Enhanced toxicity of ‘bulk' titanium dioxide compared to ‘fresh' and ‘aged' nano-TiO₂ in marine mussels (Mytilus galloprovincialis)

References

• Al-Jubory AR, Handy RD. 2012. Uptake of titanium from TiO2 nanoparticle exposure in the isolated perfused intestine of rainbow trout: vanadate and novel CO2- sensitive components. Nanotoxicology in press; DOI: 10.3109/17435390.2012.735268.
   PubMedGoogle Scholar
• Al-Subiai SN, Arlt VM, Frickers PE, Readman JW, Stolpe B, Lead JR, et al. 2012. Merging nano-genotoxicology with eco-genotoxicology: An integrated approach to determine interactive genotoxic and sub-lethal toxic effects of C60 fullerenes and fluoranthene in marine mussels, Mytilus sp. Mutat Res Gen Tox En 745:92–103.
   PubMedGoogle Scholar
• Al-Subiai SN, Jha AN, Moody AJ. 2009. Contamination of bivalve haemolymph samples by adductor muscle components: implications for biomarker studies. Ecotoxicology 18:334–342.
   PubMedGoogle Scholar
• Al-Subiai SN, Moody AJ, Mustafa SA, Jha AN. 2011. A multiple biomarker approach to investigate the effects of copper on the marine bivalve mollusc, Mytilus edulis. Ecotox Environ Safe 74:1913–1920.
   PubMed Web of Science ®Google Scholar
• Baun A, Hartmann N, Grieger K, Kusk K. 2008. Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing. Ecotoxicology 17:387–395.
   PubMed Web of Science ®Google Scholar
• Bettercourt R, Dando P, Rosa D, Riou V, Colaco A, Sarrazin J, et al. 2008. Changes of gill and hemocyte-related bio-indicators during long term maintenance of the vent mussel Bathymodiolus azoricus held in aquaria at atmospheric pressure. Comp Biochem Physiol Part A 150:1–7.
   PubMedGoogle Scholar
• Bolognesi C, Landini E, Roggieri P, Fabbri R, Viarengo A. 1999. Genotoxicity biomarkers in the assessment of heavy metal effects in mussels: Experimental studies. Environ Mol Mutagen 33:287–292.
   PubMed Web of Science ®Google Scholar
• Brendler-Schwaab S, Hartmann A, Pfuhler S, Speit G. 2005. The in vivo comet assay: use and status in genotoxicity testing. Mutagenesis 20:245–254.
   PubMed Web of Science ®Google Scholar
• Brunelli E, Mauceri A, Maisano M, Bernabò I, Giannetto A, De Domenico E, et al. 2011. Ultrastructural and immunohistochemical investigation on the gills of the teleost, Thalassoma pavo L., exposed to cadmium. Acta Histochem 113(2):201–213.
   PubMedGoogle Scholar
• Canesi L, Ciacci C, Fabbri R, Marcomini A, Pojana G, Gallo G. 2012. Bivalve molluscs as a unique target group for nanoparticle toxicity. Mar Environ Res 76:16–21.
   PubMed Web of Science ®Google Scholar
• Canesi L, Fabbri R, Gallo G, Vallotto D, Marcomini A, Pojana G. 2010. Biomarkers in Mytilus galloprovincialis exposed to suspensions of selected nanoparticles (Nano carbon black, C60 fullerene, Nano-TiO2, Nano-SiO2). Aquat Toxicol 100:168–177.
   PubMed Web of Science ®Google Scholar
• Canty MN, Hutchinson TH, Brown RJ, Jones MB, Jha AN. 2009. Linking genotoxic responses with cytotoxic and behavioural or physiological consequences: Differential sensitivity of echinoderms (Asterias rubens) and marine molluscs (Mytilus edulis). Aquat Toxicol 94:68–76.
   PubMed Web of Science ®Google Scholar
• Cappello T, Maisano M, D'Agata A, Natalotto A, Mauceri A, Fasulo S. 2013. Effects of environmental pollution in caged mussels (Mytilus galloprovincialis). Mar Environ Res doi: 10.1016/j.marenvres.2012.12.010.
   Google Scholar
• Chen J, Liu M, Zhang J, Ying X, Jin L. 2004. Photocatalytic degradation of organic wastes by electrochemically assisted TiO2 photocatalytic system. J Environ Manage 70:43–47.
   PubMed Web of Science ®Google Scholar
• Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal Biochem 162:156–159.
   PubMed Web of Science ®Google Scholar
• Ciacci C, Barmo C, Gallo G, Maisano M, Cappello T, D'Agata A, et al. 2012. Effects of sub-lethal, environmentally relevant concentrations of hexavalent Chromium in the gills of Mytilus galloprovincialis. Aquat Toxicol 120–121:109–118.
   PubMed Web of Science ®Google Scholar
• Collins AR, Ma AG, Duthie SJ. 1995. The kinetics of repair of oxidative DNA damage (strand breaks and oxidised pyrimidines) in human cells. Mutat Res 336:69–77.
   PubMed Web of Science ®Google Scholar
• Dallas LJ, Bean TP, Turner A, Lyons BP, Jha A. 2013. Oxidative DNA damage may not mediate Ni-induced genotoxicity in marine mussels: Assessment of genotoxic biomarkers and transcriptional responses of key stress genes. Mutat Res 754:22–31.
   PubMedGoogle Scholar
• Dodd NJF, Jha AN. 2009. Titanium dioxide induced cell damage: a proposed role of the carboxyl radical. Mutat Res 660:79–82.
   PubMed Web of Science ®Google Scholar
• Dodd NJF, Jha AN. 2011. Photoexcitation of aqueous suspensions of titanium dioxide nanoparticles: an electron spin resonance spin trapping study of potentially oxidative reactions. Photochem Photobiol 87:632–640.
   PubMedGoogle Scholar
• Dondero F, Piacentini L, Banni M, Rebelo M, Burlando B, Viarengo A. 2005. Quantitative PCR analysis of two molluscan metallothionein genes unveils differential expression and regulation. Gene 345:259–270.
   PubMed Web of Science ®Google Scholar
• Esterkin CR, Negro AC, Alfano OM, Cassano AE. 2005. Air pollution remediation in a fixed bed photocatalytic reactor coated with TiO2. AIChE J 51(8):2298–2310.
   Google Scholar
• European Commission. 2005. Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR). Modified Opinion (after public consultation) on the appropriateness of existing methodologies to assess the potential risks associated with engineered and adventitious products of nanotechnologies. http://ec.europa.eu/health/ph_risk/committees/04_scenihr/docs/scenihr_o_003b.pdf; Luxembourg, European Commission: 1-79.
   Google Scholar
• Farré M, Gajda-Schrantz K, Kantiani L, Barceló D. 2009. Ecotoxicity and analysis of nanomaterials in the aquatic environment. Anal Bioanal Chem 393:81–95.
   PubMed Web of Science ®Google Scholar
• Fasulo S, Iacono F, Cappello T, Corsaro C, Maisano M, D'Agata A, et al. 2012. Metabolomic investigation of Mytilus galloprovincialis (Lamarck 1819) caged in aquatic environments. Ecotox Envir Saf 84:139–146.
   PubMed Web of Science ®Google Scholar
• Fasulo S, Marino S, Mauceri A, Maisano M, Giannetto A, D'Agata A, et al. 2010b. A multi biomarker approach in Coris julis living in a natural Environment. Ecotox Environ Safe 73:1565–1573.
   PubMed Web of Science ®Google Scholar
• Fasulo S, Mauceri A, Giannetto A, Maisano M, Bianchi N, Parrino V. 2008. Expression of metallothionein mRNAs by in situ hybridization in the gills of Mytilus galloprovincialis, from natural polluted environments. Aquat Toxicol 88:62–68.
   PubMed Web of Science ®Google Scholar
• Fasulo S, Mauceri A, Maisano M, Giannetto A, Parrino V, Gennuso F, et al. 2010a. Immunohistochemical and molecular biomarkers in Coris julis exposed to environmental contaminants. Ecotox Environ Safe 73:873–882.
   PubMed Web of Science ®Google Scholar
• Federici G, Shaw BJ, Handy RD. 2007. Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): Gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 84:415–430.
   PubMed Web of Science ®Google Scholar
• Fouqueray M, Dufils B, Vollat B, Chaurand P, Botta C, Abacci K, et al. 2012. Effects of aged TiO2 nanomaterial from sunscreen on Daphnia magna exposed by dietary route. Environ Pollut 163:55–61.
   PubMed Web of Science ®Google Scholar
• Handy R, Shaw B. 2007. Toxic effects of nanoparticles and nanomaterials: implications for public health, risk assessment and the public perception of nanotechnology. Health Risk Soc 9:125–144.
   Web of Science ®Google Scholar
• Handy R, von der Kammer F, Lead J, HasselloÌM, Owen R, et al. 2008. The ecotoxicology and chemistry of manufactured nanoparticles. Ecotoxicology 17:287–314.
   PubMed Web of Science ®Google Scholar
• Handy RD, van den Brink N, Chappell M, Mühling M, Behra R, Dusinskà M, et al. 2012. Practical considerations for conducting ecotoxicity test methods with manufactured nanomaterials: what have we learnt so far? Ecotoxicology 21:933–972.
   PubMed Web of Science ®Google Scholar
• Hartwig A, Asmuss M, Ehleben I, Herzer U, Kostelac D, Pelzer A, et al. 2002. Interference by toxic metal ions with DNA repair processes and cell cycle control: molecular mechanisms. Environ Health Perspect 110 S5:797–799.
   Google Scholar
• Henderson L, Wolfreys A, Fedyk J, Bourner C, Windebank S. 1998. The ability of the Comet assay to discriminate between genotoxins and cytotoxins. Mutagenesis 13:89–94.
   PubMed Web of Science ®Google Scholar
• Jassby D, Budarz JF, Wiesner M. 2012. Impact of aggregate size and structure on the photocatalytic properties of TiO2 and NO nanoparticles. Environ Sci Technol 46:6934–6941.
   PubMed Web of Science ®Google Scholar
• Jha AN, Dogra Y, Turner A, Millward GE. 2005. Impact of low doses of tritium on the marine mussel, Mytilus edulis: genotoxic effects and tissue-specific bioconcentration. Mutat Res 586:47–57.
   PubMed Web of Science ®Google Scholar
• Jha AN. 2008. Ecotoxicological applications and significance of the comet assay. Mutagenesis 23:207–221.
   PubMed Web of Science ®Google Scholar
• Kaegi R, Ulrich A, Sinnet B, Vonbank R, Wichser A, Zuleeg S, et al. 2008. Synthetic TiO2 nanoparticle emission from exterior facades into the aquatic environment. Environ Pollut 156(2):233–239.
   PubMed Web of Science ®Google Scholar
• Kiser MA, Westerhoff P, Benn T, Wang Y, Perez-Rivera J, Hristovski K. 2009. Titanium nanomaterial removal and release from wastewater treatment plants. Environ Sci Technol 43(17):6757–6763.
   PubMed Web of Science ®Google Scholar
• Klaine SJ, Alvarez PJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, et al. 2008. Nanomaterials in the environment: Behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27(9):1825–1851.
   PubMed Web of Science ®Google Scholar
• Labille J, Feng J, Botta C, Borschneck D, Sammut M, Cabie M, et al. 2010. Aging of TiO2 nanocomposite used in sunscreen. Dispersion and fate of the degradation products in aqueous environment. Environ Pollut 158. 3482:3489.
   Google Scholar
• Lapied E, Nahmani JY, Moudilou E, Chaurand P, Labille J, Rose J, et al. 2011. Ecotoxicological effects of an aged TiO2 nanocomposite measured as apoptosis in the anecic earthworm Lumbricus terrestris after exposure through water, food and soil. Environ Int 37:1105–1110.
   PubMed Web of Science ®Google Scholar
• Lemoine S, Bigot Y, Sellos D, Cosson RP, Laulier M. 2000. Metallothionein isoforms in Mytilus edulis (Mollusca, Bivalvia): complementary DNA characterization and quantification of expression in different organs after exposure to cadmium, zinc, and copper. Mar Biotechnol 2:195–203.
   PubMed Web of Science ®Google Scholar
• Lin H, Huang CP, Li W, Ni C, Shah SI, Tseng YH. 2006. Size dependency of nanocrystalline TiO2 on its optical property and photocatalytic reactivity exemplified by 2-chlorophenol. Appl Catal B 68:1–11.
   Web of Science ®Google Scholar
• Millward GE, Kadam S, Jha AN. 2012. Tissue-specific assimilation, depuration and toxicity of nickel in Mytilus edulis. Environ Pollut 162:406–412.
   Google Scholar
• Minniti F, Maisano M, Mauceri A, Giannetto A, Fasulo S. 2009. GTH I and GTH II in the pituitary gland of swordfish (Xiphias gladius). Ital J Zool 76(3):269–278.
   Google Scholar
• Moore MN. 2006. Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ Int 32:967–976.
   PubMed Web of Science ®Google Scholar
• Mustafa SA, Davies SJ, Jha AJ. 2012. Determination of hypoxia and dietary copper mediated sub-lethal toxicity in carp, Cyprinus carpio, at different levels of biological organisation. Chemosphere 87:413–422.
   PubMed Web of Science ®Google Scholar
• Nagaveni K, Sivalingam G, Hegde MS, Madras G. 2004. Photocatalytic degradation of organic compounds over combustion-synthesized nano-TiO2. Environ Sci Technol 38:1600–1604.
   PubMed Web of Science ®Google Scholar
• Nakagawa Y, Wakuri S, Sakamoto K, Tanaka N. 1997. The photogenotoxicity of titanium dioxide particles. Mutat Res Genet Toxicol Environ Mutagen 394:125–132.
   PubMed Web of Science ®Google Scholar
• Nowack B, Bucheli TD. 2007. Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 150:5–22.
   PubMed Web of Science ®Google Scholar
• Oberdörster G, Oberdörster E, Oberdörster J. 2005. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Persp 113:823–839.
   PubMed Web of Science ®Google Scholar
• Ramsden CS, Smith TJ, Shaw BJ, Handy RD. 2009. Dietary exposure to titanium dioxide nanoparticles in rainbow trout (Oncorhynchus mykiss): no effect on growth, but subtle biochemical disturbances in the brain. Ecotoxicology 18:939–951.
   PubMed Web of Science ®Google Scholar
• Reeves JF, Davies SJ, Dodd NJF, Jha AN. 2008. Hydroxyl radicals (OH) are associated with titanium dioxide (TiO2) nanoparticle-induced cytotoxicity and oxidative DNA damage in fish cells. Mutat Res 640:113–122.
   PubMed Web of Science ®Google Scholar
• Scown TM, van Aerle R, Tyler CR. 2010. Review: Do engineered nanoparticles pose a significant threat to the aquatic environment? Crit Rev Toxicol 40:653–670.
   PubMed Web of Science ®Google Scholar
• Singh J, Mclean JA, Pritchard DE, Montaser A, Patierno SR. 1998. Sensitive quantitation of chromium-DNA adducts by inductively coupled plasma mass spectrometry with a direct injection high-efficiency nebulizer. Toxicol Sci 46:260–265.
   PubMed Web of Science ®Google Scholar
• Tseng YH, Lin HY, Kuo CS, Li YY, Huang CP. 2006. Thermostability of nano-TiO2 and its photolytic activity. React Kine Catal Lett 89:63–69.
   Google Scholar
• Tsuang Y, Sun J, Huang Y, Lu C, Chang W, Wang C. 2008. Studies of photokilling of bacteria using titanium dioxide nanoparticles. Artif Organs 32:167–174.
   PubMed Web of Science ®Google Scholar
• Uchino T, Tokunaga H, Ando M, Utsumi H. 2002. Quantitative determination of OH radical generation and its cytotoxicity induced by TiO2-UVA treatment. Toxicol In Vitro 16:629–635.
   PubMed Web of Science ®Google Scholar
• Van Herwijnen R, Laverye T, Poole J, Hodson ME, Hutchings TR. 2007. The effect of organic materials on the mobility and toxicity of metals in contaminated soils. Appl Geochem 22:2422–2434.
   Web of Science ®Google Scholar
• Vevers WF, Jha AN. 2008. Genotoxic and cytotoxic potential of titanium dioxide (TiO2) nanoparticles on fish cells in vitro. Ecotoxicology 17:410–420.
   PubMed Web of Science ®Google Scholar
• Wang H, Wick R, Xing B. 2009. Toxicity of nanoparticulate and bulk ZnO, Al2O3 and TiO2 to the nematode Caenorhabditis elegans. Environ Pollut 157:1171–1177.
   PubMed Web of Science ®Google Scholar
• Ward JE, Kach DJ. 2009. Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. Mar Environ Res 68(3):137–142.
   PubMedGoogle Scholar
• Weir A, Westerhoff P, Fabricius L, Hristovski K and von Goetz N. 2012. Titanium dioxide nanoparticles in food and personal care products. Environ Sci Technol 46(4):2242–2250.
   PubMed Web of Science ®Google Scholar
• Windeatt KM, Handy RD. 2012. Effect of nanomaterials on the compound action of the shore crab, Carcinus maenas. Nanotoxicology DOI: 10.3109/17435390.2012.663809.
   PubMedGoogle Scholar
• Xiong D, Fang T, Yu J, Sima X, Zhu W. 2011. Effects of nano-scale TiO2, ZnO and their bulk counterparts on zebra fish: Acute toxicity, oxidative stress and oxidative damage. Sci Total Environ 409:1444–1452.
   PubMed Web of Science ®Google Scholar
• Zhu XS, Zhu I, Duan ZH, Qi RQ, Li Y, Lang YP. 2008. Comparative toxicity of several metal oxide nanoparticle aqueous suspensions to Zebrafish (Danio rerio) early developmental stage. J Environ Sci Health A Tox Hazard Subst Environ Eng 43:278–284.
   PubMed Web of Science ®Google Scholar