Oxidative Stress-Mediated Apoptosis and Genotoxicity Induced by Silver Nanoparticles in Freshwater Snail Lymnea luteola L.
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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.
Keywords
Silver nanoparticles Oxidative stress Apoptosis DNA damage Lymnea luteola LNotes
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.
References
- 1.Oberdorster G, Oberdorster E, Oberdorster J (2005) Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113:823–839PubMedCentralPubMedCrossRefGoogle Scholar
- 2.Moore MN (2006) Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ Sci Technol 32:967–976Google 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 444:267–269PubMedCrossRefGoogle Scholar
- 4.Benn TM, Westerhoff P (2008) Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 42:4133–4139PubMedCrossRefGoogle 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 371:47–55PubMedCrossRefGoogle 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):5421–5429PubMedCrossRefGoogle Scholar
- 7.Mueller NC, Nowack B (2008) Exposure modelling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–4453PubMedCrossRefGoogle Scholar
- 8.Purcell TW, Peters JJ (1998) Sources of silver in the environment. Environ Toxicol Chem 17:539–546CrossRefGoogle 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 6–9:181–184Google Scholar
- 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 31:723–731CrossRefGoogle Scholar
- 11.Simon KS, Simon MA, Benfield EF (2009) Variation in ecosystem function in Appalachian streams along an acidity gradient. Ecol Appl 19:1147–1160PubMedCrossRefGoogle 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 54:419–423PubMedCrossRefGoogle 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 205–229Google 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 35:206–221CrossRefGoogle 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 71:1823–1831PubMedCrossRefGoogle Scholar
- 16.APHA, AWWA, WPCF (2005) Standard methods for the examination of water and wastewater, 21st edn. American Publication of Health Association, Washington, DCGoogle Scholar
- 17.Finney DJ (1971) Probit analysis 3rd ed. Cambridge University Press, London, p 318Google Scholar
- 18.Nair V, Turner GE (1984) The thiobarbituric acid test for lipid peroxidation structure of the adduct with malondialdehyde. Lipids 19:84–95CrossRefGoogle Scholar
- 19.Owens WI, Belcher RV (1965) A colorimetric micro-method for the determination of glutathione. Bioch J 94:705–711Google Scholar
- 20.Beers RF Jr, Sizers IW (1952) Spectrophotometric method for measuring the break-down of hydrogen peroxide by catalase. J of Bio Chem 195:133–140Google 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 73:492–499CrossRefGoogle 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 175:184–191PubMedCrossRefGoogle 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 307:261–271CrossRefGoogle 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 72:248–254CrossRefGoogle 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 12:1945–1958CrossRefGoogle 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 27:1972–1978CrossRefGoogle 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 25:746–752PubMedCrossRefGoogle 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 40:641–650CrossRefGoogle 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 32:134–141PubMedCrossRefGoogle Scholar
- 31.Simon HU, Haj-Yehia A, Levi-Schaffer A (2000) Role of reactive oxygen species in apoptosis induction. Apoptosis 5:415–418PubMedCrossRefGoogle 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 1:133–143PubMedCentralPubMedCrossRefGoogle 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 112:265–276CrossRefGoogle 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 270:3778–3786PubMedCrossRefGoogle Scholar
- 35.Verma RS, Mehta A, Srivastava N (2007) In vivo chlorpyrifos induced oxidative stress: attenuation by antioxidant vitamins. Pest Bioch and Phys 88:191–196CrossRefGoogle 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 45–52Google Scholar
- 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 35:594–601CrossRefGoogle 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 49:386–392CrossRefGoogle Scholar
- 39.Roling JA, Baldwin WS (2006) Alterations in hepatic gene expression by trivalent chromium in Fundulus heteroclitus. Mar Environ Res 62:122–127CrossRefGoogle 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 139:1–9PubMedCrossRefGoogle Scholar