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Comparison of Dissolved Nickel and Nickel Nanoparticles Toxicity in Larval Zebrafish in Terms of Gene Expression and DNA Damage

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Abstract

With the use of nanoparticles (NPs) in many industrial activities and consumer products, it is important to evaluate the effects of their release into the environment. Metal NPs (e.g., Ni-NPs or Cu-NPs) can release metal ions that are toxic to aquatic organisms; however, whether the toxicity is from metal ions rather than unique “nano-scale” effects of the NPs is unresolved. This research investigated Ni-NP toxicity in zebrafish Danio rerio larvae to clarify whether toxic effects are attributable to release of Ni ions. First, the acute (96-h lethal) toxicity of Ni-NPs was determined in comparison to aqueous Ni in fish exposed to Ni(II) by water-soluble NiCl2. Subsequently, sublethal experiments with Ni-NPs and Ni(II) were conducted to assess changes in expression of stress-related genes (mt2, rad51, and p53) by quantitative PCR. Acute toxicity of Ni in fish exposed to Ni(II) was higher (96-h LC50 = 32.6 mg/L) than for fish exposed to Ni-NPs (96-h LC50 = 122.2 mg/L). Also, DNA strand breaks were higher in Ni(II)- than Ni-NPs-exposed larvae. Induction of stress-related genes in larvae was complex and was not directly related to Ni-NPs and Ni(II) concentration, although there was a significant induction in the mt2 and p53 gene of the larvae exposed to Ni-NPs and Ni(II) relative to controls. Results indicated that while Ni-NPs induced gene expression (presumably by the release of Ni ions), the differences in concentration relationships of gene expression between Ni-NPs and Ni(II) suggest that factors in addition to the release of Ni ions from Ni-NPs influence acute toxicity of Ni-NPs.

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References

  • Ahamed M, Alhadlaq HA (2014) Nickel nanoparticle-induced dose-dependent cyto-genotoxicity in human breast carcinoma MCF-7 cells. Onco Targets Ther 7:269–280

    Article  Google Scholar 

  • Boran H, Ulutas G (2016) Genotoxic effects and gene expression changes in larval zebrafish after exposure to ZnCl2 and ZnO nanoparticles. Dis Aquat Org 117:205–214

    Article  CAS  Google Scholar 

  • Boyle D, Boran H, Atfield AJ, Henry TB (2015) Use of an exposure chamber to maintain aqueous phase nanoparticle dispersions for improved toxicity testing in fish. Environ Toxicol Chem 34:583–588

    Article  CAS  Google Scholar 

  • Buekers J, De Brouwere K, Lefebvre W, Willems H, Vandenbroele M, Van Sprang P, Eliat-Eliat M, Hicks K, Schlekat CE, Oller AR (2015) Assessment of human exposure to environmental sources of nickel in Europe: inhalation exposure. Sci Total Environ 521–522:359–371

    Article  Google Scholar 

  • Calatayud MP, Sanz B, Raffa V, Riggio C, Ibarra MR, Goya GF (2014) The effect of surface charge of functionalized Fe3O4 nanoparticles on protein adsorption and cell uptake. Biomaterials 35:6389–6399

    Article  CAS  Google Scholar 

  • Capdevila M, Bofill R, Palacios Ò, Atrian S (2012) State-of-the-art of metallothioneins at the beginning of the 21st century. Coord Chem Rev 256:46–62

    Article  CAS  Google Scholar 

  • Chan KM, Ku LL, Chan PCY, Cheuk WK (2006) Metallothionein gene expression in zebrafish embryo-larvae and ZFL cell-line exposed to heavy metal ions. Mar Environ Res 62:83–87

    Article  Google Scholar 

  • Chechik G, Koller D (2009) Timing of gene expression responses to environmental changes. J Comput Biol 16:279–290

    Article  CAS  Google Scholar 

  • Chiou YH, Wong RH, Chao MR, Chen CY, Liou SH, Lee H (2014) Nickel accumulation in lung tissues is associated with increased risk of p53 mutation in lung cancer patients. Environ Mol Mutagen 55:624–632

    Article  CAS  Google Scholar 

  • Cho YS, Lee SY, Kim KY, Nam YK (2009) Two metallothionein genes from mud loach Misgurnus mizolepis (Teleostei; Cypriniformes): gene structure, genomic organization, and mRNA expression analysis. Comp Biochem Physiol B Biochem Mol Biol 153:317–326

    Article  Google Scholar 

  • Choi JE, Kim S, Ahn JH, Youn P, Kang JS, Park K, Yi J, Ryu D-Y (2010) Induction of oxidative stress and apoptosis by silver nanoparticles in the liver of adult zebrafish. Aquat Toxicol 100:151–159

    Article  CAS  Google Scholar 

  • Chusuei CC, Wu C-H, Mallavarapu S, Hou FYS, Hsu C-M, Winiarz JG, Aronstam RS, Huang Y-W (2013) Cytotoxicity in the age of nano: the role of fourth period transition metal oxide nanoparticle physicochemical properties. Chem Biol Interact 206:319–326

    Article  CAS  Google Scholar 

  • Du Z, ZhangY Wang G, Peng J, Wang Z, Gao S (2016) TPhP exposure disturbs carbohydrate metabolism, lipid metabolism, and the DNA damage repair system in zebrafish liver. Sci Rep 6:21827

    Article  CAS  Google Scholar 

  • Garcia GJM, Schroeter JD, Kimbell JS (2015) Olfactory deposition of inhaled nanoparticles in humans. Inhal Toxicol 27:394–403

    Article  CAS  Google Scholar 

  • Griffitt RJ, Luo J, Gao J, Bonzongo J-C, Barber DS (2008) Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 27:1972–1978

    Article  CAS  Google Scholar 

  • Horie M, Nishio K, Fujita K, Kato H, Nakamura A, Kinugasa S, Endoh S, Miyauchi A, Yamamoto K, Murayama H, Niki E, Iwahashi H, Yoshida Y, Nakanishi J (2009) Ultrafine NiO particles induce cytotoxicity in vitro by cellular uptake and subsequent Ni(II) release. Chem Res Toxicol 22:1415–1426

    Article  CAS  Google Scholar 

  • Horie M, Nishio K, Endoh S, Kato H, Fujita K, Miyauchi A, Nakamura A, Kinugasa S, Yamamoto K, Niki E, Yoshida Y, Iwahashi H (2013) Chromium(III) oxide nanoparticles induced remarkable oxidative stress and apoptosis on culture cells. Environ Toxicol 28:61–75

    Article  CAS  Google Scholar 

  • INSG Insight (2015) An overview of the nickel ındustry in Latin America. Newsletter, ıssue no. 26

  • Ispas C, Andreescu D, Patel A, Goia DV, Andreescu S, Wallace KN (2009) Toxicity and developmental defects of different sizes and shape nickel nanoparticles in zebrafish. Environ Sci Technol 43:6349–6356

    Article  CAS  Google Scholar 

  • Jiang J, Oberdörster G, Biswas PJ (2009) Characterization of size, surface charge, and agglomeration state of nanoparticle dispersions for toxicological studies. Nanopart Res 11:77–89

    Article  CAS  Google Scholar 

  • Ju-Nam Y, Lead JR (2008) Manufactured nanoparticles: an overview of their chemistry, interactions and potential environmental implications. Sci Total Environ 400:396–414

    Article  CAS  Google Scholar 

  • Kango S, Kalia S, Celli A, Njuguna J, Habibi Y, Kumar R (2013) Surface modification of inorganic nanoparticles for development of organic–inorganic nanocomposites—a review. Prog Polym Sci 38:1232–1261

    Article  CAS  Google Scholar 

  • Kanold JM, Wang J, Brümmer F, Siller L (2016) Metallic nickel nanoparticles and their effect on the embryonic development of the sea urchin Paracentrotus lividus. Environ Pollut 212:224–229

    Article  CAS  Google Scholar 

  • Kim SO, Kim YJ, Seo YR (2015) An overview of carcinogenic heavy metal: molecular toxicity mechanism and prevention. J Cancer Prev 20:232–240

    Article  Google Scholar 

  • Kimura T, Itoh N (2008) Function of metallothionein in gene expression and signal transduction: newly found protective role of metallothionein. J Health Sci 54:251–260

    Article  CAS  Google Scholar 

  • Kong L, Tang M, Zhang T, Wang D, Hu K, Lu W, Wei C, Liang G, Pu Y (2014) Nickel nanoparticles exposure and reproductive toxicity in healthy adult rats. Int J Mol Sci 15:21253–21269

    Article  CAS  Google Scholar 

  • Ling X-B, Wei H-W, Wang J, KongY-Q WuY-Y, Guo J-L, Li T-F, Li J-K (2016) Mammalian metallothionein-2A and oxidative stress. Int J Mol Sci 17:1483

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2∆∆C(T) method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Luo X, Morrin A, Killard AJ, Smyth MR (2006) Application of nanoparticles in electrochemical sensors and biosensors. Electroanalysis 18:319–326

    Article  CAS  Google Scholar 

  • Macirella R, Guardia A, Pellegrino D, Bernabò I, Tronci V, Ebbesson LOE, Sesti S, Tripepi S, Brunelli E (2016) Effects of two sublethal concentrations of mercury chloride on the morphology and metallothionein activity in the liver of zebrafish (Danio rerio). Int J Mol Sci 17:361

    Article  Google Scholar 

  • Magaye R, Zhao J (2012) Recent progress in studies of metallic nickel and nickelbased nanoparticles’ genotoxicity and carcinogenicity. Environ Toxicol Pharmacol 34:644–650

    Article  CAS  Google Scholar 

  • Mahoney S, Najera M, Bai Q, Burton EA, Veser G (2016) The developmental toxicity of complex silica-embedded nickel nanoparticles is determined by their physicochemical properties. PLoS ONE 11:1–20

    Google Scholar 

  • Maurer-Jones MA, Gunsolus IL, Murphy CJ, Haynes CL (2013) Toxicity of engineered nanoparticles in the environment. Anal Chem 85:3036–3049

    Article  CAS  Google Scholar 

  • Minghetti M, Leaver MJ, George SG (2010) Multiple Cu-ATPase genes are differentially expressed and transcriptionally regulated by Cu exposure in sea bream, Sparus aurata. Aquat Toxicol 97:23–33

    Article  CAS  Google Scholar 

  • Mueller NC, Nowack B (2008) Exposure modelling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–4453

    Article  CAS  Google Scholar 

  • Örn S, Holbech H, Madsen TH, Norrgren L, Petersen GI (2003) Gonad development and vitellogenin production in zebrafish (Danio rerio) exposed to ethinylestradiol and methyltestosterone. Aquat Toxicol 65:397–411

    Article  Google Scholar 

  • Rao KV, Sunandana CS (2008) Effect of fuel to oxidizer ratio on the structure, micro structure and EPR of combustion synthesized NiO nanoparticles. J Nanosci Nanotechnol 8:4247–4253

    Article  CAS  Google Scholar 

  • Reinardy HC, Dharamshi J, Jha AN, Henry TB (2013) Changes in expression profiles of genes associated with DNA repair following induction of DNA damage in larval zebrafish Danio rerio. Mutagenesis 28:601–608

    Article  CAS  Google Scholar 

  • Schrand AM, Rahman MF, Hussain SM, Schlager JJ, Smith DA, Syed AF (2010) Metal-based nanoparticles and their toxicity assessment. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2:544–568

    Article  CAS  Google Scholar 

  • Segner H, Caroll K, Fenske M, Janssen CR, Maack G, Pascoe D, Schäffers C, Vanderbergh GF, Watts M, Wenzel A (2003) Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project. Ecotoxicol Environ Saf 54:302–314

    Article  CAS  Google Scholar 

  • Stark WJ, Stoessel PR, Wohlleben W, Hafner A (2015) Industrial applications of nanoparticles. Chem Soc Rev 44:5793–5805

    Article  CAS  Google Scholar 

  • Vliegenthart AD, Tucker CS, Del PJ, Dear JW (2014) Zebrafish as model organisms for studying drug-induced liver injury. Br J Clin Pharmacol 78:1217–1227

    Article  CAS  Google Scholar 

  • Xiong D, Fang T, Yu L, Sima X, Zhu W (2011) Effects of nano-scale TiO2, ZnO and their bulk counterparts on zebrafish: acute toxicity, oxidative stress and oxidative damage. Sci Total Environ 409:1444–1452

    Article  CAS  Google Scholar 

  • Yeo MK, Pak SW (2008) Exposing zebrafish to silver nanoparticles during caudal fin regeneration disrupts caudal fin growth and p53 signaling. Mol Cell Toxicol 4:311–317

    Google Scholar 

  • Yu LP, Fang T, Xiong DW, ZhuWT Sima XF (2011) Comparative toxicity of nano-ZnO and bulk ZnO suspensions to zebrafish and the effects of sedimentation, ·OH production and particle dissolution in distilled water. J Environ Monit 13:1975–1982

    Article  CAS  Google Scholar 

  • Zeinalov OA, Kombarova SP, Bagrov DV, Petrosyan MA, Tolibova GH, Feofanov AV, Shaitan KV (2016) About the influence of silver nanoparticles on living organisms physiology. Rev Clin Pharmacol Drug Ther 14:42–51

    Article  Google Scholar 

  • Zhao X, Ren X, Zhu R, Luo Z, Ren B (2016) Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria-mediated apoptosis in zebrafish embryos. Aquat Toxicol 180:56–70

    Article  CAS  Google Scholar 

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Acknowledgements

This project was funded by Recep Tayyip Erdoğan University, Scientific Research Projects Fund (Project No: 2013.103.01.4). The information contained in this article was extracted from a doctorate thesis by the author, Savaş Şaffak.

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Correspondence to Halis Boran.

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Boran, H., Şaffak, S. Comparison of Dissolved Nickel and Nickel Nanoparticles Toxicity in Larval Zebrafish in Terms of Gene Expression and DNA Damage. Arch Environ Contam Toxicol 74, 193–202 (2018). https://doi.org/10.1007/s00244-017-0468-8

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  • DOI: https://doi.org/10.1007/s00244-017-0468-8

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