Reduced susceptibility of DNA methyltransferase 1 hypomorphic (Dnmt1N/+) mice to hepatic steatosis upon feeding liquid alcohol diet
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BACKGROUND: Methylation at C-5 (5-mdC) of CpG base pairs, the most abundant epigenetic modification of DNA, is catalyzed by 3 essential DNA methyltransferases (Dnmt1, Dnmt3a and Dnmt3b). Aberrations in DNA methylation and Dnmts are linked to different diseases including cancer. However, their role in alcoholic liver disease (ALD) has not been elucidated. METHODOLOGY/PRINCIPAL FINDINGS: Dnmt1 wild type (Dnmt1(+/+)) and hypomorphic (Dnmt1(N/+)) male mice that express reduced level of Dnmt1 were fed Lieber-DeCarli liquid diet containing ethanol for 6 weeks. Control mice were pair-fed calorie-matched alcohol-free liquid diet, and Dnmtase activity, 5-mdC content, gene expression profile and liver histopathology were evaluated. Ethanol feeding caused pronounced decrease in hepatic Dnmtase activity in Dnmt1(+/+) mice due to decrease in Dnmt1 and Dnmt3b protein levels and upregulation of miR-148 and miR-152 that target both Dnmt1 and Dnmt3b. Microarray and qPCR analysis showed that the genes involved in lipid, xenobiotic and glutathione metabolism, mitochondrial function and cell proliferation were dysregulated in the wild type mice fed alcohol. Surprisingly, Dnmt1(N/+) mice were less susceptible to alcoholic steatosis compared to Dnmt1(+/+) mice. Expression of several key genes involved in alcohol (Aldh3b1), lipid (Ppara, Lepr, Vldlr, Agpat9) and xenobiotic (Cyp39a1) metabolism, and oxidative stress (Mt-1, Fmo3) were significantly (P<0.05) altered in Dnmt1(N/+) mice relative to the wild type mice fed alcohol diet. However, CpG islands encompassing the promoter regions of Agpat9, Lepr, Mt1 and Ppara were methylation-free in both genotypes irrespective of the diet, suggesting that promoter methylation does not regulate their expression. Similarly, 5-mdC content of the liver genome, as measured by LC-MS/MS analysis, was not affected by alcohol diet in the wild type or hypomorphic mice. CONCLUSIONS/SIGNIFICANCE: Although feeding alcohol diet reduced Dnmtase activity, the loss of one copy of Dnmt1 protected mice from alcoholic hepatosteatosis by dysregulating genes involved in lipid metabolism and oxidative stress.
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Several genes were previously connected with fatty liver disease such as Nr3c1, Nr3c2, Zbtb16, Dnmt1, and Keap1, but most of the top genes had no connections with liver disease or NASH.
“Several genes were previously connected with fatty liver disease such as the glucocorticoid receptor Nr3c128,29, the mineralocorticoid receptor Nr3c230,31, the transcription factor Zbtb1632, the DNA methyltransferase Dnmt133, and the E3 ubiquitin ligase adaptor Keap134,35, but most of the top genes had no connections with liver disease or NASH.”
From Positive selection of somatically mutated clones identifies adaptive pathways in metabolic liver disease (2023) · cites this paper as [33]
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- Authors
- Kutay, H., Klepper, C., Wang, B., Hsu, S.-H., Datta, J., Yu, L., Zhang, X., Majumder, S., Motiwala, T., Khan, N., Belury, M., McClain, C., Jacob, S., & Ghoshal, K.
- Affiliations
- The Ohio State University (US)
- University of Louisville (US)
- Corresponding author
- Jacob, Samson
- Ghoshal, Kalpana
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-08-08
- Volume
- 7
- Issue
- 8
- Pages
- e41949
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3414497
- OpenAlex
- W1973151557
- Cited by
- 23
- References
- 47
- Citations by year
- 2024: 2 · 2023: 4 · 2022: 2 · 2021: 2 · 2020: 1 · 2018: 1 · 2017: 1 · 2016: 1 · 2015: 2 · 2014: 6 · 2013: 1
- FWCI
- 2.08
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Pelotonia
- National Institutes of Health
- National Institute on Alcohol Abuse and Alcoholism (R21AA016677, AA016677)
- National Cancer Institute (CA086978, R01CA086978, P30CA016058)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK088076, DK088076)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Alcohol Consumption and Health Effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Keywords
- DNMT1, alcoholic liver disease, hepatic steatosis, DNA methylation, 5-methylcytosine, DNMT3B, miR-148, miR-152, ethanol feeding, lipid metabolism, xenobiotic metabolism, oxidative stress, promoter methylation, gene expression dysregulation
- MeSH terms
- DNA (Cytosine-5-)-Methyltransferase 1, DNA Methyltransferase 3A, DNA Methyltransferase 3B, Ethanol, Alcohols, Animals, Animal Feed, Cell Line, Chromatography, Liquid, Disease Models, Animal, DNA, DNA (Cytosine-5-)-Methyltransferases, Fatty Liver, Humans, Liver Diseases, Alcoholic, Male, Xenobiotics, Genome, Oxidative Stress, CpG Islands, DNA Methylation, Epigenesis, Genetic, Lipid Metabolism, Mice, Tandem Mass Spectrometry
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