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Title: Crumpling of silver nanowires by endolysosomes strongly reduces toxicity

Abstract

Fibrous particles interact with cells and organisms in complex ways that can lead to cellular dysfunction, cell death, inflammation, and disease. The development of conductive transparent networks (CTNs) composed of metallic silver nanowires (AgNWs) for flexible touchscreen displays raises new possibilities for the intimate contact between novel fibers and human skin. Here, we report that a material property, nanowire-bending stiffness that is a function of diameter, controls the cytotoxicity of AgNWs to nonimmune cells from humans, mice, and fish without deterioration of critical CTN performance parameters: electrical conductivity and optical transparency. Both 30- and 90-nm-diameter AgNWs are readily internalized by cells, but thinner NWs are mechanically crumpled by the forces imposed during or after endocytosis, while thicker nanowires puncture the enclosing membrane and release silver ions and lysosomal contents to the cytoplasm, thereby initiating oxidative stress. This finding extends the fiber pathology paradigm and will enable the manufacture of safer products incorporating AgNWs.

Authors:
; ; ; ; ; ; ; ORCiD logo; ORCiD logo; ORCiD logo; ; ; ORCiD logo; ; ; ; ; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1564566
Alternate Identifier(s):
OSTI ID: 1559232
Grant/Contract Number:  
[AC02-05CH11231]
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
[Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 30]; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; nanotechnology; endocytosis; fiber toxicity

Citation Formats

Lehmann, Sylvia G., Toybou, Djadidi, Pradas del Real, Ana-Elena, Arndt, Devrah, Tagmount, Abderrahmane, Viau, Muriel, Safi, Malak, Pacureanu, Alexandra, Cloetens, Peter, Bohic, Sylvain, Salomé, Murielle, Castillo-Michel, Hiram, Omaña-Sanz, Brenda, Hofmann, Annette, Vulpe, Christopher, Simonato, Jean-Pierre, Celle, Caroline, Charlet, Laurent, and Gilbert, Benjamin. Crumpling of silver nanowires by endolysosomes strongly reduces toxicity. United States: N. p., 2019. Web. doi:10.1073/pnas.1820041116.
Lehmann, Sylvia G., Toybou, Djadidi, Pradas del Real, Ana-Elena, Arndt, Devrah, Tagmount, Abderrahmane, Viau, Muriel, Safi, Malak, Pacureanu, Alexandra, Cloetens, Peter, Bohic, Sylvain, Salomé, Murielle, Castillo-Michel, Hiram, Omaña-Sanz, Brenda, Hofmann, Annette, Vulpe, Christopher, Simonato, Jean-Pierre, Celle, Caroline, Charlet, Laurent, & Gilbert, Benjamin. Crumpling of silver nanowires by endolysosomes strongly reduces toxicity. United States. doi:10.1073/pnas.1820041116.
Lehmann, Sylvia G., Toybou, Djadidi, Pradas del Real, Ana-Elena, Arndt, Devrah, Tagmount, Abderrahmane, Viau, Muriel, Safi, Malak, Pacureanu, Alexandra, Cloetens, Peter, Bohic, Sylvain, Salomé, Murielle, Castillo-Michel, Hiram, Omaña-Sanz, Brenda, Hofmann, Annette, Vulpe, Christopher, Simonato, Jean-Pierre, Celle, Caroline, Charlet, Laurent, and Gilbert, Benjamin. Mon . "Crumpling of silver nanowires by endolysosomes strongly reduces toxicity". United States. doi:10.1073/pnas.1820041116.
@article{osti_1564566,
title = {Crumpling of silver nanowires by endolysosomes strongly reduces toxicity},
author = {Lehmann, Sylvia G. and Toybou, Djadidi and Pradas del Real, Ana-Elena and Arndt, Devrah and Tagmount, Abderrahmane and Viau, Muriel and Safi, Malak and Pacureanu, Alexandra and Cloetens, Peter and Bohic, Sylvain and Salomé, Murielle and Castillo-Michel, Hiram and Omaña-Sanz, Brenda and Hofmann, Annette and Vulpe, Christopher and Simonato, Jean-Pierre and Celle, Caroline and Charlet, Laurent and Gilbert, Benjamin},
abstractNote = {Fibrous particles interact with cells and organisms in complex ways that can lead to cellular dysfunction, cell death, inflammation, and disease. The development of conductive transparent networks (CTNs) composed of metallic silver nanowires (AgNWs) for flexible touchscreen displays raises new possibilities for the intimate contact between novel fibers and human skin. Here, we report that a material property, nanowire-bending stiffness that is a function of diameter, controls the cytotoxicity of AgNWs to nonimmune cells from humans, mice, and fish without deterioration of critical CTN performance parameters: electrical conductivity and optical transparency. Both 30- and 90-nm-diameter AgNWs are readily internalized by cells, but thinner NWs are mechanically crumpled by the forces imposed during or after endocytosis, while thicker nanowires puncture the enclosing membrane and release silver ions and lysosomal contents to the cytoplasm, thereby initiating oxidative stress. This finding extends the fiber pathology paradigm and will enable the manufacture of safer products incorporating AgNWs.},
doi = {10.1073/pnas.1820041116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = [30],
volume = [116],
place = {United States},
year = {2019},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1820041116

Figures / Tables:

Fig. 1 Fig. 1: Diameter-dependent performance and cytotoxicity of AgNWs. (A) Scanning-electron microscopy images of 8- to 9-μm long AgNW with 3 mean diameters. (B) Relationship between optical transparency and sheet resistance for CTNs fabricated by ∼9-μm-long AgNWs with three different diameters. Each data point represents a spray-coated network at a differentmore » AgNW density. Yellow-shaded region represents the technological target for commercial CTNs. (C) Viability of murine fibroblasts cells following 24-h exposure with AgNWs of different diameter, as determined by the MTT assay. The dashed lines are model predictions as described in the text. (D) Viability of rainbow trout gut cells following 24-h exposure with AgNWs of different diameter determined by CellTiter-Glo assay. Cell-viability data are presented as a percentages relative to the nontreated control cells. Error bars on triplicate measurements are 1 SD.« less

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    journal, April 2013

    • Chen, Ruiyi; Das, Suprem R.; Jeong, Changwook
    • Advanced Functional Materials, Vol. 23, Issue 41
    • DOI: 10.1002/adfm.201300124

    Metallic Nanowire-Based Transparent Electrodes for Next Generation Flexible Devices: a Review
    journal, October 2016


    The effect of silver nanoparticles and silver ions on mammalian and plant cells in vitro
    journal, October 2016

    • Jiravova, Jana; Tomankova, Katerina Barton; Harvanova, Monika
    • Food and Chemical Toxicology, Vol. 96
    • DOI: 10.1016/j.fct.2016.07.015

    An introduction to the short-term toxicology of respirable industrial fibres
    journal, September 2004

    • Donaldson, Ken; Tran, C. Lang
    • Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 553, Issue 1-2
    • DOI: 10.1016/j.mrfmmm.2004.06.011

    High performance transparent multi-touch sensors based on silver nanowires
    journal, June 2016


    A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra
    journal, January 2007

    • Solé, V. A.; Papillon, E.; Cotte, M.
    • Spectrochimica Acta Part B: Atomic Spectroscopy, Vol. 62, Issue 1
    • DOI: 10.1016/j.sab.2006.12.002

    Autophagy induction by silver nanowires: A new aspect in the biocompatibility assessment of nanocomposite thin films
    journal, November 2012

    • Verma, Navin K.; Conroy, Jennifer; Lyons, Philip E.
    • Toxicology and Applied Pharmacology, Vol. 264, Issue 3
    • DOI: 10.1016/j.taap.2012.08.023

    Silver Nanowire Particle Reactivity with Human Monocyte-Derived Macrophage Cells: Intracellular Availability of Silver Governs Their Cytotoxicity
    journal, September 2017


    Environmental Transformations of Silver Nanoparticles: Impact on Stability and Toxicity
    journal, February 2012

    • Levard, Clément; Hotze, E. Matt; Lowry, Gregory V.
    • Environmental Science & Technology, Vol. 46, Issue 13
    • DOI: 10.1021/es2037405

    Crystalline Silver Nanowires by Soft Solution Processing
    journal, February 2002

    • Sun, Yugang; Gates, Byron; Mayers, Brian
    • Nano Letters, Vol. 2, Issue 2
    • DOI: 10.1021/nl010093y

    Designed Synthesis of CeO 2 Nanorods and Nanowires for Studying Toxicological Effects of High Aspect Ratio Nanomaterials
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    • Ji, Zhaoxia; Wang, Xiang; Zhang, Haiyuan
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    • DOI: 10.1021/nn3012114

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    • ACS Nano, Vol. 7, Issue 12
    • DOI: 10.1021/nn4034103

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    Holotomography: Quantitative phase tomography with micrometer resolution using hard synchrotron radiation x rays
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    • Applied Physics Letters, Vol. 75, Issue 19
    • DOI: 10.1063/1.125225

    Efficient correction of wavefront inhomogeneities in X-ray holographic nanotomography by random sample displacement
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    • Hubert, Maxime; Pacureanu, Alexandra; Guilloud, Cyril
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    • DOI: 10.1063/1.5026462

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    • Proceedings of the National Academy of Sciences, Vol. 108, Issue 49
    • DOI: 10.1073/pnas.1110013108

    Kinks, rings, and rackets in filamentous structures
    journal, October 2003

    • Cohen, A. E.; Mahadevan, L.
    • Proceedings of the National Academy of Sciences, Vol. 100, Issue 21
    • DOI: 10.1073/pnas.1534600100

    Nanomechanical mechanism for lipid bilayer damage induced by carbon nanotubes confined in intracellular vesicles
    journal, October 2016

    • Zhu, Wenpeng; von dem Bussche, Annette; Yi, Xin
    • Proceedings of the National Academy of Sciences, Vol. 113, Issue 44
    • DOI: 10.1073/pnas.1605030113

    Engineered nanomaterial-induced lysosomal membrane permeabilization and anti-cathepsin agents
    journal, May 2017

    • Bunderson-Schelvan, Melisa; Holian, Andrij; Hamilton, Raymond F.
    • Journal of Toxicology and Environmental Health, Part B, Vol. 20, Issue 4
    • DOI: 10.1080/10937404.2017.1305924

    The dependence of the optoelectrical properties of silver nanowire networks on nanowire length and diameter
    journal, April 2012


    Flexible transparent conductive materials based on silver nanowire networks: a review
    journal, October 2013


    Toxic Potential of Materials at the Nanolevel
    journal, February 2006


    Mechanisms of Nanoparticle-Induced Oxidative Stress and Toxicity
    journal, January 2013

    • Manke, Amruta; Wang, Liying; Rojanasakul, Yon
    • BioMed Research International, Vol. 2013
    • DOI: 10.1155/2013/942916

    Antioxidant and Cell-Signaling Functions of Hydrogen Sulfide in the Central Nervous System
    journal, January 2018

    • Shefa, Ulfuara; Kim, Min-Sik; Jeong, Na Young
    • Oxidative Medicine and Cellular Longevity, Vol. 2018
    • DOI: 10.1155/2018/1873962

    Particle length-dependent titanium dioxide nanomaterials toxicity and bioactivity
    journal, January 2009

    • Hamilton, Raymond F.; Wu, Nianqiang; Porter, Dale
    • Particle and Fibre Toxicology, Vol. 6, Issue 1
    • DOI: 10.1186/1743-8977-6-35

    Shape matters: effects of silver nanospheres and wires on human alveolar epithelial cells
    journal, January 2011

    • Stoehr, Linda C.; Gonzalez, Edgar; Stampfl, Andreas
    • Particle and Fibre Toxicology, Vol. 8, Issue 1
    • DOI: 10.1186/1743-8977-8-36

    Use of silver nanowires to determine thresholds for fibre length-dependent pulmonary inflammation and inhibition of macrophage migration in vitro
    journal, January 2012

    • Schinwald, Anja; Chernova, Tanya; Donaldson, Ken
    • Particle and Fibre Toxicology, Vol. 9, Issue 1
    • DOI: 10.1186/1743-8977-9-47

    Short versus long silver nanowires: a comparison of in vivo pulmonary effects post instillation
    journal, October 2014


    Silver nanowires as prospective carriers for drug delivery in cancer treatment: an in vitro biocompatibility study on lung adenocarcinoma cells and fibroblasts
    journal, January 2013

    • Singh, Manisha; Movia, Dania; Mahfoud, Omar K.
    • European Journal of Nanomedicine, Vol. 5, Issue 4
    • DOI: 10.1515/ejnm-2013-0024

    Early Combination of Material Characteristics and Toxicology Is Useful in the Design of Low Toxicity Carbon Nanofiber
    journal, September 2012

    • Jensen, Ellen K.; Larsen, Sten Y.; Nygaard, Unni C.
    • Materials, Vol. 5, Issue 9
    • DOI: 10.3390/ma5091560

    In Vitro Dermal Safety Assessment of Silver Nanowires after Acute Exposure: Tissue vs. Cell Models
    journal, April 2018

    • Lehmann, Sylvia; Gilbert, Benjamin; Maffeis, Thierry
    • Nanomaterials, Vol. 8, Issue 4
    • DOI: 10.3390/nano8040232

      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.