Oxidative stress-induced inflammation in susceptible airways by anthropogenic aerosol

Ambient air pollution is one of the leading five health risks worldwide. One of the most harmful air pollutants is particulate matter (PM), which has different physical characteristics (particle size and number, surface area and morphology) and a highly complex and variable chemical composition. Our...

Full description

Bibliographic Details
Main Authors: Zaira Leni, Laure Estelle Cassagnes, Kaspar R. Daellenbach, Imad El Haddad, Athanasia Vlachou, Gaelle Uzu, André S. H. Prévôt, Jean-Luc Jaffrezo, Nathalie Baumlin, Matthias Salathe, Urs Baltensperger, Josef Dommen, Marianne Geiser, Rodrigo Franco
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7673561/?tool=EBI
_version_ 1818116340765949952
author Zaira Leni
Laure Estelle Cassagnes
Kaspar R. Daellenbach
Imad El Haddad
Athanasia Vlachou
Gaelle Uzu
André S. H. Prévôt
Jean-Luc Jaffrezo
Nathalie Baumlin
Matthias Salathe
Urs Baltensperger
Josef Dommen
Marianne Geiser
Rodrigo Franco
author_facet Zaira Leni
Laure Estelle Cassagnes
Kaspar R. Daellenbach
Imad El Haddad
Athanasia Vlachou
Gaelle Uzu
André S. H. Prévôt
Jean-Luc Jaffrezo
Nathalie Baumlin
Matthias Salathe
Urs Baltensperger
Josef Dommen
Marianne Geiser
Rodrigo Franco
author_sort Zaira Leni
collection DOAJ
description Ambient air pollution is one of the leading five health risks worldwide. One of the most harmful air pollutants is particulate matter (PM), which has different physical characteristics (particle size and number, surface area and morphology) and a highly complex and variable chemical composition. Our goal was first to comparatively assess the effects of exposure to PM regarding cytotoxicity, release of pro-inflammatory mediators and gene expression in human bronchial epithelia (HBE) reflecting normal and compromised health status. Second, we aimed at evaluating the impact of various PM components from anthropogenic and biogenic sources on the cellular responses. Air-liquid interface (ALI) cultures of fully differentiated HBE derived from normal and cystic fibrosis (CF) donor lungs were exposed at the apical cell surface to water-soluble PM filter extracts for 4 h. The particle dose deposited on cells was 0.9–2.5 and 8.8–25.4 μg per cm2 of cell culture area for low and high PM doses, respectively. Both normal and CF HBE show a clear dose-response relationship with increasing cytotoxicity at higher PM concentrations. The concurrently enhanced release of pro-inflammatory mediators at higher PM exposure levels links cytotoxicity to inflammatory processes. Further, the PM exposure deregulates genes involved in oxidative stress and inflammatory pathways leading to an imbalance of the antioxidant system. Moreover, we identify compromised defense against PM in CF epithelia promoting exacerbation and aggravation of disease. We also demonstrate that the adverse health outcome induced by PM exposure in normal and particularly in susceptible bronchial epithelia is magnified by anthropogenic PM components. Thus, including health-relevant PM components in regulatory guidelines will result in substantial human health benefits and improve protection of the vulnerable population.
first_indexed 2024-12-11T04:20:58Z
format Article
id doaj.art-084f8f19369942f59e09e0d5d2d0d7f6
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-11T04:20:58Z
publishDate 2020-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-084f8f19369942f59e09e0d5d2d0d7f62022-12-22T01:21:06ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-011511Oxidative stress-induced inflammation in susceptible airways by anthropogenic aerosolZaira LeniLaure Estelle CassagnesKaspar R. DaellenbachImad El HaddadAthanasia VlachouGaelle UzuAndré S. H. PrévôtJean-Luc JaffrezoNathalie BaumlinMatthias SalatheUrs BaltenspergerJosef DommenMarianne GeiserRodrigo FrancoAmbient air pollution is one of the leading five health risks worldwide. One of the most harmful air pollutants is particulate matter (PM), which has different physical characteristics (particle size and number, surface area and morphology) and a highly complex and variable chemical composition. Our goal was first to comparatively assess the effects of exposure to PM regarding cytotoxicity, release of pro-inflammatory mediators and gene expression in human bronchial epithelia (HBE) reflecting normal and compromised health status. Second, we aimed at evaluating the impact of various PM components from anthropogenic and biogenic sources on the cellular responses. Air-liquid interface (ALI) cultures of fully differentiated HBE derived from normal and cystic fibrosis (CF) donor lungs were exposed at the apical cell surface to water-soluble PM filter extracts for 4 h. The particle dose deposited on cells was 0.9–2.5 and 8.8–25.4 μg per cm2 of cell culture area for low and high PM doses, respectively. Both normal and CF HBE show a clear dose-response relationship with increasing cytotoxicity at higher PM concentrations. The concurrently enhanced release of pro-inflammatory mediators at higher PM exposure levels links cytotoxicity to inflammatory processes. Further, the PM exposure deregulates genes involved in oxidative stress and inflammatory pathways leading to an imbalance of the antioxidant system. Moreover, we identify compromised defense against PM in CF epithelia promoting exacerbation and aggravation of disease. We also demonstrate that the adverse health outcome induced by PM exposure in normal and particularly in susceptible bronchial epithelia is magnified by anthropogenic PM components. Thus, including health-relevant PM components in regulatory guidelines will result in substantial human health benefits and improve protection of the vulnerable population.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7673561/?tool=EBI
spellingShingle Zaira Leni
Laure Estelle Cassagnes
Kaspar R. Daellenbach
Imad El Haddad
Athanasia Vlachou
Gaelle Uzu
André S. H. Prévôt
Jean-Luc Jaffrezo
Nathalie Baumlin
Matthias Salathe
Urs Baltensperger
Josef Dommen
Marianne Geiser
Rodrigo Franco
Oxidative stress-induced inflammation in susceptible airways by anthropogenic aerosol
PLoS ONE
title Oxidative stress-induced inflammation in susceptible airways by anthropogenic aerosol
title_full Oxidative stress-induced inflammation in susceptible airways by anthropogenic aerosol
title_fullStr Oxidative stress-induced inflammation in susceptible airways by anthropogenic aerosol
title_full_unstemmed Oxidative stress-induced inflammation in susceptible airways by anthropogenic aerosol
title_short Oxidative stress-induced inflammation in susceptible airways by anthropogenic aerosol
title_sort oxidative stress induced inflammation in susceptible airways by anthropogenic aerosol
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7673561/?tool=EBI
work_keys_str_mv AT zairaleni oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT laureestellecassagnes oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT kasparrdaellenbach oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT imadelhaddad oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT athanasiavlachou oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT gaelleuzu oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT andreshprevot oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT jeanlucjaffrezo oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT nathaliebaumlin oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT matthiassalathe oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT ursbaltensperger oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT josefdommen oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT mariannegeiser oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol
AT rodrigofranco oxidativestressinducedinflammationinsusceptibleairwaysbyanthropogenicaerosol