Integrative Analysis of lncRNA-mRNA Coexpression in Human Lung Epithelial Cells Exposed to Dimethyl Selenide-Derived Secondary Organic Aerosols

C. M. Sabbir Ahmed; Biplab Chandra Paul; Yumeng Cui; Alexander L. Frie; Abigail Burr; Rohan Kamath; Jin Y. Chen; Tara M. Nordgren; Roya Bahreini; Ying Hsuan Lin

doi:10.1021/acs.chemrestox.0c00516

Integrative Analysis of lncRNA-mRNA Coexpression in Human Lung Epithelial Cells Exposed to Dimethyl Selenide-Derived Secondary Organic Aerosols

C. M. Sabbir Ahmed, Biplab Chandra Paul, Yumeng Cui, Alexander L. Frie, Abigail Burr, Rohan Kamath, Jin Y. Chen, Tara M. Nordgren, Roya Bahreini, Ying Hsuan Lin

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Abstract

Dimethyl selenide (DMSe) is one of the major volatile organoselenium compounds released into the atmosphere through plant metabolism and microbial methylation. DMSe has been recently revealed as a precursor of secondary organic aerosol (SOA), and its resultant SOA possesses strong oxidizing capability toward thiol groups that can perturb several major biological pathways in human airway epithelial cells and is linked to genotoxicity, DNA damage, and p53-mediated stress responses. Mounting evidence has suggested that long noncoding RNAs (lncRNAs) are involved in stress responses to internal and environmental stimuli. However, the underlying molecular interactions remain to be elucidated. In this study, we performed integrative analyses of lncRNA-mRNA coexpression in the transformed human bronchial epithelial BEAS-2B cell line exposed to DMSe-derived SOA. We identified a total of 971 differentially expressed lncRNAs in BEAS-2B cells exposed to SOA derived from O3 and OH oxidation of DMSe. Gene ontology (GO) network analysis of cis-targeted genes showed significant enrichment of DNA damage, apoptosis, and p53-mediated stress response pathways. trans-Acting lncRNAs, including PINCR, PICART1, DLGAP1-AS2, and LINC01629, known to be associated with human carcinogenesis, also showed altered expression in cell treated with DMSe-SOA. Overall, this study highlights the regulatory role of lncRNAs in altered gene expression induced by DMSe-SOA exposure.

Original language	English (US)
Pages (from-to)	892-900
Number of pages	9
Journal	Chemical research in toxicology
Volume	34
Issue number	3
DOIs	https://doi.org/10.1021/acs.chemrestox.0c00516
State	Published - Mar 15 2021
Externally published	Yes

Bibliographical note

Funding Information:
This work was supported in part by the USDA National Institute of Food and Agriculture (Hatch projects with accession numbers 1015963 and 1023777). Data analyses were performed using the computer clusters and data storage resources of the UCR High-Performance Computing Center (HPCC), which were funded by grants from NSF (MRI-1429826) and NIH (1S10OD016290-01A1).

Publisher Copyright:
© 2021 American Chemical Society.

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.

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10.1021/acs.chemrestox.0c00516

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Sabbir Ahmed, C. M., Paul, B. C., Cui, Y., Frie, A. L., Burr, A., Kamath, R., Chen, J. Y., Nordgren, T. M., Bahreini, R., & Lin, Y. H. (2021). Integrative Analysis of lncRNA-mRNA Coexpression in Human Lung Epithelial Cells Exposed to Dimethyl Selenide-Derived Secondary Organic Aerosols. Chemical research in toxicology, 34(3), 892-900. https://doi.org/10.1021/acs.chemrestox.0c00516

Sabbir Ahmed, CM, Paul, BC, Cui, Y, Frie, AL, Burr, A, Kamath, R, Chen, JY, Nordgren, TM, Bahreini, R & Lin, YH 2021, 'Integrative Analysis of lncRNA-mRNA Coexpression in Human Lung Epithelial Cells Exposed to Dimethyl Selenide-Derived Secondary Organic Aerosols', Chemical research in toxicology, vol. 34, no. 3, pp. 892-900. https://doi.org/10.1021/acs.chemrestox.0c00516

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title = "Integrative Analysis of lncRNA-mRNA Coexpression in Human Lung Epithelial Cells Exposed to Dimethyl Selenide-Derived Secondary Organic Aerosols",

abstract = "Dimethyl selenide (DMSe) is one of the major volatile organoselenium compounds released into the atmosphere through plant metabolism and microbial methylation. DMSe has been recently revealed as a precursor of secondary organic aerosol (SOA), and its resultant SOA possesses strong oxidizing capability toward thiol groups that can perturb several major biological pathways in human airway epithelial cells and is linked to genotoxicity, DNA damage, and p53-mediated stress responses. Mounting evidence has suggested that long noncoding RNAs (lncRNAs) are involved in stress responses to internal and environmental stimuli. However, the underlying molecular interactions remain to be elucidated. In this study, we performed integrative analyses of lncRNA-mRNA coexpression in the transformed human bronchial epithelial BEAS-2B cell line exposed to DMSe-derived SOA. We identified a total of 971 differentially expressed lncRNAs in BEAS-2B cells exposed to SOA derived from O3 and OH oxidation of DMSe. Gene ontology (GO) network analysis of cis-targeted genes showed significant enrichment of DNA damage, apoptosis, and p53-mediated stress response pathways. trans-Acting lncRNAs, including PINCR, PICART1, DLGAP1-AS2, and LINC01629, known to be associated with human carcinogenesis, also showed altered expression in cell treated with DMSe-SOA. Overall, this study highlights the regulatory role of lncRNAs in altered gene expression induced by DMSe-SOA exposure. ",

author = "{Sabbir Ahmed}, {C. M.} and Paul, {Biplab Chandra} and Yumeng Cui and Frie, {Alexander L.} and Abigail Burr and Rohan Kamath and Chen, {Jin Y.} and Nordgren, {Tara M.} and Roya Bahreini and Lin, {Ying Hsuan}",

note = "Funding Information: This work was supported in part by the USDA National Institute of Food and Agriculture (Hatch projects with accession numbers 1015963 and 1023777). Data analyses were performed using the computer clusters and data storage resources of the UCR High-Performance Computing Center (HPCC), which were funded by grants from NSF (MRI-1429826) and NIH (1S10OD016290-01A1). Publisher Copyright: {\textcopyright} 2021 American Chemical Society.",

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doi = "10.1021/acs.chemrestox.0c00516",

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AU - Sabbir Ahmed, C. M.

AU - Paul, Biplab Chandra

AU - Cui, Yumeng

AU - Frie, Alexander L.

AU - Burr, Abigail

AU - Kamath, Rohan

AU - Chen, Jin Y.

AU - Nordgren, Tara M.

AU - Bahreini, Roya

AU - Lin, Ying Hsuan

N1 - Funding Information: This work was supported in part by the USDA National Institute of Food and Agriculture (Hatch projects with accession numbers 1015963 and 1023777). Data analyses were performed using the computer clusters and data storage resources of the UCR High-Performance Computing Center (HPCC), which were funded by grants from NSF (MRI-1429826) and NIH (1S10OD016290-01A1). Publisher Copyright: © 2021 American Chemical Society.

PY - 2021/3/15

Y1 - 2021/3/15

N2 - Dimethyl selenide (DMSe) is one of the major volatile organoselenium compounds released into the atmosphere through plant metabolism and microbial methylation. DMSe has been recently revealed as a precursor of secondary organic aerosol (SOA), and its resultant SOA possesses strong oxidizing capability toward thiol groups that can perturb several major biological pathways in human airway epithelial cells and is linked to genotoxicity, DNA damage, and p53-mediated stress responses. Mounting evidence has suggested that long noncoding RNAs (lncRNAs) are involved in stress responses to internal and environmental stimuli. However, the underlying molecular interactions remain to be elucidated. In this study, we performed integrative analyses of lncRNA-mRNA coexpression in the transformed human bronchial epithelial BEAS-2B cell line exposed to DMSe-derived SOA. We identified a total of 971 differentially expressed lncRNAs in BEAS-2B cells exposed to SOA derived from O3 and OH oxidation of DMSe. Gene ontology (GO) network analysis of cis-targeted genes showed significant enrichment of DNA damage, apoptosis, and p53-mediated stress response pathways. trans-Acting lncRNAs, including PINCR, PICART1, DLGAP1-AS2, and LINC01629, known to be associated with human carcinogenesis, also showed altered expression in cell treated with DMSe-SOA. Overall, this study highlights the regulatory role of lncRNAs in altered gene expression induced by DMSe-SOA exposure.

AB - Dimethyl selenide (DMSe) is one of the major volatile organoselenium compounds released into the atmosphere through plant metabolism and microbial methylation. DMSe has been recently revealed as a precursor of secondary organic aerosol (SOA), and its resultant SOA possesses strong oxidizing capability toward thiol groups that can perturb several major biological pathways in human airway epithelial cells and is linked to genotoxicity, DNA damage, and p53-mediated stress responses. Mounting evidence has suggested that long noncoding RNAs (lncRNAs) are involved in stress responses to internal and environmental stimuli. However, the underlying molecular interactions remain to be elucidated. In this study, we performed integrative analyses of lncRNA-mRNA coexpression in the transformed human bronchial epithelial BEAS-2B cell line exposed to DMSe-derived SOA. We identified a total of 971 differentially expressed lncRNAs in BEAS-2B cells exposed to SOA derived from O3 and OH oxidation of DMSe. Gene ontology (GO) network analysis of cis-targeted genes showed significant enrichment of DNA damage, apoptosis, and p53-mediated stress response pathways. trans-Acting lncRNAs, including PINCR, PICART1, DLGAP1-AS2, and LINC01629, known to be associated with human carcinogenesis, also showed altered expression in cell treated with DMSe-SOA. Overall, this study highlights the regulatory role of lncRNAs in altered gene expression induced by DMSe-SOA exposure.

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Integrative Analysis of lncRNA-mRNA Coexpression in Human Lung Epithelial Cells Exposed to Dimethyl Selenide-Derived Secondary Organic Aerosols

Abstract

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