Carboxylation of multiwalled carbon nanotubes reduces their toxicity in primary human alveolar macrophages

Sinbad Sweeney, Sheng Hu, Pakatip Ruenraroengsak, Shu Chen, Andrew Gow, Stephan Schwander, Junfeng Zhang, Kian Fan Chung, Mary P. Ryan, Alexandra E. Porter, Milo S. Shaffer, Teresa D. Tetley

Research output: Contribution to journalArticle

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Abstract

Surface functionalisation of multiwalled carbon nanotubes (MWCNT) is commonly used to facilitate their various and diverse applications. Inhaled nanomaterials, such as MWCNTs, have a high deposition rate in the alveolar units of the deep lung, where alveolar macrophages (AM) provide the front line of cellular immune defence by removing foreign matter (microbes, particles etc.). The toxicity of MWCNTs (with or without functionalisation) towards primary human AMs is not known. We investigated the physicochemical characteristics and toxicity of two MWCNT materials: acid purified 'Purified-MWCNT' and concentrated acid functionalised 'COOH-MWCNT'. We hypothesised that the bioreactivity with primary human AM would differ between the materials. Full characterisation of the MWCNTs revealed that -COOH functionalisation yielded shorter MWCNTs, accompanied by a greater occurrence of framework defects, in comparison to Purified-MWCNT. In agreement with our hypothesis that the bioreactivity would differ, Purified-MWCNT were significantly more toxic as measured by reduced cell viability and increased inflammatory mediator release. For example, IL-1β and IL-8 release by AMs significantly increased 3.5- and 2.4-fold, respectively (P < 0.05), 24 hours after treatment with Purified-MWCNT. In contrast, IL-1β and IL-8 release by AMs did not significantly change 24 hours after treatment with COOH-MWCNT. We determined that the mechanism of this toxicity is likely due to activation of the inflammasome, as lipopolysaccharide priming of primary human AMs was necessary to see the inflammatory response and this was accompanied by lysosomal disruption and increased generation of reactive oxygen species. This study contributes further to our understanding of the effects of MWCNTs and surface modification on highly relevant human lung AMs; the findings have important implications for the manufacture, application and use of MWCNTs. In particular, this is relevant where applications prefer biocompatible MWCNTs.

Original languageEnglish (US)
Pages (from-to)1340-1350
Number of pages11
JournalEnvironmental Science: Nano
Volume3
Issue number6
DOIs
StatePublished - Jan 1 2016

Fingerprint

Carboxylation
Multiwalled carbon nanotubes (MWCN)
Toxicity
toxicity
Interleukin-8
Interleukin-1
Inflammasomes
Acids
Alveolar Macrophages
carbon nanotube
Poisons
acid
Deposition rates
Nanostructured materials
defect
Lipopolysaccharides
Surface treatment
Reactive Oxygen Species
viability
Chemical activation

All Science Journal Classification (ASJC) codes

  • Environmental Science(all)
  • Materials Science (miscellaneous)

Cite this

Sweeney, Sinbad ; Hu, Sheng ; Ruenraroengsak, Pakatip ; Chen, Shu ; Gow, Andrew ; Schwander, Stephan ; Zhang, Junfeng ; Chung, Kian Fan ; Ryan, Mary P. ; Porter, Alexandra E. ; Shaffer, Milo S. ; Tetley, Teresa D. / Carboxylation of multiwalled carbon nanotubes reduces their toxicity in primary human alveolar macrophages. In: Environmental Science: Nano. 2016 ; Vol. 3, No. 6. pp. 1340-1350.
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abstract = "Surface functionalisation of multiwalled carbon nanotubes (MWCNT) is commonly used to facilitate their various and diverse applications. Inhaled nanomaterials, such as MWCNTs, have a high deposition rate in the alveolar units of the deep lung, where alveolar macrophages (AM) provide the front line of cellular immune defence by removing foreign matter (microbes, particles etc.). The toxicity of MWCNTs (with or without functionalisation) towards primary human AMs is not known. We investigated the physicochemical characteristics and toxicity of two MWCNT materials: acid purified 'Purified-MWCNT' and concentrated acid functionalised 'COOH-MWCNT'. We hypothesised that the bioreactivity with primary human AM would differ between the materials. Full characterisation of the MWCNTs revealed that -COOH functionalisation yielded shorter MWCNTs, accompanied by a greater occurrence of framework defects, in comparison to Purified-MWCNT. In agreement with our hypothesis that the bioreactivity would differ, Purified-MWCNT were significantly more toxic as measured by reduced cell viability and increased inflammatory mediator release. For example, IL-1β and IL-8 release by AMs significantly increased 3.5- and 2.4-fold, respectively (P < 0.05), 24 hours after treatment with Purified-MWCNT. In contrast, IL-1β and IL-8 release by AMs did not significantly change 24 hours after treatment with COOH-MWCNT. We determined that the mechanism of this toxicity is likely due to activation of the inflammasome, as lipopolysaccharide priming of primary human AMs was necessary to see the inflammatory response and this was accompanied by lysosomal disruption and increased generation of reactive oxygen species. This study contributes further to our understanding of the effects of MWCNTs and surface modification on highly relevant human lung AMs; the findings have important implications for the manufacture, application and use of MWCNTs. In particular, this is relevant where applications prefer biocompatible MWCNTs.",
author = "Sinbad Sweeney and Sheng Hu and Pakatip Ruenraroengsak and Shu Chen and Andrew Gow and Stephan Schwander and Junfeng Zhang and Chung, {Kian Fan} and Ryan, {Mary P.} and Porter, {Alexandra E.} and Shaffer, {Milo S.} and Tetley, {Teresa D.}",
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Sweeney, S, Hu, S, Ruenraroengsak, P, Chen, S, Gow, A, Schwander, S, Zhang, J, Chung, KF, Ryan, MP, Porter, AE, Shaffer, MS & Tetley, TD 2016, 'Carboxylation of multiwalled carbon nanotubes reduces their toxicity in primary human alveolar macrophages', Environmental Science: Nano, vol. 3, no. 6, pp. 1340-1350. https://doi.org/10.1039/c6en00055j

Carboxylation of multiwalled carbon nanotubes reduces their toxicity in primary human alveolar macrophages. / Sweeney, Sinbad; Hu, Sheng; Ruenraroengsak, Pakatip; Chen, Shu; Gow, Andrew; Schwander, Stephan; Zhang, Junfeng; Chung, Kian Fan; Ryan, Mary P.; Porter, Alexandra E.; Shaffer, Milo S.; Tetley, Teresa D.

In: Environmental Science: Nano, Vol. 3, No. 6, 01.01.2016, p. 1340-1350.

Research output: Contribution to journalArticle

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T1 - Carboxylation of multiwalled carbon nanotubes reduces their toxicity in primary human alveolar macrophages

AU - Sweeney, Sinbad

AU - Hu, Sheng

AU - Ruenraroengsak, Pakatip

AU - Chen, Shu

AU - Gow, Andrew

AU - Schwander, Stephan

AU - Zhang, Junfeng

AU - Chung, Kian Fan

AU - Ryan, Mary P.

AU - Porter, Alexandra E.

AU - Shaffer, Milo S.

AU - Tetley, Teresa D.

PY - 2016/1/1

Y1 - 2016/1/1

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