The protein corona suppresses the cytotoxic and pro-inflammatory response in lung epithelial cells and macrophages upon exposure to nanosilica

Regina Leibe, I-Lun Hsiao, Susanne Fritsch-Decker, Ulrike Kielmeier, Ane Marit Wagbo, Benjamin Voss, Annemarie Schmidt, Sarah Dorothea Hessman, Albert Duschl, Gertie Janneke Oostingh, Silvia Diabaté, Carsten Weiss

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Engineered amorphous silica nanoparticles (nanosilica) are one of the most abundant nanomaterials and are widely used in industry. Furthermore, novel nanosilica materials are promising theranostic tools for biomedicine. However, hazardous effects of nanosilica especially after inhalation into the lung have been documented. Therefore, the safe development of nanosilica materials urgently requires predictive assays to monitor toxicity. Here, we further investigate the impact of the protein corona on the biological activity of two different types of nanosilica (colloidal and pyrogenic) in lung cells. As previously described, adsorption of serum proteins to the nanosilica surface suppresses cytotoxicity in macrophages and lung epithelial cells. As the increase of pro-inflammatory mediators is a hallmark of inflammation in the lung upon nanosilica exposure, we studied the potential coupling of the cytotoxic and pro-inflammatory response in A549 human lung epithelial cells and RAW264.7 mouse macrophages. Indeed, cytotoxicity precedes the onset of pro-inflammatory gene expression and cytokine release as exemplified for IL-8 in A549 cells and TNF-alpha in RAW264.7 macrophages after exposure to 0–100 µg/mL nanosilica in medium without serum. Formation of a protein corona not only inhibited cellular toxicity, but also the pro-inflammatory response. Of note, uptake of nanosilica into cells was negligible in the absence, but enhanced in the presence of a protein corona. Hence, the prevailing explanation that the protein corona simply interferes with cellular uptake thus preventing adverse effects needs to be revisited. In conclusion, for the reliable prediction of adverse effects of nanosilica in the lung, in vitro assays should be performed in media not complemented with complete serum. However, in case of different exposure routes, e.g., injection into the blood stream as intended for biomedicine, the protein corona prevents acute toxic actions of nanosilica.

Original languageEnglish
JournalArchives of Toxicology
DOIs
Publication statusPublished - Jan 1 2019
Externally publishedYes

Fingerprint

Macrophages
Epithelial Cells
Lung
Cytotoxicity
Toxicity
Assays
Toxic Actions
Nanostructures
Bioactivity
Serum
Interleukin-8
Nanostructured materials
Gene expression
Silicon Dioxide
Nanoparticles
Inhalation
Adsorption
Blood Proteins
Pneumonia
Industry

Keywords

  • Cell death
  • Inflammation
  • Lung cells
  • Nanoparticle
  • Nano–bio-interface
  • Protein corona
  • Silica

ASJC Scopus subject areas

  • Toxicology
  • Health, Toxicology and Mutagenesis

Cite this

The protein corona suppresses the cytotoxic and pro-inflammatory response in lung epithelial cells and macrophages upon exposure to nanosilica. / Leibe, Regina; Hsiao, I-Lun; Fritsch-Decker, Susanne; Kielmeier, Ulrike; Wagbo, Ane Marit; Voss, Benjamin; Schmidt, Annemarie; Hessman, Sarah Dorothea; Duschl, Albert; Oostingh, Gertie Janneke; Diabaté, Silvia; Weiss, Carsten.

In: Archives of Toxicology, 01.01.2019.

Research output: Contribution to journalArticle

Leibe, R, Hsiao, I-L, Fritsch-Decker, S, Kielmeier, U, Wagbo, AM, Voss, B, Schmidt, A, Hessman, SD, Duschl, A, Oostingh, GJ, Diabaté, S & Weiss, C 2019, 'The protein corona suppresses the cytotoxic and pro-inflammatory response in lung epithelial cells and macrophages upon exposure to nanosilica', Archives of Toxicology. https://doi.org/10.1007/s00204-019-02422-9
Leibe, Regina ; Hsiao, I-Lun ; Fritsch-Decker, Susanne ; Kielmeier, Ulrike ; Wagbo, Ane Marit ; Voss, Benjamin ; Schmidt, Annemarie ; Hessman, Sarah Dorothea ; Duschl, Albert ; Oostingh, Gertie Janneke ; Diabaté, Silvia ; Weiss, Carsten. / The protein corona suppresses the cytotoxic and pro-inflammatory response in lung epithelial cells and macrophages upon exposure to nanosilica. In: Archives of Toxicology. 2019.
@article{d42053aff1584888a9cd2267030ce344,
title = "The protein corona suppresses the cytotoxic and pro-inflammatory response in lung epithelial cells and macrophages upon exposure to nanosilica",
abstract = "Engineered amorphous silica nanoparticles (nanosilica) are one of the most abundant nanomaterials and are widely used in industry. Furthermore, novel nanosilica materials are promising theranostic tools for biomedicine. However, hazardous effects of nanosilica especially after inhalation into the lung have been documented. Therefore, the safe development of nanosilica materials urgently requires predictive assays to monitor toxicity. Here, we further investigate the impact of the protein corona on the biological activity of two different types of nanosilica (colloidal and pyrogenic) in lung cells. As previously described, adsorption of serum proteins to the nanosilica surface suppresses cytotoxicity in macrophages and lung epithelial cells. As the increase of pro-inflammatory mediators is a hallmark of inflammation in the lung upon nanosilica exposure, we studied the potential coupling of the cytotoxic and pro-inflammatory response in A549 human lung epithelial cells and RAW264.7 mouse macrophages. Indeed, cytotoxicity precedes the onset of pro-inflammatory gene expression and cytokine release as exemplified for IL-8 in A549 cells and TNF-alpha in RAW264.7 macrophages after exposure to 0–100 µg/mL nanosilica in medium without serum. Formation of a protein corona not only inhibited cellular toxicity, but also the pro-inflammatory response. Of note, uptake of nanosilica into cells was negligible in the absence, but enhanced in the presence of a protein corona. Hence, the prevailing explanation that the protein corona simply interferes with cellular uptake thus preventing adverse effects needs to be revisited. In conclusion, for the reliable prediction of adverse effects of nanosilica in the lung, in vitro assays should be performed in media not complemented with complete serum. However, in case of different exposure routes, e.g., injection into the blood stream as intended for biomedicine, the protein corona prevents acute toxic actions of nanosilica.",
keywords = "Cell death, Inflammation, Lung cells, Nanoparticle, Nano–bio-interface, Protein corona, Silica",
author = "Regina Leibe and I-Lun Hsiao and Susanne Fritsch-Decker and Ulrike Kielmeier and Wagbo, {Ane Marit} and Benjamin Voss and Annemarie Schmidt and Hessman, {Sarah Dorothea} and Albert Duschl and Oostingh, {Gertie Janneke} and Silvia Diabat{\'e} and Carsten Weiss",
year = "2019",
month = "1",
day = "1",
doi = "10.1007/s00204-019-02422-9",
language = "English",
journal = "Archiv fur Toxikologie",
issn = "0003-9446",
publisher = "Springer Verlag",

}

TY - JOUR

T1 - The protein corona suppresses the cytotoxic and pro-inflammatory response in lung epithelial cells and macrophages upon exposure to nanosilica

AU - Leibe, Regina

AU - Hsiao, I-Lun

AU - Fritsch-Decker, Susanne

AU - Kielmeier, Ulrike

AU - Wagbo, Ane Marit

AU - Voss, Benjamin

AU - Schmidt, Annemarie

AU - Hessman, Sarah Dorothea

AU - Duschl, Albert

AU - Oostingh, Gertie Janneke

AU - Diabaté, Silvia

AU - Weiss, Carsten

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Engineered amorphous silica nanoparticles (nanosilica) are one of the most abundant nanomaterials and are widely used in industry. Furthermore, novel nanosilica materials are promising theranostic tools for biomedicine. However, hazardous effects of nanosilica especially after inhalation into the lung have been documented. Therefore, the safe development of nanosilica materials urgently requires predictive assays to monitor toxicity. Here, we further investigate the impact of the protein corona on the biological activity of two different types of nanosilica (colloidal and pyrogenic) in lung cells. As previously described, adsorption of serum proteins to the nanosilica surface suppresses cytotoxicity in macrophages and lung epithelial cells. As the increase of pro-inflammatory mediators is a hallmark of inflammation in the lung upon nanosilica exposure, we studied the potential coupling of the cytotoxic and pro-inflammatory response in A549 human lung epithelial cells and RAW264.7 mouse macrophages. Indeed, cytotoxicity precedes the onset of pro-inflammatory gene expression and cytokine release as exemplified for IL-8 in A549 cells and TNF-alpha in RAW264.7 macrophages after exposure to 0–100 µg/mL nanosilica in medium without serum. Formation of a protein corona not only inhibited cellular toxicity, but also the pro-inflammatory response. Of note, uptake of nanosilica into cells was negligible in the absence, but enhanced in the presence of a protein corona. Hence, the prevailing explanation that the protein corona simply interferes with cellular uptake thus preventing adverse effects needs to be revisited. In conclusion, for the reliable prediction of adverse effects of nanosilica in the lung, in vitro assays should be performed in media not complemented with complete serum. However, in case of different exposure routes, e.g., injection into the blood stream as intended for biomedicine, the protein corona prevents acute toxic actions of nanosilica.

AB - Engineered amorphous silica nanoparticles (nanosilica) are one of the most abundant nanomaterials and are widely used in industry. Furthermore, novel nanosilica materials are promising theranostic tools for biomedicine. However, hazardous effects of nanosilica especially after inhalation into the lung have been documented. Therefore, the safe development of nanosilica materials urgently requires predictive assays to monitor toxicity. Here, we further investigate the impact of the protein corona on the biological activity of two different types of nanosilica (colloidal and pyrogenic) in lung cells. As previously described, adsorption of serum proteins to the nanosilica surface suppresses cytotoxicity in macrophages and lung epithelial cells. As the increase of pro-inflammatory mediators is a hallmark of inflammation in the lung upon nanosilica exposure, we studied the potential coupling of the cytotoxic and pro-inflammatory response in A549 human lung epithelial cells and RAW264.7 mouse macrophages. Indeed, cytotoxicity precedes the onset of pro-inflammatory gene expression and cytokine release as exemplified for IL-8 in A549 cells and TNF-alpha in RAW264.7 macrophages after exposure to 0–100 µg/mL nanosilica in medium without serum. Formation of a protein corona not only inhibited cellular toxicity, but also the pro-inflammatory response. Of note, uptake of nanosilica into cells was negligible in the absence, but enhanced in the presence of a protein corona. Hence, the prevailing explanation that the protein corona simply interferes with cellular uptake thus preventing adverse effects needs to be revisited. In conclusion, for the reliable prediction of adverse effects of nanosilica in the lung, in vitro assays should be performed in media not complemented with complete serum. However, in case of different exposure routes, e.g., injection into the blood stream as intended for biomedicine, the protein corona prevents acute toxic actions of nanosilica.

KW - Cell death

KW - Inflammation

KW - Lung cells

KW - Nanoparticle

KW - Nano–bio-interface

KW - Protein corona

KW - Silica

UR - http://www.scopus.com/inward/record.url?scp=85062650563&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85062650563&partnerID=8YFLogxK

U2 - 10.1007/s00204-019-02422-9

DO - 10.1007/s00204-019-02422-9

M3 - Article

JO - Archiv fur Toxikologie

JF - Archiv fur Toxikologie

SN - 0003-9446

ER -