Effects of silver nanoparticles of different sizes on cytotoxicity and oxygen metabolism disorders in both reproductive and respiratory system cells

• Autorzy: Zapór L.

Identyfikatory

DOI

10.1515/aep-2016-0038

Warianty tytułu

PL

Wpływ różnej wielkości nanocząstek srebra na cytotoksyczność i zaburzenia metabolizmu tlenowego w komórkach układu oddechowego i rozrodczego

• Języki publikacji: EN

Abstrakty

EN

Silver nanoparticles (AgNPs) are widely used in numerous industries and areas of daily life, mainly as antimicrobial agents. The particles size is very important, but still not suffi ciently recognized parameter infl uencing the toxicity of nanosilver. The aim of this study was to investigate the cytotoxic effects of AgNPs with different particle size (~ 10, 40 and 100 nm). The study was conducted on both reproductive and pulmonary cells (CHO-9, 15P-1 and RAW264.7). We tested the effects of AgNPs on cell viability, cell membrane integrity, mitochondrial metabolic activity, lipid peroxidation, total oxidative and antioxidative status of cells and oxidative DNA damage. All kinds of AgNPs showed strong cytotoxic activity at low concentrations (2÷13 μg/ml), and caused an overproduction of reactive oxygen species (ROS) at concentrations lower than cytotoxic ones. The ROS being formed in the cells induced oxidative damage of DNA in alkaline comet assay. The most toxic was AgNPs<10 nm. The results indicate that the silver nanoparticles, especially less than 10 nm, may be harmful to the organisms. Therefore, risk should be considered when using nanosilver preparations and provide appropriate protective measures when they are applied.

PL

Nanocząstki srebra (AgNPs), ze względu na silne właściwości bakteriobójcze, mają szerokie zastosowanie w wielu dziedzinach przemysłu, biomedycynie i produktach konsumenckich. Rozmiar cząstek jest istotnym, ale wciąż niewystarczająco zbadanym parametrem wpływającym na toksyczność nanosrebra. W pracy oceniono toksyczne działanie różnej wielkości cząstek srebra (~ 10, 40 i 100 nm) na komórki układu rozrodczego i oddechowego (CHO-9, 15P-1 i RAW264.7). Badano wpływ AgNPs na przeżywalność komórek, przepuszczalność błon komórkowych i aktywność metaboliczną komórek, zaburzenia metabolizmu tlenowego oraz odległe skutki działania w postaci uszkodzeń materiału genetycznego (DNA). Wszystkie badane AgNPs wykazywały silne działanie cytotoksyczne, w zakresie niskich stężeń (2÷13 μg/ml) oraz powodowały powstawanie stresu oksydacyjnego w komórkach w stężeniach niższych niż cytotoksyczne. Powstające w komórkach reaktywne formy tlenu powodowały oksydacyjne uszkodzenia DNA wykrywane w teście kometowym. Najsilniejsze działanie wykazywały cząstki o wielkości < 10 nm. Otrzymane wyniki wskazują, że nanocząstki srebra, zwłaszcza poniżej 10 nm, mogą stanowić zagrożenie dla organizmów. Dlatego też należy rozważyć ryzyko stosowania preparatów z nanosrebrem i zapewnić środki zapobiegające ich niekontrolowanemu uwalnianiu.

Słowa kluczowe

EN

silver nanoparticles; cytotoxicity; reactive oxygen species; DNA damage

PL

nanocząstki srebra; cytotoksyczność; reaktywne formy tlenu; uszkodzenia DNA

• Wydawca: Institute of Environmental Engineering, Polish Academy of Sciences
• Czasopismo: Archives of Environmental Protection
• Rocznik: 2016
• Tom: Vol. 42, no. 4
• Strony: 32--47
• Opis fizyczny: Bibliogr. 69 poz., wykr.

Twórcy

autor

Zapór L.

• Central Institute for Labour Protection – National Research Institute, Poland

Bibliografia

• [1]. Arora, S., Jain, J., Rajwade, J.M. & Paknikar, K. (2008). Cellular responses induced by silver nanoparticles: in vitro studies, Toxicology Letters, 179, pp. 93-100. doi:
• [2]. Arora, S., Jain, J., Rajwade, J.M. & Paknikar, K. (2009). Interactions of silver nanoparticles with primary mouse fibroblasts and liver cells, Toxicology and Applied Pharmacology, 236, pp. 310-318.
• [3]. Asare, N., Instanes, C., Sandberg, W.J., Refsnes, M., Schwarze, P., Kruszewski, M. & Brunborg, G. (2012). Cytotoxic and genotoxic effects of silver nanoparticles in testicular cells, Toxicology, 291, pp. 65-72.
• [4]. Asharani, P.V., Mun, G.L.K., Hande, M.P. & Valiyaveettil, S. (2009). Cytotoxicity and genotoxicity of silver nanoparticles in human cells, ACS Nano, 3, pp. 279-290.
• [5]. Barillet, S., Simon-Deckers, A., Herlin-Boime, N., Mayene-L’Hermite, M., Reynaud, C., Cassio, D., Gouget, B. & Carriere, M. (2010). Toxicological consequences of TiO2, SiC nanoparticles and multiwalled carbon nanotubes exposure in several mammalian cell types: an in vitro study, Journal of Nanoparticle Research, 12, pp. 61-73.
• [6]. Beer, C., Foldbjerg, R., Hayashi, Y., Sutherland, D.S. & Autrup, H. (2012). Toxicity of silver nanoparticles - nanoparticle or silver ion? Toxicology Letters, 208, 3, pp. 286-292.
• [7]. Bihari, P., Vippola, M., Schultes, S., Praetner, M., Khandoga, A.G., Reichel, C.A., Coester, C., Tuomi, T., Rehberg, M. & Krombach, F. (2008). Optimized dispersion of nanoparticles for biological in vitro and in vivo studies, Particle and Fibre Toxicology, 5, 14.
• [8]. Carlson, C., Hussain, S.M., Schrand, A.M., Braydich-Stolle, L.K., Hess, K.L., Jones, R.L. & Schlager, J.J. (2008). Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species, The Journal of Physical Chemistry B, 112, pp. 13608-13619.
• [9]. Choi, O. & Hu, Z. (2008). Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria, Environmental Science & Technology, 42, pp. 4583-4588.
• [10]. Colman, B.P., Arnaout, C.L., Anciaux, S., Gunsch, C.K., Hochella, M.F., Kim, B., Lowry, G.V., McGill, B.M., Reinsch, B.C., Richardson, C.J., Unrine, J.M., Wright, J.P., Yin, L. & Bernhardt, E.S. (2013). Low concentrations of silver nanoparticles in biosolids cause adverse ecosystem responses under realistic field scenario, PLOS ONE, 8(2): e57189.
• [11]. Commission Staff Working Paper: Types and uses of nanomaterials, including safety aspects. Accompanying the Communication from the Commission to the European Parliament, the Council and the European Economic and Social Committee on the Second Regulatory Review on Nanomaterials., Brussels, 3.10.2012, SWD(2012) 288 fi nal (http://ec.europa.eu/health/nanotechnology/docs/swd_2012_288_en.pdf. (27.02. 2015)).
• [12]. Cronholm, P., Karlsson, H.L., Hedberg, J., Lowe, T.A, Winnberg, L., Elihn, K., Wallinder, I.O. & Möller, L. (2013). Intracellular uptake and toxicity of Ag and CuO nanoparticles: a comparison between nanoparticles and their corresponding metal ions, Small, 9, 7, pp. 970-82.
• [13]. Dopp, E., Hartmann, L.M., Florea, A.M., von Recklinghausen, U., Pieper, R., Shokouhi, B., Rettenmeier, A.W., Hirner, A.V. & Obe, G. (2004). Uptake of inorganic and organic derivatives of arsenic associated with induced cytotoxic and genotoxic effects in Chinese hamster ovary (CHO) cells, Toxicology and Applied Pharmacology, 1, 201(2), pp. 156-165.
• [14]. EPA, The Danish Environmental Protection Agency (2015). Exposure assessment of nanomaterials in consumer products. Environmental project No. 1636, (http://www2.mst.dk/Udgiv/publications/2015/01/978-87-93283-57-2.pdf (6.07.2015)).
• [15]. Fabrega, J., Luoma, S.N., Tyler, Ch.R., Galloway, T.S. & Lead, J.R. (2011). Silver nanoparticles: Behaviour and effects in the aquatic environment, Environment International, 37, pp. 517-531.
• [16]. Gao, J., Sepúlved, M.S., Klinkhamer, C., Wei, A., Gao, Y. & Mahapatra, C.T. (2015). Nanosilver-coated socks and their toxicity to zebrafish (Danio rerio) embryos, Chemosphere, 119, pp. 948-952.
• [17]. George, S., Lin, S., Ji, Z., Thomas, C.R., Li, L., Mecklenburg, M., Meng, H., Wang, X., Zhang, H., Xia, T., Hohman, J.N., Lin, S., Zink, J.I., Weiss, P.S. & Nel, A.E. (2012). Surface defects on plate-shaped silver nanoparticles contribute to its hazard potential in a fish gill cell line and zebrafi sh embryos, ACS Nano, 6(5) pp. 3745-3759.
• [18]. Gliga, A.R., Skoglund, S., Wallinder, I.O., Fadeel, B. & Karlsson, H.L. (2014). Size-dependent cytotoxicity of silver nanoparticles in human lung cells: the role of cellular uptake, agglomeration and Ag release, Particle and Fibre Toxicology, 11, pp. 11.
• [19]. Gosens, I., Post, J.A., de la Fonteyne, L.J., Jansen, E.H., Geus, J.W., Cassee, F.R. & de Jong, W.H. (2010). Impact of agglomeration state of nano- and submicron sized gold particles on pulmonary inflammation, Particle and Fibre Toxicology, 7, 37.
• [20]. Gottschalk, F. & Nowack, B. (2011). The release of engineered nanomaterials to the environment, Journal of Environmental Monitoring, 13 (5), pp. 1145-1155.
• [21]. Hussain, S.M., Hess, K.L., Gearhart, J.M., Geiss, K,T. & Schlager, J.J. (2005). In vitro toxicity of nanoparticles in BRL 3A rat liver cells, Toxicology in Vitro, 19, pp. 975-983.
• [22]. Impellitteri, C.A., Harmon, S., Silva, R.G., Miller, B.W., Scheckel, K.G., Luxton, T.P., Schupp, D. & Panguluri, S. (2013). Transformation of silver nanoparticles in fresh, aged, and incinerated biosolids, Water Research, 4, 7, pp. 3878-3886.
• [23]. INVITTOX Protocol No 17: MTT Assay (1990) The ERGATT/ FRAME Data Bank of In Vitro Techniques in Toxicology, Nottingham, 1990.
• [24]. INVITTOX Protocol No 64: The Neutral Red Cytotoxicity Assay (1992) The ERGATT/FRAME Data Bank of In Vitro Techniques in Toxicology, Nottingham, 1992.
• [25]. Jankowska, E. & Łukaszewska, J. (2013). Potential exposure to silver nanoparticles during spraying pereparation for air-conditioning cleaning, Medycyna Pracy, 64 (1), pp. 57-67. (in polish)
• [26]. Jiao, Z-H., Li, M., Feng, Y-X., Shi, J-Ch., Zhang, J. & Shao, B. (2014). Hormesis effects of silver nanoparticles at non-cytotoxic doses to human hepatoma cells, PLoS ONE, 9(7): e102564.
• [27]. Jingkun, J., Oberdorster, G. & Pratim, B. (2009). Characterization of size, surface charge, and agglomeration state of nanoparticle dispersions for toxicological studies, Journal of Nanoparticles Research, 11, pp. 77-89.
• [28]. Johari, S.A., Kalbassi, M.R., Soltani, M. & Yu, I.J. (2013). Toxicity comparison of colloidal silver nanoparticles in various life stages of rainbow trout (Oncorhynchus mykiss), Iranian Journal of Fisheries Sciences, 12 (1), pp. 76-95.
• [29]. Kaegi, R., Voegelin, A., Ort, Ch., Sinnet, B., Thalmann, B., Krismer, J., Hagendorfer, H., Elumelu, M. & Mueller, E. (2013). Fate and transformation of silver nanoparticles in urban wastewater systems, Water Research, 47 (12), pp. 3866-3877.
• [30]. Kaegi, R., Voegelin, A., Sinnet, B., Zuleeg, S., Hagendorfer, H., Burkhardt, M. & Siegrist, H. (2011). Behavior of metallic silver nanoparticles in a pilot wastewater treatment plant, Environmental Science & Technology, 45 (9), pp. 3902-3908.
• [31]. Karlsson, H.L. (2010). The comet assay in nanotoxicology research, Analytical and Bioanalytical Chemistry, 398(2), pp. 651-666.
• [32]. Kim, B., Park, C.S., Murayama, M. & Hochella, M.F. (2010). Discovery and characterization of silver sulfi de nanoparticles in final sewage sludge products, Environmental Science & Technology, 44 (19), pp. 7509-7514.
• [33]. Kim, S., Choi, J.E., Chung, K.-H., Park, K., Yi, J. & Ryu, D.-Y. (2009). Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells, Toxicology In Vitro, 23, pp. 1076-1084.
• [34]. Kim, T.H., Kim, M., Park, H.S., Shin, U.S., Gong, M.S. & Kim, H.W. (2012). Size-dependent cellular toxicity of silver nanoparticles, Journal of Biomedical Materials Research A, 100, pp. 1033-1043.
• [35]. Kim, Y.-J., Yang, S.I. & Ryu, J.-Ch. (2010). Cytotoxicity and genotoxicity of nano-silver in mammalian cell lines, Molecular and Cellular Toxicology, 6(2), pp. 119-125.
• [36]. Kittler, S., Greulich, C., Diendorf, J., Koller, M. & Epple, M. (2010). Toxicity of silver nanoparticles increases during storage because of slow dissolution under release of silver ions, Chemistry of Materials, 22, pp. 4548-4554.
• [37]. Kruszewski, M., Grądzka, I., Bartłomiejczyk, T., Chwastowska, J., Sommer, S., Grzelak, A., Zuberek, M., Lankoff, A., Dusinska, M. & Wojewodzka, M. (2013). Oxidative DNA damage corresponds to the long term survival of human cells treated with silver nanoparticles, Toxicology Letters, 219, pp. 151-159.
• [38]. Lankoff, A., Sandberg, W.J., Wegierek-Ciuk, A., Lisowska, H., Refsnes, M., Sartowska, B., Schwarze, P.E., Meczynska- -Wielgosz, S., Wojewodzka, M. & Kruszewski, M. (2012). The effect of agglomeration state of silver and titanium dioxide nanoparticles on cellular response of HepG2, A549 and THP-1 cells, Toxicology Letters, 208, pp. 197-213.
• [39]. Levard, C., Reinsch, B.C., Michel, F.M., Oumahi, C., Lowry, G.V. & Brown, G.E. (2011). Sulfi dation processes of PVP-coated silver nanoparticles in aqueous solution: impact on dissolution rate, Environmental Science & Technology, 45, pp. 5260-5266.
• [40]. Levard, C., Hotze, E.M., Colman, B.P., Dale, A.L., Truong, L., Yang, X.Y., Bone, A.J., Brown, G.E., Tanguay, R.L., Di Giulio, R.T., Bernhardt, E.S., Meyer, J.N., Wiesner, M.R. & Lowry, G.V. (2013). Sulfidation of silver nanoparticles: natural antidote to their toxicity, Environmental Science & Technology, 47(23), pp. 13440-13448.
• [41]. Lison, D., Thomassen, L.C., Rabolli, V., Gonzalez, L., Napierska, D., Seo, J.W., Kirsch-Volders, M., Hoet, P., Kirschhock, C.E. & Martens, J.A. (2008). Nominal and effective dosimetry of silica nanoparticles in cytotoxicity assays, Toxicological Sciences, 104, pp. 155-162.
• [42]. Liu, W., Wu, Y., Wang, C., Li, H.C., Wang, T., Liao, C.Y., Cui, L., Zhou, Q.F., Yan, B. & Jiang, G.B. (2010). Impact of silver nanoparticles on human cells: effect of particle size, Nanotoxicology, 4(3), pp. 319-330.
• [43]. Luoma, S.N. (2008). Silver nanotechnologies and the environment: old problems or new challenges? PEN 15. The Project on Emerging nanotechnologies. (http://www.nanotechproject.org (27.02.2015)).
• [44]. Manke, A., Wang, L. & Rojanasakul, Y. (2013). Mechanisms of nanoparticle-induced oxidative stress and toxicity, BioMed Research International, 2013, 20, ID 942916. http://dx.doi. org/10.1155/2013/942916.
• [45]. Marambio-Jones, C. & Hoek, E.M. (2010). A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment, Journal of Nanoparticles Research, 12, pp. 1531-1551. Doi: 10.1007/s11051-010-9900-y.
• [46]. Miethling-Graff, R., Rumpker, R., Richter, M., Verano-Braga, T., Kjeldsen, F., Brewer, J., Hoyland, J., Rubahn, H.-G. & Erdmann, H. (2014). Exposure to silver nanoparticles induces size- and dose-dependent oxidative stress and cytotoxicity in human colon carcinoma cells, Toxicology in Vitro, 28, pp.1280-1289.
• [47]. Moaddab, S., Ahari, H., Shahbazzadeh, D., Motallebi, A.A., Anvar, A.A., Rahman-Nya,. J. & Shokrgozar, M.R. (2011).Toxicity study of nanosilver (nanocid) on osteoblast cancer cell line, International Nano Letters, 1, pp. 11-16.
• [48]. Montes-Burgos, I., Walczyk, D., Hole, P., Smith, J., Lynch, I. & Dawson, K. (2010). Characterisation of nanoparticle size and state prior to nanotoxicological studies, Journal of Nanoparticles Research, 12, pp. 47-53.
• [49]. Mukherjee, S.G., O’Claonadh, N., Casey, A. & Chambers, G. (2012). Comparative in vitro cytotoxicity study of silver nanoparticle on two mammalian cell lines, Toxicology iv Vitro, 26, pp. 238-251.
• [50]. Murdock, R.C., Braydich-Stolle, L., Schrand, A.M., Schlager, J.J. & Hussain, S.M. (2008). Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique, Toxicological Sciences, 101, pp. 239-253.
• [51]. Park, E.J., Yi ,J., Kim, Y., Choi, K. & Park, K. (2010). Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism, Toxicology In Vitro, 24, pp. 872-878.
• [52]. Park, M.V., Neigh, A.M., Vermeulen, J.P., de la Fonteyne, L.J., Verharen, H.W., Briede, J.J., Van, L.H. & De Jong, W.H. (2011). The effect of particle size on the cytotoxicity, inflammation, developmental toxicity and genotoxicity of silver nanoparticles, Biomaterials, 32, pp. 9810-9817.
• [53]. Samberg, M.E, Loboa, E.G., Oldenburg, S.J & Monteiro-Riviere, N.A. (2012). Silver nanoparticles do not influence stem cell differentiation but cause minimal toxicity, Nanomedicine, 7(8), pp. 1197-1209.
• [54]. Samberg, M.E, Oldenburg, S.J. & Monteiro-Riviere, N.A. (2010). Evaluation of silver nanoparticle toxicity in skin in vivo and keratinocytes in vitro, Environmental Health Perspectives, 118(3), pp. 407-413.
• [55]. SCENIHR (Scientific Committee on Emerging and Newly Identified Health Risks), 2014. Nanosilver: safety, health and environmental effects and role in antimicrobial resistance. (http://ec.europa.eu/health/scientific_committees/emerging/docs/scenihr_o_039.pdf (03.07.2015)).
• [56]. Schlich, K., Klawonn, T., Terytze, K. & Hund-Rinke, K. (2013). Hazard assessment of a silver nanoparticle in soil applied via sewage sludge, Environmental Sciences Europe, 25: 17.
• [57]. Senjen, R., FoE Australia & Ian Illuminato, FoE U.S (2009). Nano and Biocidal Silver. Extreme germ killers present a growing threat to public health. Nanosilver Report, Health Care Without Harm Europe (HCWHE) (http://www.shrimpnews.com/PDFsFolder/VietnamNanoSilverSolutions.pdf (27.02.2015)).
• [58]. Sheehy, K., Casey, A., Murphy, A. & Chambers, G. (2015). Antimicrobial properties of nano-silver: A cautionary approach to ionic interference, Journal of Colloid and Interface Science, 443, pp. 56-64.
• [59]. SIGMA, (http://www.sigmaaldrich.com/materials-science/nanomaterials/silver-nanoparticles.html#sthash.GcKXIXiP.dpuf (08.09.2016)).
• [60]. Singh, R.P. & Ramaro, P. (2012). Cellular uptake, intracellular trafficking and cytotoxicity of silver nanoparticles, Toxicology Letters, 213(2), pp. 249-259.
• [61]. Sohaebuddin, S.K., Thevenot, P.T., Baker, D., Eaton, J.W. & Tang, L. (2010). Nanomaterial cytotoxicity is composition, size, and cell type dependent, Particle and Fibre Toxicology, 21, pp. 7-22.
• [62]. Sohn, E.K., Johari, S.A., Kim, T.G., Kim, J.K., Kim, E., Lee, J.H., Chung, Y.S. & Yu, I.J. (2015). Aquatic toxicity comparison of silver nanoparticles and silver nanowires, BioMed Research International, 2015: 893049.
• [63]. Teeguarden, G., Hinderliter, P.M., Orr, G., Thrall, B.D. & Pounds, J.G. (2007). Particokinetics in vitro: dosimetry considerations for in vitro nanoparticle toxicity assessments, Toxicological Sciences, 95, pp. 300-312.
• [64]. Verano-Braga, T., Miethling-Graff, R., Wojdyla, K., Rogowska-Wrzesinska, A., Brewer, J.R., Erdmann, H. & Kjeldsen, F. (2014). Insights into the cellular response triggered by silver nanoparticles using quantitative proteomics, ACS Nano, 8 (3), pp. 2161-2175.
• [65]. Vippola, M., Falc, G.C.M., Lindberg, H.K., Suhonen, S., Vanhala, E., Norppa, H., Savolainen, K., Tossavainen, A. & Tuomi, T. (2009). Preparation of nanoparticle dispersions for in-vitro toxicity testing, Human and Experimental Toxicology, 28, pp. 377-385.
• [66]. Wang, H., Wu, L. & Reinhard, B.M. (2012). Scavenger receptor mediated endocytosis of silver nanoparticles into J774A.1 macrophages is heterogeneous, ACS Nano, 6(8), pp. 7122-7132.
• [67]. Wang, X., Ji Z., Chang, C.H., Zhang, H., Wang, M., Liao, Y.P., Lin, S., Meng, H., Li, R., Sun, B., Van Winkle, L., Pinkerton, K.E., Zink, J.I., Xia, T. & Nel, A.E. (2014). Use of coated silver nanoparticles to understand the relationship of particle dissolution and bioavailability to cell and lung toxicological potential, Small, 29(10), pp. 389-398.
• [68]. Wijnhoven, S.W.P., Peijnenburg, W.J.G.M., Herberts, C.A., Hagens, W.I., Oomen, A.G., Heugens, E.H.W., Roszek, B., Bisschops, J., Gosens, I., van de Meent, D., Dekkers, S., de Jong, W.H., van Zijverden, M., Sips, A.J.A.M. & Geertsma, R.E. (2009). Nano-silver - a review of available data and knowledge gaps in human and environmental risk assessment, Nanotoxicology, 3, pp. 109-138.
• [69]. Wojewodzka, M., Kruszewski, M., Iwanenko, T., Collins, A.R. & Szumiel, I. (1998). Application of the comet assay for monitoring DNA damage in workers exposed to chronic low-dose irradiation. I. Strand breakage, Mutation Research, 416, pp. 21-35.

Uwagi

Opracowanie ze środków MNiSW w ramach umowy 812/P-DUN/2016 na działalność upowszechniającą naukę.