Cited by 396Epigenetics and DNA MethylationLiver Disease Diagnosis and TreatmentLiver physiology and pathology

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Relationship Between Methylome and Transcriptome in Patients With Nonalcoholic Fatty Liver Disease

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Murphy, Susan K., Yang, Hyuna, Moylan, Cynthia A., Pang, Herbert, Dellinger, Andrew, Abdelmalek, Manal F., Garrett, Melanie E., Ashley–Koch, Allison, Suzuki, Ayako, Tillmann, Hans L., Hauser, Michael A., Diehl, Anna Mae·2013·Gastroenterology

DOI 10.1053/j.gastro.2013.07.047PMC PMC3805742

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Abstract

Background & aims Cirrhosis and liver cancer are potential outcomes of advanced nonalcoholic fatty liver disease (NAFLD). It is not clear what factors determine whether patients will develop advanced or mild NAFLD, limiting noninvasive diagnosis and treatment before clinical sequelae emerge. We investigated whether DNA methylation profiles can distinguish patients with mild disease from those with advanced NAFLD, and how these patterns are functionally related to hepatic gene expression.Methods We collected frozen liver biopsies and clinical data from patients with biopsy-proven NAFLD (56 in the discovery cohort and 34 in the replication cohort). Samples were divided into groups based on histologic severity of fibrosis: F0-1 (mild) and F3-4 (advanced). DNA methylation profiles were determined and coupled with gene expression data from the same biopsies; differential methylation was validated in subsets of the discovery and replication cohorts. We then analyzed interactions between the methylome and transcriptome.Results Clinical features did not differ between patients known to have mild or advanced fibrosis based on biopsy analysis. There were 69,247 differentially methylated CpG sites (76% hypomethylated, 24% hypermethylated) in patients with advanced vs mild NAFLD (P < .05). Methylation at fibroblast growth factor receptor 2, methionine adenosyl methyltransferase 1A, and caspase 1 was validated by bisulfite pyrosequencing and the findings were reproduced in the replication cohort. Methylation correlated with gene transcript levels for 7% of differentially methylated CpG sites, indicating that differential methylation contributes to differences in expression. In samples with advanced NAFLD, many tissue repair genes were hypomethylated and overexpressed, and genes in certain metabolic pathways, including 1-carbon metabolism, were hypermethylated and underexpressed.Conclusions Functionally relevant differences in methylation can distinguish patients with advanced vs mild NAFLD. Altered methylation of genes that regulate processes such as steatohepatitis, fibrosis, and carcinogenesis indicate the role of DNA methylation in progression of NAFLD.

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Additional file 1 of Differential DNA methylation and changing cell-type proportions as fibrotic stage progresses in NAFLD
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Additional file 1 of Identification of differentially methylated regions associated with both liver fibrosis and hepatocellular carcinoma
Kurokawa, S., Kobori, T., Yoneda, M., Ogawa, Y., Honda, Y., Kessoku, T., Imajo, K., Saito, S., Nakajima, A., & Hotta, K. (2024) · Figshare · doi:10.6084/m9.figshare.26675435
Additional file 5 of Alterations in the hepatocyte epigenetic landscape in steatosis
Maji, R. K., Czepukojc, B., Scherer, M., Tierling, S., Cadenas, C., Gianmoena, K., Gasparoni, N., Nordström, K. J. V., Gasparoni, G., Laggai, S., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26602456
Additional file 2 of Identification of differentially methylated regions associated with both liver fibrosis and hepatocellular carcinoma
Kurokawa, S., Kobori, T., Yoneda, M., Ogawa, Y., Honda, Y., Kessoku, T., Imajo, K., Saito, S., Nakajima, A., & Hotta, K. (2024) · Figshare · doi:10.6084/m9.figshare.26675438
Additional file 6 of Alterations in the hepatocyte epigenetic landscape in steatosis
Maji, R. K., Czepukojc, B., Scherer, M., Tierling, S., Cadenas, C., Gianmoena, K., Gasparoni, N., Nordström, K. J. V., Gasparoni, G., Laggai, S., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26602459
Additional file 1 of Alterations in the hepatocyte epigenetic landscape in steatosis
Maji, R. K., Czepukojc, B., Scherer, M., Tierling, S., Cadenas, C., Gianmoena, K., Gasparoni, N., Nordström, K. J. V., Gasparoni, G., Laggai, S., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26602441
Additional file 2 of Alterations in the hepatocyte epigenetic landscape in steatosis
Maji, R. K., Czepukojc, B., Scherer, M., Tierling, S., Cadenas, C., Gianmoena, K., Gasparoni, N., Nordström, K. J. V., Gasparoni, G., Laggai, S., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26602444
Additional file 3 of Identification of differentially methylated regions associated with both liver fibrosis and hepatocellular carcinoma
Kurokawa, S., Kobori, T., Yoneda, M., Ogawa, Y., Honda, Y., Kessoku, T., Imajo, K., Saito, S., Nakajima, A., & Hotta, K. (2024) · Figshare · doi:10.6084/m9.figshare.26675441
Additional file 4 of Alterations in the hepatocyte epigenetic landscape in steatosis
Maji, R. K., Czepukojc, B., Scherer, M., Tierling, S., Cadenas, C., Gianmoena, K., Gasparoni, N., Nordström, K. J. V., Gasparoni, G., Laggai, S., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26602453
Additional file 7 of Alterations in the hepatocyte epigenetic landscape in steatosis
Maji, R. K., Czepukojc, B., Scherer, M., Tierling, S., Cadenas, C., Gianmoena, K., Gasparoni, N., Nordström, K. J. V., Gasparoni, G., Laggai, S., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26602462
Additional file 4 of Identification of differentially methylated regions associated with both liver fibrosis and hepatocellular carcinoma
Kurokawa, S., Kobori, T., Yoneda, M., Ogawa, Y., Honda, Y., Kessoku, T., Imajo, K., Saito, S., Nakajima, A., & Hotta, K. (2024) · Figshare · doi:10.6084/m9.figshare.26675444
Additional file 3 of Alterations in the hepatocyte epigenetic landscape in steatosis
Maji, R. K., Czepukojc, B., Scherer, M., Tierling, S., Cadenas, C., Gianmoena, K., Gasparoni, N., Nordström, K. J. V., Gasparoni, G., Laggai, S., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26602447
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Epigenetic reprogramming in metabolic dysfunction–associated steatotic liver disease: from metabolic memory to precision medicine
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“[13] These aberrant modifications are susceptible of inhibition, as it has been tested in hepatocellular carcinoma (HCC).”
Integrative analysis reveals gut microbiota-associated host regulatory networks in liver fibrosis
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Integrative multi-omics analysis identifies stellate cell-derived complement component 7 as a predictor of fibrosis and liver-related events in MASLD
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Authors: Murphy, S. K., Yang, H., Moylan, C. A., Pang, H., Dellinger, A., Abdelmalek, M. F., Garrett, M. E., Ashley–Koch, A., Suzuki, A., Tillmann, H. L., Hauser, M. A., & Diehl, A. M.
Affiliations: Duke University (US)
Corresponding author: Diehl, Anna Mae
ORCID: Murphy, Susan K.
Yang, Hyuna
Moylan, Cynthia A.
Pang, Herbert
Dellinger, Andrew
Abdelmalek, Manal F.
Suzuki, Ayako
Tillmann, Hans L.
Hauser, Michael A.
Diehl, Anna Mae
Venue: Gastroenterology
Publisher: Elsevier BV
Published: 2013-11
Volume: 145
Issue: 5
Pages: 1076-1087
ISSN: 0016-5085 (ISSN-L)
DOI: 10.1053/j.gastro.2013.07.047
PMC: PMC3805742
OpenAlex: W2150020322
Cited by: 391
References: 48
Citations by year: 2026: 14 · 2025: 23 · 2024: 36 · 2023: 37 · 2022: 31 · 2021: 35 · 2020: 31 · 2019: 38 · 2018: 40 · 2017: 32 · 2016: 26 · 2015: 28 · 2014: 17 · 2013: 2
FWCI: 10.89
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Gastroenterology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
The HKU Scholars Hub (University of Hong Kong) (submittedVersion)
Funders: National Institutes of Health (5rc2aa019399-02)
National Institute on Alcohol Abuse and Alcoholism (5RC2-AA019399, RC2-AA019399)
National Institute of Diabetes and Digestive and Kidney Diseases (T32DK007568)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Health Sciences › Medicine › Hepatology › Liver Disease Diagnosis and Treatment
Health Sciences › Medicine › Hepatology › Liver physiology and pathology
Keywords: non-alcoholic fatty liver disease, DNA methylation, transcriptome, liver fibrosis, disease severity, differentially methylated CpG sites, gene expression, FGF2, MAT1A, caspase-1, one-carbon metabolism, NAFLD progression, non-invasive diagnosis
MeSH terms: Adult, Biopsy, Diagnosis, Differential, Fatty Liver, Female, Gene Expression Regulation, Humans, Liver, Male, Methionine Adenosyltransferase, Middle Aged, Severity of Illness Index, Cohort Studies, Disease Progression, CpG Islands, DNA Methylation, Caspase 1, Receptor, Fibroblast Growth Factor, Type 2, Transcriptome, Non-alcoholic Fatty Liver Disease

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