Can the Ames test provide an insight into nano-object mutagenicity? Investigating the interaction between nano-objects and bacteria

Abstract The aim of this study was to assess the interaction of a series of well characterised nano-objects with the Gram negative bacterium Salmonella typhimurium, and how such an interaction may relate to the potential mutagenicity of nano-objects. Transmission electron microscopy showed that nano-objects (Au-PMA-ATTO NPs, CeO2 NPs, SWCNTs and MWCNTs), as well as CAFs entered S. typhimurium. Only DEPs did not penetrate/enter the bacteria, however, were the only particle stimulus to induce any significant mutagenicity through the Ames test. Comparison with a sophisticated 3D in vitro cell model showed CAFs, DEPs, SWCNTs and MWCNTs to cause a significant increase in mammalian cell proliferation, whilst both the Au-PMA-ATTO NPs and CeO2 NPs had not significant adverse effects. In conclusion, these results indicate that various of different nano-objects are able to penetrate the double-lipid bilayer of Gram negative bacteria, although the Ames test may not be a good indicator for nano-object mutagenicity.

[1]  U. Vogel,et al.  Diesel exhaust particles are mutagenic in FE1-MutaMouse lung epithelial cells. , 2008, Mutation research.

[2]  Roel P F Schins,et al.  Genotoxicity of Poorly Soluble Particles , 2007, Inhalation toxicology.

[3]  Vicki Stone,et al.  Intracellular imaging of nanoparticles: Is it an elemental mistake to believe what you see? , 2010, Particle and Fibre Toxicology.

[4]  X. Pan,et al.  Mutagenicity evaluation of metal oxide nanoparticles by the bacterial reverse mutation assay. , 2010, Chemosphere.

[5]  M. Kirsch‐Volders,et al.  The in vitro MN assay in 2011: origin and fate, biological significance, protocols, high throughput methodologies and toxicological relevance , 2011, Archives of Toxicology.

[6]  Li Wei,et al.  Sharper and faster "nano darts" kill more bacteria: a study of antibacterial activity of individually dispersed pristine single-walled carbon nanotube. , 2009, ACS nano.

[7]  Markus Schulz,et al.  Genotoxicity investigations on nanomaterials: methods, preparation and characterization of test material, potential artifacts and limitations--many questions, some answers. , 2009, Mutation research.

[8]  Walter H. Chang,et al.  Design of an amphiphilic polymer for nanoparticle coating and functionalization. , 2008, Small.

[9]  S. Iijima Helical microtubules of graphitic carbon , 1991, Nature.

[10]  Jennifer A. Higgins,et al.  DNA damage of macrophages at an air-tissue interface induced by metal nanoparticles , 2009 .

[11]  Antonio Marcomini,et al.  Genotoxicity, cytotoxicity, and reactive oxygen species induced by single‐walled carbon nanotubes and C60 fullerenes in the FE1‐Muta™Mouse lung epithelial cells , 2008, Environmental and molecular mutagenesis.

[12]  Larry D. Claxton,et al.  The Salmonella Mutagenicity Assay: The Stethoscope of Genetic Toxicology for the 21st Century , 2010, Environmental health perspectives.

[13]  V. Castranova,et al.  Effects of exposure to diesel exhaust particles (DEP) on pulmonary metabolic activation of mutagenic agents. , 2004, Mutation research.

[14]  Minnamari Vippola,et al.  Genotoxicity of nanomaterials: DNA damage and micronuclei induced by carbon nanotubes and graphite nanofibres in human bronchial epithelial cells in vitro. , 2009, Toxicology letters.

[15]  S. Faux,et al.  Fibre-induced lipid peroxidation leads to DNA adduct formation in Salmonella typhimurium TA104 and rat lung fibroblasts. , 1996, Carcinogenesis.

[16]  David B Warheit,et al.  Rationale of genotoxicity testing of nanomaterials: Regulatory requirements and appropriateness of available OECD test guidelines , 2010, Nanotoxicology.

[17]  M Chamberlain,et al.  Asbestos and glass fibres in bacterial mutation tests. , 1977, Mutation research.

[18]  Lang Tran,et al.  Safe handling of nanotechnology , 2006, Nature.

[19]  F. Oesch,et al.  Gene toxicity studies on titanium dioxide and zinc oxide nanomaterials used for UV-protection in cosmetic formulations , 2010, Nanotoxicology.

[20]  Peter Wick,et al.  Nanotoxicology: an interdisciplinary challenge. , 2011, Angewandte Chemie.

[21]  Alok Dhawan,et al.  Cellular uptake and mutagenic potential of metal oxide nanoparticles in bacterial cells. , 2011, Chemosphere.

[22]  W. Stark,et al.  The degree and kind of agglomeration affect carbon nanotube cytotoxicity. , 2007, Toxicology letters.

[23]  G. Oberdörster,et al.  Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology , 2010, Journal of internal medicine.

[24]  W Zhou,et al.  Effects of two new lubricants on the mutagenicity of scooter exhaust particulate matter. , 1998, Mutation research.

[25]  S. Maenosono,et al.  Mutagenicity of water-soluble ZnO nanoparticles in Ames test. , 2007, The Journal of toxicological sciences.

[26]  A. Kahru,et al.  From ecotoxicology to nanoecotoxicology. , 2010, Toxicology.

[27]  S. Doak,et al.  NanoGenotoxicology: the DNA damaging potential of engineered nanomaterials. , 2009, Biomaterials.

[28]  Christof Asbach,et al.  Nanoparticle exposure at nanotechnology workplaces: A review , 2011, Particle and Fibre Toxicology.

[29]  M. Madigan,et al.  Brock Biology of Microorganisms , 1996 .

[30]  Joel G Pounds,et al.  Particokinetics in vitro: dosimetry considerations for in vitro nanoparticle toxicity assessments. , 2007, Toxicological sciences : an official journal of the Society of Toxicology.

[31]  Iseult Lynch,et al.  Reproducible comet assay of amorphous silica nanoparticles detects no genotoxicity. , 2008, Nano letters.

[32]  Jiri Aubrecht,et al.  Bioluminescent Salmonella reverse mutation assay: a screen for detecting mutagenicity with high throughput attributes. , 2007, Mutagenesis.

[33]  Peter Wick,et al.  A brief summary of carbon nanotubes science and technology: a health and safety perspective. , 2011, ChemSusChem.

[34]  S. Ye,et al.  Mutagenicity of scooter exhaust particulate matter. , 1997, Journal of toxicology and environmental health.

[35]  B. Ames,et al.  An improved bacterial test system for the detection and classification of mutagens and carcinogens. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Albert Duschl,et al.  The suitability of different cellular in vitro immunotoxicity and genotoxicity methods for the analysis of nanoparticle-induced events , 2010, Nanotoxicology.

[37]  S. Maenosono,et al.  Mutagenicity of water-soluble FePt nanoparticles in Ames test. , 2007, The Journal of toxicological sciences.

[38]  M. Andersen,et al.  Inhaled Carbon Nanotubes Reach the Sub-Pleural Tissue in Mice , 2009, Nature nanotechnology.

[39]  Craig A. Poland,et al.  Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. , 2008, Nature nanotechnology.

[40]  Jim Willis,et al.  Science policy considerations for responsible nanotechnology decisions. , 2011, Nature nanotechnology.

[41]  E. Zeiger,et al.  The Ames Salmonella/microsome mutagenicity assay. , 2000, Mutation research.

[42]  B. Bay,et al.  Current Studies into the Genotoxic Effects of Nanomaterials , 2010, Journal of nucleic acids.

[43]  J. Kanno,et al.  Induction of mesothelioma in p53+/- mouse by intraperitoneal application of multi-wall carbon nanotube. , 2008, The Journal of toxicological sciences.

[44]  Vincent Castranova,et al.  Single-walled Carbon Nanotubes: Geno- and Cytotoxic Effects in Lung Fibroblast V79 Cells , 2007, Journal of toxicology and environmental health. Part A.

[45]  D. DeMarini,et al.  Sample characterization of automobile and forklift diesel exhaust particles and comparative pulmonary toxicity in mice. , 2004, Environmental health perspectives.

[46]  Martin J. D. Clift,et al.  Nanotoxicology: a perspective and discussion of whether or not in vitro testing is a valid alternative , 2010, Archives of Toxicology.

[47]  Nicklas Raun Jacobsen,et al.  Lung inflammation and genotoxicity following pulmonary exposure to nanoparticles in ApoE-/- mice , 2009, Particle and Fibre Toxicology.

[48]  M. Benedetti,et al.  Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. , 2006, Nano letters.

[49]  L. Levy,et al.  Iron-dependent formation of 8-hydroxydeoxyguanosine in isolated DNA and mutagenicity in Salmonella typhimurium TA102 induced by crocidolite. , 1994, Carcinogenesis.

[50]  N. Miyata,et al.  Mutagenicity of the fullerene C60-generated singlet oxygen dependent formation of lipid peroxides. , 1996, Carcinogenesis.

[51]  Stefano Bellucci,et al.  Multi-walled carbon nanotubes: Lack of mutagenic activity in the bacterial reverse mutation assay. , 2009, Toxicology letters.

[52]  T Satoh,et al.  Advantage of the use of human liver S9 in the Ames test. , 1999, Mutation research.

[53]  A. Busnaina,et al.  The adhesion of dry particles in the nanometer to micrometer-size range , 2000 .

[54]  V. Buonocore,et al.  Biological availability of mutagenic compounds adsorbed onto diesel exhaust particulate. , 1984, Mutation research.

[55]  Peter Gehr,et al.  Dendritic cells and macrophages form a transepithelial network against foreign particulate antigens. , 2007, American journal of respiratory cell and molecular biology.

[56]  Andrew D Maynard,et al.  Nanotechnology: the next big thing, or much ado about nothing? , 2007, The Annals of occupational hygiene.

[57]  Ken Donaldson,et al.  Possible genotoxic mechanisms of nanoparticles: Criteria for improved test strategies , 2010, Nanotoxicology.

[58]  Peter Wick,et al.  Comprehensive evaluation of in vitro toxicity of three large-scale produced carbon nanotubes on human Jurkat T cells and a comparison to crocidolite asbestos , 2009 .

[59]  P. M. Williams,et al.  Confounding experimental considerations in nanogenotoxicology. , 2009, Mutagenesis.

[60]  M. Jaurand,et al.  Particle and Fibre Toxicology Mesothelioma: Do Asbestos and Carbon Nanotubes Pose the Same Health Risk? , 2022 .

[61]  M. Jaurand,et al.  Role of Mutagenicity in Asbestos Fiber-Induced Carcinogenicity and Other Diseases , 2011, Journal of toxicology and environmental health. Part B, Critical reviews.

[62]  J. Krahl,et al.  Mutagenic and cytotoxic effects of exhaust particulate matter of biodiesel compared to fossil diesel fuel. , 1998, Mutation research.

[63]  Wolfgang J Parak,et al.  Fluorescent-magnetic hybrid nanoparticles induce a dose-dependent increase in proinflammatory response in lung cells in vitro correlated with intracellular localization. , 2010, Small.

[64]  Iseult Lynch,et al.  Minimal analytical characterization of engineered nanomaterials needed for hazard assessment in biological matrices , 2011, Nanotoxicology.

[65]  Thomas Hartung,et al.  From alternative methods to a new toxicology. , 2011, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[66]  G. Oberdörster,et al.  Nanotoxicology: An Emerging Discipline Evolving from Studies of Ultrafine Particles , 2005, Environmental health perspectives.

[67]  H. Krug,et al.  Nanoecotoxicology: nanoparticles at large. , 2008, Nature nanotechnology.

[68]  O. Schmid,et al.  Effects and uptake of gold nanoparticles deposited at the air-liquid interface of a human epithelial airway model. , 2010, Toxicology and applied pharmacology.

[69]  Steffen Foss Hansen,et al.  Categorization framework to aid hazard identification of nanomaterials , 2007 .

[70]  A. Collins,et al.  The comet assay for DNA damage and repair , 2004, Molecular biotechnology.

[71]  Craig A. Poland,et al.  Asbestos, carbon nanotubes and the pleural mesothelium: a review of the hypothesis regarding the role of long fibre retention in the parietal pleura, inflammation and mesothelioma , 2010, Particle and Fibre Toxicology.

[72]  M. Roller,et al.  Carcinogenicity of inhaled nanoparticles , 2009, Inhalation toxicology.

[73]  U. Wirnitzer,et al.  Studies on the in vitro genotoxicity of baytubes, agglomerates of engineered multi-walled carbon-nanotubes (MWCNT). , 2009, Toxicology letters.

[74]  Christian Mühlfeld,et al.  In vitro models of the human epithelial airway barrier to study the toxic potential of particulate matter , 2008, Expert opinion on drug metabolism & toxicology.

[75]  W. Stark,et al.  Cerium oxide nanoparticle uptake kinetics from the gas-phase into lung cells in vitro is transport limited. , 2011, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[76]  H. Norppa,et al.  Genotoxicity testing of nanomaterials – Conclusions , 2010, Nanotoxicology.

[77]  Roger Frost,et al.  International Organization for Standardization (ISO) , 2004 .

[78]  W. Wallace,et al.  Mutagenicity of diesel exhaust particles and oil shale particles dispersed in lecithin surfactant. , 1987, Journal of toxicology and environmental health.

[79]  Vicki Stone,et al.  Toxicology of nanoparticles: A historical perspective , 2007 .

[80]  Helinor J Johnston,et al.  A critical review of the biological mechanisms underlying the in vivo and in vitro toxicity of carbon nanotubes: The contribution of physico-chemical characteristics , 2010, Nanotoxicology.

[81]  Helinor Johnston,et al.  Development of in vitro systems for nanotoxicology: methodological considerations , 2009, Critical reviews in toxicology.

[82]  K. Donaldson,et al.  Interactions between ultrafine particles and transition metals in vivo and in vitro. , 2002, Toxicology and applied pharmacology.

[83]  C. Sonnenschein,et al.  The tissue organization field theory of cancer: A testable replacement for the somatic mutation theory , 2011, BioEssays : news and reviews in molecular, cellular and developmental biology.