Oxidative Stress, DNA Damage, and Inflammation Induced by Ambient Air and Wood Smoke Particulate Matter in Human A549 and THP-1 Cell Lines

Pernille Høgh Danielsen, Peter Møller, Keld Alstrup Jensen, Anoop Kumar Sharma, Håkan Wallin, Rossana Bossi, Herman Autrup, Lars Mølhave, Jean-Luc Ravanat, Jacob Jan Briede, Theo Martinus de Kok, Steffen Loft

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

Combustion of biomass and wood for residential heating and/or cooking contributes substantially to both ambient air and indoor levels of particulate matter (PM). Toxicological characterization of ambient air PM, especially related to traffic, is well advanced, whereas the toxicology of wood smoke PM (WSPM) is poorly assessed. We assessed a wide spectrum of toxicity end points in human A549 lung epithelial and THP-1 monocytic cell lines comparingWSPM from high or low oxygen combustion and ambient PM collected in a village with many operating wood stoves and from a rural background area. In both cell types, all extensively characterized PM samples (1.25-100 μg/mL) induced dose-dependent formation of reactive oxygen species and DNA damage in terms of strand breaks and formamidopyrimidine DNA glycosylase sites assessed by the comet assay with WSPM being most potent. The WSPM contained more polycyclic aromatic hydrocarbons (PAH), less soluble metals, and expectedly also had a smaller particle size than PM collected from ambient air. All four types of PM combined increased the levels of 8-oxo-7,8-dihydro-20-deoxyguanosine dose-dependently in A549 cells, whereas there was no change in the levels of etheno-adducts or bulky DNA adducts. Furthermore, mRNA expression of the proinflammatory genes monocyte chemoattractant protein-1, interleukin-8, and tumor necrosis factor-R as well as the oxidative stress gene heme oxygenase-1 was upregulated in the THP-1 cells especially by WSPM and ambient PM sampled from the wood stove area. Expression of oxoguanine glycosylase 1, lymphocyte function-associated antigen-1, and interleukin-6 did not change. We conclude that WSPM has small particle size, high level of PAH, low level of water-soluble metals, and produces high levels of free radicals, DNA damage as well as inflammatory and oxidative stress response gene expression in cultured human cells.
Original languageEnglish
JournalChemical Research in Toxicology
Volume24
Pages (from-to)168-184
ISSN0893-228X
DOIs
Publication statusPublished - 2011

Cite this

Danielsen, Pernille Høgh ; Møller, Peter ; Jensen, Keld Alstrup ; Sharma, Anoop Kumar ; Wallin, Håkan ; Bossi, Rossana ; Autrup, Herman ; Mølhave, Lars ; Ravanat, Jean-Luc ; Briede, Jacob Jan ; Martinus de Kok, Theo ; Loft, Steffen. / Oxidative Stress, DNA Damage, and Inflammation Induced by Ambient Air and Wood Smoke Particulate Matter in Human A549 and THP-1 Cell Lines. In: Chemical Research in Toxicology. 2011 ; Vol. 24. pp. 168-184.
@article{8242c07902be40438f6688b1b123c60f,
title = "Oxidative Stress, DNA Damage, and Inflammation Induced by Ambient Air and Wood Smoke Particulate Matter in Human A549 and THP-1 Cell Lines",
abstract = "Combustion of biomass and wood for residential heating and/or cooking contributes substantially to both ambient air and indoor levels of particulate matter (PM). Toxicological characterization of ambient air PM, especially related to traffic, is well advanced, whereas the toxicology of wood smoke PM (WSPM) is poorly assessed. We assessed a wide spectrum of toxicity end points in human A549 lung epithelial and THP-1 monocytic cell lines comparingWSPM from high or low oxygen combustion and ambient PM collected in a village with many operating wood stoves and from a rural background area. In both cell types, all extensively characterized PM samples (1.25-100 μg/mL) induced dose-dependent formation of reactive oxygen species and DNA damage in terms of strand breaks and formamidopyrimidine DNA glycosylase sites assessed by the comet assay with WSPM being most potent. The WSPM contained more polycyclic aromatic hydrocarbons (PAH), less soluble metals, and expectedly also had a smaller particle size than PM collected from ambient air. All four types of PM combined increased the levels of 8-oxo-7,8-dihydro-20-deoxyguanosine dose-dependently in A549 cells, whereas there was no change in the levels of etheno-adducts or bulky DNA adducts. Furthermore, mRNA expression of the proinflammatory genes monocyte chemoattractant protein-1, interleukin-8, and tumor necrosis factor-R as well as the oxidative stress gene heme oxygenase-1 was upregulated in the THP-1 cells especially by WSPM and ambient PM sampled from the wood stove area. Expression of oxoguanine glycosylase 1, lymphocyte function-associated antigen-1, and interleukin-6 did not change. We conclude that WSPM has small particle size, high level of PAH, low level of water-soluble metals, and produces high levels of free radicals, DNA damage as well as inflammatory and oxidative stress response gene expression in cultured human cells.",
author = "Danielsen, {Pernille H{\o}gh} and Peter M{\o}ller and Jensen, {Keld Alstrup} and Sharma, {Anoop Kumar} and H{\aa}kan Wallin and Rossana Bossi and Herman Autrup and Lars M{\o}lhave and Jean-Luc Ravanat and Briede, {Jacob Jan} and {Martinus de Kok}, Theo and Steffen Loft",
year = "2011",
doi = "10.1021/tx100407m",
language = "English",
volume = "24",
pages = "168--184",
journal = "Chemical Research in Toxicology",
issn = "0893-228X",
publisher = "American Chemical Society",

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Danielsen, PH, Møller, P, Jensen, KA, Sharma, AK, Wallin, H, Bossi, R, Autrup, H, Mølhave, L, Ravanat, J-L, Briede, JJ, Martinus de Kok, T & Loft, S 2011, 'Oxidative Stress, DNA Damage, and Inflammation Induced by Ambient Air and Wood Smoke Particulate Matter in Human A549 and THP-1 Cell Lines', Chemical Research in Toxicology, vol. 24, pp. 168-184. https://doi.org/10.1021/tx100407m

Oxidative Stress, DNA Damage, and Inflammation Induced by Ambient Air and Wood Smoke Particulate Matter in Human A549 and THP-1 Cell Lines. / Danielsen, Pernille Høgh; Møller, Peter; Jensen, Keld Alstrup; Sharma, Anoop Kumar; Wallin, Håkan; Bossi, Rossana; Autrup, Herman; Mølhave, Lars; Ravanat, Jean-Luc; Briede, Jacob Jan; Martinus de Kok, Theo; Loft, Steffen.

In: Chemical Research in Toxicology, Vol. 24, 2011, p. 168-184.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Oxidative Stress, DNA Damage, and Inflammation Induced by Ambient Air and Wood Smoke Particulate Matter in Human A549 and THP-1 Cell Lines

AU - Danielsen, Pernille Høgh

AU - Møller, Peter

AU - Jensen, Keld Alstrup

AU - Sharma, Anoop Kumar

AU - Wallin, Håkan

AU - Bossi, Rossana

AU - Autrup, Herman

AU - Mølhave, Lars

AU - Ravanat, Jean-Luc

AU - Briede, Jacob Jan

AU - Martinus de Kok, Theo

AU - Loft, Steffen

PY - 2011

Y1 - 2011

N2 - Combustion of biomass and wood for residential heating and/or cooking contributes substantially to both ambient air and indoor levels of particulate matter (PM). Toxicological characterization of ambient air PM, especially related to traffic, is well advanced, whereas the toxicology of wood smoke PM (WSPM) is poorly assessed. We assessed a wide spectrum of toxicity end points in human A549 lung epithelial and THP-1 monocytic cell lines comparingWSPM from high or low oxygen combustion and ambient PM collected in a village with many operating wood stoves and from a rural background area. In both cell types, all extensively characterized PM samples (1.25-100 μg/mL) induced dose-dependent formation of reactive oxygen species and DNA damage in terms of strand breaks and formamidopyrimidine DNA glycosylase sites assessed by the comet assay with WSPM being most potent. The WSPM contained more polycyclic aromatic hydrocarbons (PAH), less soluble metals, and expectedly also had a smaller particle size than PM collected from ambient air. All four types of PM combined increased the levels of 8-oxo-7,8-dihydro-20-deoxyguanosine dose-dependently in A549 cells, whereas there was no change in the levels of etheno-adducts or bulky DNA adducts. Furthermore, mRNA expression of the proinflammatory genes monocyte chemoattractant protein-1, interleukin-8, and tumor necrosis factor-R as well as the oxidative stress gene heme oxygenase-1 was upregulated in the THP-1 cells especially by WSPM and ambient PM sampled from the wood stove area. Expression of oxoguanine glycosylase 1, lymphocyte function-associated antigen-1, and interleukin-6 did not change. We conclude that WSPM has small particle size, high level of PAH, low level of water-soluble metals, and produces high levels of free radicals, DNA damage as well as inflammatory and oxidative stress response gene expression in cultured human cells.

AB - Combustion of biomass and wood for residential heating and/or cooking contributes substantially to both ambient air and indoor levels of particulate matter (PM). Toxicological characterization of ambient air PM, especially related to traffic, is well advanced, whereas the toxicology of wood smoke PM (WSPM) is poorly assessed. We assessed a wide spectrum of toxicity end points in human A549 lung epithelial and THP-1 monocytic cell lines comparingWSPM from high or low oxygen combustion and ambient PM collected in a village with many operating wood stoves and from a rural background area. In both cell types, all extensively characterized PM samples (1.25-100 μg/mL) induced dose-dependent formation of reactive oxygen species and DNA damage in terms of strand breaks and formamidopyrimidine DNA glycosylase sites assessed by the comet assay with WSPM being most potent. The WSPM contained more polycyclic aromatic hydrocarbons (PAH), less soluble metals, and expectedly also had a smaller particle size than PM collected from ambient air. All four types of PM combined increased the levels of 8-oxo-7,8-dihydro-20-deoxyguanosine dose-dependently in A549 cells, whereas there was no change in the levels of etheno-adducts or bulky DNA adducts. Furthermore, mRNA expression of the proinflammatory genes monocyte chemoattractant protein-1, interleukin-8, and tumor necrosis factor-R as well as the oxidative stress gene heme oxygenase-1 was upregulated in the THP-1 cells especially by WSPM and ambient PM sampled from the wood stove area. Expression of oxoguanine glycosylase 1, lymphocyte function-associated antigen-1, and interleukin-6 did not change. We conclude that WSPM has small particle size, high level of PAH, low level of water-soluble metals, and produces high levels of free radicals, DNA damage as well as inflammatory and oxidative stress response gene expression in cultured human cells.

U2 - 10.1021/tx100407m

DO - 10.1021/tx100407m

M3 - Journal article

VL - 24

SP - 168

EP - 184

JO - Chemical Research in Toxicology

JF - Chemical Research in Toxicology

SN - 0893-228X

ER -