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
Abstract
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)more »
- Authors:
-
[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)
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE; National Institutes of Health (NIH)
- OSTI Identifier:
- 1489240
- Report Number(s):
- PNNL-SA-135829
Journal ID: ISSN 1743-8977
- Grant/Contract Number:
- AC05-76RL01830; U19-ES019544
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Particle and Fibre Toxicology
- Additional Journal Information:
- Journal Volume: 15; Journal Issue: 1; Journal ID: ISSN 1743-8977
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; Nanoparticle; Dissolution; ISDD; ISD3; Dosimetry
Citation Formats
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., and Teeguarden, Justin G. 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. United States: N. p., 2018.
Web. doi:10.1186/s12989-018-0283-z.
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. 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. United States. https://doi.org/10.1186/s12989-018-0283-z
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., and Teeguarden, Justin G. Wed .
"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". United States. https://doi.org/10.1186/s12989-018-0283-z. https://www.osti.gov/servlets/purl/1489240.
@article{osti_1489240,
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},
author = {Smith, Jordan N. and Thomas, Dennis G. and Jolley, Hadley and Kodali, Vamsi K. and Littke, Matthew H. and Munusamy, Prabhakaran and Baer, Donald R. and Gaffrey, Matthew J. and Thrall, Brian D. and Teeguarden, Justin G.},
abstractNote = {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.},
doi = {10.1186/s12989-018-0283-z},
journal = {Particle and Fibre Toxicology},
number = 1,
volume = 15,
place = {United States},
year = {Wed Dec 05 00:00:00 EST 2018},
month = {Wed Dec 05 00:00:00 EST 2018}
}
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- Aldossari, Abdullah A.; Shannahan, Jonathan H.; Podila, Ramakrishna
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- Beer, Christiane; Foldbjerg, Rasmus; Hayashi, Yuya
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Trojan-Horse Mechanism in the Cellular Uptake of Silver Nanoparticles Verified by Direct Intra- and Extracellular Silver Speciation Analysis
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- Munusamy, Prabhakaran; Wang, Chongmin; Engelhard, Mark H.
- Biointerphases, Vol. 10, Issue 3
Gold/silver core-shell 20 nm nanoparticles extracted from citrate solution examined by XPS
journal, June 2016
- Engelhard, Mark H.; Smith, Jordan N.; Baer, Donald R.
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Size-dependent cytotoxicity of silver nanoparticles in human lung cells: the role of cellular uptake, agglomeration and Ag release
journal, January 2014
- Gliga, Anda R.; Skoglund, Sara; Odnevall Wallinder, Inger
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An integrated approach for the in vitro dosimetry of engineered nanomaterials
journal, January 2014
- Cohen, Joel M.; Teeguarden, Justin G.; Demokritou, Philip
- Particle and Fibre Toxicology, Vol. 11, Issue 1
ISDD: A computational model of particle sedimentation, diffusion and target cell dosimetry for in vitro toxicity studies
journal, January 2010
- Hinderliter, Paul M.; Minard, Kevin R.; Orr, Galya
- Particle and Fibre Toxicology, Vol. 7, Issue 1
Comparative iron oxide nanoparticle cellular dosimetry and response in mice by the inhalation and liquid cell culture exposure routes
journal, September 2014
- Teeguarden, Justin G.; Mikheev, Vladimir B.; Minard, Kevin R.
- Particle and Fibre Toxicology, Vol. 11, Issue 1
ISD3: a particokinetic model for predicting the combined effects of particle sedimentation, diffusion and dissolution on cellular dosimetry for in vitro systems
journal, January 2018
- Thomas, Dennis G.; Smith, Jordan N.; Thrall, Brian D.
- Particle and Fibre Toxicology, Vol. 15, Issue 1
Silver Nanoparticle Protein Corona Composition in Cell Culture Media
journal, September 2013
- Shannahan, Jonathan H.; Lai, Xianyin; Ke, Pu Chun
- PLoS ONE, Vol. 8, Issue 9
Macrophage scavenger receptor A mediates the uptake of gold colloids by macrophages in vitro
journal, September 2011
- França, Angela; Aggarwal, Parag; Barsov, Eugene V.
- Nanomedicine, Vol. 6, Issue 7
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
journal, February 2010
- Johnston, Helinor J.; Hutchison, Gary; Christensen, Frans M.
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Cellular recognition and trafficking of amorphous silica nanoparticles by macrophage scavenger receptor A
journal, September 2010
- Orr, Galya A.; Chrisler, William B.; Cassens, Kaylyn J.
- Nanotoxicology, Vol. 5, Issue 3
Iron oxide nanoparticle agglomeration influences dose rates and modulates oxidative stress-mediated dose–response profiles in vitro
journal, June 2013
- Sharma, Gaurav; Kodali, Vamsi; Gaffrey, Matthew
- Nanotoxicology, Vol. 8, Issue 6
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