Skip to main content

Advertisement

SpringerLink
Log in

Oxidative Stress-Mediated Apoptosis and Genotoxicity Induced by Silver Nanoparticles in Freshwater Snail Lymnea luteola L.

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Silver is one of the most toxic metals to freshwater aquatic organisms. Limited efforts have been made to study apoptosis and genotoxic potential of silver nanoparticles (AgNPs) in freshwater snail Lymnea luteola L. (L. luteola). Therefore, the present investigation was aimed to study the induction of apoptosis and DNA damage by AgNPs in L. luteola. AgNPs showed molluscicidal activity against L. luteola and three concentrations of AgNPs were selected, the concentration I (4 μg/l), concentration II (12 μg/l), and the concentration III (24 μg/l). Induction of oxidative stress in snail hemolymph was observed by a decrease in reduced glutathione (GSH) and glutathione S-transferase (GST) levels at different concentration of AgNPs, and on the other hand, malondialdehyde (MDA) levels increased at lower concentrations but decreased in higher concentration of AgNPs. Catalase (CAT) activity was also decreased at lower concentrations and increased in higher concentration of AgNPs. Flow cytometry data showed that AgNPs exposed hemocyte cells promote apoptotic and necrotic-mediated cell death when AgNPs concentrations were 12 and 24 μg/l compared to control. DNA damage scores increased with the exposure levels of AgNPs, and dose- and time-dependent effects were observed. A significant positive correlation was observed among reactive oxygen species (ROS) generation, apoptosis, and DNA damage. The study suggests that ROS may be involved in inducing apoptosis and DNA damage in the AgNPs exposed hemocyte cells of L. luteola. This study demonstrates that AgNPs is lethal to freshwater snail L. luteola.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Oberdorster G, Oberdorster E, Oberdorster J (2005) Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113:823–839

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Moore MN (2006) Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ Sci Technol 32:967–976

    CAS  Google Scholar 

  3. Maynard AD, Aitken RJ, Butz T, Colvin V, Donaldson K, Oberdorster G, Philbert M, Ryan J, Seaton A, Stone V, Tinkle SS, Tran L, Walker NJ, Warheit DB (2006) Safe handling of nanotechnology. Nature 444:267–269

    Article  CAS  PubMed  Google Scholar 

  4. Benn TM, Westerhoff P (2008) Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 42:4133–4139

    Article  CAS  PubMed  Google Scholar 

  5. Mersch J, Beauvais MN, Nagel P (1996) Induction of micronuclei in haemocytes and gill cells of zebra mussels, Dreissena polymorpha, exposed to clastogens. Mutat Res 371:47–55

    Article  CAS  PubMed  Google Scholar 

  6. Lin J, Zhang H, Chen Z, Zheng Y (2010) Penetration of lipid membranes by gold nanoparticles: insights into cellular uptake, cytotoxicity, and their relationship. ACS Nano 4(9):5421–5429

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. Purcell TW, Peters JJ (1998) Sources of silver in the environment. Environ Toxicol Chem 17:539–546

    Article  CAS  Google Scholar 

  9. Rozan TF, Hunter KS, Benoit G (1995) Silver in fresh water: sources, transport and fate in Connecticut rivers. In: Proceedings of the 3th argentum international conference on the transport, fate and effects of silver in the environment, Washington, DC, USA, August 6–9:181–184

  10. Wen LS, Santschi PH, Gill GA, Paternostro CL, Lehman RD (1997) Colloidal and particulate silver in river and estuarine waters of Texas. Environ Sci Techno 31:723–731

    Article  CAS  Google Scholar 

  11. Simon KS, Simon MA, Benfield EF (2009) Variation in ecosystem function in Appalachian streams along an acidity gradient. Ecol Appl 19:1147–1160

    Article  CAS  PubMed  Google Scholar 

  12. Regoli F, Gorbi S, Frenzilli G, Nigro M, Cors I, Forcardi S, Winston GW (2002) Oxidative stress in ecotoxicology: from the analysis of individual antioxidants to a more integrated approach. Mar Environ Res 54:419–423

    Article  CAS  PubMed  Google Scholar 

  13. Kovochich M, Xia T, Xu J, Yeh JI, Nel AE (2007) Principles and procedures to assess nanomaterial toxicity. In: Wiesner MR, Bottero JY (eds) Environmental nanotechnology. Applications and impacts of nanomaterials. McGraw Hill, New York, pp 205–229

    Google Scholar 

  14. Tice RR, Agurell E, Anderson D, Burlinson B, Hartmenn A, Kobatashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF (2000) Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Muta 35:206–221

    Article  CAS  Google Scholar 

  15. Ali D, Nagpure NS, Kumar S, Kumar R, Kushwaha B (2008) Genotoxicity assessment of acute exposure of chlorpyrifos to freshwater fish Channa punctatus (Bloch) using micronucleus assay and alkaline single-cell gel electrophoresis. Chemosphere 71:1823–1831

    Article  CAS  PubMed  Google Scholar 

  16. APHA, AWWA, WPCF (2005) Standard methods for the examination of water and wastewater, 21st edn. American Publication of Health Association, Washington, DC

    Google Scholar 

  17. Finney DJ (1971) Probit analysis 3rd ed. Cambridge University Press, London, p 318

    Google Scholar 

  18. Nair V, Turner GE (1984) The thiobarbituric acid test for lipid peroxidation structure of the adduct with malondialdehyde. Lipids 19:84–95

    Article  Google Scholar 

  19. Owens WI, Belcher RV (1965) A colorimetric micro-method for the determination of glutathione. Bioch J 94:705–711

    CAS  Google Scholar 

  20. Beers RF Jr, Sizers IW (1952) Spectrophotometric method for measuring the break-down of hydrogen peroxide by catalase. J of Bio Chem 195:133–140

    CAS  Google Scholar 

  21. Vessey DA, Boyer TD (1984) Differential activation and inhibition of different forms of rat liver glutathione S-transferase by the herbicides 2,4-dichloro phenoxy acetate (2,4-D) and 2,4, strichloro phenoxy acetate (2,4, S-T). Toxic and App Pharm 73:492–499

    Article  CAS  Google Scholar 

  22. Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantization of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191

    Article  CAS  PubMed  Google Scholar 

  23. Anderson D, Yu TW, Phillips BJ, Schmerzer P (1994) The effect of various antioxidants and other modifying agents on oxygen-radical generated DNA damage inhuman lymphocytes in the comet assay. Muta Res 307:261–271

    Article  CAS  Google Scholar 

  24. Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Bioch 72:248–254

    Article  CAS  Google Scholar 

  25. Woodrow Wilson International Center for Scholars (2008) The project on emerging nanotechnologies. Consumer products. An inventory of nanotechnology-based consumer products currently on the Market http://www.nanotechproject.org/inventories/consumer.

  26. Elzey S, Grassian VH (2010) Agglomeration, isolation and dissolution of commercially manufactured silver nanoparticles in aqueous environments. J Nanopart Res 12:1945–1958

    Article  CAS  Google Scholar 

  27. Griffitt RJ, Luo J, Gao J, Bonzango JC, Barber DS (2008) Effects of particle composition and species on toxicity of metallic nanoparticles in aquatic organisms. Environ Toxic and Chem 27:1972–1978

    Article  CAS  Google Scholar 

  28. Tola EN, Mungan MT, Uğuz AC, Naziroğlu M (2013) Intracellular Ca2+ and antioxidant values induced positive effect on fertilisation ratio and oocyte quality of granulosa cells in patients undergoing in vitro fertilization. Reprod Fertil Dev 25:746–752

    Article  CAS  PubMed  Google Scholar 

  29. Valencia A, Kochevar IE (2006) Ultraviolet A induces apoptosis via reactive oxygen species in a model for Smith-Lemli-Opitz syndrome. Free Rad Bio and Med 40:641–650

    Article  CAS  Google Scholar 

  30. Naziroglu M (2012) Molecular role of catalase on oxidative stress-induced Ca2+ signaling and TRP cation channel activation in nervous system. J Recept Signal Transduct Res 32:134–141

    Article  CAS  PubMed  Google Scholar 

  31. Simon HU, Haj-Yehia A, Levi-Schaffer A (2000) Role of reactive oxygen species in apoptosis induction. Apoptosis 5:415–418

    Article  CAS  PubMed  Google Scholar 

  32. Lee KJ, Nallathamby PD, Browning LM, Osgood CJ, Xu XHN (2007) In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. ACS Nano 1:133–143

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Livingstone DR, Lips F, Garcia MP, Pipe RK (1992) Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Mar Bio 112:265–276

    Article  CAS  Google Scholar 

  34. Zhao M, Antunes F, Eaton JW, Brunk UT (2003) Lysosomal enzymes promote mitochondrial oxidant production, cytochrome c release and apoptosis. Eur J Biochem 270:3778–3786

    Article  CAS  PubMed  Google Scholar 

  35. Verma RS, Mehta A, Srivastava N (2007) In vivo chlorpyrifos induced oxidative stress: attenuation by antioxidant vitamins. Pest Bioch and Phys 88:191–196

    Article  CAS  Google Scholar 

  36. Jamil K (2001) Bioindicators and biomarkers of environmental pollution and risk assessment. (Science Publishers, Inc., Enfield (Nh). USA and Plymouth, U.K. pp 45–52

  37. Regoli F, Hummel H, Amiard-Triquet C, Larroux C, Sukhotin A (1998) Trace metals and variations of antioxidant enzymes in Arctic bivalve populations. Archives of Environ Conta and Toxic 35:594–601

    Article  CAS  Google Scholar 

  38. Almeida EA, Miyamoto S, Bainy ACD, Medeiros MH, Mascio P (2004) Protective effect of phosphor lipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels Perna perna exposed to different metals. Mar Poll Bull 49:386–392

    Article  Google Scholar 

  39. Roling JA, Baldwin WS (2006) Alterations in hepatic gene expression by trivalent chromium in Fundulus heteroclitus. Mar Environ Res 62:122–127

    Article  Google Scholar 

  40. Ozkaya OM, Nazıroglu M, Barak C, Berkkanoglu M (2011) Effects of multivitamin/mineral supplementation on trace element levels in serum and follicular fluid of women undergoing in vitro fertilization (IVF). Biol Trace Elem Res 139:1–9

    Article  PubMed  Google Scholar 

Download references

Acknowledgement

The authors would like to extend their sincere appreciation to the Deanship of Scientific Research at King Saud University for its funding this Research group NO (RG −1435-076).

Conflict of Interest

There are no conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Zoology, College of Science, King Saud University, P.O. Box 2454, Riyadh, 11451, Saudi Arabia

    Daoud Ali

Authors
  1. Daoud Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daoud Ali.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ali, D. Oxidative Stress-Mediated Apoptosis and Genotoxicity Induced by Silver Nanoparticles in Freshwater Snail Lymnea luteola L.. Biol Trace Elem Res 162, 333–341 (2014). https://doi.org/10.1007/s12011-014-0158-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-014-0158-6

Keywords

Search

Navigation