergency response; 2014 (5106P), EPA505-F-14-002. https://www.epa.gov/sites/production/files/201403/documents/ffrrofactsheet_emergingcontaminant_nanomaterials_jan2014_final.pdf. Accessed 5 May 2019.
  37. 37.
    Xue W, Huang D, Zeng G, Wan J, Cheng M, Zhang C, Hu Li J. Performance and toxicity assessment of nanoscale zero valent iron particles in the remediation of contaminated soil: a review. Chemosphere. 2018;210:1145–56.CrossRefGoogle Scholar
  38. 38.
    Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H. Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol. 2002;128:63–72.CrossRefGoogle Scholar

Copyright information

© Archana Sharma Foundation of Calcutta 2019

Authors and Affiliations

  1. 1.Cell Biology and Genetic Toxicology Laboratory, Centre of Advanced Study, Department of BotanyUniversity of CalcuttaKolkataIndia
  2. 2.Plant Molecular Cytogenetics Laboratory, Centre of Advanced Study, Department of BotanyUniversity of CalcuttaKolkataIndia
  3. 3.Graduate School of Science and EngineeringSaitama UniversitySaitamaJapan

Personalised recommendations