All that is silver is not toxic: silver ion and particle kinetics reveals the role of silver ion aging and dosimetry on the toxicity of silver nanoparticles

Smith, Jordan N.; Thomas, Dennis G.; Jolley, Hadley; Kodali, Vamsi K.; Littke, Matthew H.; Munusamy, Prabhakaran; Baer, Donald R.; Gaffrey, Matthew J.; Thrall, Brian D.; Teeguarden, Justin G.

doi:10.1186/s12989-018-0283-z

Title: All that is silver is not toxic: silver ion and particle kinetics reveals the role of silver ion aging and dosimetry on the toxicity of silver nanoparticles

Journal Article · 04 December 2018 · Particle and Fibre Toxicology

DOI: https://doi.org/10.1186/s12989-018-0283-z · OSTI ID:1489240

^[1]; Thomas, Dennis G. ^[2]; Jolley, Hadley ^[2]; Kodali, Vamsi K. ^[2]; Littke, Matthew H. ^[2]; Munusamy, Prabhakaran ^[2]; Baer, Donald R. ^[2]; Gaffrey, Matthew J. ^[2]; Thrall, Brian D. ^[2]; Teeguarden, Justin G. ^[1]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Oregon State Univ., Corvallis, OR (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

When suspended in cell culture medium, nano-objects composed of soluble metals such as silver can dissolve resulting in ion formation, altered particle properties (e.g. mass, morphology, etc.), and modulated cellular dose. Cultured cells are exposed not just to nanoparticles but to a complex, dynamic mixture of altered nanoparticles, free ions, and ion-ligand complexes. Here, three different cell types (RAW 264.7 macrophages and bone marrow derived macrophages from wild-type C57BL/6J mice and Scavenger Receptor A deficient (SR-A^(-/-)) mice) were exposed to 20 and 110 nm silver nanoparticles, and RAW 264.7 cells were exposed to freshly mixed silver ions, aged silver ions (ions incubated in cell culture medium), and ions formed from nanoparticle dissolution. The In Vitro Sedimentation, Diffusion, Dissolution, and Dosimetry Model (ISD3) was used to predict dose metrics for each exposure scenario. Silver nanoparticles, freshly mixed ions, and ions from nanoparticle dissolution were toxic, while aged ions were not toxic. Macrophages from SR-A^(-/-) mice did not take up 20 nm silver nanoparticles as well as wild-types but demonstrated no differences in silver levels after exposure to 110 nm nanoparticles. Dose response modeling with ISD3 predicted dose metrics suggest that amount of ions in cells and area under the curve (AUC) of ion amount in cells are the most predictive of cell viability after nanoparticle and combined nanoparticle/dissolution-formed-ions exposures, respectively. Results of this study suggest that the unbound silver cation is the ultimate toxicant, and ions formed extracellularly drive toxicity after exposure to nanoparticles. Applying computational modeling (ISD3) to better understand dose metrics for soluble nanoparticles allows for better interpretation of in vitro hazard assessments.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1489240

Report Number(s):: PNNL-SA--135829

Journal Information:: Particle and Fibre Toxicology, Journal Name: Particle and Fibre Toxicology Journal Issue: 1 Vol. 15; ISSN 1743-8977

Country of Publication:: United States

Language:: English

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Iron oxide nanoparticle agglomeration influences dose rates and modulates oxidative stress-mediated dose–response profiles in vitro Sharma, Gaurav; Kodali, Vamsi; Gaffrey, Matthew Nanotoxicology, Vol. 8, Issue 6 https://doi.org/10.3109/17435390.2013.822115	journal	June 2013
Quantitative proteomics analysis of adsorbed plasma proteins classifies nanoparticles with different surface properties and size Zhang, Haizhen; Burnum, Kristin E.; Luna, Maria L. PROTEOMICS, Vol. 11, Issue 23 https://doi.org/10.1002/pmic.201100037	journal	November 2011
Use of Coated Silver Nanoparticles to Understand the Relationship of Particle Dissolution and Bioavailability to Cell and Lung Toxicological Potential Wang, Xiang; Ji, Zhaoxia; Chang, Chong Hyun Small, Vol. 10, Issue 2 https://doi.org/10.1002/smll.201301597	journal	August 2013
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Influence of physicochemical properties of silver nanoparticles on mast cell activation and degranulation Aldossari, Abdullah A.; Shannahan, Jonathan H.; Podila, Ramakrishna Toxicology in Vitro, Vol. 29, Issue 1 https://doi.org/10.1016/j.tiv.2014.10.008	journal	February 2015
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Cellular uptake, intracellular trafficking and cytotoxicity of silver nanoparticles Singh, Raman Preet; Ramarao, Poduri Toxicology Letters, Vol. 213, Issue 2 https://doi.org/10.1016/j.toxlet.2012.07.009	journal	September 2012
Quantifying the Impact of Nanoparticle Coatings and Nonuniformities on XPS Analysis: Gold/Silver Core–Shell Nanoparticles Wang, Yung-Chen; Engelhard, Mark. H.; Baer, Donald R. Analytical Chemistry, Vol. 88, Issue 7 https://doi.org/10.1021/acs.analchem.6b00100	journal	March 2016
Silver Nanowire Particle Reactivity with Human Monocyte-Derived Macrophage Cells: Intracellular Availability of Silver Governs Their Cytotoxicity Theodorou, Ioannis G.; Müller, Karin H.; Chen, Shu ACS Biomaterials Science & Engineering, Vol. 3, Issue 10 https://doi.org/10.1021/acsbiomaterials.7b00479	journal	September 2017
Use of Synchrotron Radiation-Analytical Techniques To Reveal Chemical Origin of Silver-Nanoparticle Cytotoxicity Wang, Liming; Zhang, Tianlu; Li, Panyun ACS Nano, Vol. 9, Issue 6 https://doi.org/10.1021/acsnano.5b02483	journal	May 2015
Estimating Production Data for Five Engineered Nanomaterials As a Basis for Exposure Assessment Hendren, Christine Ogilvie; Mesnard, Xavier; Dröge, Jocelyn Environmental Science & Technology, Vol. 45, Issue 7 https://doi.org/10.1021/es103300g	journal	April 2011
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Estimating Production Data for Five Engineered Nanomaterials As a Basis for Exposure Assessment Hendren, Christine Ogilvie; Mesnard, Xavier; Dröge, Jocelyn Environmental Science & Technology, Vol. 45, Issue 9 https://doi.org/10.1021/es2009924	journal	April 2011
Cysteine-Induced Modifications of Zero-valent Silver Nanomaterials: Implications for Particle Surface Chemistry, Aggregation, Dissolution, and Silver Speciation Gondikas, Andreas P.; Morris, Amanda; Reinsch, Brian C. Environmental Science & Technology, Vol. 46, Issue 13 https://doi.org/10.1021/es3001757	journal	April 2012
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Ion Release Kinetics and Particle Persistence in Aqueous Nano-Silver Colloids Liu, Jingyu; Hurt, Robert H. Environmental Science & Technology, Vol. 44, Issue 6 https://doi.org/10.1021/es9035557	journal	March 2010
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Chemical Transformations of Nanosilver in Biological Environments Liu, Jingyu; Wang, Zhongying; Liu, Frances D. ACS Nano, Vol. 6, Issue 11 https://doi.org/10.1021/nn303449n	journal	October 2012
Dysregulation of Macrophage Activation Profiles by Engineered Nanoparticles Kodali, Vamsi; Littke, Matthew H.; Tilton, Susan C. ACS Nano, Vol. 7, Issue 8 https://doi.org/10.1021/nn402145t	journal	July 2013
Estimating the effective density of engineered nanomaterials for in vitro dosimetry DeLoid, Glen; Cohen, Joel M.; Darrah, Tom Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4514	journal	March 2014
Assessing nanoparticle toxicity in cell-based assays: influence of cell culture parameters and optimized models for bridging the in vitro–in vivo gap Joris, Freya; Manshian, Bella B.; Peynshaert, Karen Chemical Society Reviews, Vol. 42, Issue 21 https://doi.org/10.1039/c3cs60145e	journal	January 2013
Particokinetics In Vitro: Dosimetry Considerations for In Vitro Nanoparticle Toxicity Assessments Teeguarden, Justin G.; Hinderliter, Paul M.; Orr, Galya Toxicological Sciences, Vol. 95, Issue 2 https://doi.org/10.1093/toxsci/kfl165	journal	November 2006
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Gold/silver core-shell 20 nm nanoparticles extracted from citrate solution examined by XPS Engelhard, Mark H.; Smith, Jordan N.; Baer, Donald R. Surface Science Spectra, Vol. 23, Issue 1 https://doi.org/10.1116/1.4953792	journal	June 2016
Size-dependent cytotoxicity of silver nanoparticles in human lung cells: the role of cellular uptake, agglomeration and Ag release Gliga, Anda R.; Skoglund, Sara; Odnevall Wallinder, Inger Particle and Fibre Toxicology, Vol. 11, Issue 1 https://doi.org/10.1186/1743-8977-11-11	journal	January 2014
An integrated approach for the in vitro dosimetry of engineered nanomaterials Cohen, Joel M.; Teeguarden, Justin G.; Demokritou, Philip Particle and Fibre Toxicology, Vol. 11, Issue 1 https://doi.org/10.1186/1743-8977-11-20	journal	January 2014
ISDD: A computational model of particle sedimentation, diffusion and target cell dosimetry for in vitro toxicity studies Hinderliter, Paul M.; Minard, Kevin R.; Orr, Galya Particle and Fibre Toxicology, Vol. 7, Issue 1 https://doi.org/10.1186/1743-8977-7-36	journal	January 2010
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Comparative iron oxide nanoparticle cellular dosimetry and response in mice by the inhalation and liquid cell culture exposure routes Teeguarden, Justin G.; Mikheev, Vladimir B.; Minard, Kevin R. Particle and Fibre Toxicology, Vol. 11, Issue 1 https://doi.org/10.1186/s12989-014-0046-4	journal	September 2014
ISD3: a particokinetic model for predicting the combined effects of particle sedimentation, diffusion and dissolution on cellular dosimetry for in vitro systems Thomas, Dennis G.; Smith, Jordan N.; Thrall, Brian D. Particle and Fibre Toxicology, Vol. 15, Issue 1 https://doi.org/10.1186/s12989-018-0243-7	journal	January 2018
Silver Nanoparticle Protein Corona Composition in Cell Culture Media Shannahan, Jonathan H.; Lai, Xianyin; Ke, Pu Chun PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0074001	journal	September 2013
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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 Johnston, Helinor J.; Hutchison, Gary; Christensen, Frans M. Critical Reviews in Toxicology, Vol. 40, Issue 4 https://doi.org/10.3109/10408440903453074	journal	February 2010
Cellular recognition and trafficking of amorphous silica nanoparticles by macrophage scavenger receptor A Orr, Galya A.; Chrisler, William B.; Cassens, Kaylyn J. Nanotoxicology, Vol. 5, Issue 3 https://doi.org/10.3109/17435390.2010.513836	journal	September 2010
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Iron oxide nanoparticle agglomeration influences dose rates and modulates oxidative stress-mediated dose–response profiles in vitro Sharma, Gaurav; Kodali, Vamsi; Gaffrey, Matthew Nanotoxicology, Vol. 8, Issue 6 https://doi.org/10.3109/17435390.2013.822115	journal	June 2013
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60 APPLIED LIFE SCIENCES
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Title: All that is silver is not toxic: silver ion and particle kinetics reveals the role of silver ion aging and dosimetry on the toxicity of silver nanoparticles

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