Electronic cigarette smoke reduces ribosomal protein gene expression to impair protein synthesis in primary human airway epithelial cells

Abstract The widespread use of electronic cigarettes (e-cig) is a serious public health concern; however, mechanisms by which e-cig impair the function of airway epithelial cells—the direct target of e-cig smoke—are not fully understood. Here we report transcriptomic changes, including decreased exp...

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Main Authors: Hae-Ryung Park, Jose Vallarino, Michael O’Sullivan, Charlotte Wirth, Ronald A. Panganiban, Gabrielle Webb, Maya Shumyatcher, Blanca E. Himes, Jin-Ah Park, David C. Christiani, Joseph Allen, Quan Lu
Format: Article
Language:English
Published: Nature Publishing Group 2021-09-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-97013-z
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spelling doaj-e98fd73566834d71945540b957f892982021-09-05T11:33:30ZengNature Publishing GroupScientific Reports2045-23222021-09-0111111110.1038/s41598-021-97013-zElectronic cigarette smoke reduces ribosomal protein gene expression to impair protein synthesis in primary human airway epithelial cellsHae-Ryung Park0Jose Vallarino1Michael O’Sullivan2Charlotte Wirth3Ronald A. Panganiban4Gabrielle Webb5Maya Shumyatcher6Blanca E. Himes7Jin-Ah Park8David C. Christiani9Joseph Allen10Quan Lu11Program in Molecular and Integrative Physiological Sciences, Department of Environmental Health, Harvard T.H. Chan School of Public Health, Harvard School of Public HealthProgram in Molecular and Integrative Physiological Sciences, Department of Environmental Health, Harvard T.H. Chan School of Public Health, Harvard School of Public HealthProgram in Molecular and Integrative Physiological Sciences, Department of Environmental Health, Harvard T.H. Chan School of Public Health, Harvard School of Public HealthProgram in Molecular and Integrative Physiological Sciences, Department of Environmental Health, Harvard T.H. Chan School of Public Health, Harvard School of Public HealthProgram in Molecular and Integrative Physiological Sciences, Department of Environmental Health, Harvard T.H. Chan School of Public Health, Harvard School of Public HealthProgram in Molecular and Integrative Physiological Sciences, Department of Environmental Health, Harvard T.H. Chan School of Public Health, Harvard School of Public HealthDepartment of Biostatistics, Epidemiology and Informatics, University of PennsylvaniaDepartment of Biostatistics, Epidemiology and Informatics, University of PennsylvaniaProgram in Molecular and Integrative Physiological Sciences, Department of Environmental Health, Harvard T.H. Chan School of Public Health, Harvard School of Public HealthProgram in Molecular and Integrative Physiological Sciences, Department of Environmental Health, Harvard T.H. Chan School of Public Health, Harvard School of Public HealthProgram in Molecular and Integrative Physiological Sciences, Department of Environmental Health, Harvard T.H. Chan School of Public Health, Harvard School of Public HealthProgram in Molecular and Integrative Physiological Sciences, Department of Environmental Health, Harvard T.H. Chan School of Public Health, Harvard School of Public HealthAbstract The widespread use of electronic cigarettes (e-cig) is a serious public health concern; however, mechanisms by which e-cig impair the function of airway epithelial cells—the direct target of e-cig smoke—are not fully understood. Here we report transcriptomic changes, including decreased expression of many ribosomal genes, in airway epithelial cells in response to e-cig exposure. Using RNA-seq we identify over 200 differentially expressed genes in air–liquid interface cultured primary normal human bronchial epithelial (NHBE) exposed to e-cig smoke solution from commercial e-cig cartridges. In particular, exposure to e-cig smoke solution inhibits biological pathways involving ribosomes and protein biogenesis in NHBE cells. Consistent with this effect, expression of corresponding ribosomal proteins and subsequent protein biogenesis are reduced in the cells exposed to e-cig. Gas chromatography/mass spectrometry (GC/MS) analysis identified the presence of five flavoring chemicals designated as ‘high priority’ in regard to respiratory health, and methylglyoxal in e-cig smoke solution. Together, our findings reveal the potential detrimental effect of e-cig smoke on ribosomes and the associated protein biogenesis in airway epithelium. Our study calls for further investigation into how these changes in the airway epithelium contribute to the current epidemic of lung injuries in e-cig users.https://doi.org/10.1038/s41598-021-97013-z
collection DOAJ
language English
format Article
sources DOAJ
author Hae-Ryung Park
Jose Vallarino
Michael O’Sullivan
Charlotte Wirth
Ronald A. Panganiban
Gabrielle Webb
Maya Shumyatcher
Blanca E. Himes
Jin-Ah Park
David C. Christiani
Joseph Allen
Quan Lu
spellingShingle Hae-Ryung Park
Jose Vallarino
Michael O’Sullivan
Charlotte Wirth
Ronald A. Panganiban
Gabrielle Webb
Maya Shumyatcher
Blanca E. Himes
Jin-Ah Park
David C. Christiani
Joseph Allen
Quan Lu
Electronic cigarette smoke reduces ribosomal protein gene expression to impair protein synthesis in primary human airway epithelial cells
Scientific Reports
author_facet Hae-Ryung Park
Jose Vallarino
Michael O’Sullivan
Charlotte Wirth
Ronald A. Panganiban
Gabrielle Webb
Maya Shumyatcher
Blanca E. Himes
Jin-Ah Park
David C. Christiani
Joseph Allen
Quan Lu
author_sort Hae-Ryung Park
title Electronic cigarette smoke reduces ribosomal protein gene expression to impair protein synthesis in primary human airway epithelial cells
title_short Electronic cigarette smoke reduces ribosomal protein gene expression to impair protein synthesis in primary human airway epithelial cells
title_full Electronic cigarette smoke reduces ribosomal protein gene expression to impair protein synthesis in primary human airway epithelial cells
title_fullStr Electronic cigarette smoke reduces ribosomal protein gene expression to impair protein synthesis in primary human airway epithelial cells
title_full_unstemmed Electronic cigarette smoke reduces ribosomal protein gene expression to impair protein synthesis in primary human airway epithelial cells
title_sort electronic cigarette smoke reduces ribosomal protein gene expression to impair protein synthesis in primary human airway epithelial cells
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-09-01
description Abstract The widespread use of electronic cigarettes (e-cig) is a serious public health concern; however, mechanisms by which e-cig impair the function of airway epithelial cells—the direct target of e-cig smoke—are not fully understood. Here we report transcriptomic changes, including decreased expression of many ribosomal genes, in airway epithelial cells in response to e-cig exposure. Using RNA-seq we identify over 200 differentially expressed genes in air–liquid interface cultured primary normal human bronchial epithelial (NHBE) exposed to e-cig smoke solution from commercial e-cig cartridges. In particular, exposure to e-cig smoke solution inhibits biological pathways involving ribosomes and protein biogenesis in NHBE cells. Consistent with this effect, expression of corresponding ribosomal proteins and subsequent protein biogenesis are reduced in the cells exposed to e-cig. Gas chromatography/mass spectrometry (GC/MS) analysis identified the presence of five flavoring chemicals designated as ‘high priority’ in regard to respiratory health, and methylglyoxal in e-cig smoke solution. Together, our findings reveal the potential detrimental effect of e-cig smoke on ribosomes and the associated protein biogenesis in airway epithelium. Our study calls for further investigation into how these changes in the airway epithelium contribute to the current epidemic of lung injuries in e-cig users.
url https://doi.org/10.1038/s41598-021-97013-z
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