Skip to main content

Silver nanoparticles affects the expression of biomarker genes mRNA in rainbow trout (Oncorhynchus mykiss)

Abstract

Due to their strong antiseptic properties, silver nanoparticles (AgNPs) are widely used in consumer products, and therefore there is a high risk of their release to the aquatic environment. In the present study, we investigated chronic effect of waterborne AgNPs on the mRNA expression of four important biomarker genes including metallothionein (MT), glutathione S-transferase (GST), superoxide dismutase (SOD), and glutathione peroxidase (GPX) in the gill tissue of rainbow trout. Twenty-one-day exposure to AgNPs significantly increased MT and GST mRNA levels in the gills in a dose-dependent manner. Although mRNA levels of SOD significantly increased in the gills of fish exposed to AgNPs, but its increase was not dose-dependent. In contrast, exposure to AgNPs significantly decreased GPX mRNA levels in the gills. The results suggest that exposure to AgNPs can significantly change the expression of biomarker genes mRNA in rainbow trout.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  • Asghari S, Johari SA, Lee JH, Kim YS, Jeon YB, Choi HJ, Moon MC, Yu IJ (2012) Toxicity of various silver nanoparticles compared to silver ions in Daphnia magna. J Nanobiotechnology 10:14

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Basha PS, Rani AU (2003) Cadmium-induced antioxidant defense mechanism in freshwater teleost Oreochromis mossambicus (Tilapia). Ecotoxicol Environ Saf 56:218–221

    CAS  Article  PubMed  Google Scholar 

  • Batley GE, Kirby JK, McLaughlin MJ (2013) Fate and risks of nanomaterials in aquatic and terrestrial environments. Acc Chem Res 46:854–862

    CAS  Article  PubMed  Google Scholar 

  • Carlson C, Hussain SM, Schrand AM, Braydich-Stolle LK, Hess KL, Jones RL, Schlager JJ (2008) Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B 112(43):13608–13619

    CAS  Article  PubMed  Google Scholar 

  • Chae YJ, Pham CH, Lee J, Bae E, Yi J, Gu MB (2009) Evaluation of the toxic impact of silver nanoparticles on Japanese medaka (Oryzias latipes). Aquat Toxicol 94:320–327

    CAS  Article  PubMed  Google Scholar 

  • Choi O, Hu Z (2008) Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42(12):4583–4588

    CAS  Article  PubMed  Google Scholar 

  • Choi CY, An KW, Nelson ER, Habibi HR (2007) Cadmium affects the expression of metallothionein (MT) and glutathione peroxidase (GPX) mRNA in goldfish, Carassius auratus. Comp Biochem Physiol, Part C 145:595–600

    Google Scholar 

  • Choi JE, Kim S, Ahn JH, Youn P, Kang JS, Park K, Yi J, Ryu DY (2010) Induction of oxidative stress and apoptosis by silver nanoparticles in the liver of adult zebrafish. Aquat Toxicol 100(2):151–159

    CAS  Article  PubMed  Google Scholar 

  • Crago J, Corsi SR, Weber D, Bannerman R, Klaper R (2011) Linking biomarkers to reproductive success of caged fathead minnows in streams with increasing urbanization. Chemosphere 82:1669–1674

    CAS  Article  PubMed  Google Scholar 

  • Farmen E, Mikkelsen HN, Evensen Ø, Einset J, Heier LS, Rosseland BO, Salbu B, Tollefsen KE, Oughton DH (2012) Acute and sub-lethal effects in juvenile Atlantic salmon exposed to low μg/L concentrations of Ag nanoparticles. Aquat Toxicol 108:78–84

    CAS  Article  PubMed  Google Scholar 

  • Foldbjerg R, Olesen P, Hougaard M, Dang DA, Hoffmann HJ, Autrup H (2009) PVP-coated silver nanoparticles and silver ions induce reactive oxygen species, apoptosis and necrosis in THP-1 monocytes. Toxicol Lett 190(2):156–162

    CAS  Article  PubMed  Google Scholar 

  • Fu PP, Xia Q, Hwang HM, Ray PC, Yu H (2014) Mechanisms of nanotoxicity: generation of reactive oxygen species. J Food Drug Anal 22(1):64–75

    CAS  Article  PubMed  Google Scholar 

  • Gagné F, Auclair J, Fortier M, Bruneau A, Fournier M, Turcotte P, Pilote M, Gagnon C (2013) Bioavailability and immunotoxicity of silver nanoparticles to the freshwater mussel Elliptio complanata. J Toxic Environ Health A 76(13):767–777

    Article  Google Scholar 

  • Giovanni M, Tay CY, Setyawati MI, Xie J, Ong CN, Fan R, Yue J, Zhang L, Leong DT (2014) Toxicity profiling of water contextual zinc oxide, silver, and titanium dioxide nanoparticles in human oral and gastrointestinal cell systems. Environ Toxicol. doi:10.1002/tox.22015

    PubMed  Google Scholar 

  • Hermesz E, Abrahám M, Nemcsók J (2001) Tissue-specific expression of two metallothionein genes in common carp during cadmium exposure and temperature shock. Comp Biochem Physiol Part C 128:457–465

    CAS  Google Scholar 

  • Johari SA, Kalbassi MR, Soltani M, Yu IJ (2013) Toxicity comparison of colloidal silver nanoparticles in various life stages of rainbow trout (Oncorhynchus mykiss). Iran J Fish Sci 12(1):76–95

    Google Scholar 

  • Johari SA, Kalbassi MR, Yu IJ, Lee JH (2014a) Chronic effect of waterborne silver nanoparticles on rainbow trout (Oncorhynchus mykiss): histopathology and bioaccumulation. Comp Clin Pathol. doi:10.1007/s00580-014-2019-2

    Google Scholar 

  • Johari SA, Sourinejad I, Bärsch N, Saed-Moocheshi S, Kaseb A, Nazdar N (2014b) Does physical production of nanoparticles reduce their ecotoxicity? A case of lower toxicity of AgNPs produced by laser ablation to zebrafish (Danio rerio). Int J Aquat Biol 2(4):188–192

    Google Scholar 

  • Johari SA, Habibi L, Hosseini SJ (2014c) Toxicity of colloidal nano-silver to zebrafish, Danio rerio: ions, nanoparticles, or both? J Aquat Nutr Biochem 1(1):59–68

    Google Scholar 

  • Johari SA, Kalbassi MR, Sltani M, Yu IJ (2015) Application of nanosilver-coated zeolite as water filter media for fungal disinfection of rainbow trout (Oncorhynchus mykiss) eggs. Aquac Int. doi:10.1007/s10499-015-9906-7

    Google Scholar 

  • Keller AA, McFerran S, Lazareva A, Suh S (2013) Global life cycle releases of engineered nanomaterials. J Nanoparticle Res 15:1692

    Article  Google Scholar 

  • Lange A, Ausseil O, Segner H (2002) Alterations of tissue glutathione levels and metallothionein mRNA in rainbow trout during single and combined exposure to cadmium and zinc. Comp Biochemi Physiol Part C 131:231–243

    Google Scholar 

  • Li H, Turner A, Brown MT (2012) Accumulation of aqueous and nanoparticulate silver by the marine gastropod Littorina littorea. Water Air Soil Pollut 224:1354

    Article  Google Scholar 

  • Ng KW, Khoo SP, Heng BC, Setyawati MI, Tan EC, Zhao X, Xiong S, Fang W, Leong DT, Loo JS (2011) The role of the tumor suppressor p53 pathway in the cellular DNA damage response to zinc oxide nanoparticles. Biomaterials 32(32):8218–8225

    CAS  Article  PubMed  Google Scholar 

  • Nickum JG, Bart HL Jr, Bowser PR, Greer IE, Hubbs C, Jenkins JA, MacMillan JR, Rachlin JW, Rose JD, Sorensen PW, Tomasso JR (2004) Guidelines for the use of fishes in research. American Fisheries Society, Bethesda, p 54

    Google Scholar 

  • OECD (1984) OECD guidelines for the testing of chemicals. Test No. 204: fish, prolonged toxicity test: 14-day study. Organization for Economic Cooperation and Development, Paris

    Google Scholar 

  • Oukarroum A, Samadani M, Dewez D (2014) Influence of pH on the toxicity of silver nanoparticles in the green alga Chlamydomonas acidophila. Water Air Soil Pollut 225:2038

    Article  Google Scholar 

  • Pham CH, Yi J, Gu MB (2012) Biomarker gene response in male Medaka (Oryzias latipes) chronically exposed to silver nanoparticle. Ecotoxicol Environ Saf 78:239–245

    CAS  Article  PubMed  Google Scholar 

  • Ribeiro F, Gallego-Urrea JA, Jurkschat K, Crossley A, Hassellöv M, Taylor C, Soares AM, Loureiro S (2014) Silver nanoparticles and silver nitrate induce high toxicity to Pseudokirchneriella subcapitata, Daphnia magna and Danio rerio. Sci Total Environ 466–467:232–241

    Article  PubMed  Google Scholar 

  • Roberts AP, Oris JT (2004) Multiple biomarker response in rainbow trout during exposure to hexavalent chromium. Comp Biochem Physiol, Part C 138:221–228

    Google Scholar 

  • Roesijadi G (1992) Metallothioneins in metal regulation and toxicity in aquatic animals. Aquat Toxicol 22:81–114

    CAS  Article  Google Scholar 

  • Roesijadi G (1996) Metallothionein and its role in toxic metal regulation. Comp Biochem Physiol, Part C 113(2):117–123

    Google Scholar 

  • Salari Joo H, Kalbassi MR, Yu IJ, Lee JH, Johari SA (2013) Bioaccumulation of silver nanoparticles in rainbow trout (Oncorhynchus mykiss): influence of concentration and salinity. Aquat Toxicol 140–141:398–406

    Article  PubMed  Google Scholar 

  • Scown TM, Santos EM, Johnston BD, Gaiser B, Baalousha M, Mitov S, Lead JR, Stone V, Fernandes TF, Jepson M, van Aerle R, Tyler CR (2010) Effects of aqueous exposure to silver nanoparticles of different sizes in rainbow trout. Toxicol Sci 115(2):521–534

    CAS  Article  PubMed  Google Scholar 

  • Setyawati MI, Tay CY, Leong DT (2013) Effect of zinc oxide nanomaterials-induced oxidative stress on the p53 pathway. Biomaterials 34(38):10133–10142

    CAS  Article  PubMed  Google Scholar 

  • Setyawati MI, Yuan X, Xie J, Leong DT (2014) The influence of lysosomal stability of silver nanomaterials on their toxicity to human cells. Biomaterials 35(25):6707–6715

    CAS  Article  PubMed  Google Scholar 

  • Sohn EK, Johari SA, Kim TG, Kim JK, Kim E, Lee JH, Chung YS, Yu IJ (2015) Aquatic toxicity comparison of silver nanoparticles and silver nanowires. BioMed Res Int. doi:10.1155/2015/893049

    Google Scholar 

  • Tay CY, Setyawati MI, Xie J, Parak WJ, Leong DT (2014) Back to basics: exploiting the innate physico-chemical characteristics of nanomaterials for biomedical applications. Adv Funct Mater 24(38):5936–5955

    CAS  Article  Google Scholar 

  • van Heerden D, Vosloo A, Nikinmaa M (2004) Effects of short-term copper exposure on gill structure, metallothionein and hypoxia-inducible factor-1alpha (HIF-1alpha) levels in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 69:271–280

    Article  PubMed  Google Scholar 

  • Welsh PG, Lipton J, Mebane CA, Marr JCA (2008) Influence of flow-through and renewal exposures on the toxicity of copper to rainbow trout. Ecotoxicol Environ Saf 69:199–208

    CAS  Article  PubMed  Google Scholar 

  • Woodrow Wilson Database (2013) Nanotechnology consumer product inventory. http://www.nanotechproject.org/cpi/about/analysis/. Accessed at 10 June 2015

  • Xia T, Zhao Y, Sager T, George S, Pokhrel S, Li N, Schoenfeld D, Meng H, Lin S, Wang X, Wang M, Ji Z, Zink JI, Mädler L, Castranova V, Lin S, Nel AE (2011) Decreased dissolution of ZnO by iron doping yields nanoparticles with reduced toxicity in the rodent lung and zebrafish embryos. ACS Nano 5(2):1223–1235

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the support of the Tarbiat Modares University of I. R. Iran, and Korea University who funded this research.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Seyed Ali Johari or Mohammad Reza Kalbassi.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Johari, S.A., Kalbassi, M.R., Lee, S.B. et al. Silver nanoparticles affects the expression of biomarker genes mRNA in rainbow trout (Oncorhynchus mykiss). Comp Clin Pathol 25, 85–90 (2016). https://doi.org/10.1007/s00580-015-2144-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00580-015-2144-6

Keywords

  • Aquatic nanotoxicology
  • Silver nanoparticles
  • Metallothionein
  • Superoxide dismutase
  • Glutathione s-transferase
  • Glutathione peroxidase