Environmental Science and Pollution Research

, Volume 24, Issue 2, pp 2055–2064 | Cite as

Cytotoxicity and oxidative stress responses of silica-coated iron oxide nanoparticles in CHSE-214 cells

  • K. Srikanth
  • Tito Trindade
  • A. C. Duarte
  • E. Pereira
Research Article

Abstract

The present study aimed at investigating cytotoxicity and oxidative stress induced by silica-coated iron oxide nanoparticles functionalized with dithiocarbamate (Fe3O4 NPs) in Chinook salmon cells (CHSE-214) derived from Oncorhynchus tshawytscha embryos. A significant reduction in cell viability was evident in response to Fe3O4 NPs as revealed by the 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT) assay after 24 h of exposure. Out of the tested concentrations (10, 20, and 30 μg/ml), the highest concentration has shown significant decrease in the viability of cells after 24 h of exposure. Alterations in the morphology of CHSE-214 cells was also evident at 10 μg/ml concentration of Fe3O4 NPs after 24 h. Fe3O4 NPs elicited a significant dose-dependent reduction in total glutathione content (TGSH), catalase (CAT), glutathione reductase (GR) with a concomitant increase in lipid peroxidation (LPO), and protein carbonyl (PC) at highest concentration (30 μg/ml) after 24 h of exposure. In conclusion, our data demonstrated that Fe3O4 NPs have potential to induce cytotoxicity in CHSE-214 cells, which is likely to be mediated through reactive oxygen species generation and oxidative stress.

Keywords

Chinook salmon Iron oxide nanoparticles Cytotoxicity Oxidative stress Lipid peroxidation Protein carbonyl 

References

  1. Ahamed M, Alhadlaq HA, Alam J, Khan MA, Ali D, Alarafi S (2013) Iron oxide nanoparticle-induced oxidative stress and genotoxicity in human skin epithelial and lung epithelial cell lines. Curr Pharm Des 19:6681–6690CrossRefGoogle Scholar
  2. Ahne W (1985) Use of fish cell cultures for toxicity determination in order to reduce and replace the fish tests. Zentralbl Bakteriol Mikrobiol Hyg B 180:480–504Google Scholar
  3. Alarifi S, Ali D, Alkahtani S, Alhader MS (2014) Iron oxide nanoparticles induce oxidative stress, DNA damage, and caspase activation in the human breast cancer cell line. Biol Trace Elem Res 159:416–424CrossRefGoogle Scholar
  4. Arbab AS, Wilson LB, Ashari P, Jordan EK, Lewis BK, Frank JA (2005) A model of lysosomal metabolism of dextran coated superparamagnetic iron oxide (SPIO) nanoparticles: implications for cellular magnetic resonance imaging. NMR Biomed 18:383–389CrossRefGoogle Scholar
  5. AshaRani P, Low Kah Mun G, Hande MP, Valiyaveettil S (2008) Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3:279–290CrossRefGoogle Scholar
  6. Baker MA, Cerniglia GJ, Zaman A (1990) Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples. Anal Biochem 190:360–365CrossRefGoogle Scholar
  7. Beutler E (1984) Red cell metabolism: a manual of biochemical methods. Second edition, Ernest Beutler. Grune & Stratton, New York, 1975, XVI, pp 160Google Scholar
  8. Billiard S, Bols N, Hodson P (2004) In vitro and in vivo comparisons of fish-specific CYP1A induction relative potency factors for selected polycyclic aromatic hydrocarbons. Ecotox Environ Safety 59:292–299CrossRefGoogle Scholar
  9. Bird RP, Draper AH (1984) Comparative studies on different methods of malondialdehyde determination. Methods Enzymol 105:299–305Google Scholar
  10. Bols N, Dayeh V, Lee L, Schirmer K (2005) Use of fish cell lines in the toxicology and ecotoxicology of fish. Piscine cell lines in environmental toxicology. Biochemistry and molecular biology of fishes 6: 43–84Google Scholar
  11. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  12. Carlberg I, Mannervik B (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250:5475–5480Google Scholar
  13. Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, pp 283–284Google Scholar
  14. Dalle-Donne I, Aldini G, Carini M, Colombo R, Rossi R, Milzani A (2006) Protein carbonylation, cellular dysfunction, and disease progression. J Cell Mol Med 10:389–406CrossRefGoogle Scholar
  15. Dwivedi S, Siddiqui MA, Farshori NN, Ahamed M, Musarrat J, Al-Khedhairy AA (2014) Synthesis, characterization and toxicological evaluation of iron oxide nanoparticles in human lung alveolar epithelial cells. Colloids Surf B Biointerfaces 122:209–215CrossRefGoogle Scholar
  16. Filipak Neto F, Zanata S, Silva de Assis H, Nakao L, Randi M, Oliveira Ribeiro C (2008) Toxic effects of DDT and methyl mercury on the hepatocytes from Hoplias malabaricus. Toxicol in Vitro 22:1705–1713CrossRefGoogle Scholar
  17. Floor E, Wetzel MG (1998) Increased protein oxidation in human substantia nigra pars compacta in comparison with basal ganglia and prefrontal cortex measured with an improved dinitrophenylhydrazine assay. J Neurochem 70:268–275CrossRefGoogle Scholar
  18. Gaharwar US, Paulraj R (2015) Iron oxide nanoparticles induced oxidative damage in peripheral blood cells of rat. J Biomedical Science and Engineering 8:274–286CrossRefGoogle Scholar
  19. Grottone GT, Loureiro RR, Covre J, Rodrigues EB, Gomes JÁ (2014) ARPE-19 cell uptake of small and ultrasmall superparamagnetic iron oxide. Curr Eye Res 39:403–410CrossRefGoogle Scholar
  20. Guadagnini R, Moreau K, Hussain S, Marano F, Boland S (2015) Toxicity evaluation of engineered nanoparticles for medical applications using pulmonary epithelial cells. Nanotoxicology 9:25–32CrossRefGoogle Scholar
  21. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
  22. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Method Enzymol 186:464CrossRefGoogle Scholar
  23. Levy M, Lagarde F, Maraloiu VA, Blanchin MG, Gendron F, Wilhelm C, Gazeau F (2010) Degradability of superparamagnetic nanoparticles in a model of intracellular environment: follow-up of magnetic, structural and chemical properties. Nanotechnology 21:395103CrossRefGoogle Scholar
  24. Li K, Shen M, Zheng L, Zhao J, Quan Q, Shi X, Zhang G (2014) Magnetic resonance imaging of glioma with novel APTS-coated superparamagnetic iron oxide nanoparticles. Nanoscale Res Lett 9:304CrossRefGoogle Scholar
  25. Magdolenova Z, Drlickova M, Henjum K, Rundén-Pran E, Tulinska J, Bilanicova D, Pojana G, Kazimirova A, Barancokova M, Kuricova M, Liskova A, Staruchova M, Ciampor F, Vavra I, Lorenzo Y, Collins A, Rinna A, Fjellsbø L, Volkovova K, Marcomini A, Amiry-Moghaddam M, Dusinska M (2015) Coating-dependent induction of cytotoxicity and genotoxicity of iron oxide nanoparticles. Nanotoxicology 9:44–56CrossRefGoogle Scholar
  26. Mahmoudi M, Shokrgozar MA, Simchi A, Imani M, Milani AS, Stroeve P, Vali H, Häfeli UO, Bonakdar S (2009a) Multiphysics flow modeling and in vitro toxicity of iron oxide nanoparticles coated with poly (vinyl alcohol). J Physical Chem C 113:2322–2331CrossRefGoogle Scholar
  27. Mahmoudi M, Simchi A, Vali H, Imani M, Shokrgozar MA, Azadmanesh K, Azari F (2009b) Cytotoxicity and cell cycle effects of bare and poly (vinyl alcohol)-coated iron oxide nanoparticles in mouse fibroblasts. Adv Eng Mater 11:B243–B250CrossRefGoogle Scholar
  28. Malvindi MA, De Matteis V, Galeone A, Brunetti V, Anyfantis GC, Athanassiou A, Cingolani R, Pompa PP (2014) Toxicity assessment of silica coated iron oxide nanoparticles and biocompatibility improvement by surface engineering. PLoS One 9:e85835CrossRefGoogle Scholar
  29. Marroqui L, Estepa A, Perez L (2008) Inhibitory effect of mycophenolic acid on the replication of infectious pancreatic necrosis virus and viral hemorrhagic septicemia virus. Antivir Res 80:332–338CrossRefGoogle Scholar
  30. Mori M, Wakabayashi M, Kaneko Y, Hasobe M (1998) Application of a suspension-cultured salmonid cell line CHSE-sp to cytotoxicity test. Fish Sci: FS 64:991–992Google Scholar
  31. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immun Methods 65:55–63CrossRefGoogle Scholar
  32. Murray AR, Kisin E, Inman A, Young SH, Muhammed M, Burks T, Uheida A, Tkach A, Waltz M, Castranova V (2013) Oxidative stress and dermal toxicity of iron oxide nanoparticles in vitro. Cell Biochem Biophys 67:461–476CrossRefGoogle Scholar
  33. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358CrossRefGoogle Scholar
  34. Rachlin JW, Perlmutter A (1968) Fish cells in culture for study of aquatic toxicants. Water Res 2:409–414CrossRefGoogle Scholar
  35. Radu M, Cristina Munteanu M, Petrache S, Iren Serban A, Dinu D, Hermenean A, Sima C, Dinischiotu A (2010) Depletion of intracellular glutathione and increased lipid peroxidation mediate cytotoxicity of hematite nanoparticles in MRC-5 cells. Acta Biochim Pol 57:355Google Scholar
  36. Remya AS, Ramesh M, Sarvanan M, Poopal RK, Bharathi S, Nataraj D (2015) Iron oxide nanoparticles to an Indian major carp, Labeo rohita: impacts on hematology, iono regulation and gill Na+/K+ ATPase activity. J King Saud Univ Sci 27:151–160CrossRefGoogle Scholar
  37. Schirmer K (2006) Proposal to improve vertebrate cell cultures to establish them as substitutes for the regulatory testing of chemicals and effluents using fish. Toxicology 224:163–183CrossRefGoogle Scholar
  38. Singh N, Jenkins GJ, Asadi R, Doak SH (2010) Potential toxicity of superparamagnetic iron oxide nanoparticles (SPION). Nano Rev 1:5358CrossRefGoogle Scholar
  39. Skjelbred B, Horsberg TE, Tollefsen KE, Andersen T, Edvardsen B (2011) Toxicity of the ichthyotoxic marine flagellate Pseudochattonella (Dictyochophyceae, Heterokonta) assessed by six bioassays. Harmful Algae 10:144–154CrossRefGoogle Scholar
  40. Soenen SJ, Himmelreich U, Nuytten N, De Cuyper M (2011) Cytotoxic effects of iron oxide nanoparticles and implications for safety in cell labelling. Biomaterials 32:195–205CrossRefGoogle Scholar
  41. Song L, Connolly M, Fernández-Cruz ML, Vijver MG, Fernández M, Conde E, de Snoo GR, Peijnenburg WJ, Navas JM (2014) Species-specific toxicity of copper nanoparticles among mammalian and piscine cell lines. Nanotoxicology 8:383–393CrossRefGoogle Scholar
  42. Srikanth K, Pereira E, Duarte AC, Ahmad I (2013) Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish—a review. Environ Sci Pollut Res 20:2133–2149CrossRefGoogle Scholar
  43. Srikanth K, Mahajan A, Duarte AC, Pereira E, Rao JV (2015a) Aluminium oxide nanoparticles induced morphological changes, cytotoxicity and oxidative stress in Chinook salmon (CHSE-214) cells. J Appl Toxicol 10:1133–1140CrossRefGoogle Scholar
  44. Srikanth K, Anjum NA, Trindade T, Duarte AC, Pereira E, Ahmad I (2015b) Lipid peroxidation and its control in Anguilla anguilla hepatocytes under silica-coated iron oxide nanoparticles (with or without mercury) exposure. Environ Sci Pollut Res 13:9617–9625CrossRefGoogle Scholar
  45. Srikanth K, Pereira E, Duarte AC, Rao JV (2016) Evaluation of cytotoxicity, morphological alterations and oxidative stress in Chinook salmon cells exposed to copper oxide nanoparticles. Protoplasma 253:873–884CrossRefGoogle Scholar
  46. Taju G, Abdul Majeed S, Nambi K, Sahul Hameed A (2014) In vitro assay for the toxicity of silver nanoparticles using heart and gill cell lines of Catla catla and gill cell line of Labeo rohita. Comp Biochem Physiol Part C: Toxicol & Pharmacol 161:41–52Google Scholar
  47. Tavares DS, Lopes CB, Daniel-da-Silva AL, Duarte AC, Trindade T, Pereira E (2014) The role of operational parameters on the uptake of mercury by dithiocarbamate functionalized particles. Chem Eng J 254:559–570CrossRefGoogle Scholar
  48. Tietze F (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27:502–522CrossRefGoogle Scholar
  49. Zhu XM, Wang YX, Leung KC, Lee SF, Zhao F, Wang DW, Lai JM, Wan C, Cheng CH, Ahuja AT (2012a) Enhanced cellular uptake of aminosilane-coated superparamagnetic iron oxide nanoparticles in mammalian cell lines. Int J Nanomedicine 7:953–964CrossRefGoogle Scholar
  50. Zhu X, Tian S, Cai Z (2012b) Toxicity assessment of iron oxide nanoparticles in zebrafish (Danio rerio) early life stages. PLoS One 7:e46286CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • K. Srikanth
    • 1
  • Tito Trindade
    • 1
    • 2
  • A. C. Duarte
    • 1
  • E. Pereira
    • 1
  1. 1.CESAM-Centre for Environmental and Marine Studies, Department of ChemistryUniversity of AveiroAveiroPortugal
  2. 2.Department of Chemistry, CICECO and CESAM, Aveiro Institute of NanotechnologyUniversity of AveiroAveiroPortugal

Personalised recommendations