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3 Biotech

, 8:441 | Cite as

In vivo toxicity evaluation of biologically synthesized silver nanoparticles and gold nanoparticles on adult zebrafish: a comparative study

  • Rajan Ramachandran
  • Chandran Krishnaraj
  • V. K. Abhay Kumar
  • Stacey L. Harper
  • Thangavelu P. Kalaichelvan
  • Soon-Il Yun
Original Article
  • 33 Downloads

Abstract

In this study, toxicity of biologically synthesized silver nanoparticles (AgNPs) and gold nanoparticles (AuNPs) was compared using zebrafish as a model organism. At 96 h, LC50 of AgNPs and AuNPs was found to be 24.5 µg/L and 41 mg/L, respectively. Following the LC50 determination, half of the LC50 of AgNPs (12.25 µg/L) and AuNPs (20.5 mg/L) was exposed to adult zebrafishes for 14 days. Morphological changes, liver marker enzymes, reactive oxygen species (ROS) generation, genotoxic effects and mRNA expression levels of oxidative stress and innate immune response related genes were studied using nanoparticle treated gill, liver and blood cells. In this study, AgNP-treated gill and liver tissues showed a number of morphological changes such as cell membrane damage, irregular cell outlines, pyknotic nuclei and complete disruption of gill and liver cells; on the contrary, AuNPs treated liver tissues alone showed such changes. The levels of liver marker enzymes such as alanine aminotransferase and aspartate aminotransferase were increased after AgNPs treatment when compared to AuNPs treatment. AgNP-treated liver cells showed higher levels of ROS generation than the control; on the other hand, AuNPs treatment exhibited lower levels of ROS generation than the control. Interestingly, AgNP-treated blood cells showed micronuclei formation and nuclear abnormalities, while AuNPs treatment did not show such effects. Based on these observations, it is clear that AgNPs may cause oxidative stress and immunotoxicity to adult zebrafish than the AuNPs. However, these results clearly reveal the significance of relatively safe and less toxic bionanomaterials for possible biomedical applications.

Keywords

Toxicity Biologically synthesized nanoparticles Zebrafish Liver marker enzymes Reactive oxygen species qPCR 

Notes

Acknowledgements

RR sincerely acknowledges University Grants Commission (UGC), Government of India for awarding UGC-BSR Meritorious Fellowship in Sciences. This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2013R1A1A2007953) and also funds from Chonbuk National University, Republic of Korea.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Supplementary material

13205_2018_1457_MOESM1_ESM.pptx (333 kb)
Supplementary material 1 (PPTX 333 KB)
13205_2018_1457_MOESM2_ESM.doc (42 kb)
Supplementary material 2 (DOC 42 KB)

References

  1. Aerle RV, Johnston BD, Lange A, Bastos ED, Moorhouse A, Booth T, Paszkiewicz K, Tyler CR, Ball K, Santos EM (2013) Molecular mechanisms of toxicity of silver nanoparticles in zebrafish embryos. Environ Sci Technol 47:8005–8014CrossRefGoogle Scholar
  2. Asharani PV, Wu YL, Gong Z, Valiyaveettil S (2008) Toxicity of silver nanoparticles in zebrafish models. Nanotechnology 19:255102CrossRefGoogle Scholar
  3. Asharani PV, Wu YL, Gong Z, Valiyaveettil S (2011) Comparison of the toxicity of silver, gold and platinum nanoparticles in developing zebrafish embryos. Nanotoxicology 5:43–54CrossRefGoogle Scholar
  4. Ayllon FE, Garcia-Vazquez (2000) Induction of micronuclei and other nuclear abnormalities in European minnow Phoxinus phoxinus and mollie Poecilia latipinna: an assessment of the fish micronucleus test. Mutation Res 467:177–186CrossRefGoogle Scholar
  5. Balakumaran MD, Ramachandran R, Balashanmugam P, Mukeshkumar DJ, Kalaichelvan PT (2016) Mycosynthesis of silver and gold nanoparticles: optimization, characterization and antimicrobial activity against human pathogens. Microbiol Res 182:8–20CrossRefGoogle Scholar
  6. Bar-Ilan O, Albrecht RM, Fako VE, Furgeson DY (2009) Toxicity assessments of multisized gold and silver nanoparticles in zebrafish embryos. Small 5:1897–1910CrossRefGoogle Scholar
  7. Bilberg K, Hovgaard MB, Besenbacher F, Baatrup E (2012) In vivo toxicity of silver nanoparticles and silver ions in zebrafish (Danio rerio). J Toxicol 2012:293784Google Scholar
  8. Brasier AR (2006) The NF-κB regulatory network. Cardiovasc Toxicol 6:111–130CrossRefGoogle Scholar
  9. Buzea C, Pacheco II, Robbie K (2007) Nanomaterials and nanoparticles: sources and toxicity. Biointerphases 2:MR17–MR71CrossRefGoogle Scholar
  10. 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 100:151–159CrossRefGoogle Scholar
  11. Gilmore TD, Herscovitch M (2006) Inhibitors of NF-κB signaling: 785 and counting. Oncogene 25:6887–6899CrossRefGoogle Scholar
  12. Girilal M, Krishnakumar V, Poornima P, Fayaz AM, Kalaichelvan PT (2015) A comparative study on biologically and chemically synthesized silver nanoparticles induced heat shock proteins on fresh water fish Oreochromis niloticus. Chemosphere 139:461–468CrossRefGoogle Scholar
  13. Griffitt RJ, Hyndman K, Denslow ND, Barber DS (2009) Comparison of molecular and histological changes in zebrafish gills exposed to metallic nanoparticles. Toxicol Sci 107:404–415CrossRefGoogle Scholar
  14. Gunes C, Heuchel R, Georgiev O, Muller KH, Lichtlen P, Bluthmann H, Marino S, Aguzzi A, Schaffner W (1998) Embryonic lethality and liver degeneration in mice lacking the metal-responsive transcriptional activator MTF-1. Embo J 17:2846–2854CrossRefGoogle Scholar
  15. Haynes CL (2010) The emerging field of nanotoxicology. Anal Bioanal Chem 398:587–588CrossRefGoogle Scholar
  16. Hotchkiss RD (1948) A microchemical reaction resulting in the staining of polysaccharide structure in fixed tissue preparations. Arch Biochem 16:131–141PubMedGoogle Scholar
  17. Hu YL, Qi W, Han F, Shao J, Gao J (2011) Toxicity evaluation of biodegradable chitosan nanoparticles using a zebrafish embryo model. Int J Nanomedicine 6:3351–3359PubMedPubMedCentralGoogle Scholar
  18. Impellitteri CA, Tolaymat TM, Scheckel KG (2009) The speciation of silver nanoparticles in antimicrobial fabric before and after exposure to a hypochlorite/detergent solution. J Environ Qual 38:1528–1530CrossRefGoogle Scholar
  19. Kiernan JA (1999) Histological and histochemical methods: theory and practice, 3rd edn. Butterworth-Heinemann, OxfordGoogle Scholar
  20. Kim S, Choi JE, Choi J, Chung K-H, Park K, Yi J, Ryu D-Y (2009) Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol In Vitro 23:1076–1084CrossRefGoogle Scholar
  21. Krishnaraj C, Ramachandran R, Mohan K, Kalaichelvan PT (2012) Optimization for rapid synthesis of silver nanoparticles and its effect on phytopathogenic fungi. Spectrochim Acta A Mol Biomol Spectrosc 93:95–99CrossRefGoogle Scholar
  22. Krishnaraj C, Muthukumaran P, Ramachandran R, Balakumaran MD, Kalaichelvan PT (2014) Acalypha indica Linn: biogenic synthesis of silver and gold nanoparticles and their cytotoxic effects against MDA-MB-231, human breast cancer cells. Biotechnol Rep 4:42–49CrossRefGoogle Scholar
  23. Krishnaraj C, Harper SL, Yun S-I (2016) In vivo toxicological assessment of biologically synthesized silver nanoparticles in adult zebrafish (Danio rerio). J Hazard Mater 301:480–491CrossRefGoogle Scholar
  24. Marcolin E, Miguel BS, Vallejo D, Tieppo J, Marroni N, Gallego JG, Tunon MJ (2012) Quercetin treatment ameliorates inflammation and fibrosis in mice with nonalcoholic Steatohepatitis 1–3. J Nutr 142:1821–1828CrossRefGoogle Scholar
  25. Massarsky A, Dupuis L, Taylor J, Eisa-Beygi S, Strek L, Trudeau VL, Moon TW (2013) Assessment of nanosilver toxicity during zebrafish (Danio rerio) development. Chemosphere 92:59–66CrossRefGoogle Scholar
  26. Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627CrossRefGoogle Scholar
  27. Nowack B, Bucheli TD (2007) Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 150:5–22CrossRefGoogle Scholar
  28. Oberdörster G, Oberdörster E, Oberdörster J (2005) Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113:823–839CrossRefGoogle Scholar
  29. OECD (1992) Test No. 203: fish, acute toxicity test. OECD Publishing, ParisCrossRefGoogle Scholar
  30. Olasagasti M, Gatti AM, Capitani F, Barranco A, Pardo MA, Escuredo K, Rainieri S (2014) Toxic effects of colloidal nanosilver in zebrafish embryos. J Appl Toxicol 34:562–575CrossRefGoogle Scholar
  31. Project on Emerging Nanotechnologies (2018) Consumer products inventory. http://www.nanotechproject.org/cpi/products/. Accessed 7 June 2018
  32. Rajan R, Chandran K, Harper SL, Yun S-I, Kalaichelvan PT (2015) Plant extract synthesized silver nanoparticles: an ongoing source of novel biocompatible materials. Ind Crops Prod 70:356–373CrossRefGoogle Scholar
  33. Rajan R, Chandran K, Sivakumar AS, Prasannakumar P, Abhay Kumar VK, Shim KS, Song C-G, Yun S-I (2017) Anticancer activity of biologically synthesized silver and gold nanoparticles on mouse myoblast cancer cells and their toxicity against embryonic zebrafish. Mater Sci Eng C Mater Biol Appl 73:674–683CrossRefGoogle Scholar
  34. Saquib Q, Al-Khedhairy AA, Siddiqui MA, Abou-Tarboush FM, Azam A, Musarrat J (2012) Titanium dioxide nanoparticles induced cytotoxicity, oxidative stress and DNA damage in human amnion epithelial (WISH) cells. Toxicol In Vitro 26:351–361CrossRefGoogle Scholar
  35. Sarkar B, Netam SP, Mahanty A, Saha A, Bosu R, Krishnani KK (2014) Toxicity evaluation of chemically and plant derived silver nanoparticles on zebrafish (Danio rerio). Proc Natl Acad Sci India Sect B Biol Sci 84:885–892CrossRefGoogle Scholar
  36. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C T method. Nat Protoc 3:1101–1108CrossRefGoogle Scholar
  37. Scown TM, Santos EM, Johnston BD, Gaiser B, Tyler CR (2010) Effects of aqueous exposure to silver nanoparticles of different sizes in Rainbow Trout. Toxicol Sci 115:521–534CrossRefGoogle Scholar
  38. Shah D, Savaliya R, Patel P, Kansara K, Pandya A, Dhawan A, Singh S (2018) Curcumin Ag nanoconjugates for improved therapeutic effects in cancer. Int J Nanomed 13:75–77CrossRefGoogle Scholar
  39. Shankar SS, Rai A, Ahmad A, Sastry M (2004a) Rapid synthesis of Au, Ag, and bimetallic Au core–Ag shell nanoparticles using Neem (Azadirachta indica) leaf broth. J Colloid Interface Sci 275:496–502CrossRefGoogle Scholar
  40. Shankar SS, Rai A, Ankamwar B, Singh A, Ahmad A, Sastry M (2004b) Biological synthesis of triangular gold nanoprisms. Nat Mater 3:482–488CrossRefGoogle Scholar
  41. Singh S, D’Britto V, Prabhune AA, Ramana CV, Dhawan A, Prasad BLV (2010) Cytotoxic and genotoxic assessment of glycolipid-reduced and -capped gold and silver nanoparticles. New J Chem 34:294–301CrossRefGoogle Scholar
  42. Smirnova IV, Bittel DC, Ravindra R, Jiang H, Andrews GK (2000) Zinc and cadmium can promote the rapid nuclear translocation of MTF-1. J Biol Chem 275:9377–9384CrossRefGoogle Scholar
  43. Srivastava M, Singh S, Self WT (2012) Exposure to silver nanoparticles inhibits selenoprotein synthesis and the activity of thioredoxin reductase. Environ Health Perspect 120:56–61CrossRefGoogle Scholar
  44. Tsukada J, Yoshida Y, Kominato Y, Auron PE (2011) The CCAAT/enhancer binding (C/EBP) family of basic-leucine zipper (bZIP) transcription factors is a multifaceted highly-regulated system for gene regulation. Cytokine 54:6–19CrossRefGoogle Scholar
  45. Williams JH, Farag AM, Stansbury MA, Young PA, Bergman HL, Petersen NS (1996) Accumulation of hsp70 in juvenile and adult rainbow trout gill exposed to metal-contaminated water and/or diet. Environ Toxicol Chem 15:1324–1328CrossRefGoogle Scholar
  46. Zakin MM (1992) Regulation of transferrin gene expression. FASEB J 6:3253–3258xCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Rajan Ramachandran
    • 1
  • Chandran Krishnaraj
    • 2
    • 3
  • V. K. Abhay Kumar
    • 3
  • Stacey L. Harper
    • 4
  • Thangavelu P. Kalaichelvan
    • 1
  • Soon-Il Yun
    • 2
  1. 1.Centre for Advanced Studies in Botany, School of Life SciencesUniversity of Madras, Guindy CampusChennaiIndia
  2. 2.Department of Food Science and Technology, College of Agriculture and Life SciencesChonbuk National UniversityJeonjuRepublic of Korea
  3. 3.R&D CentreEureka Forbes LtdBangaloreIndia
  4. 4.Department of Environmental and Molecular ToxicologyOregon State UniversityCorvallisUSA

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