Inhalation exposure to cigarette smoke and inflammatory agents induces epigenetic changes in the lung.

Animals Carcinogens / metabolism Cell Proliferation Chromatography, High Pressure Liquid CpG Islands Cytosine / chemistry DNA / metabolism DNA Methylation Epigenesis, Genetic Female High-Throughput Nucleotide Sequencing Histones / chemistry Inflammation Inhalation Exposure Lung / drug effects Lung Neoplasms / genetics Mice Mice, Inbred Strains Nitrosamines / metabolism Smoke / adverse effects Smoking Sulfites / pharmacology Nicotiana Tobacco Products

Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
09 07 2020
Historique:
received: 16 01 2020
accepted: 09 06 2020
entrez: 11 7 2020
pubmed: 11 7 2020
medline: 26 1 2021
Statut: epublish

Résumé

Smoking-related lung tumors are characterized by profound epigenetic changes including scrambled patterns of DNA methylation, deregulated histone acetylation, altered gene expression levels, distorted microRNA profiles, and a global loss of cytosine hydroxymethylation marks. Here, we employed an enhanced version of bisulfite sequencing (RRBS/oxRRBS) followed by next generation sequencing to separately map DNA epigenetic marks 5-methyl-dC and 5-hydroxymethyl-dC in genomic DNA isolated from lungs of A/J mice exposed whole-body to environmental cigarette smoke for 10 weeks. Exposure to cigarette smoke significantly affected the patterns of cytosine methylation and hydroxymethylation in the lungs. Differentially hydroxymethylated regions were associated with inflammatory response/disease, organismal injury, and respiratory diseases and were involved in regulation of cellular development, function, growth, and proliferation. To identify epigenetic changes in the lung associated with exposure to tobacco carcinogens and inflammation, A/J mice were intranasally treated with the tobacco carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK), the inflammatory agent lipopolysaccharide (LPS), or both. NNK alone caused minimal epigenetic alterations, while exposure either to LPS or NNK/LPS in combination led to increased levels of global cytosine methylation and formylation, reduced cytosine hydroxymethylation, decreased histone acetylation, and altered expression levels of multiple genes. Our results suggest that inflammatory processes are responsible for epigenetic changes contributing to lung cancer development.

Identifiants

DOI: 10.1038/s41598-020-67502-8 PMID: 32647312 PMC: PMC7347915
pubmed: 32647312
doi: 10.1038/s41598-020-67502-8
pii: 10.1038/s41598-020-67502-8
pmc: PMC7347915
doi:

Substances chimiques

Carcinogens 0
Histones 0
Nitrosamines 0
Smoke 0
Sulfites 0
Cytosine 8J337D1HZY
DNA 9007-49-2
hydrogen sulfite OJ9787WBLU

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

11290

Subventions

Organisme : NCI NIH HHS
ID : R50 CA211249
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA138338
Pays : United States

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Auteurs

Christopher L Seiler (CL)

Department of Medicinal Chemistry, University of Minnesota, Minneapolis, MN, 55455, USA.
Masonic Cancer Center, University of Minnesota, 2231 6th Street SE, 2-147 CCRB, Minneapolis, 55455, USA.

J Ung Min Song (JUM)

Department of Veterinary Medicine, University of Minnesota, Minneapolis, MN, 55455, USA.
Masonic Cancer Center, University of Minnesota, 2231 6th Street SE, 2-147 CCRB, Minneapolis, 55455, USA.

Delshanee Kotandeniya (D)

Department of Medicinal Chemistry, University of Minnesota, Minneapolis, MN, 55455, USA.
Masonic Cancer Center, University of Minnesota, 2231 6th Street SE, 2-147 CCRB, Minneapolis, 55455, USA.

Jianji Chen (J)

Department of Biochemistry, Molecular Biology and Biophysics, University of Minnesota, Minneapolis, MN, 55455, USA.

Thomas J Y Kono (TJY)

Minnesota Supercomputing Institute, University of Minnesota, Minneapolis, MN, 55455, USA.

Qiyuan Han (Q)

Department of Biochemistry, Molecular Biology and Biophysics, University of Minnesota, Minneapolis, MN, 55455, USA.

Mathia Colwell (M)

Department of Animal Science, University of Minnesota, Minneapolis, MN, 55455, USA.

Benjamin Auch (B)

Genomics Center, University of Minnesota, Minneapolis, MN, 55455, USA.

Aaron L Sarver (AL)

Institute for Health Informatics, University of Minnesota, Minneapolis, MN, 55455, USA.
Masonic Cancer Center, University of Minnesota, 2231 6th Street SE, 2-147 CCRB, Minneapolis, 55455, USA.

Pramod Upadhyaya (P)

Masonic Cancer Center, University of Minnesota, 2231 6th Street SE, 2-147 CCRB, Minneapolis, 55455, USA.

Yanan Ren (Y)

Biostatistics Core, University of Minnesota, Minneapolis, MN, 55455, USA.

Christopher Faulk (C)

Department of Animal Science, University of Minnesota, Minneapolis, MN, 55455, USA.

Silvio De Flora (S)

Department of Health Sciences, University of Genoa, 16132, Genoa, Italy.

Sebastiano La Maestra (S)

Department of Health Sciences, University of Genoa, 16132, Genoa, Italy.

Yue Chen (Y)

Department of Biochemistry, Molecular Biology and Biophysics, University of Minnesota, Minneapolis, MN, 55455, USA.

Fekadu Kassie (F)

Department of Veterinary Medicine, University of Minnesota, Minneapolis, MN, 55455, USA.
Masonic Cancer Center, University of Minnesota, 2231 6th Street SE, 2-147 CCRB, Minneapolis, 55455, USA.

Natalia Y Tretyakova (NY)

Department of Medicinal Chemistry, University of Minnesota, Minneapolis, MN, 55455, USA. trety001@umn.edu.
Masonic Cancer Center, University of Minnesota, 2231 6th Street SE, 2-147 CCRB, Minneapolis, 55455, USA. trety001@umn.edu.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Actions chimiques et utilisations › Actions toxiques › Noxas › Cancérogènes › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Phénomènes physiologiques › Croissance et développement › Croissance › Processus de croissance cellulaire › Prolifération cellulaire › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Techniques d'investigation › Techniques de chimie analytique › Chromatographie › Chromatographie en phase liquide › Chromatographie en phase liquide à haute performance › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Ilots CpG › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Composés hétérocycliques › Composés hétéromonocycliques › Pyrimidines › Pyrimidinones › Cytosine › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ADN › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Phénomènes génétiques › Méthylation de l'ADN › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Épigenèse génétique › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Techniques d'investigation › Techniques génétiques › Analyse de séquence › Séquençage nucléotidique à haut débit › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Histone › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › États, signes et symptômes pathologiques › Processus pathologiques › Inflammation › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Environnement et santé publique › Santé publique › Pollution de l'environnement › Exposition environnementale › Exposition par inhalation › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Appareil respiratoire › Poumon › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Maladies de l'appareil respiratoire › Tumeurs de l'appareil respiratoire › Tumeurs du poumon › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Lignées consanguines de souris › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Composés chimiques organiques › Composés nitrosés › Nitrosamines › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Mélanges complexes › Matière particulaire › Fumée › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Comportement et mécanismes comportementaux › Comportement › Fumer › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Produits chimiques inorganiques › Sulfites › Inhalation exposure to cigarette smoke and...
questionsmedicales.fr › Technologie, industrie et agriculture › Produits manufacturés › Dispositifs pour fumer › Produits du tabac › Inhalation exposure to cigarette smoke and...