Mechanisms of toxic action of Ag, ZnO and CuO nanoparticles to selected ecotoxicological test organisms and mammalian cells in vitro: A comparative review

Nanotoxicology

Volumn 8, Issue SUPPL. 1, 2014, Pages 57-71

  Ivask, Angela ^a   Juganson, Katre ^a,b   Bondarenko, Olesja ^a   Mortimer, Monika ^c   Aruoja, Villem ^a   Kasemets, Kaja ^a   Blinova, Irina ^a   Heinlaan, Margit ^a   Slaveykova, Vera ^c   Kahru, Anne ^a  

^a NATIONAL INSTITUTE OF CHEMICAL PHYSICS AND BIOPHYSICS   (Estonia)

^b TALLINN UNIVERSITY OF TECHNOLOGY   (Estonia)

^c UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Antimicrobials; Metal ions; Oxidative stress; QNARs; Uptake

Indexed keywords

ACETYLCYSTEINE; CATALASE; COPPER NANOPARTICLE; COPPER OXIDE; COPPER OXIDE NANOPARTICLE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; REACTIVE OXYGEN METABOLITE; SILVER NANOPARTICLE; UNCLASSIFIED DRUG; ZINC OXIDE NANOPARTICLE; COPPER; CUPROUS OXIDE; METAL NANOPARTICLE; SILVER; ZINC OXIDE;

ALGA; AQUATIC FAUNA; BACTERIUM; CELL DAMAGE; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; COMPARATIVE STUDY; CRUSTACEA; CYTOTOXICITY; DISSOLUTION; DNA DAMAGE; ECOTOXICOLOGY; ENVIRONMENTAL STRESS; FISH; HUMAN; IN VITRO STUDY; INFLAMMATION; LIPID PEROXIDATION; MAMMAL CELL; MEMBRANE DAMAGE; MICROORGANISM; MITOCHONDRIAL TOXICITY; MOLECULAR MODEL; NANOTOXICOLOGY; NONHUMAN; ORGANISM SOCIAL GROUP; OXIDATIVE STRESS; PRIORITY JOURNAL; QUANTITATIVE STRUCTURE ACTIVITY RELATION; REVIEW; TOXICITY TESTING; YEAST; CHEMISTRY;

COPPER; IN VITRO TECHNIQUES; METAL NANOPARTICLES; SILVER; ZINC OXIDE;

EID: 84905968993     PISSN: 17435390     EISSN: 17435404     Source Type: Journal    
DOI: 10.3109/17435390.2013.855831     Document Type: Review

References (147)

1. Anderson MA, Morel FMM, Guillard RRL. 1978. Growth limitation of a coastal diatom by low zinc ion activity. Nature 276: 70-1.
2. Applerot G, Lellouche J, Lipovsky A, Nitzan Y, Lubart R, Gedanken A, Banin E. 2012. Understanding the antibacterial mechanism of CuO nanoparticles: Revealing the route of induced oxidative stress. Small 8: 3326-37.
3. Applerot G, Lipovsky A, Dror R, Perkas N, Nitzan Y, Lubart R, Gedanken A. 2009. Enhanced antibacterial activity of nanocrystalline ZnO due to increased ROS-mediated cell injury. Adv Funct Mater 19: 842-52.
4. Arora S, Jain J, Rajwade JM, Paknikar KM. 2008. Cellular responses induced by silver nanoparticles: in vitro studies. Toxicol Lett 179: 93-100.
5. 2 to microalgae Pseudokirchneriella subcapitata. Sci Total Environ 407: 1461-8.
6. Arvizo RR, Bhattacharyya S, Kudgus RA, Giri K, Bhattacharya R, Mukherjee P. 2012. Intrinsic therapeutic applications of noble metal nanoparticles: Past, present and future. Chem Soc Rev 41: 2943-70.
7. Bachand GD, Allen A, Bachand M, Achyuthan KE, Seagrave JC, Brozik SM. 2012. Cytotoxicity and inflammation in human alveolar epithelial cells following exposure to occupational levels of gold and silver nanoparticles. J Nanopart Res 14: 1212.
8. Bar-Ilan O, Albrecht RM, Fako VE, Furgeson DY. 2009. Toxicity assessments of multisized gold and silver nanoparticles in zebrafish embryos. Small 5: 1897-910.
9. Batley GE, Kirby JK, McLaughlin MJ. 2012. Fate and risks of nanomaterials in aquatic and terrestrial environments. Acc Chem Res 46: 854-62.
10. Bian S-W, Mudunkotuwa IA, Rupasinghe T, Grassian VH. 2011. Aggregation and dissolution of 4 nm ZnO nanoparticles in aqueous environments: influence of pH, ionic strength, size, and adsorption of humic acid. Langmuir 27: 6059-68.
11. Blinova I, Ivask A, Heinlaan M, Mortimer M, Kahru A. 2010. Ecotoxicity of nanoparticles of CuO and ZnO in natural water. Environ Pollut 158: 41-7.
12. Blinova I, Niskanen J, Kajankari P, Kanarbik L, Kakinen A, Tenhu H, et al. 2013. Toxicity of two types of silver nanoparticles to aquatic crustaceans Daphnia magna and Thamnocephalus platyurus. Environ Sci Pollut R 20: 3456-63.
13. Blokhina O, Virolainen E, Fagerstedt KV. 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot London 91: 179-94.
14. Bondarenko O, Ivask A, Kakinen A, Kahru A. 2012. Sub-toxic effects of CuO nanoparticles on bacteria: kinetics, role of Cu ions and possible mechanisms of action. Environ Pollut 169: 81-9.
15. Bondarenko O, Juganson K, Ivask A, Kasemets K, Mortimer M, Kahru A. 2013a. Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review. Arch Toxicol 84: 1181-200.
16. Bondarenko O, Ivask A, Käkinen A, Kurvet I, Kahru A. 2013b. Particlecell contact enhances antibacterial activity of silver nanoparticles. PLoS ONE 8: e64060.
17. Brayner R, Ferrari-Iliou R, Brivois N, Djediat S, Benedetti MF, Fiévet F. 2006. Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Lett 6: 866-70.
18. Brunner TJ, Wick P, Manser P, Spohn P, Grass RN, Limbach LK, Bruinink A, Stark WJ. 2006. In vitro cytotoxicity of oxide nanoparticles: Comparison to asbestos, silica, and the effect of particle solubility. Environ Sci Technol 40: 4374-81.
19. Buffet P-E, Tankoua OF, Pan J-F, Berhanu D, Herrenknecht C, Poirier L, et al. 2011. Behavioural and biochemical responses of two marine invertebrates Scrobicularia plana and Hediste diversicolor to copper oxide nanoparticles. Chemosphere 84: 166-74.
20. Buffle J, Wilkinson KJ, van Leeuwen HP. 2009. Chemodynamics and bioavailability in natural waters. Environ Sci Technol 43: 7170-4.
21. Burello E, Worth A. 2011a. Computational nanotoxicology: Predicting toxicity of nanoparticles. Nat Nanotechnol 6: 138-9.
22. Burello E, Worth AP. 2011b. QSAR modeling of nanomaterials. WIREs Nanomed Nanobiotechnol 3: 298-306.
23. CEC. 1996. Technical Guidance Documents in support of the Commission Directive 93/67/EEC on Risk Assessment for New Notified Substances and the Commission Regulation (EC) 1488/94 on Risk Assessment for Existing Substances. Commission of the European Communities/European Chemicals Bureau, Ispra.
24. Cedervall T, Lynch I, Lindman S, Berggard T, Thulin E, Nilsson H, et al. 2007. Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc Natl Acad Sci USA 104: 2050-5.
25. Chau YT, Yap CW. 2012. Quantitative nanostructure-activity relationship modelling of nanoparticles. RSC Adv 2: 8489-96.
26. Cheloni G, Slaveykova VI. 2013. Optimization of the C11-BODIPY581/591 dye for the determination of lipid oxidation in Chlamydomonas reinhardtii by flow cytometry. Cytometry A. doi: 10.1002/cyto.a.22338.
27. Chen P, Powell BA, Mortimer M, Ke PC. 2012. Adaptive interactions between zinc oxide nanoparticles and Chlorella sp. Environ Sci Technol 46: 12178-85.
28. Chithrani BD, Chan WCW. 2007. Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett 7: 1542-50.
29. Cho W-S, Duffin R, Poland CA, Duschl A, Oostingh GJ, MacNee W, et al. 2012. Differential pro-inflammatory effects of metal oxide nanoparticles and their soluble ions in vitro and in vivo; zinc and copper nanoparticles, but not their ions, recruit eosinophils to the lungs. Nanotoxicology 6: 22-35.
30. Choi O, Hu Z. 2008. Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ Sci Technol 42: 4583-8.
31. Cronholm P, Midander K, Karlsson HL, Elihn K, Wallinder IO, Moller L. 2011. Effect of sonication and serum proteins on copper release from copper nanoparticles and the toxicity towards lung epithelial cells. Nanotoxicology 5: 269-81.
32. Damoiseaux R, George S, Li M, Pokhrel S, Ji Z, France B, et al. 2011. No time to lose-high throughput screening to assess nanomaterial safety. Nanoscale 3: 1345-60.
33. Dimkpa CO, Calder A, Britt DW, McLean JE, Anderson AJ. 2011. Responses of a soil bacterium, Pseudomonas chlororaphis O6 to commercial metal oxide nanoparticles compared with responses to metal ions. Environ Pollut 159: 1749-56.
34. Epa VC, Burden FR, Tassa C, Weissleder R, Shaw S, Winkler DA. 2012. Modeling biological activities of nanoparticles. Nano Lett 12: 5808-12.
35. Fabian E, Landsiedel R, Ma-Hock L, Wiench K, Wohlleben W, Ravenzwaay B. 2008. Tissue distribution and toxicity of intravenously administered titanium dioxide nanoparticles in rats. Arch Toxicol 82: 151-7.
36. Fabrega J, Fawcett SR, Renshaw JC, Lead JR. 2009. Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. Environ Sci Technol 43: 7285-90.
37. Fahmy B, Cormier SA. 2009. Copper oxide nanoparticles induce oxidative stress and cytotoxicity in airway epithelial cells. Toxicol In Vitro 23: 1365-71.
38. Fairbairn EA, Keller AA, Maedler L, Zhou D, Pokhrel S, Cherr GN. 2011. Metal oxide nanomaterials in seawater: linking physicochemical characteristics with biological response in sea urchin development. J Hazard Mater 192: 1565-71.
39. Fan WH, Shi ZW, Yang XP, Cui MM, Wang XL, Zhang DF, et al. 2012. Bioaccumulation and biomarker responses of cubic and octahedral Cu2O micro/nanocrystals in Daphnia magna. Water Res 46: 5981-8.
40. Foldbjerg R, Dang DA, Autrup H. 2011. Cytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549. Arch Toxicol 85: 743-50.
41. Fourches D, Pu D, Tassa C, Weissleder R, Shaw SY, Mumper RJ, Tropsha A. 2010. Quantitative nanostructure-activity relationship modeling. ACS Nano 4: 5703-12.
42. Fourches D, Pu D, Tropsha A. 2011. Exploring quantitative nanostructure- activity relationships (QNAR) modeling as a tool for predicting biological effects of manufactured nanoparticles. Comb Chem High T Scr 14: 217-225.
43. Franklin NM, Rogers NJ, Apte SC, Batley GE, Gadd GE, Casey PS. 2007. Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environ Sci Technol 41: 8484-90.
44. Gajewicz A, Rasulev B, Dinadayalane TC, Urbaszek P, Puzyn T, Leszczynska D, Leszczynski J. 2012. Advancing risk assessment of engineered nanomaterials: application of computational approaches. Adv Drug Deliver Rev 64: 1663-93.
45. Gao J, Youn S, Hovsepyan A, Llaneza VnL, Wang Y, Bitton G, Bonzongo J-CJ. 2009. Dispersion and toxicity of selected manufactured nanomaterials in natural river water samples: effects of water chemical composition. Environ Sci Technol 43: 3322-8.
46. George S, Xia T, Rallo R, Zhao Y, Ji Z, Lin S, et al. 2011. Use of a highthroughput screening approach coupled with in vivo zebrafish embryo screening to develop hazard ranking for engineered nanomaterials. ACS Nano 5: 1805-17.
47. Gogoi SK, Gopinath P, Paul A, Ramesh A, Ghosh SS, Chattopadhyay A. 2006. green fluorescent protein-expressing Escherichia coli as a model system for investigating the antimicrobial activities of silver nanoparticles. Langmuir 22: 9322-8.
48. Griffitt RJ, Hyndman K, Denslow ND, Barber DS. 2009. Comparison of molecular and histological changes in zebrafish gills exposed to metallic nanoparticles. Toxicol Sci 107: 404-15.
49. Gunawan C, Teoh WY, Marquis CP, Lifia J, Amal R. 2009. Reversible antimicrobial photoswitching in nanosilver. Small 5: 341-4.
50. Hao L, Chen L. 2012. Oxidative stress responses in different organs of carp (Cyprinus carpio) with exposure to ZnO nanoparticles. Ecotox Environ Safe 80: 103-10.
51. Harrison RG, Lunt G. 1980. Membrane Components in Biological Membranes: Their Structure and Function, 2nd ed. Glasgow, London: Blackie, Vol. 62, 101.
52. He L, Liu Y, Mustapha A, Lin M. 2011. Antifungal activity of zinc oxide nanoparticles against Botrytis cinerea and Penicillium expansum. Microbiol Res 166: 207-15.
53. 2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere 71: 1308-16.
54. Heinlaan M, Kahru A, Kasemets K, Arbeille B, Prensier G, Dubourguier H-C. 2011. Changes in the Daphnia magna midgut upon ingestion of copper oxide nanoparticles: a transmission electron microscopy study. Water Res 45: 179-90.
55. Hoheisel SM, Diamond S, Mount D. 2012. Comparison of nanosilver and ionic silver toxicity in Daphnia magna and Pimephales promelas. Environ Toxicol Chem 31: 2557-63.
56. 2 and ZnO nanoparticles in soil on earthworm Eisenia fetida. Soil Biol Biochem 42: 586-91.
57. Hu X, Cook S, Wang P, Hwang H-m. 2009. In vitro evaluation of cytotoxicity of engineered metal oxide nanoparticles. Sci Total Environ 407: 3070-2.
58. Huang Z, Zheng X, Yan D, Yin G, Liao X, Kang Y, et al. 2008. Toxicological effect of ZnO nanoparticles based on bacteria. Langmuir 24: 4140-4.
59. Hussain SM, Hess KL, Gearhart JM, Geiss KT, Schlager JJ. 2005. In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol In Vitro 19: 975-83.
60. 2, silver and fullerene nanoparticles using a set of recombinant luminescent Escherichia coli strains: differentiating the impact of particles and solubilised metals. Anal Bioanal Chem 398: 701-16.
61. Ivask A, George S, Bondarenko O, Kahru A. 2012. Metal-containing nano-antimicrobials: differentiating the impact of solubilized metals and particles. In: Cioffi A & Rai M, eds. Nano-Antimicrobials: Progress and Prospects. New York: Springer, 253-90.
62. Jo HJ, Choi JW, Lee SH, Hong SW. 2012. Acute toxicity of Ag and CuO nanoparticle suspensions against Daphnia magna: the importance of their dissolved fraction varying with preparation methods. J Hazard Mater 227: 301-8.
63. Johnston HJ, Hutchison G, Christensen FM, Peters S, Hankin S, Stone V. 2010. A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanisms responsible for the observed toxicity. Crit Rev Toxicol 40: 328-46.
64. Juganson K, Mortimer M, Ivask A, Kasemets K, Kahru A. 2013. Extracellular conversion of silver ions into silver nanoparticles by protozoan Tetrahymena thermophila. Environ Sci Process Impacts 15: 244-50.
65. Kahru A, Dubourguier H-C. 2010. From ecotoxicology to nanoecotoxicology. Toxicology 269: 105-19.
66. Kahru A, Ivask A. 2013. Mapping the dawn of nanoecotoxicological research. Acc Chem Res 46: 823-33.
67. Käkinen A, Ding F, Chen P, Mortimer M, Kahru A, Ke PC. 2013. Interaction of firefly luciferase and silver nanoparticles and its impact on enzyme activity. Nanotechnology 24: 345101.
68. Karlsson HL, Cronholm P, Gustafsson J, Moeller L. 2008. Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21: 1726-32.
69. 2 to yeast Saccharomyces cerevisiae. Toxicol In Vitro 23: 1116-22.
70. Kasemets K, Suppi S, Kunnis-Beres K, Kahru A. 2013. Toxicity of CuO nanoparticles to yeast Saccharomyces cerevisiae BY4741 wild-type and its nine isogenic single-gene deletion mutants. Chem Res Toxicol 26: 356-67.
71. Kaur J, Tikoo K. 2013. Evaluating cell specific cytotoxicity of differentially charged silver nanoparticles. Food Chem Toxicol 51: 1-14.
72. Kim J, Kim S, Lee S. 2011. Differentiation of the toxicities of silver nanoparticles and silver ions to the Japanese medaka (Oryzias latipes) and the cladoceran Daphnia magna. Nanotoxicology 5: 208-14.
73. Kim K-J, Sung W, Suh B, Moon S-K, Choi J-S, Kim J, Lee D. 2009a. Antifungal activity and mode of action of silver nano-particles on Candida albicans. BioMetals 22: 235-42.
74. Kim S, Choi JE, Choi J, Chung K-H, Park K, Yi J, Ryu D-Y. 2009b. Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol In Vitro 23: 1076-84.
75. Kim YH, Fazlollahi F, Kennedy IM, Yacobi NR, Hamm-Alvarez SF, Borok Z, et al. 2010. Alveolar epithelial cell injury due to zinc oxide nanoparticle exposure. Am J Resp Crit Care 182: 1398-409.
76. Kloepfer JA, Mielke RE, Nadeau JL. 2005. Uptake of CdSe and CdSe/ZnS quantum dots into bacteria via purine-dependent mechanisms. Appl Environ Microb 71: 2548-57.
77. Kumar A, Pandey AK, Singh SS, Shanker R, Dhawan A. 2011a. Cellular uptake and mutagenic potential of metal oxide nanoparticles in bacterial cells. Chemosphere 83: 1124-32.
78. 2 nanoparticles induce oxidative stress and DNA damage leading to reduced viability of Escherichia coli. Free Radical Bio Med 51: 1872-81.
79. Lee KJ, Nallathamby PD, Browning LM, Osgood CJ, Xu X-HN. 2007. In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. ACS Nano 1: 133-43.
80. Lesniak A, Salvati A, Santos-Martinez MJ, Radomski MW, Dawson KA, Aberg C. 2013. Nanoparticle adhesion to the cell membrane and its effect on nanoparticle uptake efficiency. J Am Chem Soc 135: 1438-44.
81. Levard C, Hotze EM, Lowry GV, Brown Jr GE, . 2012. Environmental transformations of silver nanoparticles: impact on stability and toxicity. Environ Sci Technol 46: 6900-14.
82. Li J-H, Liu X-R, Zhang Y, Tian F-F, Zhao G-Y, Yu Q-L-Y, Jiang F-L, Liu Y. 2012. Toxicity of nano zinc oxide to mitochondria. Toxicol Res 1: 137-44.
83. Li M, Lin D, Zhu L. 2013. Effects of water chemistry on the dissolution of ZnO nanoparticles and their toxicity to Escherichia coli. Environ Pollut 173: 97-102.
84. Li M, Zhu L, Lin D. 2011. Toxicity of ZnO nanoparticles to Escherichia coli: mechanism and the influence of medium components. Environ Sci Technol 45: 1977-83.
85. Limbach LK, Li Y, Grass RN, Brunner TJ, Hintermann MA, Muller M, et al. 2005. Oxide nanoparticle uptake in human lung fibroblasts: effects of particle size, agglomeration, and diffusion at low concentrations. Environ Sci Technol 39: 9370-6.
86. Lin S, Zhao Y, Ji Z, Ear J, Chang CH, Zhang H, et al. 2013. Zebrafish high-throughput screening to study the impact of dissolvable metal oxide nanoparticles on the hatching enzyme, ZHE1. Small 9: 1776-85.
87. Liu R, Rallo R, George S, Ji Z, Nair S, Nel AE, Cohen Y. 2011. Classification nanoSAR development for cytotoxicity of metal oxide nanoparticles. Small 7: 1118-26.
88. Liu W, Wu Y, Wang C, Li HC, Wang T, Liao CY, et al. 2010. Impact of silver nanoparticles on human cells: effect of particle size. Nanotoxicology 4: 319-30.
89. Liu Y, He L, Mustapha A, Li H, Hu ZQ, Lin M. 2009. Antibacterial activities of zinc oxide nanoparticles against Escherichia coli O157: H7. J Appl Microbiol 107: 1193-201.
90. Lok C-N, Ho C-M, Chen R, He Q-Y, Yu W-Y, Sun H, et al. 2007. Silver nanoparticles: partial oxidation and antibacterial activities. J Biol Inorg Chem 12: 527-34.
91. Luoma SN, Rainbow PS. 2005. Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Environ Sci Technol 39: 1921-31.
92. Lux-Research. 2008. Nanomaterials state of the market Q3 2008: Stealth success, broad impact. Report. [Online] https://portal.luxresea rchinc.com/research/document-excerpt/3735 [Last accessed 30 October 2013].
93. Ma H, Williams PL, Diamond SA. 2013. Ecotoxicity of manufactured ZnO nanoparticles: A review. Environ Pollut 172: 76-85.
94. Manusadzianas L, Caillet C, Fachetti L, Gylyte B, Grigutyte R, Jurkoniene S, et al. 2012. Toxicity of copper oxide nanoparticle suspensions to aquatic biota. Environ Toxicol Chem 31: 108-14.
95. McDonnell G, Russell AD. 1999. Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12: 147-79.
96. Miao A-J, Luo Z, Chen C-S, Chin W-C, Santschi PH, Quigg A. 2010. Intracellular uptake: a possible mechanism for silver engineered nanoparticle toxicity to a freshwater alga Ochromonas danica. PLoS ONE 5: e15196.
97. Misra SK, Dybowska A, Berhanu D, Luoma SN, Valsami-Jones E. 2012. The complexity of nanoparticle dissolution and its importance in nanotoxicological studies. Sci Total Environ 438: 225-32.
98. Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramírez JT, Yacaman MJ. 2005. The bactericidal effect of silver nanoparticles. Nanotechnology 16: 2346-53.
99. Mortimer M, Kasemets K, Kahru A. 2010. Toxicity of ZnO and CuO nanoparticles to ciliated protozoa Tetrahymena thermophila. Toxicology 269: 182-9.
100. Mortimer M, Kasemets K, Vodovnik M, Marinsek-Logar R, Kahru A. 2011. Exposure to CuO nanoparticles changes the fatty acid composition of protozoa Tetrahymena thermophila. Environ Sci Technol 45: 6617-24.
101. Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak N, et al. 2008. Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ Sci Technol 42: 8959-64.
102. Nel A, Xia T, Madler L, Li N. 2006. Toxic potential of materials at the nanolevel. Science 311: 622-7.
103. Niazi JH, Sang B-I, Kim YS, Gu MB. 2011. Global gene response in Saccharomyces cerevisiae exposed to silver nanoparticles. Appl Biochem Biotech 164: 1278-91.
104. Norzila MZ, Fakes K, Henry RL, Simpson J, Gibson PG. 2000. Interleukin-8 secretion and neutrophil recruitment accompanies induced sputum eosinophil activation in children with acute asthma. Am J Resp Crit Care 161: 769-74.
105. Nowrouzi A, Meghrazi K, Golmohammadi T, Golestani A, Ahmadian S, Shafiezadeh M, et al. 2010. Cytotoxicity of subtoxic AgNP in human hepatoma cell line (HepG2) after long-term exposure. Iran Biomed J 14: 23-32.
106. Paquin PR, Gorsuch JW, Apte S, Batley GE, Bowles KC, Campbell PGC, et al. 2002. The biotic ligand model: a historical overview. Comp Biochem Phys C 133: 3-35.
107. Park E-J, Yi J, Kim Y, Choi K, Park K. 2010. Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol In Vitro 24: 872-8.
108. Park MVDZ, Neigh AM, Vermeulen JP, de la Fonteyne LJJ, Verharen HW, Briede JJ, et al. 2011. The effect of particle size on the cytotoxicity, inflammation, developmental toxicity and genotoxicity of silver nanoparticles. Biomaterials 32: 9810-7.
109. Peng X, Palma S, Fisher NS, Wong SS. 2011. Effect of morphology of ZnO nanostructures on their toxicity to marine algae. Aquat Toxicol 102: 186-96.
110. Piret JP, Jacques D, Audinot JN, Mejia J, Boilan E, Noel F, et al. 2012. Copper(II) oxide nanoparticles penetrate into HepG2 cells, exert cytotoxicity via oxidative stress and induce pro-inflammatory response. Nanoscale 4: 7168-84.
111. Podila R, Chen R, Ke PC, Rao AM. 2012. Effects of surface functional groups on the formation of nanoparticle-protein corona. Appl Phys Lett 101: 263701.
112. Poynton HC, Lazorchak JM, Impellitteri CA, Blalock BJ, Rogers K, Allen HJ, et al. 2012. Toxicogenomic responses of nanotoxicity in Daphnia magna exposed to silver nitrate and coated silver nanoparticles. Environ Sci Technol 46: 6288-96.
113. Poynton HC, Lazorchak JM, Impellitteri CA, Smith ME, Rogers K, Patra M, et al. 2011. Differential gene expression in Daphnia magna suggests distinct modes of action and bioavailability for ZnO nanoparticles and Zn ions. Environ Sci Technol 45: 762-8.
114. Puzyn T, Rasulev B, Gajewicz A, Hu X, Dasari TP, Michalkova A, et al. 2011. Using nano-QSAR to predict the cytotoxicity of metal oxide nanoparticles. Nat Nanotechnol 6: 175-8.
115. Reyes VC, Li M, Hoek EMV, Mahendra S, Damoiseaux R. 2012. Genome-wide assessment in Escherichia coli reveals time-dependent nanotoxicity paradigms. ACS Nano 6: 9402-15.
116. Roh J-Y, Sim SJ, Yi J, Park K, Chung KH, Ryu D-Y, Choi J. 2009. Ecotoxicity of silver nanoparticles on the soil nematode Caenorhabditis elegans using functional ecotoxicogenomics. Environ Sci Technol 43: 3933-40.
117. Rousk J, Ackermann K, Curling SF, Jones DL. 2012. Comparative toxicity of nanoparticulate CuO and ZnO to soil bacterial communities. PLoS ONE 7: e34197.
118. Sayre L, Moreira P, Smith M, Perry G. 2005. Metal ions and oxidative protein modification in neurological disease. Ann Ist Super Sanita 41: 143-64.
119. Sharma V, Anderson D, Dhawan A. 2012. Zinc oxide nanoparticles induce oxidative DNA damage and ROS-triggered mitochondria mediated apoptosis in human liver cells (HepG2). Apoptosis 17: 852-70.
120. Shaw BJ, Al-Bairuty G, Handy RD. 2012. Effects of waterborne copper nanoparticles and copper sulphate on rainbow trout, (Oncorhynchus mykiss): physiology and accumulation. Aquat Toxicol 116: 90-101.
121. Shaw SY, Westly EC, Pittet MJ, Subramanian A, Schreiber SL, Weissleder R. 2008. Perturbational profiling of nanomaterial biologic activity. Proc Natl Acad Sci USA 105: 7387-92.
122. Shi JP, Ma CY, Xu B, Zhang HW, Yu CP. 2012. Effect of light on toxicity of nanosilver to Tetrahymena pyriformis. Environ Toxicol Chem 31: 1630-8.
123. Shvedova AA, Kagan VE, Fadeel B. 2010. Close encounters of the small kind: Adverse effects of man-made materials interfacing with the nanocosmos of biological systems. Annu Rev Pharmacol 50: 63-88.
124. Slaveykova VI, Wilkinson KJ. 2005. Predicting the bioavailability of metals and metal complexes: critical review of the biotic ligand model. Environ Chem 2: 9-24.
125. Sotiriou GA, Meyer A, Knijnenburg JTN, Panke S, Pratsinis SE. 2012. Quantifying the origin of released Ag+ ions from nanosilver. Langmuir 28: 15929-36.
126. Sotiriou GA, Pratsinis SE. 2010. Antibacterial activity of nanosilver ions and particles. Environ Sci Technol 44: 5649-54.
127. Tardito S, Bassanetti I, Bignardi C, Elviri L, Tegoni M, Mucchino C, et al. 2011. Copper binding agents acting as copper ionophores lead to caspase inhibition and paraptotic cell death in human cancer cells. J Am Chem Soc 133: 6235-42.
128. Thomas CR, George S, Horst AM, Ji Z, Miller RJ, Peralta-Videa JR, et al. 2011. Nanomaterials in the environment: from materials to highthroughput screening to organisms. ACS Nano 5: 13-20.
129. Valko M, Morris H, Cronin MTD. 2005. Metals, toxicity and oxidative stress. Curr Med Chem 12: 1161-208.
130. Visnapuu M, Joost U, Juganson K, Künnis-Beres K, Kahru A, Kisand V, Ivask A. 2013. Dissolution of silver nanowires and nanospheres dictates their toxicity to Escherichia coli. BioMed Res Int 2013: 819252.
131. von Moos N, Slaveykova VI. 2013. Oxidative stress induced by inorganic nanoparticles in bacteria and aquatic microalgae - state of the art and knowledge gaps. Nanotoxicology. DOI: 10.3109/17435390.2013.809810.
132. Wang Z, Chen J, Li X, Shao J, Peijnenburg WJGM. 2012a. Aquatic toxicity of nanosilver colloids to different trophic organisms: contributions of particles and free silver ion. Environ Toxicol Chem 31: 2408-13.
133. Wang ZY, Li N, Zhao J, White JC, Qu P, Xing BS. 2012b. CuO nanoparticle interaction with human epithelial cells: Cellular uptake, location, export, and genotoxicity. Chem Res Toxicol 25: 1512-21.
134. Weissleder R, Kelly K, Sun EY, Shtatland T, Josephson L. 2005. Cellspecific targeting of nanoparticles by multivalent attachment of small molecules. Nat Biotechnol 23: 1418-23.
135. 2 and ZnO particles on mobility and reproduction of the freshwater invertebrate Daphnia magna. Chemosphere 76: 1356-65.
136. Wong SWY, Leung PTY, Djurisic AB, Leung KMY. 2010. Toxicities of nano zinc oxide to five marine organisms: influences of aggregate size and ion solubility. Anal Bioanal Chem 396: 609-18.
137. Xia T, Kovochich M, Liong M, Maedler L, Gilbert B, Shi H, et al. 2008. Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2: 2121-34.
138. Xie Y, He Y, Irwin PL, Jin T, Shi X. 2011. Antibacterial activity and mechanism of action of zinc oxide nanoparticles against Campylobacter jejuni. Appl Environ Microb 77: 2325-31.
139. 2, ZnO and their bulk counterparts on zebrafish: acute toxicity, oxidative stress and oxidative damage. Sci Total Environ 409: 1444-52.
140. Xiu Z-M, Zhang Q-B, Puppala HL, Colvin VL, Alvarez PJJ. 2012. Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett 12: 4271-5.
141. Yang X, Gondikas AP, Marinakos SM, Auffan M, Liu J, Hsu-Kim H, Meyer JN. 2012. Mechanism of silver nanoparticle toxicity is dependent on dissolved silver and surface coating in Caenorhabditis elegans. Environ Sci Technol 46: 1119-27.
142. Yu L-P, Fang T, Xiong D-W, Zhu W-T, Sima X-F. 2011. Comparative toxicity of nano-ZnO and bulk ZnO suspensions to zebrafish and the effects of sedimentation, (OH)-O-center dot production and particle dissolution in distilled water. J Environ Monitor 13: 1975-82.
143. Zhang H, Ji Z, Xia T, Meng H, Low-Kam C, Liu R, et al. 2012. Use of metal oxide nanoparticle band gap to develop a predictive paradigm for oxidative stress and acute pulmonary inflammation. ACS Nano 6: 4349-68.
144. Zhao C-M, Wang W-X. 2011. Comparison of acute and chronic toxicity of silver nanoparticles and silver nitrate to Daphnia magna. Environ Toxicol Chem 30: 885-92.
145. Zhao J, Wang Z, Liu X, Xie X, Zhang K, Xing B. 2011. Distribution of CuO nanoparticles in juvenile carp (Cyprinus carpio) and their potential toxicity. J Hazard Mater 197: 304-10.
146. Zhu X, Zhu L, Duan Z, Qi R, Li Y, Lang Y. 2008. Comparative toxicity of several metal oxide nanoparticle aqueous suspensions to Zebrafish (Danio rerio) early developmental stage. J Environ Sci Heal A 43: 278-84.
147. Zook J, Halter M, Cleveland D, Long S. 2012. Disentangling the effects of polymer coatings on silver nanoparticle agglomeration, dissolution, and toxicity to determine mechanisms of nanotoxicity. J Nanopart Res 14: 1-9.