Nanoparticle size and combined toxicity of TiO₂ and DSLS (surfactant) contribute to lysosomal responses in digestive cells of mussels exposed to TiO₂ nanoparticles

References

• Ates M, Daniels J, Arslan Z, Farah IO. 2013a. Effects of aqueous suspensions of titanium dioxide nanoparticles on Artemia salina: assessment of nanoparticle aggregation, accumulation, and toxicity. Environ Monit Assess 185:3339–48
   PubMed Web of Science ®Google Scholar
• Ates M, Demir V, Adiguzel R, Arslan Z. 2013b. Bioaccumulation, subacute toxicity, and tissue distribution of engineered titanium dioxide nanoparticles in goldfish (Carassius auratus). J Nanomater 2013:460518
   PubMed Web of Science ®Google Scholar
• BAuA UBA, BfR BAm. PTB. (2013). Nanotechnology – Risks related to nanomaterials for humans and the environment (2007–2011). First evaluation on the Joint Research Strategy of German Governmental Research Institutions; German Federal Ministry of Environment. 60 pp
   Google Scholar
• Barmo C, Ciacci C, Canonico B, Fabbri R, Cortese K, Balbi T, et al 2013. In vivo effects of n-TiO2 on digestive gland and immune function of the marine bivalve Mytilus galloprovincialis. Aquat Toxicol 132:9–18
   PubMed Web of Science ®Google Scholar
• Baun A, Hartmann NB, Grieger K, Kusk KO. 2008. Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing. Ecotoxicology 17:387–95
   PubMed Web of Science ®Google Scholar
• Berry CC, Wells S, Charles S, Aitchison G, Curtis ASG. 2003. Dextran and albumin derivatised iron oxide nanoparticles: influence on fibroblasts in vitro. Biomaterials 24:4551–7
   PubMed Web of Science ®Google Scholar
• Berry CC, Charles S, Wells S, Dalby MJ, Curtis ASG. 2004a. The influence of transferrin stabilised magnetic nanoparticles on human dermal fibroblasts in culture. Int J Pharm 269:211–25
   PubMed Web of Science ®Google Scholar
• Berry CC, Wells S, Charles S, Aitchison G, Curtis ASG. 2004b. Cell response to dextran-derivatised iron oxide nanoparticles post internalisation. Biomaterials 25:5405–13
   PubMed Web of Science ®Google Scholar
• Brunelli A, Pojana G, Callegaro S, Marcomini A. 2013. Agglomeration and sedimentation of titanium dioxide nanoparticles (n-TiO2) in synthetic and real waters. J Nanopart Res 15:1684–94
   Web of Science ®Google Scholar
• Buffet PE, Tankoua OF, Pan JF, 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
   PubMed Web of Science ®Google Scholar
• Canesi L, Ciacci C, Betti M, Fabbri R, Canonico B, Fantinati A, et al 2008. Immunotoxicity of carbon black nanoparticles to blue mussel hemocytes. Environ Int 34:1114–19
   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 100:168–77
   PubMed Web of Science ®Google 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, Frenzilli G, Balbi T, Bernardeschi M, Ciacci M, Corsolini S, et al 2014. Interactive effects of n-TiO2 and 2,3,7,8-TCDD on the marine bivalve Mytilus galloprovincialis. Aquat Toxico 153:53–65
   PubMed Web of Science ®Google Scholar
• Cserháti T, Forgács E, Oros G. 2002. Biological activity and environmental impact of anionic surfactants. Environ Int 28:337–48
   PubMed Web of Science ®Google Scholar
• D’Agata A, Fasulo S, Dallas LJ, Fisher AS, Maisano M, Readman JW, Jha AW. 2014. Enhanced toxicity of ‘bulk’ titanium dioxide compared to ‘fresh’ and ‘aged’ nano-TiO2 in marine mussels (Mytilus galloprovincialis). Nanotoxicology 8:549–58
   PubMed Web of Science ®Google Scholar
• Danscher G, Hacker G, Hauser-Kronberger C, Grimelius L. 1995. Trends in autometallographic silver amplification of colloidal gold particles. In: Hayat MA, ed. Immunogold Silver Staining: Principles, Methods and Applications. Boca Raton, FL: CRC Press
   Google Scholar
• Efron B, Tibshirani RJ. 1993. An Introduction to the Bootstrap. London: Chapman & Hall
   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 84:415–30
   PubMed Web of Science ®Google Scholar
• Galloway T, Lewis C, Dolciotti I, Johnston BD, Moger J, Regoli F. 2010. Sublethal toxicity of nano-titanium dioxide and carbon nanotubes in a sediment dwelling marine polychaete. Environ Pollut 158:1748–55
   PubMed Web of Science ®Google Scholar
• Garmendia L, Izagirre U, Cajaraville MP, Marigómez I. 2011a. Application of a battery of biomarkers in mussel digestive gland to assess long-term effects of the Prestige oil spill in Galicia and the Bay of Biscay: lysosomal responses. J Environ Monit 13:901–14
   PubMedGoogle Scholar
• Garmendia L, Soto M, Vicario U, Kim Y, Cajaraville MP, Marigómez I. 2011b. Application of a battery of biomarkers in mussel digestive gland to assess long-term effects of the Prestige oil spill in Galicia and Bay of Biscay: tissue-level biomarkers and histopathology. J Environ Monitor 13:915–32
   PubMedGoogle Scholar
• Gottschalk F, Nowack B. 2012. Modeling the environmental release and exposure of engineered nanomaterials. In: Leszczynski J, Puzyn T, eds. Towards Efficient Designing of Safe Nanomaterials: Innovative Merge of Computational Approaches and Experimental Techniques. Cambridge, UK: Royal Society of Chemistry, 284–313
   Google Scholar
• Griffitt RJ, Luo J, Gao J, Bonzongo JC, Barber DS. 2008. Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 27:1972–8
   PubMed Web of Science ®Google Scholar
• Handy R, Von der Kammer F, Lead J, Hassellöv M, Owen R, Crane M. 2008. The ecotoxicology and chemistry of manufactured nanoparticles. Ecotoxicology 17:287–314
   PubMed Web of Science ®Google Scholar
• Handy R, Van den Brink N, Chappell M, Mühling M, Behra R, Dušinská M, et al 2012. Practical considerations for conducting ecotoxicity test methods with manufactured nanomaterials: what have we learnt so far? Ecotoxicology 21:933–72
   PubMed Web of Science ®Google Scholar
• Hartmann NB, Von der Kammer F, Hoffman T, Baalousha M, Ottofueling S, Baun A. 2010. Algal testing of titanium dioxide nanoparticles-testing considerations, inhibitory effects and modification of cadmium bioavailability. Toxicology 269:190–7
   PubMed Web of Science ®Google Scholar
• Hayat MA. 2000. Principles and Techniques of Electron Microscopy: Biological Applications. Cambridge: Cambridge University Press
   Google Scholar
• IARC. 2010. IARC Monographs on the evaluation of carcinogenic risks to humans. Vol. 93. Carbon black, titanium dioxide, and talc. International Agency for Research on Cancer. Lyon, France: World Health Organisation
   Google Scholar
• Jemec A, Drobne D, Remskar M, Sepcic D, Tisler T. 2008. Effects of ingested nano-sized titanium dioxide on terrestrial isopods (Porcellio scaber). Environ Toxicol Chem 27:1904–14
   PubMed Web of Science ®Google Scholar
• Jiang J, Oberdorster G, Elder A, Gelein R, Mercer P, Biswas P. 2008. Does nanoparticle activity depend upon size and crystal phase? Nanotoxicology 2:33–42
   PubMed Web of Science ®Google Scholar
• Katsumiti A, Berhanu D, Howard KT, Arostegui I, Oron M, Reip P, et al 2014a. Cytotoxicity of TiO2 nanoparticles to mussel hemocytes and gill cells in vitro: influence of synthesis method, crystalline structure, size and additive. Nanotoxicology 4:1–11
   Google Scholar
• Katsumiti A, Gilliland D, Arostegui I, Cajaraville MP. 2014b. Cytotoxicity and cellular mechanisms involved in the toxicity of CdS quantum dots in hemocytes and gill cells of the mussel Mytilus galloprovincialis. Aquat Toxicol 153:39–52
   PubMed Web of Science ®Google Scholar
• Klaine SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD, Lyon DY. 2008. Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27:1825–51
   PubMed Web of Science ®Google Scholar
• Liu B, Yu Z, Song X, Yang F. 2010. Effects of sodium dodecylbenzene sulfonate and sodium dodecyl sulfate on the Mytilus galloprovincialis biomarker system. Ecotox Environ Safe 73:835–41
   PubMed Web of Science ®Google Scholar
• Marigómez I, Soto M, Cajaraville MP, Angulo E, Giamberini L. 2002. Cellular and subcellular distribution of metals in molluscs. Microsc Res Techniq 56:358–92
   PubMed Web of Science ®Google Scholar
• Marigomez I, Soto M, Cancio I, Orbea A, Garmendia L, Cajaraville MP. 2006. Cell and tissue biomarkers in mussel, and histopathology in hake and anchovy from Bay of Biscay after the prestige oil spill (monitoring campaign 2003). Mar Pollut Bull 53:287–304
   PubMed Web of Science ®Google Scholar
• Menard A, Damjana D, Jemec A. 2011. Ecotoxicity of nanosized TiO2. Review of in vivo data. Environ Pollut 159:677–84
   PubMed Web of Science ®Google Scholar
• Moore MN. 2006. Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ Int 32:967–76
   PubMed Web of Science ®Google Scholar
• Mueller NC, Nowack B. 2008. Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–53
   PubMed Web of Science ®Google Scholar
• Musyanovych A, Dausend J, Dass M, Walther P, Mailänder V V, Landfester K. 2011. Criteria impacting the cellular uptake of nanoparticles: a study emphasizing polymer type and surfactant effects. Acta Biomater 7:4160–8
   PubMed Web of Science ®Google Scholar
• Park EJ, 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
   PubMed Web of Science ®Google Scholar
• Ringwood AH, Levi Polyachenko N, Carroll DL. 2009. Fullerene exposures with oysters: embryonic, adult, and cellular responses. Environ Sci Technol 43:7136–41
   PubMed Web of Science ®Google Scholar
• Ringwood AH, McCarthy M, Bates TC, Carroll DL. 2010. The effects of silver nanoparticles on oyster embryos. Mar Environ Res 69:49–51
   PubMed Web of Science ®Google Scholar
• Rudel RA, Attfield KR, Schifano JN, Brody JG. 2007. Chemicals causing mammary gland tumors in animals signal new directions for epidemiology, chemicals testing, and risk assessment for breast cancer prevention. Cancer 109:2635–66
   PubMed Web of Science ®Google Scholar
• Soto M, Zaldibar B, Cancio I, Taylor MG, Turner M, Morgan AJ, Marigómez I. 2002. Subcellular distribution of cadmium and its cellular ligands in mussel digestive gland cells as revealed by combined autometallography and X-ray microprobe analysis. Histochem J 34:273–80
   PubMedGoogle Scholar
• Tedesco S, Doyle H, Redmond G, Sheehan D. 2008. Gold nanoparticles and oxidative stress in Mytilus edulis. Mar Environ Res 66:131–3
   PubMed Web of Science ®Google Scholar
• Uboldi C, Urbán P, Gilliland D, Bajak E, Valsami-Jones E, Ponti J, Rossi F. 2016. Role of the crystalline form of titanium dioxide nanoparticles: rutile, and not anatase, induces toxic effects in Balb/3T3 mouse fibroblasts. Toxicology In Vitro 31:137–45
   PubMed Web of Science ®Google Scholar
• UNEP/RAMOGE. 1999. Manual on the biomarkers recommended for the MED POL Biomonitoring Programme. UNEP, Athens
   Google Scholar
• USEPA. (2010a) Nanomaterial case studies: nanoscale titanium dioxide in water treatment and in topical sunscreen (Final). U.S. Environmental Protection Agency, Washington DC, EPA/600/R-09/057F
   Google Scholar
• USEPA. (2010b). State of the Science Literature Review: Nano Titanium Dioxide Environmental Matters (STREAMS Final Report Contract No. EP-C-05-059); EPA/600/R-10/089; U.S. Environmental Protection Agency: Washington DC
   Google Scholar
• Vicario-Parés U, Castañaga L, Lacave JM, Oron M, Reip P, Berhanu D, et al 2014. Comparative toxicity of metal oxide nanoparticles (CuO, ZnO and TiO2) on developing zebrafish embryos. J Nanopart Res 16:2550
   Web of Science ®Google Scholar
• Ward JE, Kach DJ. 2009. Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. Mar Environ Res 68:137–42
   PubMed Web of Science ®Google Scholar
• Zhu X, Zhou J, Cai Z. 2011. The toxicity and oxidative stress of TiO2 nanoparticles in marine abalone (Haliotis diversicolor supertexta). Mar Pollut Bull 63:334–8
   PubMed Web of Science ®Google Scholar
• Zhu Y, Eaton JW, Li C. 2012. Titanium dioxide (TiO2) nanoparticles preferentially induce cell death in transformed cells in a Bak/Bax- independent fashion. PLoS One 7:e50607
   Google Scholar