Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review

Olesja Bondarenko, Katre Juganson, Angela Ivask, Kaja Kasemets, Monika Mortimer, Anne Kahru, Olesja Bondarenko, Katre Juganson, Angela Ivask, Kaja Kasemets, Monika Mortimer, Anne Kahru

Abstract

Nanoparticles (NPs) of copper oxide (CuO), zinc oxide (ZnO) and especially nanosilver are intentionally used to fight the undesirable growth of bacteria, fungi and algae. Release of these NPs from consumer and household products into waste streams and further into the environment may, however, pose threat to the 'non-target' organisms, such as natural microbes and aquatic organisms. This review summarizes the recent research on (eco)toxicity of silver (Ag), CuO and ZnO NPs. Organism-wise it focuses on key test species used for the analysis of ecotoxicological hazard. For comparison, the toxic effects of studied NPs toward mammalian cells in vitro were addressed. Altogether 317 L(E)C50 or minimal inhibitory concentrations (MIC) values were obtained for algae, crustaceans, fish, bacteria, yeast, nematodes, protozoa and mammalian cell lines. As a rule, crustaceans, algae and fish proved most sensitive to the studied NPs. The median L(E)C50 values of Ag NPs, CuO NPs and ZnO NPs (mg/L) were 0.01, 2.1 and 2.3 for crustaceans; 0.36, 2.8 and 0.08 for algae; and 1.36, 100 and 3.0 for fish, respectively. Surprisingly, the NPs were less toxic to bacteria than to aquatic organisms: the median MIC values for bacteria were 7.1, 200 and 500 mg/L for Ag, CuO and ZnO NPs, respectively. In comparison, the respective median L(E)C50 values for mammalian cells were 11.3, 25 and 43 mg/L. Thus, the toxic range of all the three metal-containing NPs to target- and non-target organisms overlaps, indicating that the leaching of biocidal NPs from consumer products should be addressed.

Figures

Fig. 1
Fig. 1
Schematic representation of the scope of the current review
Fig. 2
Fig. 2
a Annual production volumes of nanomaterials (data are adapted from Piccinno et al. 2012). bd Fields of application of Ag (b), CuO (c) and ZnO (d) nanoparticles based on the publications indexed by Thomson Reuters ISI Web of Science. Search was done in March 2013. The following search terms were used: ‘silver’ OR ‘CuO’ OR ‘ZnO’ AND ‘nano*’ AND ‘application category’ (indicated in the figure). Numbers next to each application category indicate the number of articles retrieved and their respective percent share. The numerical data are presented in Supplementary Table S1
Fig. 3
Fig. 3
a Labels of bulk CuO and nanosized CuO. Note the same CAS number. b 200 mg/L stock suspensions of CuO. c TEM image of nano CuO and bulk CuO. Note 43-fold difference in the SSAs of bulk CuO and nanosized CuO
Fig. 4
Fig. 4
Uncoated Ag (50 mg/L), PVP-coated Ag (50 mg/L), uncoated CuO (50 mg/L) and ZnO NPs (200 mg/L) after 0, 2 and 24 h incubation in different (eco)toxicological test environments: 1 deionized water; 2 artificial freshwater for the tests with Daphnia sp. (OECD 202); 3 AFW for Thamnocephalus sp. (Thamnotoxkit F™ 1995); 4 algal growth medium (OECD 201); 5 protozoan mineral test medium (Osterhout’s); 6 yeast extract peptone dextrose medium; 7 bacterial M9 medium supplemented with 0.1 % glucose and 0.5 % amino acids; 8 bacterial LB medium containing tryptone and yeast extract. Detailed composition of test media is given in Käkinen et al. (2011)
Fig. 5
Fig. 5
Number and share of individual L(E)C50 or MIC values used to derive the median L(E)C50 or MIC for nanoparticles (a) and metal salts (b). Total number of individual values: 317
Fig. 6
Fig. 6
Toxicity of CuO, ZnO and Ag nanoparticles to different organisms. Median L(E)C50 values for all other organisms except bacteria and MIC for bacteria ± minimum and maximum values are presented. Different organisms/cells are shown by respective pictograms and the number on the pictogram indicates the number of L(E)C50 values used to derive the median value. Note the logarithmic scale of x-axis and that L(E)C50 and MIC values of NPs reflect nominal concentrations. The classification to hazard categories is explained in Table 1
Fig. 7
Fig. 7
Plots of the median L(E)C50 values of Ag, CuO and ZnO NPs versus the median L(E)C50 values of the respective soluble metal salts to different organism groups. Data are plotted from Table 1
Fig. 8
Fig. 8
Variation in individual L(E)C50 or MIC values used to derive the median L(E)C50 or MIC value for mammalian cells in vitro (a) and bacteria (b)
Fig. 9
Fig. 9
L(E)C50 values of PVP-coated Ag NPs to mammalian cells versus size of nanoparticles. a All collected data were used; b data from one article (Liu et al. 2010) were used; c data from one article for one cell type were used (Liu et al. 2010)

References

    1. Ahamed M, Siddiqui MA, Akhtar MJ, Ahmad I, Pant AB, Alhadlaq HA. Genotoxic potential of copper oxide nanoparticles in human lung epithelial cells. Biochem Biophys Res Commun. 2010;396(2):578–583. doi: 10.1016/j.bbrc.2010.04.156.
    1. Albers CE, Hofstetter W, Siebenrock K, Landmann R, Klenke F. Cytotoxic effects of ionic silver and silver nano-particles on osteoblasts and osteoclasts in vitro. J Bone Joint Surg Br. 2012;94-B((SUPP 37):163.
    1. Alsop D, Wood CM. Metal uptake and acute toxicity in zebrafish: common mechanisms across multiple metals. Aquat Toxicol. 2011;105(3–4):385–393. doi: 10.1016/j.aquatox.2011.07.010.
    1. Ansari M, Khan H, Khan A, Sultan A, Azam A. Characterization of clinical strains of MSSA, MRSA and MRSE isolated from skin and soft tissue infections and the antibacterial activity of ZnO nanoparticles. World J Microb Biot. 2012;28(4):1605–1613. doi: 10.1007/s11274-011-0966-1.
    1. Apte SC, Batley GE, Bowles KC, Brown PL, Creighton NM, Hales LT, Hyne RV, Julli M, Markich SJ, Pablo F, Rogers NJ, Stauber JL, Wilde K. A comparison of copper speciation measurements with the toxic responses of three sensitive freshwater organisms. Environ Chem. 2005;2(4):320–330. doi: 10.1071/EN05048.
    1. Aruoja V, Dubourguier HC, Kasemets K, Kahru A. Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Sci Total Environ. 2009;407(4):1461–1468. doi: 10.1016/j.scitotenv.2008.10.053.
    1. Baker J, Sitthisak S, Sengupta M, Johnson M, Jayaswal RK, Morrissey JA. Copper stress induces a global stress response in Staphylococcus aureus and represses sae and agr expression and biofilm formation. Appl Environ Microb. 2010;76(1):150–160. doi: 10.1128/AEM.02268-09.
    1. Bandyopadhyay S, Peralta-Videa JR, Hernandez-Viezcas JA, Montes MO, Keller AA, Gardea-Torresdey JL. Microscopic and spectroscopic methods applied to the measurements of nanoparticles in the environment. Appl Spectrosc Rev. 2012;47(3):180–206. doi: 10.1080/05704928.2011.637186.
    1. Bao VW, Leung KM, Qiu JW, Lam MH. Acute toxicities of five commonly used antifouling booster biocides to selected subtropical and cosmopolitan marine species. Mar Pollut Bull. 2011;62(5):1147–1151. doi: 10.1016/j.marpolbul.2011.02.041.
    1. Bayat N, Rajapakse K, Marinsek-Logar R, Drobne D, Cristobal S. The effects of engineered nanoparticles on the cellular structure and growth of Saccharomyces cerevisiae. Nanotoxicology. 2013
    1. Binaeian E, Rashidi AM, Attar H. Toxicity study of two different synthesized silver nanoparticles on bacteria Vibrio fischeri. WASET. 2012;67:1219–1225.
    1. Blaise C, Gagné F, Férard JF, Eullaffroy P. Ecotoxicity of selected nano-materials to aquatic organisms. Environ Toxicol. 2008;23(5):591–598. doi: 10.1002/tox.20402.
    1. Blinova I, Ivask A, Heinlaan M, Mortimer M, Kahru A. Ecotoxicity of nanoparticles of CuO and ZnO in natural water. Environ Pollut. 2010;158(1):41–47. doi: 10.1016/j.envpol.2009.08.017.
    1. Blinova I, Niskanen J, Kajankari P, Kanarbik L, Käkinen A, Tenhu H, Penttinen OP, Kahru A. Toxicity of two types of silver nanoparticles to aquatic crustaceans Daphnia magna and Thamnocephalus platyurus. Environ Sci Pollut Res Int. 2012
    1. Böhmert L, Niemann B, Thünemann AF, Lampen A. Cytotoxicity of peptide-coated silver nanoparticles on the human intestinal cell line Caco-2. Arch Toxicol. 2012;86(7):1107–1115. doi: 10.1007/s00204-012-0840-4.
    1. Bondarenko O, Ivask A, Käkinen A, Kahru A. Sub-toxic effects of CuO nanoparticles on bacteria: kinetics, role of Cu ions and possible mechanisms of action. Environ Pollut. 2012;169:81–89. doi: 10.1016/j.envpol.2012.05.009.
    1. Borkow G, Gabbay J. Putting copper into action: copper-impregnated products with potent biocidal activities. FASEB J. 2004;18(14):1728–1730.
    1. Borkow G, Zatcoff RC, Gabbay J. Reducing the risk of skin pathologies in diabetics by using copper impregnated socks. Med Hypotheses. 2009;73(6):883–886. doi: 10.1016/j.mehy.2009.02.050.
    1. Borkow G, Gabbay J, Dardik R, Eidelman AI, Lavie Y, Grunfeld Y, Ikher S, Huszar M, Zatcoff RC, Marikovsky M. Molecular mechanisms of enhanced wound healing by copper oxide-impregnated dressings. Wound Repair Regen. 2010;18(2):266–275. doi: 10.1111/j.1524-475X.2010.00573.x.
    1. Borkow G, Zhou SS, Page T, Gabbay J. A novel anti-influenza copper oxide containing respiratory face mask. PLoS ONE. 2010;5(6):e11295. doi: 10.1371/journal.pone.0011295.
    1. Borovanský J, Riley PA. Cytotoxicity of zinc in vitro. Chem Biol Interact. 1989;69(2–3):279–291. doi: 10.1016/0009-2797(89)90085-9.
    1. Brandt O, Mildner M, Egger AE, Groessl M, Rix U, Posch M, Keppler BK, Strupp C, Mueller B, Stingl G. Nanoscalic silver possesses broad-spectrum antimicrobial activities and exhibits fewer toxicological side effects than silver sulfadiazine. Nanomedicine. 2012;8(4):478–488. doi: 10.1016/j.nano.2011.07.005.
    1. Bystrzejewska-Piotrowska G, Golimowski J, Urban PL. Nanoparticles: their potential toxicity, waste and environmental management. Waste Manag. 2009;29(9):2587–2595. doi: 10.1016/j.wasman.2009.04.001.
    1. Calafato S, Swain S, Hughes S, Kille P, Stürzenbaum SR. Knock down of Caenorhabditis eleganscutc-1 exacerbates the sensitivity toward high levels of copper. Toxicol Sci. 2008;106(2):384–391. doi: 10.1093/toxsci/kfn180.
    1. Cao B, Zheng Y, Xi T, Zhang C, Song W, Burugapalli K, Yang H, Ma Y. Concentration-dependent cytotoxicity of copper ions on mouse fibroblasts in vitro: effects of copper ion release from TCu380A vs TCu220C intra-uterine devices. Biomed Microdevices. 2012;14(4):709–720. doi: 10.1007/s10544-012-9651-x.
    1. Carnes LC, Klabunde KJ. The catalytic methanol synthesis over nanoparticle metal oxide catalysts. J Mol Catal A Chem. 2003;194(1–2):227–236. doi: 10.1016/S1381-1169(02)00525-3.
    1. Casals E, Gonzalez E, Puntes VF. Reactivity of inorganic nanoparticles in biological environments: insights into nanotoxicity mechanisms. J Phys D Appl Phys. 2012;45(44):443001. doi: 10.1088/0022-3727/45/44/443001.
    1. CEC (1996) CEC (Commission of the European Communities) technical guidance document in support of commission directive 93/67/EEC on risk assessment for new notified substances. Part II, Environmental Risk Assessment. Office for official publications of the European Communities, Luxembourg
    1. Cerkez I, Kocer HB, Worley SD, Broughton RM, Huang TS. Multifunctional cotton fabric: antimicrobial and durable press. J Appl Polym Sc. 2012;124(5):4230–4238. doi: 10.1002/app.35402.
    1. Chae YJ, Pham CH, Lee J, Bae E, Yi J, Gu MB. Evaluation of the toxic impact of silver nanoparticles on Japanese medaka (Oryzias latipes) Aquat Toxicol. 2009;94(4):320–327. doi: 10.1016/j.aquatox.2009.07.019.
    1. Chen X, Shi J, Chen Y, Xu X, Xu S, Wang Y. Tolerance and biosorption of copper and zinc by Pseudomonas putida CZ1 isolated from metal-polluted soil. Can J Microbiol. 2006;52(4):308–316. doi: 10.1139/w05-157.
    1. Chen QL, Luo Z, Liu X, Song YF, Liu CX, Zheng JL, Zhao YH. Effects of waterborne chronic copper exposure on hepatic lipid metabolism and metal-element composition in Synechogobius hasta. Arch Environ Contam Toxicol. 2010;73:1286–1291.
    1. Chernousova S, Epple M. Silver as antibacterial agent: ion, nanoparticle, metal. Angew Chem. 2013
    1. Cho K-H, Park J-E, Osaka T, Park S-G. The study of antimicrobial activity and preservative effects of nanosilver ingredient. Electrochim Acta. 2005;51(5):956–960. doi: 10.1016/j.electacta.2005.04.071.
    1. Contreras RG, Sakagami H, Nakajima H, Shimada J. Type of cell death induced by various metal cations in cultured human gingival fibroblasts. In Vivo. 2010;24(4):513–517.
    1. Crane M, Handy RD, Garrod J, Owen R. Ecotoxicity test methods and environmental hazard assessment for engineered nanoparticles. Ecotoxicology. 2008;17(5):421–437. doi: 10.1007/s10646-008-0215-z.
    1. Dastjerdi R, Montazer M. A review on the application of inorganic nano-structured materials in the modification of textiles: focus on anti-microbial properties. Colloid Surf B. 2010;79(1):5–18. doi: 10.1016/j.colsurfb.2010.03.029.
    1. De Boeck G, Meeus W, De Coen W, Blust R. Tissue-specific Cu bioaccumulation patterns and differences in sensitivity to waterborne Cu in three freshwater fish: rainbow trout (Oncorhynchus mykiss), common carp (Cyprinus carpio), and gibel carp (Carassius auratus gibelio) Aquat Toxicol. 2004;70(3):179–188. doi: 10.1016/j.aquatox.2004.07.001.
    1. de Oliveira-Filho EC, Lopes RM, Paumgartten FJ. Comparative study on the susceptibility of freshwater species to copper-based pesticides. Chemosphere. 2004;56(4):369–374. doi: 10.1016/j.chemosphere.2004.04.026.
    1. Debabrata D, Giasuddin A. Cellular responses of Saccharomyces cerevisiae to silver nanoparticles. Res J Biotech. 2013;8(1):11.
    1. Dechsakulthorn F, Hayes A, Bakand S, Joeng L, Winder C. In vitro cytotoxicity assessment of selected nanoparticles using human skin fibroblasts. AATEX. 2007;14(Special Issue):397–400.
    1. Dimkpa CO, Calder A, Britt DW, McLean JE, Anderson AJ. Responses of a soil bacterium, Pseudomonas chlororaphis O6 to commercial metal oxide nanoparticles compared with responses to metal ions. Environ Pollut. 2011;159(7):1749–1756. doi: 10.1016/j.envpol.2011.04.020.
    1. Dua P, Chaudhari KN, Lee CH, Chaudhari NK, Hong SW, Yu JS, Kim S, Lee D. Evaluation of toxicity and gene expression changes triggered by oxide nanoparticles. Bull Korean Chem Soc. 2011;2(6):2051.
    1. Ebrahimnia-Bajestan E, Niazmand H, Duangthongsuk W, Wongwises S. Numerical investigation of effective parameters in convective heat transfer of nanofluids flowing under a laminar flow regime. Int J Heat Mass Transf. 2011;54(19–20):4376–4388. doi: 10.1016/j.ijheatmasstransfer.2011.05.006.
    1. Ebrahimpour M, Alipour H, Rakhshah S. Influence of water hardness on acute toxicity of copper and zinc on fish. Toxicol Ind Health. 2010;26(6):361–365. doi: 10.1177/0748233710369123.
    1. EC (2008) Follow-up to the 6th Meeting of the REACH Competent Authorities for the implementation of Regulation (EC) 1907/2006; (REACH). European Commission, Brussels, Belgium.
    1. Ellegaard-Jensen L, Jensen KA, Johansen A. Nano-silver induces dose-response effects on the nematode Caenorhabditis elegans. Ecotoxicol Environ Saf. 2012;80:216–223. doi: 10.1016/j.ecoenv.2012.03.003.
    1. Emami-Karvani Z, Chehrazi P. Antibacterial activity of ZnO nanoparticle on grampositive and gram-negative bacteria. Afr J Microbiol Res. 2011;5(12):1368–1373.
    1. Ershov YuA, Pleteneva TV, Slonskaya TK. Evaluation of biological activity of toxic agents in a unicellular model. Bull Exp Biol Med. 1997;123(5):519–524. doi: 10.1007/BF02445337.
    1. European Commission (2007) SCENIHR (EU Scientific Committee on Emerging and Newly identified health risks). Report “Opinion on the appropriateness of the risk assessment methodology in accordance with the technical guidance documents for new and existing substances for assessing the risks of nanomaterials”.
    1. European Commission (2013) Communication from the Commission to the European Parliament, the Council and the European Economic and Social Committee. Second regulatory review on nanomaterials. Brussels, 3.10.2012, COM(2012) 572 final
    1. European Parliament and European Council Directive 2006/121/EC. Off J Eur Union. 2006;561(L396):850.
    1. European Union (2011) Commission Regulation No 286/2011 of 10 March 2011 amending, for the purposes of its adaptation to technical and scientific progress, Regulation (EC) No 1272/2008 of the European Parliament and of the Council on classification, labelling and packaging of substances and mixtures.
    1. Fabrega J, Luoma SN, Tyler CR, Galloway TS, Lead JR. Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int. 2011;37(2):517–531. doi: 10.1016/j.envint.2010.10.012.
    1. Foldbjerg R, Olesen P, Hougaard M, Dang DA, Hoffmann HJ, Autrup H. PVP-coated silver nanoparticles and silver ions induce reactive oxygen species, apoptosis and necrosis in THP-1 monocytes. Toxicol Lett. 2009;190(2):156–162. doi: 10.1016/j.toxlet.2009.07.009.
    1. Foldbjerg R, Dang DA, Autrup H. Cytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549. Arch Toxicol. 2011;85(7):743–750. doi: 10.1007/s00204-010-0545-5.
    1. Franklin NM, Stauber JL, Lim RP, Petocz P. Toxicity of metal mixtures to a tropical freshwater alga (Chlorella sp.): the effect of interactions between copper, cadmium, and zinc on metal cell binding and uptake. Environ Toxicol Chem. 2002;21(11):2412–2422.
    1. Franklin NM, Rogers NJ, Apte SC, Batley GE, Gadd GE, Casey PS. Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environ Sci Technol. 2007;41(24):8484–8490. doi: 10.1021/es071445r.
    1. Gabbay J, Mishal J, Magen E, Zatcoff RC, Shemer-Avni Y, Borkow G. Copper oxide impregnated textiles with potent biocidal activities. J Ind Textil. 2006;35:323–335. doi: 10.1177/1528083706060785.
    1. Gallego A, Martín-González A, Ortega R, Gutiérrez JC. Flow cytometry assessment of cytotoxicity and reactive oxygen species generation by single and binary mixtures of cadmium, zinc and copper on populations of the ciliated protozoan Tetrahymena thermophila. Chemosphere. 2007;68(4):647–661. doi: 10.1016/j.chemosphere.2007.02.031.
    1. Gao J, Youn S, Hovsepyan A, Llaneza VL, Wang Y, Bitton G, Bonzongo JC. Dispersion and toxicity of selected manufactured nanomaterials in natural river water samples: effects of water chemical composition. Environ Sci Technol. 2009;43(9):3322–3328. doi: 10.1021/es803315v.
    1. Govindasamy R, Rahuman AA. Histopathological studies and oxidative stress of synthesized silver nanoparticles in Mozambique tilapia (Oreochromis mossambicus) J Environ Sci. 2012;24(6):1091–1098. doi: 10.1016/S1001-0742(11)60845-0.
    1. Graff L, Isnard P, Cellier P, Bastide J, Cambon JP, Narbonne JF, Budzinski H, Vasseur P. Toxicity of chemicals to microalgae in river and in standard waters. Environ Toxicol Chem. 2003;22(6):1368–1379. doi: 10.1002/etc.5620220625.
    1. Grass G, Rensing C. Genes involved in copper homeostasis in Escherichia coli. J Bacteriol. 2001;183(6):2145–2147. doi: 10.1128/JB.183.6.2145-2147.2001.
    1. Greulich C, Braun D, Peetsch A, Diendorf J, Siebers B, Epple M, Koller M. The toxic effect of silver ions and silver nanoparticles towards bacteria and human cells occurs in the same concentration range. RSC Adv. 2012;2(17):6981–6987. doi: 10.1039/c2ra20684f.
    1. Griffitt RJ, Luo J, Gao J, Bonzongo JC, Barber DS. Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem. 2008;27(9):1972–1978. doi: 10.1897/08-002.1.
    1. Guo Z, Ng HW, Yee GL, Hahn HT. Differential scanning calorimetry investigation on vinyl ester resin curing process for polymer nanocomposite fabrication. J Nanosci Nanotechnol. 2009;9(5):3278–3285. doi: 10.1166/jnn.2009.VC06.
    1. Haase A, Mantion A, Graf P, Plendl J, Thuenemann AF, Meier W, Taubert A, Luch A. A novel type of silver nanoparticles and their advantages in toxicity testing in cell culture systems. Arch Toxicol. 2012;86(7):1089–1098. doi: 10.1007/s00204-012-0836-0.
    1. Handy RD, Cornelis G, Fernandes T, Tsyusko O, Decho A, Sabo-Attwood T, Metcalfe C, Steevens JA, Klaine SJ, Koelmans AA, Horne N. Ecotoxicity test methods for engineered nanomaterials: practical experiences and recommendations from the bench. Environ Toxicol Chem. 2012;31(1):15–31. doi: 10.1002/etc.706.
    1. Harmon SM, Specht WL, Chandler GT. A comparison of the daphnids Ceriodaphnia dubia and Daphnia ambigua for their utilization in routine toxicity testing in the Southeastern United States. Arch Environ Contam Toxicol. 2003;45(1):79–85. doi: 10.1007/s00244-002-0116-8.
    1. Harrington JM, Boyd WA, Smith MV, Rice JR, Freedman JH, Crumbliss AL. Amelioration of metal-induced toxicity in Caenorhabditis elegans: utility of chelating agents in the bioremediation of metals. Toxicol Sci. 2012;129(1):49–56. doi: 10.1093/toxsci/kfs191.
    1. Hassan MS, Amna T, Yang OB, El-Newehy MH, Al-Deyab SS, Khil M-S. Smart copper oxide nanocrystals: synthesis, characterization, electrochemical and potent antibacterial activity. Colloid Surf B. 2012;97:201–206. doi: 10.1016/j.colsurfb.2012.04.032.
    1. He L, Liu Y, Mustapha A, Lin M. Antifungal activity of zinc oxide nanoparticles against Botrytis cinerea and Penicillium expansum. Microbiol Res. 2011;166(3):207–215. doi: 10.1016/j.micres.2010.03.003.
    1. He D, Dorantes-Aranda JJ, Waite TD. Silver nanoparticle-algae interactions: oxidative dissolution, reactive oxygen species generation and synergistic toxic effects. Environ Sci Technol. 2012;46(16):8731–8738. doi: 10.1021/es300588a.
    1. Heijerick DG, Bossuyt BT, De Schamphelaere KA, Indeherberg M, Mingazzini M, Janssen CR. Effect of varying physicochemistry of European surface waters on the copper toxicity to the green alga Pseudokirchneriella subcapitata. Ecotoxicology. 2005;14(6):661–670. doi: 10.1007/s10646-005-0014-8.
    1. Heinlaan M, Ivask A, Blinova I, Dubourguier HC, Kahru A. Toxicity of nanosized and bulk ZnO, CuO and TiO2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere. 2008;71(7):1308–1316. doi: 10.1016/j.chemosphere.2007.11.047.
    1. Hernández-Sierra JF, Ruiz F, Cruz Pena DC, Martínez-Gutiérrez F, Martínez AE, Jesús Pozos Guillén A, Tapia-Pérez H, Martínez Castañón G. The antimicrobial sensitivity of Streptococcus mutans to nanoparticles of silver, zinc oxide, and gold. Nanomed-Nanotechnol. 2008;4(3):237–240. doi: 10.1016/j.nano.2008.04.005.
    1. Hiriart-Baer VP, Fortin C, Lee DY, Campbell PG. Toxicity of silver to two freshwater algae, Chlamydomonas reinhardtii and Pseudokirchneriella subcapitata, grown under continuous culture conditions: influence of thiosulphate. Aquat Toxicol. 2006;78(2):136–148. doi: 10.1016/j.aquatox.2006.02.027.
    1. Hoheisel SM, Diamond S, Mount D. Comparison of nanosilver and ionic silver toxicity in Daphnia magna and Pimephales promelas. Environ Toxicol Chem. 2012;31(11):2557–2563. doi: 10.1002/etc.1978.
    1. Hsieh CY, Tsai MH, Ryan DK, Pancorbo OC. Toxicity of the 13 priority pollutant metals to Vibrio fisheri in the Microtox chronic toxicity test. Sci Total Environ. 2004;320(1):37–50. doi: 10.1016/S0048-9697(03)00451-0.
    1. IPPIC (International Paint and Printing Ink Council) (2012)
    1. ISO 21338:2010, Water quality—Kinetic determination of the inhibitory effects of 412 sediment, other solids and coloured samples on the light emission of Vibrio fischeri 413 (kinetic luminescent bacteria test)
    1. Ivask A, Bondarenko O, Jepihhina N, Kahru A. Profiling of the reactive oxygen species-related ecotoxicity of CuO, ZnO, TiO2, silver and fullerene nanoparticles using a set of recombinant luminescent Escherichia coli strains: differentiating the impact of particles and solubilised metals. Anal Bioanal Chem. 2010;398:701–716. doi: 10.1007/s00216-010-3962-7.
    1. Ivask A, George S, Bondarenko O, Kahru A. Metal-containing nano-antimicrobials: differentiating the impact of solubilized metals and particles. In: Cioffi N, Rai M, editors. Nano-antimicrobials: Progress and Prospects. Berlin: Springer; 2012. pp. 253–290.
    1. Jain J, Arora S, Rajwade JM, Omray P, Khandelwal S, Paknikar KM. Silver nanoparticles in therapeutics: development of an antimicrobial gel formulation for topical use. Mol Pharm. 2009;6(5):1388–1401. doi: 10.1021/mp900056g.
    1. Jeng HA, Swanson J. Toxicity of metal oxide nanoparticles in mammalian cells. J Environ Sci Heal A. 2006;41(12):2699–2711. doi: 10.1080/10934520600966177.
    1. Jin YH, Dunlap PE, McBride SJ, Al-Refai H, Bushel PR, Freedman JH. Global transcriptome and deletome profiles of yeast exposed to transition metals. PLoS Genet. 2008;4(4):e1000053. doi: 10.1371/journal.pgen.1000053.
    1. Jo HJ, Choi JW, Lee SH, Hong SW. Acute toxicity of Ag and CuO nanoparticle suspensions against Daphnia magna: the importance of their dissolved fraction varying with preparation methods. J Hazard Mater. 2012;227–228:301–308. doi: 10.1016/j.jhazmat.2012.05.066.
    1. Jonker MJ, Piskiewicz AM, Ivorra i Castellà N, Kammenga JE. Toxicity of binary mixtures of cadmium-copper and carbendazim-copper to the nematode Caenorhabditis elegans. Environ Toxicol Chem. 2004;23(6):1529–1537. doi: 10.1897/03-49.
    1. Juganson K, Mortimer M, Ivask A, Kasemets K, Kahru A. Extracellular conversion of silver ions into silver nanoparticles by protozoan Tetrahymena thermophila. Environ Sci Process Impacts. 2013;15(1):244–250. doi: 10.1039/c2em30731f.
    1. Kahru A, Dubourguier HC. From ecotoxicology to nanoecotoxicology. Toxicology. 2010;269(2–3):105–119. doi: 10.1016/j.tox.2009.08.016.
    1. Kahru A, Ivask A. Mapping the dawn of nanoecotoxicological research. Acc Chem Res. 2013;46(3):823–833. doi: 10.1021/ar3000212.
    1. Kahru A, Savolainen K. Potential hazard of nanoparticles: from properties to biological and environmental effects. Toxicology. 2010;269(2–3):89–91. doi: 10.1016/j.tox.2010.02.012.
    1. Kahru A, Dubourguier HC, Blinova I, Ivask A, Kasemets K. Biotests and biosensors for ecotoxicology of metal oxide nanoparticles: a minireview. Sensors. 2008;8(8):5153–5170. doi: 10.3390/s8085153.
    1. Käkinen A, Bondarenko O, Ivask A, Kahru A. The effect of composition of different ecotoxicological test media on free and bioavailable copper from CuSO4 and CuO nanoparticles: comparative evidence from a Cu-selective electrode and a Cu-biosensor. Sensors. 2011;11(11):10502–10521. doi: 10.3390/s111110502.
    1. Karlsson HL, Cronholm P, Gustafsson J, Möller L. Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol. 2008;21(9):1726–1732. doi: 10.1021/tx800064j.
    1. Kasemets K, Ivask A, Dubourguier HC, Kahru A. Toxicity of nanoparticles of ZnO, CuO and TiO2 to yeast Saccharomyces cerevisiae. Toxicol In Vitro. 2009;23:1116–1122. doi: 10.1016/j.tiv.2009.05.015.
    1. Kasemets K, Suppi S, Künnis K, Kahru A. Toxicity of CuO nanoparticles to yeast Saccharomyces cerevisiae BY4741 wild-type and its nine isogenic single-gene deletion mutants. Chem Res Toxicol. 2013;26(3):356–367. doi: 10.1021/tx300467d.
    1. Kashiwada S, Ariza ME, Kawaguchi T, Nakagame Y, Jayasinghe BS, Gärtner K, Nakamura H, Kagami Y, Sabo-Attwood T, Ferguson PL, Chandler GT. Silver nanocolloids disrupt medaka embryogenesis through vital gene expressions. Environ Sci Technol. 2012;46(11):6278–6287. doi: 10.1021/es2045647.
    1. Kennedy AJ, Hull MS, Bednar AJ, Goss JD, Gunter JC, Bouldin JL, Vikesland PJ, Steevens JA. Fractionating nanosilver: importance for determining toxicity to aquatic test organisms. Environ Sci Technol. 2010;44(24):9571–9577. doi: 10.1021/es1025382.
    1. Kennedy AJ, Chappell MA, Bednar AJ, Ryan AC, Laird JG, Stanley JK, Steevens JA. Impact of organic carbon on the stability and toxicity of fresh and stored silver nanoparticles. Environ Sci Technol. 2012;46(19):10772–10780. doi: 10.1021/es302322y.
    1. Kim KJ, Sung WS, Moon SK, Choi JS, Kim JG, Lee DG. Antifungal effect of silver nanoparticles on dermatophytes. J Microbiol Biotechnol. 2008;18(8):1482–1484.
    1. Kim KJ, Sung WS, Suh BK, Moon SK, Choi JS, Kim JG, Lee DG. Antifungal activity and mode of action of silver nano-particles on Candida albicans. Biometals. 2009;22(2):235–242. doi: 10.1007/s10534-008-9159-2.
    1. Kim S, Choi JE, Choi J, Chung KH, Park K, Yi J, Ryu DY. Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol In Vitro. 2009;23(6):1076–1084. doi: 10.1016/j.tiv.2009.06.001.
    1. Kim YH, Fazlollahi F, Kennedy IM, Yacobi NR, Hamm-Alvarez SF, Borok Z, Kim KJ, Crandall ED. Alveolar epithelial cell injury due to zinc oxide nanoparticle exposure. Am J Respir Crit Care Med. 2010;182(11):1398–1409. doi: 10.1164/rccm.201002-0185OC.
    1. Kim J, Kim S, Lee S. Differentiation of the toxicities of silver nanoparticles and silver ions to the Japanese medaka (Oryzias latipes) and the cladoceran Daphnia magna. Nanotoxicology. 2011;5(2):208–214. doi: 10.3109/17435390.2010.508137.
    1. Kim SW, Nam SH, An YJ. Interaction of silver nanoparticles with biological surfaces of Caenorhabditis elegans. Ecotoxicol Environ Saf. 2012;77:64–70. doi: 10.1016/j.ecoenv.2011.10.023.
    1. Kungolos A, Samaras P, Tsiridis V, Petala M, Sakellaropoulos G. Bioavailability and toxicity of heavy metals in the presence of natural organic matter. J Environ Sci Heal A. 2006;41(8):1509–1517. doi: 10.1080/10934520600754706.
    1. Kurvet I, Ivask A, Bondarenko O, Sihtmäe M, Kahru A. LuxCDABE-transformed constitutively bioluminescent Escherichia coli for toxicity screening: comparison with naturally luminous Vibrio fischeri. Sensors. 2011;11(8):7865–7878. doi: 10.3390/s110807865.
    1. Kvitek L, Vanickova M, Panacek A, Soukupova J, Dittrich M, Valentova E, Prucek R, Bancirova M, Milde D, Zboril R. Initial study on the toxicity of silver nanoparticles (NPs) against Paramecium caudatum. J Phys Chem C. 2009;113(11):4296–4300. doi: 10.1021/jp808645e.
    1. Kwok KW, Auffan M, Badireddy AR, Nelson CM, Wiesner MR, Chilkoti A, Liu J, Marinakos SM, Hinton DE. Uptake of silver nanoparticles and toxicity to early life stages of Japanese medaka (Oryzias latipes): effect of coating materials. Aquat Toxicol. 2012;120–121:59–66. doi: 10.1016/j.aquatox.2012.04.012.
    1. Laban G, Nies LF, Turco RF, Bickham JW, Sepúlveda MS. The effects of silver nanoparticles on fathead minnow (Pimephales promelas) embryos. Ecotoxicology. 2010;19(1):185–195. doi: 10.1007/s10646-009-0404-4.
    1. Lee DY, Fortin C, Campbell PG. Contrasting effects of chloride on the toxicity of silver to two green algae, Pseudokirchneriella subcapitata and Chlamydomonas reinhardtii. Aquat Toxicol. 2005;75(2):127–135. doi: 10.1016/j.aquatox.2005.06.011.
    1. Levard C, Hotze EM, Lowry GV, Brown GE., Jr Environmental transformations of silver nanoparticles: impact on stability and toxicity. Environ Sci Technol. 2012;46(13):6900–6914. doi: 10.1021/es2037405.
    1. Lewis SS, Keller SJ. Identification of copper-responsive genes in an early life stage of the fathead minnow Pimephales promelas. Ecotoxicology. 2009;18(3):281–292. doi: 10.1007/s10646-008-0280-3.
    1. Li Y, Liang J, Tao Z, Chen J. CuO particles and plates: synthesis and gas-sensor application. Mater Res Bull. 2007;43:2380–2385. doi: 10.1016/j.materresbull.2007.07.045.
    1. Li K, Chen Y, Zhang W, Pu Z, Jiang L, Chen Y. Surface interactions affect the toxicity of engineered metal oxide nanoparticles toward Paramecium. Chem Res Toxicol. 2012;25(8):1675–1681. doi: 10.1021/tx300151y.
    1. Li J, Liu X, Zhang Y, Tian F, Zhao G, Yu O, Jiang FI, Liu Y. Toxicity of nano zinc oxide to mitochondria. Toxicol Res. 2012;1:137–144. doi: 10.1039/c2tx20016c.
    1. Lian W, Liu S, Yu J, Li J, Cui M, Xu W, Huang J. Electrochemical sensor using neomycin-imprinted film as recognition element based on chitosan-silver nanoparticles/graphene-multiwalled carbon nanotubes composites modified electrode. Biosens Bioelectron. 2013;15(44):70–76. doi: 10.1016/j.bios.2013.01.002.
    1. Lim D, Roh JY, Eom HJ, Choi JY, Hyun J, Choi J. Oxidative stress-related PMK-1 P38 MAPK activation as a mechanism for toxicity of silver nanoparticles to reproduction in the nematode Caenorhabditis elegans. Environ Toxicol Chem. 2012;31(3):585–592. doi: 10.1002/etc.1706.
    1. Lin Y-SE, Vidic RD, Stout JE, Yu VL. Individual and combined effects of copper and silver ions on inactivation of Legionella pneumophila. Water Res. 1996;30(8):1905–1913. doi: 10.1016/0043-1354(96)00077-2.
    1. Lin W, Xu Y, Huang C-C, Ma Y, Shannon KB, Chen D-R, Huang Y-W. Toxicity of nano and micro-sized ZnO particles in human lung epithelial cells. J Nanopart Res. 2009;11:25–39. doi: 10.1007/s11051-008-9419-7.
    1. Lipovsky A, Nitzan Y, Gedanken A, Lubart R. Antifungal activity of ZnO nanoparticles-the role of ROS mediated cell injury. Nanotechnology. 2011;22(10):105101. doi: 10.1088/0957-4484/22/10/105101.
    1. Little EE, Calfee RD, Linder G. Toxicity of copper to early-life stage Kootenai River white sturgeon, Columbia River white sturgeon, and rainbow trout. Arch Environ Contam Toxicol. 2012;63(3):400–408. doi: 10.1007/s00244-012-9782-3.
    1. Liu Y, He L, Mustapha A, Li H, Hu ZQ, Lin M. Antibacterial activities of zinc oxide nanoparticles against Escherichia coli O157:H7. J Appl Microbiol. 2009;107(4):1193–1201. doi: 10.1111/j.1365-2672.2009.04303.x.
    1. Liu W, Wu Y, Wang C, Li HC, Wang T, Liao CY, Cui L, Zhou QF, Yan B, Jiang GB. Impact of silver nanoparticles on human cells: effect of particle size. Nanotoxicology. 2010;4(3):319–330. doi: 10.3109/17435390.2010.483745.
    1. Lux Research (2008) Nanomaterials State of the Market Q3 2008: Stealth Success, Broad Impact. Report.
    1. Ma H, Bertsch PM, Glenn TC, Kabengi NJ, Williams PL. Toxicity of manufactured zinc oxide nanoparticles in the nematode Caenorhabditis elegans. Environ Toxicol Chem. 2009;28(6):1324–1330. doi: 10.1897/08-262.1.
    1. Ma H, Kabengi NJ, Bertsch PM, Unrine JM, Glenn TC, Williams PL. Comparative phototoxicity of nanoparticulate and bulk ZnO to a free-living nematode Caenorhabditis elegans: the importance of illumination mode and primary particle size. Environ Pollut. 2011;159(6):1473–1480. doi: 10.1016/j.envpol.2011.03.013.
    1. Ma H, Williams PL, Diamond SA. Ecotoxicity of manufactured ZnO nanoparticles—a review. Environ Pollut. 2013;172:76–85. doi: 10.1016/j.envpol.2012.08.011.
    1. Madoni P, Romeo MG. Acute toxicity of heavy metals towards freshwater ciliated protists. Environ Pollut. 2006;141(1):1–7. doi: 10.1016/j.envpol.2005.08.025.
    1. Majzlik P, Strasky A, Adam V, Nemec M, Trnkova L, Zehnalek J, Hubalek J, Provaznik I, Kizek R. Influence of zinc(II) and copper(II) ions on Streptomyces bacteria revealed by electrochemistry. Int J Electrochem Sci. 2011;6:2171–2191.
    1. Manusadžianas L, Caillet C, Fachetti L, Gylytė B, Grigutytė R, Jurkonienė S, Karitonas R, Sadauskas K, Thomas F, Vitkus R, Férard JF. Toxicity of copper oxide nanoparticle suspensions to aquatic biota. Environ Toxicol Chem. 2012;31(1):108–114. doi: 10.1002/etc.715.
    1. Marambio-Jones C, Hoek EMV. A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J Nanopart Res. 2010;12:1531–1551. doi: 10.1007/s11051-010-9900-y.
    1. Martínez-Castanón G, Nino-Martínez N, Martínez-Gutierrez F, Martínez-Mendoza J, Ruiz F. Synthesis and antibacterial activity of silver nanoparticles with different sizes. J Nanopart Res. 2008;10(8):1343–1348. doi: 10.1007/s11051-008-9428-6.
    1. Mastin BJ, Rodgers JH., Jr Toxicity and bioavailability of copper herbicides (Clearigate, Cutrine-Plus, and copper sulfate) to freshwater animals. Arch Environ Contam Toxicol. 2000;39(4):445–451. doi: 10.1007/s002440010126.
    1. McCloskey JT, Newman MC, Clark SB. Predicting relative toxicity of metal ions using ion characteristics: microtoxs bioluminescence assay. Environ Toxicol Chem. 1996;15:1730–1737. doi: 10.1002/etc.5620151011.
    1. McLaughlin J, Bonzongo JC. Effects of natural water chemistry on nanosilver behavior and toxicity to Ceriodaphnia dubia and Pseudokirchneriella subcapitata. Environ Toxicol Chem. 2011;31(1):168–175. doi: 10.1002/etc.720.
    1. McQuillan JS, Infante GH, Stokes E, Shaw AM. Silver nanoparticle enhanced silver ion stress response in Escherichia coli K12. Nanotoxicology. 2012;6:857–866. doi: 10.3109/17435390.2011.626532.
    1. Meyer JN, Lord CA, Yang XY, Turner EA, Badireddy AR, Marinakos SM, Chilkoti A, Wiesner MR, Auffan M. Intracellular uptake and associated toxicity of silver nanoparticles in Caenorhabditis elegans. Aquat Toxicol. 2010;100(2):140–150. doi: 10.1016/j.aquatox.2010.07.016.
    1. Miao AJ, Luo Z, Chen CS, Chin WC, Santschi PH, Quigg A. Intracellular uptake: a possible mechanism for silver engineered nanoparticle toxicity to a freshwater alga Ochromonas danica. PLoS ONE. 2010;5(12):e15196. doi: 10.1371/journal.pone.0015196.
    1. Mobley HL, Garner RM, Chippendale GR, Gilbert JV, Kane AV, Plaut AG. Role of Hpn and NixA of Helicobacter pylori in susceptibility and resistance to bismuth and other metal ions. Helicobacter. 1999;4(3):162–169. doi: 10.1046/j.1523-5378.1999.99286.x.
    1. Monteiro DR, Silva S, Negri M, Gorup LF, de Camargo ER, Oliveira R, Barbosa DB, Henriques M. Silver nanoparticles: influence of stabilizing agent and diameter on antifungal activity against Candida albicans and Candida glabrata biofilms. Lett Appl Microbiol. 2012;54(5):383–391. doi: 10.1111/j.1472-765X.2012.03219.x.
    1. Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramírez JT, Yacaman MJ. The bactericidal effect of silver nanoparticles. Nanotechnology. 2005;16:2346–2353. doi: 10.1088/0957-4484/16/10/059.
    1. Mortimer M, Kasemets K, Heinlaan M, Kurvet I, Kahru A. High throughput kinetic Vibrio fischeri bioluminescence inhibition assay for study of toxic effects of nanoparticles. Toxicol In Vitro. 2008;22:1412–1417. doi: 10.1016/j.tiv.2008.02.011.
    1. Mortimer M, Kasemets K, Kahru A. Toxicity of ZnO and CuO nanoparticles to ciliated protozoa Tetrahymena thermophila. Toxicology. 2010;269(2–3):182–189. doi: 10.1016/j.tox.2009.07.007.
    1. Mortimer M, Kasemets K, Vodovnik M, Marinsek-Logar R, Kahru A. Exposure to CuO nanoparticles changes the fatty acid composition of protozoa Tetrahymena thermophila. Environ Sci Technol. 2011;45(15):6617–6624. doi: 10.1021/es201524q.
    1. Murphy JT, Bruinsma JJ, Schneider DL, Collier S, Guthrie J, Chinwalla A, Robertson JD, Mardis ER, Kornfeld K. Histidine protects against zinc and nickel toxicity in Caenorhabditis elegans. PLoS Genet. 2011;7(3):e1002013. doi: 10.1371/journal.pgen.1002013.
    1. Naddafi K, Zare MR, Nazmara S. Investigating potential toxicity of phenanthrene adsorbed to nano-ZnO using Daphnia magna. Toxicol Environ Chem. 2011;93(4):729–737. doi: 10.1080/02772248.2011.552505.
    1. Nair LS, Laurencin CT. Silver nanoparticles: synthesis and therapeutic applications. J Biomed Nanotechnol. 2007;3:301–316. doi: 10.1166/jbn.2007.041.
    1. Nature Nanotech Editorial (2012) 7(9):545
    1. Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak N, Sigg L, Behra R. Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ Sci Technol. 2008;42(23):8959–8964. doi: 10.1021/es801785m.
    1. Nel A, Xia T, Mädler L, Li N. Toxic potential of materials at the nanolevel. Science. 2006;311:622–662. doi: 10.1126/science.1114397.
    1. Niazi JH, Sang BI, Kim YS, Gu MB. Global gene response in Saccharomyces cerevisiae exposed to silver nanoparticles. Appl Biochem Biotechnol. 2011;164(8):1278–1291. doi: 10.1007/s12010-011-9212-4.
    1. Nowack B, Krug HF, Height M. 120 Years of nanosilver history: implications for policy makers. Environ Sci Technol. 2011;45(4):1177–1183. doi: 10.1021/es103316q.
    1. Nowrouzi A, Meghrazi K, Golmohammadi T, Golestani A, Ahmadian S, Shafiezadeh M, Shajary Z, Khaghani S, Amiri AN. Cytotoxicity of subtoxic AgNP in human hepatoma cell line (HepG2) after long-term exposure. Iran Biomed J. 2010;14(1–2):23–32.
    1. Nyholm N, Petersen HG. Laboratory bioassays with microalgae. In: Wang W, Gorsuch JW, Hughes JS, editors. Plants for environmental studies. Boca Raton: Lewis Publishers; 1997.
    1. OECD (1992) Guidelines for the testing of chemicals. Section 2: Effects on Biotic Systems. Test No. 203: Fish, acute toxicity test. Organisation for Economic Co-operation and Development, Paris, France
    1. OECD (2004) Guidelines for the testing of chemicals. Section 2: Effects on Biotic Systems. Test No. 202: Daphnia sp. acute immobilisation test. Organisation for Economic Co-operation and Development, Paris, France
    1. OECD (2011) Guidelines for the testing of chemicals. Section 2: Effects on Biotic Systems. Test No. 201: Freshwater Alga and Cyanobacteria, growth inhibition test. Organisation for Economic Co-operation and Development, Paris, France
    1. Oliva M, Garrido MC, Sales Márquez D, González de Canales ML. Sublethal and lethal toxicity in juvenile Senegal sole (Solea senegalensis) exposed to copper: a preliminary toxicity range-finding test. Exp Toxicol Pathol. 2009;61(2):113–121. doi: 10.1016/j.etp.2008.06.001.
    1. Oukarroum A, Bras S, Perreault F, Popovic R. Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Saf. 2012;78:80–85. doi: 10.1016/j.ecoenv.2011.11.012.
    1. Padmavathy N, Vijayaraghavan R. Enhanced bioactivity of ZnO nanoparticles—an antimicrobial study. Sci Technol Adv Mater. 2008;9(3):035004. doi: 10.1088/1468-6996/9/3/035004.
    1. Panáček A, Kvítek L, Prucek R, Kolář M, Večeřová R, Pizúrová N, Sharma VK, Nevěčná T, Zbořil R. Silver colloid nanoparticles: synthesis, characterization, and their antibacterial activity. J Phys Chem B. 2006;110(33):16248–16253. doi: 10.1021/jp063826h.
    1. Panjehpour M, Taher MA, Bayesteh M. The growth inhibitory effects of cadmium and copper on the MDA-MB468 human breast cancer cells. J Res Med Sci. 2010;15(5):279–286.
    1. Park K, Heo GJ. Acute and subacute toxicity of copper sulfate pentahydrate (CuSO(4)5·H(2)O) in the guppy (Poecilia reticulata) J Vet Med Sci. 2009;71(3):333–336. doi: 10.1292/jvms.71.333.
    1. Patra P, Mitra S, Debnath N, Goswami A. Biochemical-, biophysical-, and microarray-based antifungal evaluation of the buffer-mediated synthesized nano zinc oxide: an in vivo and in vitro toxicity study. Langmuir. 2012;28(49):16966–16978. doi: 10.1021/la304120k.
    1. Pavlica S, Gaunitz F, Gebhardt R. Comparative in vitro toxicity of seven zinc-salts towards neuronal PC12 cells. Toxicol In Vitro. 2009;23(4):653–659. doi: 10.1016/j.tiv.2009.03.003.
    1. Perreault F, Oukarroum A, Melegari SP, Matias WG, Popovic R. Polymer coating of copper oxide nanoparticles increases nanoparticles uptake and toxicity in the green alga Chlamydomonas reinhardtii. Chemosphere. 2012;87(11):1388–1394. doi: 10.1016/j.chemosphere.2012.02.046.
    1. Piccinno F, Gottschalk F, Seeger S, Nowack B. Industrial production quantities and uses of ten engineered nanomaterials for Europe and the world. J Nanopart Res. 2012;14:1109–1120. doi: 10.1007/s11051-012-1109-9.
    1. Piret JP, Jacques D, Audinot JN, Mejia J, Boilan E, Noël F, Fransolet M, Demazy C, Lucas S, Saout C, Toussaint O. Copper(II) oxide nanoparticles penetrate into HepG2 cells, exert cytotoxicity via oxidative stress and induce pro-inflammatory response. Nanoscale. 2012;4(22):7168–7184. doi: 10.1039/c2nr31785k.
    1. Piret JP, Vankoningsloo S, Mejia J, Noël F, Boilan E, Lambinon F, Zouboulis, Masereel B, Lucas S, Saout C, Toussaint O. Differential toxicity of copper (II) oxide nanoparticles of similar hydrodynamic diameter on human differentiated intestinal Caco-2 cell monolayers is correlated in part to copper release and shape. Nanotoxicology. 2012;6(7):789–803. doi: 10.3109/17435390.2011.625127.
    1. Poynton HC, Lazorchak JM, Impellitteri CA, Smith ME, Rogers K, Patra M, Hammer KA, Allen HJ, Vulpe CD. Differential gene expression in Daphnia magna suggests distinct modes of action and bioavailability for ZnO nanoparticles and Zn ions. Environ Sci Technol. 2011;45(2):762–768. doi: 10.1021/es102501z.
    1. Poynton HC, Lazorchak JM, Impellitteri CA, Blalock BJ, Rogers K, Allen HJ, Loguinov A, Heckman JL, Govindasmawy S. Toxicogenomic responses of nanotoxicity in Daphnia magna exposed to silver nitrate and coated silver nanoparticles. Environ Sci Technol. 2012;46(11):6288–6296. doi: 10.1021/es3001618.
    1. Rallo R, Damoiseaux R, Telesca D, Mädler L, Cohen Y, Zink JI, Nel AE. Use of metal oxide nanoparticle band gap to develop a predictive paradigm for oxidative stress and acute pulmonary inflammation. ACS Nano. 2012;6(5):4349–4368. doi: 10.1021/nn3010087.
    1. Ren X, Meng X, Chen D, Tang F, Jiao J. Using silver nanoparticle to enhance current response of biosensor. Biosens Bioelectron. 2005;21(3):433–437. doi: 10.1016/j.bios.2004.08.052.
    1. Research and Markets (2012)
    1. Ruparelia JP, Chatterjee AK, Duttagupta SP, Mukherji S. Strain specificity in antimicrobial activity of silver and copper nanoparticles. Acta Biomater. 2008;4(3):707–716. doi: 10.1016/j.actbio.2007.11.006.
    1. Sanderson H, Johnson DJ, Wilson CJ, Brain RA, Solomon KR. Probabilistic hazard assessment of environmentally occurring pharmaceuticals toxicity to fish, daphnids and algae by ECOSAR screening. Toxicol Lett. 2003;144(3):383–395. doi: 10.1016/S0378-4274(03)00257-1.
    1. Sandstead HH. Requirements and toxicity of essential trace elements, illustrated by zinc and copper. Am J Clin Nutr. 1995;61(3 Suppl):621S–624S.
    1. Sargent JF (2012) Nanotechnology: A Policy Primer.
    1. Sau TK, Rogach AL, Jäckel F, Klar TA, Feldmann J. Properties and applications of colloidal nonspherical noble metal nanoparticles. Adv Mater. 2010;22(16):1805–1825. doi: 10.1002/adma.200902557.
    1. Schrurs F, Lison D. Focusing the research efforts. Nat Nanotechnol. 2012;7:546–548. doi: 10.1038/nnano.2012.148.
    1. Seiffert JM, Baradez MO, Nischwitz V, Lekishvili T, Goenaga-Infante H, Marshall D. Dynamic monitoring of metal oxide nanoparticle toxicity by label free impedance sensing. Chem Res Toxicol. 2012;25(1):140–152. doi: 10.1021/tx200355m.
    1. Serpone N, Dondi D, Albini A. Inorganic and organic UV filters: their role and efficacy in sunscreens and suncare products. Inorg Chim Acta. 2007;360:794–802. doi: 10.1016/j.ica.2005.12.057.
    1. Shakibaie MR, Harati A. Metal accumulation in Pseudomonas aeruginosa occur in the form of nanoparticles on the cell surface. Iran J Biotech. 2004;2(1):55–60.
    1. Sharifi S, Behzadi S, Laurent S, Forrest ML, Stroeve P, Mahmoudi M. Toxicity of nanomaterials. Chem Soc Rev. 2012;41(6):2323–2343. doi: 10.1039/c1cs15188f.
    1. Shaw BJ, Al-Bairuty G, Handy RD. Effects of waterborne copper nanoparticles and copper sulphate on rainbow trout (Oncorhynchus mykiss): physiology and accumulation. Aquat Toxicol. 2012;116–117:90–101. doi: 10.1016/j.aquatox.2012.02.032.
    1. Shi JP, Ma CY, Xu B, Zhang HW, Yu CP. Effect of light on toxicity of nanosilver to Tetrahymena pyriformis. Environ Toxicol Chem. 2012;31(7):1630–1638. doi: 10.1002/etc.1864.
    1. Shvedova AA, Kagan VE, Fadeel B. Close encounters of the small kind: adverse effects of man-made materials interfacing with the nano-cosmos of biological systems. Annu Rev Pharmacol Toxicol. 2010;50:63–88. doi: 10.1146/annurev.pharmtox.010909.105819.
    1. Song W, Zhang J, Guo J, Zhang J, Ding F, Li L, Sun Z. Role of the dissolved zinc ion and reactive oxygen species in cytotoxicity of ZnO nanoparticles. Toxicol Lett. 2010;199(3):389–397. doi: 10.1016/j.toxlet.2010.10.003.
    1. Sovova T, Koci V, Kochankova L (2009) Ecotoxicity of nano and bulk forms of metal oxides. In: Proceedings, NANOCON Conference, Roznov pod Radhostem. Czech Republic, pp 62–71, 20–22 October 2009
    1. Suresh AK, Pelletier DA, Wang W, Moon J-W, Gu B, Mortensen NP, Allison DP, Joy DC, Phelps TJ, Doktycz MJ. Silver nanocrystallites: biofabrication using Shewanella oneidensis, and an evaluation of their comparative toxicity on gram-negative and gram-positive bacteria. Environ Sci Technol. 2010;44(13):5210–5215. doi: 10.1021/es903684r.
    1. Teitzel GM, Parsek MR. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl Environ Microb. 2003;69(4):2313–2320. doi: 10.1128/AEM.69.4.2313-2320.2003.
    1. Teodorovic I, Planojevic I, Knezevic P, Radak S, Nemet I. Sensitivity of bacterial vs. acute Daphnia magna toxicity tests to metals. Cent Eur J Biol. 2009;4(4):482–492. doi: 10.2478/s11535-009-0048-7.
    1. Unger C, Lück C. Inhibitory effects of silver ions on Legionella pneumophila grown on agar, intracellular in Acanthamoeba castellanii and in artificial biofilms. J Appl Microbiol. 2012;112(6):1212–1219. doi: 10.1111/j.1365-2672.2012.05285.x.
    1. Vargas-Reus MA, Memarzadeh K, Huang J, Ren GG, Allaker RP. Antimicrobial activity of nanoparticulate metal oxides against peri-implantitis pathogens. Int J Antimicrob Ag. 2012;40(2):135–139. doi: 10.1016/j.ijantimicag.2012.04.012.
    1. Wang WX, Guan R. Subcellular distribution of zinc in Daphnia magna and implication for toxicity. Environ Toxicol Chem. 2010;29(8):1841–1848.
    1. Wang H, Wick RL, Xing B. Toxicity of nanoparticulate and bulk ZnO, Al2O3 and TiO2 to the nematode Caenorhabditis elegans. Environ Pollut. 2009;157(4):1171–1177. doi: 10.1016/j.envpol.2008.11.004.
    1. Wang Z, Chen J, Li X, Shao J, Peijnenburg WJ. Aquatic toxicity of nanosilver colloids to different trophic organisms: contributions of particles and free silver ion. Environ Toxicol Chem. 2012;31(10):2408–2413. doi: 10.1002/etc.1964.
    1. Wang Z, Li N, Zhao J, White JC, Qu P, Xing B. CuO nanoparticle interaction with human epithelial cells: cellular uptake, location, export, and genotoxicity. Chem Res Toxicol. 2012;25(7):1512–1521. doi: 10.1021/tx3002093.
    1. Wiench K, Wohlleben W, Hisgen V, Radke K, Salinas E, Zok S, Landsiedel R. Acute and chronic effects of nano- and non-nano-scale TiO2 and ZnO particles on mobility and reproduction of the freshwater invertebrate Daphnia magna. Chemosphere. 2009;76(10):1356–1365. doi: 10.1016/j.chemosphere.2009.06.025.
    1. Wilson W (2012) Consumer products inventory Project on Emerging Nanotechnologies, a project of the Woodrow Wilson International Center for Scholars.
    1. Wong SW, Leung PT, Djurisić AB, Leung KM. Toxicities of nano zinc oxide to five marine organisms: influences of aggregate size and ion solubility. Anal Bioanal Chem. 2010;396(2):609–618. doi: 10.1007/s00216-009-3249-z.
    1. Wu Y, Zhou Q. Silver nanoparticles cause oxidative damage and histological changes in medaka (Oryzias latipes) after 14 days of exposure. Environ Toxicol Chem. 2013;32(1):165–173. doi: 10.1002/etc.2038.
    1. Wu J, Wang L, He J, Zhu C. In vitro cytotoxicity of Cu2+, Zn2+, Ag+ and their mixtures on primary human endometrial epithelial cells. Contraception. 2012;85(5):509–518. doi: 10.1016/j.contraception.2011.09.016.
    1. Xie Y, He Y, Irwin PL, Jin T, Shi X. Antibacterial activity and mechanism of action of zinc oxide nanoparticles against Campylobacter jejuni. Appl Environ Microb. 2011;77(7):2325–2331. doi: 10.1128/AEM.02149-10.
    1. Xiong D, Fang T, Yu L, Sima X, Zhu W. Effects of nano-scale TiO2, ZnO and their bulk counterparts on zebrafish: acute toxicity, oxidative stress and oxidative damage. Sci Total Environ. 2011;409(8):1444–1452. doi: 10.1016/j.scitotenv.2011.01.015.
    1. Xu M, Li J, Iwai H, Mei Q, Fujita D, Su H, Chen H, Hanagata N. Formation of nano-bio-complex as nanomaterials dispersed in a biological solution for understanding nanobiological interactions. Sci Rep. 2012;2:406.
    1. Yang X, Gondikas AP, Marinakos SM, Auffan M, Liu J, Hsu-Kim H, Meyer JN. Mechanism of silver nanoparticle toxicity is dependent on dissolved silver and surface coating in Caenorhabditis elegans. Environ Sci Technol. 2012;46(2):1119–1127. doi: 10.1021/es202417t.
    1. Yilmaz EI. Metal tolerance and biosorption capacity of Bacillus circulans strain EB1. Res Microbiol. 2003;154(6):409–415. doi: 10.1016/S0923-2508(03)00116-5.
    1. Yu LP, Fang T, Xiong DW, Zhu WT, Sima XF. Comparative toxicity of nano-ZnO and bulk ZnO suspensions to zebrafish and the effects of sedimentation, ˙OH production and particle dissolution in distilled water. J Environ Monit. 2011;13(7):1975–1982. doi: 10.1039/c1em10197h.
    1. Zhang L, Mu X, Fu J, Zhou Z. In vitro cytotoxicity assay with selected chemicals using human cells to predict target-organ toxicity of liver and kidney. Toxicol In Vitro. 2007;21(4):734–740. doi: 10.1016/j.tiv.2007.01.013.
    1. Zhang H, Ji Z, Xia T, Meng H, Low-Kam C, Liu R, Pokhrel S, Lin S, Wang X, Liao YP, Wang M, Li L, Rallo R, Damoiseaux R, Telesca D, Mädler L, Cohen Y, Zink JI, Nel AE. Use of metal oxide nanoparticle band gap to develop a predictive paradigm for oxidative stress and acute pulmonary inflammation. ACS Nano. 2012;6(5):4349–4368. doi: 10.1021/nn3010087.
    1. Zhang J, Song W, Guo J, Zhang J, Sun Z, Ding F, Gao M. Toxic effect of different ZnO particles on mouse alveolar macrophages. J Hazard Mater. 2012;219–220:148–155. doi: 10.1016/j.jhazmat.2012.03.069.
    1. Zhao CM, Wang WX. Importance of surface coatings and soluble silver in silver nanoparticles toxicity to Daphnia magna. Nanotoxicology. 2012;4:361–370. doi: 10.3109/17435390.2011.579632.
    1. Zhao Z, Sakagami Y, Osaka T. Relationship between residual metal ions in a solution and the inhibitory capability of the metal ions for pathogenic bacterial growth. Bull Chem Soc Jpn. 1998;71:939–945. doi: 10.1246/bcsj.71.939.
    1. Zhao J, Wang Z, Liu X, Xie X, Zhang K, Xing B. Distribution of CuO nanoparticles in juvenile carp (Cyprinus carpio) and their potential toxicity. J Hazard Mater. 2011;197:304–310. doi: 10.1016/j.jhazmat.2011.09.094.
    1. Zhao HZ, Lu GH, Xia J, Jin S. Toxicity of Nanoscale CuO and ZnO to Daphnia magna. Chem Res Chin U. 2012;28(2):209–213.
    1. Zhu X, Zhu L, Duan Z, Qi R, Li Y, Lang Y. Comparative toxicity of several metal oxide nanoparticle aqueous suspensions to Zebrafish (Danio rerio) early developmental stage. J Environ Sci Heal A. 2008;43(3):278–284. doi: 10.1080/10934520701792779.
    1. Zhu X, Zhu L, Yongsheng C, Tian S. Acute toxicities of six manufactured nanomaterial suspensions to Daphnia magna. J Nanopart Res. 2009;11:67–75. doi: 10.1007/s11051-008-9426-8.
    1. Zook JM, Halter MD, Cleveland D, Long SE. Disentangling the effects of polymer coatings on silver nanoparticle agglomeration, dissolution, and toxicity to determine mechanisms of nanotoxicity. J Nanopart Res. 2012;14:1165. doi: 10.1007/s11051-012-1165-1.

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