Effects of titanium dioxide nanoparticle exposure in Mytilus galloprovincialis gills and digestive gland

Abstract Despite the wide use of nanoscale materials in several fields, some aspects of the nanoparticle behavior have to be still investigated. In this work, we faced the aspect of environmental effects of increasing concentrations of TiO2NPs using the Mytilus galloprovincialis as an animal model and carrying out a multidisciplinary approach to better explain the results. Bioaccumulation suggested that the gills and digestive gland are the most sensitive organs to TiO2NP exposure. Histological observations have evidenced an altered tissue organization and a consistent infiltration of hemocytes, as a consequence of the immune system activation, even though an increase in lipid peroxidation is uncertain and DNA damage became relevant only at high exposure dose (10 mg/L) or for longer exposure time (96 h). However, the over expression of SOD1 mRNA strengthen the concept that the toxicity of TiO2NPs could occur indirectly by ROS production. TEM analysis showed the presence of multilamellar bodies, RER fragmentation, and cytoplasmic vacuolization within relevant presence of dense granules, residual bodies, and lipid inclusions. These findings support the evidence of an initial inflammatory response by the cells of the target organs leading to apoptosis. In conclusion, we can state that certainly the exposure to TiO2NPs has affected our animal model from cellular to molecular levels. Interestingly, the same responses are caused by lower TiO2NP concentration and longer exposure time as well as higher doses and shorter exposure. We do not know if some of the conditions detected are reversible, then further studies are required to clarify this aspect.

[1]  C. M. Krow Nanotechnology and Asbestos: Informing Industry About Carbon Nanotubes, Nanoscale Titanium Dioxide, and Nanosilver , 2012, IEEE Nanotechnology Magazine.

[2]  J. Readman,et al.  Enhanced toxicity of ‘bulk' titanium dioxide compared to ‘fresh' and ‘aged' nano-TiO2 in marine mussels (Mytilus galloprovincialis) , 2014, Nanotoxicology.

[3]  J. Widdows,et al.  Scope for growth and contaminant levels in North Sea mussels Mytilus edulis , 1995 .

[4]  J. Devoll Nanoparticle toxicity. , 2010, Aviation, space, and environmental medicine.

[5]  Amaya Azqueta,et al.  Towards a more reliable comet assay: optimising agarose concentration, unwinding time and electrophoresis conditions. , 2011, Mutation research.

[6]  G. Bernardini,et al.  In Vivo and In Vitro Models for Nanotoxicology Testing , 2009 .

[7]  H. U. Riisgård,et al.  Formation of metallothioneins in relation to accumulation of cadmium in the common mussel Mytilus edulis , 1982 .

[8]  L. Vergani,et al.  Radical scavenging abilities of fish MT-A and mussel MT-10 metallothionein isoforms: An ESR study. , 2008, Journal of inorganic biochemistry.

[9]  E. Cabiscol,et al.  Oxidative stress in bacteria and protein damage by reactive oxygen species. , 2000, International microbiology : the official journal of the Spanish Society for Microbiology.

[10]  E. Tongiorgi,et al.  Acute stress alters transcript expression pattern and reduces processing of proBDNF to mature BDNF in Dicentrarchus labrax , 2010, BMC Neuroscience.

[11]  Arezou A Ghazani,et al.  Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. , 2006, Nano letters.

[12]  Nathalie Tufenkji,et al.  Characterizing manufactured nanoparticles in the environment: multimethod determination of particle sizes. , 2009, Environmental science & technology.

[13]  J. Koropatnick,et al.  Signaling events for metallothionein induction. , 2003, Mutation research.

[14]  Salvatore Fasulo,et al.  Impact of environmental pollution on caged mussels Mytilus galloprovincialis using NMR-based metabolomics. , 2013, Marine pollution bulletin.

[15]  Richard D Handy,et al.  Manufactured nanoparticles: their uptake and effects on fish—a mechanistic analysis , 2008, Ecotoxicology.

[16]  Xiaoshan Zhu,et al.  Toxicity and bioaccumulation of TiO2 nanoparticle aggregates in Daphnia magna. , 2010, Chemosphere.

[17]  E. Kasahara,et al.  Ultraviolet irradiation of titanium dioxide in aqueous dispersion generates singlet oxygen , 2001, Redox report : communications in free radical research.

[18]  G. Pojana,et al.  Immunomodulation by Different Types of N-Oxides in the Hemocytes of the Marine Bivalve Mytilus galloprovincialis , 2012, PloS one.

[19]  D. A. Nelson,et al.  Effects of long-term exposure to silver or copper on growth, bioaccumulation and histopathology in the blue mussel Mytilus edulis , 1984 .

[20]  Alessia Giannetto,et al.  Cellular biomarkers in the mussel Mytilus galloprovincialis (Bivalvia: Mytilidae) from Lake Faro (Sicily, Italy) , 2014 .

[21]  J. Evan Ward,et al.  Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. , 2009, Marine environmental research.

[22]  B. Bernard,et al.  Toxicology and carcinogenesis studies of dietary titanium dioxide-coated mica in male and female Fischer 344 rats. , 1989, Journal of toxicology and environmental health.

[23]  L. Canesi,et al.  Persistence of vibrios in marine bivalves: the role of interactions with haemolymph components. , 2005, Environmental microbiology.

[24]  C. Gagnon,et al.  Ecotoxicity of CdTe quantum dots to freshwater mussels: impacts on immune system, oxidative stress and genotoxicity. , 2008, Aquatic toxicology.

[25]  Jamie R Lead,et al.  Nanomaterials in the environment: Behavior, fate, bioavailability, and effects , 2008, Environmental toxicology and chemistry.

[26]  K Botzenhart,et al.  Reactive Oxygen Species , 2014 .

[27]  Rosalba Gornati,et al.  Nanomedicine for the Brain and the Eye: Disease Management in Poorly Accessible Compartments of the Body , 2014 .

[28]  A. Villalba,et al.  Enzymes Involved in Defense Functions of Hemocytes of Mussel Mytilus galloprovincialis , 1997, Journal of invertebrate pathology.

[29]  J. Song,et al.  Does the Antibacterial Activity of Silver Nanoparticles Depend on the Shape of the Nanoparticle? A Study of the Gram-Negative Bacterium Escherichia coli , 2007, Applied and Environmental Microbiology.

[30]  J. M. Davis,et al.  Experimental studies in rats on the effects of asbestos inhalation coupled with the inhalation of titanium dioxide or quartz. , 1991, International journal of experimental pathology.

[31]  T. J. Naimo A review of the effects of heavy metals on freshwater mussels , 1995, Ecotoxicology.

[32]  Baoshan Xing,et al.  Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. , 2007, Environmental pollution.

[33]  N. Chandrasekaran,et al.  Acute Toxicity of TiO2 Nanoparticles to Ceriodaphnia dubia under Visible Light and Dark Conditions in a Freshwater System , 2013, PloS one.

[34]  Jan Terje Kvaløy,et al.  Error propagation in relative real-time reverse transcription polymerase chain reaction quantification models: the balance between accuracy and precision. , 2006, Analytical biochemistry.

[35]  G. Bernardini,et al.  Gene expression in nanotoxicology: A search for biomarkers of exposure to cobalt particles and ions , 2007 .

[36]  R. Mariani-Costantini,et al.  Cytotoxicity and morphological transforming potential of cobalt nanoparticles, microparticles and ions in Balb/3T3 mouse fibroblasts: an in vitro model , 2014, Nanotoxicology.

[37]  A. Villalba,et al.  Morphological characterization of the hemocytes of the clam, Ruditapes decussatus (Mollusca: Bivalvia). , 1997, Journal of invertebrate pathology.

[38]  G. Bernardini,et al.  Toxicology of Engineered Metal Nanoparticles , 2011 .

[39]  Bryce J Marquis,et al.  Analytical methods to assess nanoparticle toxicity. , 2009, The Analyst.

[40]  M. Reed,et al.  The History of Photodetection and Photodynamic Therapy¶ , 2001, Photochemistry and photobiology.

[41]  N. Wu,et al.  Particle length-dependent titanium dioxide nanomaterials toxicity and bioactivity , 2009, Particle and Fibre Toxicology.

[42]  M. Raspanti,et al.  Engineered cobalt oxide nanoparticles readily enter cells. , 2009, Toxicology letters.

[43]  M. Wiesner,et al.  Comparison of electrokinetic properties of colloidal fullerenes (n-C60) formed using two procedures. , 2005, Environmental science & technology.

[44]  B. Nowack,et al.  Occurrence, behavior and effects of nanoparticles in the environment. , 2007, Environmental pollution.

[45]  A. Marcomini,et al.  Embryotoxicity of TiO2 nanoparticles to Mytilus galloprovincialis (Lmk). , 2013, Marine environmental research.

[46]  Jin Zou,et al.  Anatase TiO2 single crystals with a large percentage of reactive facets , 2008, Nature.

[47]  H. Utsumi,et al.  Quantitative determination of OH radical generation and its cytotoxicity induced by TiO(2)-UVA treatment. , 2002, Toxicology in vitro : an international journal published in association with BIBRA.

[48]  G. Bernardini,et al.  Heparin and Carboxymethylchitosan Metal Nanoparticles: An Evaluation of Their Cytotoxicity , 2013, BioMed research international.

[49]  Ibo van de Poel,et al.  Sunscreens with Titanium Dioxide (TiO2) Nano-Particles: A Societal Experiment , 2010, Nanoethics.

[50]  Chuncheng Chen,et al.  Photosensitized degradation of dyes in polyoxometalate solutions versus TiO2 dispersions under visible-light irradiation: mechanistic implications. , 2004, Chemistry.

[51]  Salvatore Fasulo,et al.  Metabolomic investigation of Mytilus galloprovincialis (Lamarck 1819) caged in aquatic environments. , 2012, Ecotoxicology and environmental safety.

[52]  G. Pojana,et al.  Biomarkers in Mytilus galloprovincialis exposed to suspensions of selected nanoparticles (Nano carbon black, C60 fullerene, Nano-TiO2, Nano-SiO2). , 2010, Aquatic toxicology.

[53]  D. Pang,et al.  Preparation and characterization of CdS quantum dots chitosan biocomposite , 2003 .

[54]  Arturo A. Keller,et al.  TiO2 Nanoparticles Are Phototoxic to Marine Phytoplankton , 2012, PloS one.

[55]  A. Fujishima,et al.  Induction of cytotoxicity by photoexcited TiO2 particles. , 1992, Cancer research.

[56]  Salvatore Fasulo,et al.  Neurotoxicological effects on marine mussel Mytilus galloprovincialis caged at petrochemical contaminated areas (eastern Sicily, Italy): ¹H NMR and immunohistochemical assays. , 2015, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[57]  Ick Chan Kwon,et al.  Cell-permeable and biocompatible polymeric nanoparticles for apoptosis imaging. , 2006, Journal of the American Chemical Society.

[58]  G. Owen The fine structure of the digestive tubules of the Marine Bivalve Cardium edule. , 1970, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[59]  D. Minetto,et al.  Ecotoxicity of engineered TiO2 nanoparticles to saltwater organisms: an overview. , 2014, Environment international.

[60]  Maurizio Chiriva-Internati,et al.  Nanotechnology and human health: risks and benefits , 2010, Journal of applied toxicology : JAT.

[61]  Rui Qiao,et al.  In vivo biomodification of lipid-coated carbon nanotubes by Daphnia magna. , 2007, Environmental science & technology.

[62]  G. Pojana,et al.  Effects of alginate on stability and ecotoxicity of nano-TiO2 in artificial seawater. , 2015, Ecotoxicology and environmental safety.

[63]  Wolfgang Kreyling,et al.  Ultrafine Particles Cross Cellular Membranes by Nonphagocytic Mechanisms in Lungs and in Cultured Cells , 2005, Environmental health perspectives.

[64]  Nanna B. Hartmann,et al.  Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing , 2008, Ecotoxicology.

[65]  Antonio Marcomini,et al.  Agglomeration and sedimentation of titanium dioxide nanoparticles (n-TiO2) in synthetic and real waters , 2013, Journal of Nanoparticle Research.

[66]  Salvatore Fasulo,et al.  Effects of environmental pollution in caged mussels (Mytilus galloprovincialis). , 2013, Marine environmental research.

[67]  L. Pollegioni,et al.  D-amino acid oxidase-nanoparticle system: a potential novel approach for cancer enzymatic therapy. , 2013, Nanomedicine.

[68]  Damià Barceló,et al.  Ecotoxicity and analysis of nanomaterials in the aquatic environment , 2009, Analytical and bioanalytical chemistry.

[69]  H. García,et al.  Long-lived (minutes) photoinduced charge separation in a structured periodic mesoporous titania containing 2,4,6-triphenylpyrylium as guest. , 2008, Dalton transactions.