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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Background
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Background
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Background
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Moretti, V., Romeo, S., & Valenti, L. V. C. (2024) · Hepatology International · doi:10.1007/s12072-024-10667-5 · Cited by 48
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Background
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Sex difference in liver diseases: How preclinical models help to dissect the sex-related mechanisms sustaining NAFLD and hepatocellular carcinoma
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Background
Methionine Adenosyltransferase α1 Is Targeted to the Mitochondrial Matrix and Interacts with Cytochrome P450 2E1 to Lower Its Expression
Murray, B., Peng, H., Barbier‐Torres, L., Robinson, A., Li, T. W. H., Fan, W., Tomasi, M. L., Gottlieb, R. A., Eyk, J. E. V., Lu, Z., et al. (2019) · Hepatology · doi:10.1002/hep.30762 · Cited by 41
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Background
DNA methylation alters transcriptional rates of differentially expressed genes and contributes to pathophysiology in mice fed a high fat diet
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Background
Cancer-related gene expression is associated with disease severity and modifiable lifestyle factors in non-alcoholic fatty liver disease
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Background
Assessing ZNF154 methylation in patient plasma as a multicancer marker in liquid biopsies from colon, liver, ovarian and pancreatic cancer patients
Miller, B., Petrykowska, H. M., & Elnitski, L. L. (2021) · Scientific Reports · doi:10.1038/s41598-020-80345-7 · Cited by 42
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Alternative RNA Splicing in Fatty Liver Disease
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Background
Epigenetic changes and their implications in autoimmune hepatitis
Czaja, A. J. (2018) · European Journal of Clinical Investigation · doi:10.1111/eci.12899 · Cited by 36
“Epigenetic changes that influence the expression or function of genes without altering the sequence of deoxyribonucleic acid (DNA) have been implicated in the occurrence of diverse immune-mediated liver (nonalcoholic fatty liver disease [NAFLD] [34] and primary biliary cholangitis [PBC] [35]) and nonliver (systemic lu…”
Background
Differentially methylated loci in NAFLD cirrhosis are associated with key signaling pathways
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Background
Sphingolipids at the Crossroads of NAFLD and Senescence
Nikolova‐Karakashian, M. (2018) · Advances in cancer research · doi:10.1016/bs.acr.2018.05.002 · Cited by 35
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Hyperlipidemia May Synergize with Hypomethylation in Establishing Trained Immunity and Promoting Inflammation in NASH and NAFLD
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Background
Altered DNA Methylation Sites in Peripheral Blood Leukocytes from Patients with Simple Steatosis and Nonalcoholic Steatohepatitis (NASH)
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Background
Pathogenesis and pathways: nonalcoholic fatty liver disease & alcoholic liver disease
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S‐adenosylmethionine inhibits la ribonucleoprotein domain family member 1 in murine liver and human liver cancer cells
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“[1] MAT1A is down- regulated in patients with NAFLD and advanced fibrosis.[2] Patients with NAFLD with or without cirrhosis are at higher risk for HCC development.”
Background
Semaphorin 3C exacerbates liver fibrosis
Rigotti, F., Wiedmann, L., Hubert, M. O., Vacca, M., Hasan, S. S., Moll, I., Carvajal, S., Jiménez, W., Starostecka, M., Billeter, A. T., et al. (2023) · Hepatology · doi:10.1097/hep.0000000000000407 · Cited by 33
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“The next two major studies established a correlation between methylation of several target genes and the diagnosis of NAFLD based upon liver biopsy is presented in Table 4.(95,96) However, a great portion of this data vested its analysis in the epigenetic differences among various degrees of NAFLD severity, or increas…”
Background
Arid1a Loss Drives Nonalcoholic Steatohepatitis in Mice Through Epigenetic Dysregulation of Hepatic Lipogenesis and Fatty Acid Oxidation
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Background
Integrated analysis of the methylome and transcriptome of chickens with fatty liver hemorrhagic syndrome
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S-adenosylmethionine upregulates the angiotensin receptor-binding protein ATRAP via the methylation of HuR in NAFLD
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Nutrigenomics and Nutrigenetics in Metabolic- (Dysfunction) Associated Fatty Liver Disease: Novel Insights and Future Perspectives
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“On the contrary, hypermethylation status occurred for certain CpG islands in various anti-steatotic and anti-fibrotic genes, such as ApoB and peroxisome proliferator-activated receptor (PPAR)-α [75,77,78].”
Background
Deciphering the role of aberrant DNA methylation in NAFLD and NASH
Vachher, M., Bansal, S., Kumar, B., Yadav, S., & Burman, A. (2022) · Heliyon · doi:10.1016/j.heliyon.2022.e11119 · Cited by 33
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Hepatocyte Smoothened Activity Controls Susceptibility to Insulin Resistance and Nonalcoholic Fatty Liver Disease
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Self-citation
Transcriptional repression of SIRT1 by protein inhibitor of activated STAT 4 (PIAS4) in hepatic stellate cells contributes to liver fibrosis
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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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Relationship Between Methylome and Transcriptome in Patients With Nonalcoholic Fatty Liver Disease

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