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Effect of concentration and duration of particulate matter exposure on the transcriptome and DNA methylome of bronchial epithelial cells

Exposure to particulate matter (PM) from ambient air pollution is a well-known risk factor for many lung diseases, but the mechanism(s) for this is not completely understood. Bronchial epithelial cells, which line the airway of the respiratory tract, undergo genome-wide level changes in gene express...

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Autores principales: Huang, Steven K, Tripathi, Priya, Koneva, Lada A, Cavalcante, Raymond G, Craig, Nathan, Scruggs, Anne M, Sartor, Maureen A, Deng, Furong, Chen, Yahong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7928203/
https://www.ncbi.nlm.nih.gov/pubmed/33692908
http://dx.doi.org/10.1093/eep/dvaa022
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author Huang, Steven K
Tripathi, Priya
Koneva, Lada A
Cavalcante, Raymond G
Craig, Nathan
Scruggs, Anne M
Sartor, Maureen A
Deng, Furong
Chen, Yahong
author_facet Huang, Steven K
Tripathi, Priya
Koneva, Lada A
Cavalcante, Raymond G
Craig, Nathan
Scruggs, Anne M
Sartor, Maureen A
Deng, Furong
Chen, Yahong
author_sort Huang, Steven K
collection PubMed
description Exposure to particulate matter (PM) from ambient air pollution is a well-known risk factor for many lung diseases, but the mechanism(s) for this is not completely understood. Bronchial epithelial cells, which line the airway of the respiratory tract, undergo genome-wide level changes in gene expression and DNA methylation particularly when exposed to fine (<2.5 µm) PM (PM(2.5)). Although some of these changes have been reported in other studies, a comparison of how different concentrations and duration of exposure affect both the gene transcriptome and DNA methylome has not been done. Here, we exposed BEAS-2B, a bronchial epithelial cell line, to different concentrations of PM(2.5), and compared how single or repeated doses of PM(2.5) affect both the transcriptome and methylome of cells. Widespread changes in gene expression occurred after cells were exposed to a single treatment of high-concentration (30 µg/cm(2)) PM(2.5) for 24 h. These genes were enriched in pathways regulating cytokine–cytokine interactions, Mitogen-Activated Protein Kinase (MAPK) signaling, PI3K-Akt signaling, IL6, and P53. DNA methylomic analysis showed that nearly half of the differentially expressed genes were found to also have DNA methylation changes, with just a slightly greater trend toward overall hypomethylation across the genome. Cells exposed to a lower concentration (1 µg/cm(2)) of PM(2.5) demonstrated a comparable, but more attenuated change in gene expression compared to cells exposed to higher concentrations. There were also many genes affected by lower concentrations of PM(2.5), but not higher concentrations. Additionally, repeated exposure to PM(2.5) (1 µg/cm(2)) for seven days resulted in transcriptomic and DNA methylomic changes that were distinct from cells treated with PM(2.5) for only one day. Compared to single exposure, repeated exposure to PM(2.5) caused a more notable degree of hypomethylation across the genome, though certain genes and regions demonstrated increased DNA methylation. The overall increase in hypomethylation, especially with repeated exposure to PM(2.5), was associated with an increase in expression of ten–eleven translocation enzymes. These data demonstrate how variations in concentration and duration of PM(2.5) exposure induce distinct differences in the transcriptomic and DNA methylomic profile of bronchial epithelial cells, which may have important implications in the development of both acute and chronic lung disease.
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spelling pubmed-79282032021-03-09 Effect of concentration and duration of particulate matter exposure on the transcriptome and DNA methylome of bronchial epithelial cells Huang, Steven K Tripathi, Priya Koneva, Lada A Cavalcante, Raymond G Craig, Nathan Scruggs, Anne M Sartor, Maureen A Deng, Furong Chen, Yahong Environ Epigenet Research Article Exposure to particulate matter (PM) from ambient air pollution is a well-known risk factor for many lung diseases, but the mechanism(s) for this is not completely understood. Bronchial epithelial cells, which line the airway of the respiratory tract, undergo genome-wide level changes in gene expression and DNA methylation particularly when exposed to fine (<2.5 µm) PM (PM(2.5)). Although some of these changes have been reported in other studies, a comparison of how different concentrations and duration of exposure affect both the gene transcriptome and DNA methylome has not been done. Here, we exposed BEAS-2B, a bronchial epithelial cell line, to different concentrations of PM(2.5), and compared how single or repeated doses of PM(2.5) affect both the transcriptome and methylome of cells. Widespread changes in gene expression occurred after cells were exposed to a single treatment of high-concentration (30 µg/cm(2)) PM(2.5) for 24 h. These genes were enriched in pathways regulating cytokine–cytokine interactions, Mitogen-Activated Protein Kinase (MAPK) signaling, PI3K-Akt signaling, IL6, and P53. DNA methylomic analysis showed that nearly half of the differentially expressed genes were found to also have DNA methylation changes, with just a slightly greater trend toward overall hypomethylation across the genome. Cells exposed to a lower concentration (1 µg/cm(2)) of PM(2.5) demonstrated a comparable, but more attenuated change in gene expression compared to cells exposed to higher concentrations. There were also many genes affected by lower concentrations of PM(2.5), but not higher concentrations. Additionally, repeated exposure to PM(2.5) (1 µg/cm(2)) for seven days resulted in transcriptomic and DNA methylomic changes that were distinct from cells treated with PM(2.5) for only one day. Compared to single exposure, repeated exposure to PM(2.5) caused a more notable degree of hypomethylation across the genome, though certain genes and regions demonstrated increased DNA methylation. The overall increase in hypomethylation, especially with repeated exposure to PM(2.5), was associated with an increase in expression of ten–eleven translocation enzymes. These data demonstrate how variations in concentration and duration of PM(2.5) exposure induce distinct differences in the transcriptomic and DNA methylomic profile of bronchial epithelial cells, which may have important implications in the development of both acute and chronic lung disease. Oxford University Press 2021-02-28 /pmc/articles/PMC7928203/ /pubmed/33692908 http://dx.doi.org/10.1093/eep/dvaa022 Text en © The Author(s) 2021. Published by Oxford University Press. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Huang, Steven K
Tripathi, Priya
Koneva, Lada A
Cavalcante, Raymond G
Craig, Nathan
Scruggs, Anne M
Sartor, Maureen A
Deng, Furong
Chen, Yahong
Effect of concentration and duration of particulate matter exposure on the transcriptome and DNA methylome of bronchial epithelial cells
title Effect of concentration and duration of particulate matter exposure on the transcriptome and DNA methylome of bronchial epithelial cells
title_full Effect of concentration and duration of particulate matter exposure on the transcriptome and DNA methylome of bronchial epithelial cells
title_fullStr Effect of concentration and duration of particulate matter exposure on the transcriptome and DNA methylome of bronchial epithelial cells
title_full_unstemmed Effect of concentration and duration of particulate matter exposure on the transcriptome and DNA methylome of bronchial epithelial cells
title_short Effect of concentration and duration of particulate matter exposure on the transcriptome and DNA methylome of bronchial epithelial cells
title_sort effect of concentration and duration of particulate matter exposure on the transcriptome and dna methylome of bronchial epithelial cells
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7928203/
https://www.ncbi.nlm.nih.gov/pubmed/33692908
http://dx.doi.org/10.1093/eep/dvaa022
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