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Lipid peroxidation and its control in Anguilla anguilla hepatocytes under silica-coated iron oxide nanoparticles (with or without mercury) exposure

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Abstract

Having multidisciplinary applications, iron oxide nanoparticles can inevitably enter aquatic system and impact inhabitants such as fish. However, the studies in this context have ignored the significance of obvious interaction of iron oxide nanoparticles with other persistent co-contaminants such as mercury (Hg) in the modulation of the toxicity and underlying mechanisms of iron oxide nanoparticles and Hg alone, and concomitant exposures. This study aimed to evaluate lipid peroxidation (LPO) and its control with glutathione (GSH) and associated enzymes (such as glutathione reductase, GR; glutathione peroxidase, GPX; glutathione sulfo-transferase, GST) in European eel (Anguilla anguilla L.) hepatocytes exposed to stressors with following schemes: (i) no silica-coated iron oxide nanoparticles functionalized with dithiocarbamate (Fe3O4@SiO2/Si DTC, hereafter called ‘FeNPs’; size range 82 ± 21 to 100 ± 30 nm) or Hg, (ii) FeNPs (2.5 μg L−1) alone, (iii) Hg (50 μg L−1) alone and (iv) FeNPs + Hg concomitant condition during 0 to 72 h. The exhibition of a differential coordination between GSH regeneration (determined as GR activity) and GSH metabolism (determined as the activity of GPX and GST) was perceptible in A. anguilla hepatocytes in order to control FeNPs, Hg and FeNPs + Hg exposure condition-mediated LPO. This study revealed the significance of a fine tuning among GR, GPX and GST in keeping LPO level under control during FeNPs or Hg alone exposure, and a direct role of total GSH (TGSH) in the control of LPO level and impaired GSH metabolism under the concomitant (FeNPs + Hg) exposure. An interpretation of the fish risk to FeNPs in a multi-pollution state should equally consider the potential outcome of the interaction of FeNPs with other contaminants.

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References

  • Ahamed M, Alhadlaq HA, Khan MM, Akhtar MJ (2013) Selective killing of cancer cells by iron oxide nanoparticles mediated through reactive oxygen species via p53 pathway. J Nanoparticle Res 15:1225

    Article  Google Scholar 

  • Ahmad I, Maria V, Pacheco M, Santos M (2009) Juvenile sea bass (Dicentrarchus labrax L.) enzymatic and non-enzymatic antioxidant responses following 17β-estradiol exposure. Ecotoxicology 18:974–982

    Article  CAS  Google Scholar 

  • Anjum NA, Srikanth K, Mohmood I, Sayeed I, Trindade T et al (2014) Brain glutathione redox system significance for the control of silica-coated magnetite nanoparticles with or without mercury co-exposures mediated oxidative stress in European eel (Anguilla anguilla L.). Environ Sci Pollut Res 21:7746–7756

    Article  CAS  Google Scholar 

  • Auffan M, Rose J, Proux O, Masion A, Liu W et al (2012) Is there a Trojan-horse effect during magnetic nanoparticles and metalloid cocontamination of human dermal fibroblasts? Environ Sci Technol 46:10789–10796

    Article  CAS  Google Scholar 

  • 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 190:360–365

    Article  CAS  Google Scholar 

  • Bickley LK, Lange A, Winter MJ, Tyler CR (2009) Evaluation of a carp primary hepatocyte culture system for screening chemicals for oestrogenic activity. Aquat Toxicol 94:195–203

    Article  CAS  Google Scholar 

  • Bird RP, Draper HH (1984) Comparative studies on different methods of malonaldehyde determination. Method Enzymol 105:299–305

    Article  CAS  Google Scholar 

  • 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 72:248–254

    Article  CAS  Google Scholar 

  • Cossu C, Doyotte A, Jacquin MC, Babut M et al (1997) Glutathione reductase, selenium dependent glutathione peroxidase, glutathione levels, and lipid peroxidation in freshwater bivalves, Unio tumidus, as biomarkers of aquatic contamination in field studies. Ecotoxicol Environ Saf 38:122–131

    Article  CAS  Google Scholar 

  • Filipak Neto F, Zanata SM, Silva de Assis HC et al (2008) Toxic effects of DDT and methyl mercury on the hepatocytes from Hoplias malabaricus. Toxicol in Vitro 22:1705–1713

    Article  CAS  Google Scholar 

  • García A, Espinosa R, Delgado L, Casals E, González E et al (2011) Acute toxicity of cerium oxide, titanium oxide and iron oxide nanoparticles using standardized tests. Desalination 269:136–141

    Article  Google Scholar 

  • Girginova PI, Daniel-da-Silva AL, Lopes CB, Figueira P et al (2010) Silica coated magnetite particles for magnetic removal of Hg2+ from water. J Colloid Interface Sci 345:234–240

    Article  CAS  Google Scholar 

  • Grover VA, Hu J, Engates KE, Shipley HJ (2012) Adsorption and desorption of bivalent metals to hematite nanoparticles. Environ Toxicol Chem 31:86–92

    Article  CAS  Google Scholar 

  • Hardas SS, Sultana R, Warrier G, Dan M, Florence RL et al (2012) Rat brain pro-oxidant effects of peripherally administered 5 nm ceria 30 days after exposure. Neurotoxicology 33:1147–1155

    Article  CAS  Google Scholar 

  • Kortenkamp A, Backhaus T, Faust M (2009) State of the art on mixture toxicity, Report, April 2011

  • LeCluyse EL, Alexandre E, Hamilton GA, Viollon-Abadie C et al (2005) Isolation and culture of primary human hepatocytes. Methods Mol Biol 290:207–229

    Google Scholar 

  • Ma P, Luo Q, Chen J, Gan Y, Du J et al (2012) Intraperitoneal injection of magnetic Fe3O4-nanoparticle induces hepatic and renal tissue injury via oxidative stress in mice. Int J Nanomed 7:4809–4818

    CAS  Google Scholar 

  • Mahmoudi M, Simchi A, Vali H, Imani M, Shokrgozar MA et al (2009) Cytotoxicity and cell cycle effects of bare and poly(vinyl alcohol)-coated iron oxide nanoparticles in mouse fibroblasts. Adv Eng Mater 11:B243–B250

    Article  Google Scholar 

  • Mahmoudi M, Hofmann H, Rothen-Rutishauser B et al (2011) Assessing the in vitro and in vivo toxicity of superparamagnetic iron oxide nanoparticles. Chem Rev 112:2323–2338

    Article  Google Scholar 

  • Mieiro C, Ahmad I, Pereira M, Duarte A, Pacheco M (2010) Antioxidant system breakdown in brain of feral golden grey mullet (Liza aurata) as an effect of mercury exposure. Ecotoxicology 19:1034–1045

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pereira ME, Lillebø AI, Pato P, Válega M et al (2009) Mercury pollution in Ria de Aveiro (Portugal): a review of the system assessment. Environ Monit Assess 155:39–49

    Article  CAS  Google Scholar 

  • Radu M, Munteanu M, Petrache S, Serban AI, Dinu D et al (2010) Depletion of intracellular glutathione and increased lipid peroxidation mediate cytotoxicity of hematite nanoparticles in MRC-5 cells. Acta Biochim Pol 57:355–360

    CAS  Google Scholar 

  • Santos MA, Pacheco M (1996) Anguilla anguilla L. stress biomarkers recovery in clean water and secondary-treated pulp mill effluent. Ecotoxicol Environ Saf 35:96–100

    Article  CAS  Google Scholar 

  • Scown TM, Goodhead RM, Johnston BD, Moger J et al (2010) Assessment of cultured fish hepatocytes for studying cellular uptake and (eco)toxicity of nanoparticles. Environ Chem 7:36–49

    Article  CAS  Google Scholar 

  • Singh N, Manshian B, Jenkins GJS, Griffiths SM et al (2009) Nano genotoxicology: the DNA damaging potential of engineered nanomaterials. Biomaterials 30:3891–3914

    Article  CAS  Google Scholar 

  • Søfteland L, Eide I, Olsvik PA (2009) Factorial design applied for multiple endpoint toxicity evaluation in Atlantic salmon (Salmo salar L.) hepatocytes. Toxicol in Vitro 23:1455–1464

    Article  Google Scholar 

  • 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 20:2133–2149

    Article  CAS  Google Scholar 

  • Srikanth K, Ahmad I, Rao JV, Trindad T et al (2014) Modulation of glutathione and its dependent enzymes in gill cells of Anguilla anguilla exposed to silica coated iron oxide nanoparticles with or without mercury co-exposure under in vitro condition. Comp Biochem Physiol C 162:7–14

    CAS  Google Scholar 

  • Strober W (1991) Trypan blue exclusion test for cell viability. In: Coligan JE, Kruisbeek AM, Margulies DH et al (eds) Current protocols in immunology. Wiley, New York, pp 3–4

  • Tavares DS, Daniel-da-Silva AL, Lopes CB, Silva NJO et al (2013) Efficient sorbents based on magnetite coated with siliceous hybrid shells for removal of mercury ions. J Mater Chem A A1:8134–8143

    Article  Google Scholar 

  • Tavares DS, Lopes CB, Daniel-da-Silva AL, Duarte AC et al (2014) The role of operational parameters on the uptake of mercury by dithiocarbamate functionalized particles. Chem Eng J 254:559–570

    Article  CAS  Google Scholar 

  • Ueda S, Masutani H, Nakamura H, Tanaka T et al (2002) Redox control of cell death. Antioxid Redox Signal 4:405–414

    Article  CAS  Google Scholar 

  • Zhu X, Tian S, Cai Z (2012) Toxicity assessment of iron oxide nanoparticles in zebrafish (Danio rerio) early life stages. PloS One 7:e46286

Download references

Acknowledgments

The authors are grateful to the Portuguese Foundation for Science and Technology (FCT) for postdoctoral grants to KS (SFRH/BPD/79490/2011) and NAA (SFRH/BPD/84671/2012), and to the Aveiro University Research Institute/CESAM.

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Correspondence to Iqbal Ahmad.

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Responsible editor: Henner Hollert

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Srikanth, K., Anjum, N.A., Trindade, T. et al. Lipid peroxidation and its control in Anguilla anguilla hepatocytes under silica-coated iron oxide nanoparticles (with or without mercury) exposure. Environ Sci Pollut Res 22, 9617–9625 (2015). https://doi.org/10.1007/s11356-015-4125-3

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  • DOI: https://doi.org/10.1007/s11356-015-4125-3

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