Longitudinal association of peripheral blood DNA methylation with liver fat content: distinguishing between predictors and biomarkers

Abstract Background Alterations in DNA methylation (DNAm) have been observed in patients with fatty liver, but whether they are cause or consequence remains unknown. The study aimed to investigate longitudinal association of epigenome-wide DNAm with liver fat content (LFC) in Chinese participants, a...

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Main Authors: Hailuan Zeng, Wenran Li, Mingfeng Xia, Jieyu Ge, Hui Ma, Lingyan Chen, Baishen Pan, Huandong Lin, Sijia Wang, Xin Gao
Format: Article
Language:English
Published: BMC 2024-09-01
Series:Lipids in Health and Disease
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Online Access:https://doi.org/10.1186/s12944-024-02304-9
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author Hailuan Zeng
Wenran Li
Mingfeng Xia
Jieyu Ge
Hui Ma
Lingyan Chen
Baishen Pan
Huandong Lin
Sijia Wang
Xin Gao
author_facet Hailuan Zeng
Wenran Li
Mingfeng Xia
Jieyu Ge
Hui Ma
Lingyan Chen
Baishen Pan
Huandong Lin
Sijia Wang
Xin Gao
author_sort Hailuan Zeng
collection DOAJ
description Abstract Background Alterations in DNA methylation (DNAm) have been observed in patients with fatty liver, but whether they are cause or consequence remains unknown. The study aimed to investigate longitudinal association of epigenome-wide DNAm with liver fat content (LFC) in Chinese participants, and explore their temporal relationships. Methods Data were obtained from 2 waves over a four-year time period of the Shanghai Changfeng Study (discovery, n = 407 and replication, n = 126). LFC and peripheral blood DNAm were repeatedly measured using quantitative hepatic ultrasonography and the 850 K Illumina EPIC BeadChip, respectively. Longitudinal and cross-sectional epigenome-wide association studies (EWASs) were conducted with linear mixed model and linear regression model, respectively. Meta-analysis was performed using METAL. Cross-lagged panel analysis (CLPA) was carried out to infer temporal relationships between the significant CpGs and LFC. Results Longitudinal EWAS identified cg11024682 (SREBF1), cg06500161 (ABCG1), cg16740586 (ABCG1), cg15659943 (ABCA1) and cg00163198 (SNX19) significantly associated with LFC with P < 1e-7. Another 6 of the 22 previously reported CpGs were replicated in the present longitudinal EWAS. CLPA showed longitudinal effects of cg11024682 (SREBF1) (β = 0.14 [0.06, 0.23]), cg16740586 (ABCG1) (β = 0.17 [0.08, 0.25]), cg06500161 (ABCG1) (β = 0.12 [0.03, 0.20]), cg17901584 (DHCR24) (β = -0.10 [-0.18, -0.02]), cg00574958 (CPT1A) (β = -0.09 [-0.17, -0.01]), cg08309687 (LINC00649) (β = -0.11 [-0.19, -0.03]), and cg27243685 (ABCG1) (β = 0.09 [0.01, 0.18]) on subsequent LFC. The effects were attenuated when further adjusting for body mass index. High levels of LFC led to alterations in DNAm of cg15659943 (ABCA1) (β = 0.13 [0.04, 0.21]), cg07162647 (β = -0.11 [-0.19, -0.03]), cg06500161 (ABCG1) (β = 0.10 [0.02, 0.18]), and cg27243685 (ABCG1) (β = 0.10 [0.02, 0.18]). Conclusions Blood DNAm at SREBF1, ABCG1, DHCR24, CPT1A, and LINC00649 may be predictors of subsequent LFC change. The effects of DNAm at SREBF1 and ABCG1 on LFC were partially influenced by obesity. The findings have potential implications in understanding disease pathogenesis and highlight the potential of DNAm for early detection or intervention of fatty liver.
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spelling doaj-art-246843172265432ea31c7e1abe31c36c2024-12-22T12:44:52ZengBMCLipids in Health and Disease1476-511X2024-09-0123111310.1186/s12944-024-02304-9Longitudinal association of peripheral blood DNA methylation with liver fat content: distinguishing between predictors and biomarkersHailuan Zeng0Wenran Li1Mingfeng Xia2Jieyu Ge3Hui Ma4Lingyan Chen5Baishen Pan6Huandong Lin7Sijia Wang8Xin Gao9Department of Endocrinology and Metabolism, Zhongshan Hospital, Fudan UniversityCAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of SciencesDepartment of Endocrinology and Metabolism, Zhongshan Hospital, Fudan UniversityCAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of SciencesDepartment of Geriatrics, Zhongshan Hospital, Fudan UniversityDepartment of Geriatrics, Zhongshan Hospital, Fudan UniversityDepartment of Laboratory Medicine, Zhongshan Hospital, Fudan UniversityDepartment of Endocrinology and Metabolism, Zhongshan Hospital, Fudan UniversityCAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of SciencesDepartment of Endocrinology and Metabolism, Zhongshan Hospital, Fudan UniversityAbstract Background Alterations in DNA methylation (DNAm) have been observed in patients with fatty liver, but whether they are cause or consequence remains unknown. The study aimed to investigate longitudinal association of epigenome-wide DNAm with liver fat content (LFC) in Chinese participants, and explore their temporal relationships. Methods Data were obtained from 2 waves over a four-year time period of the Shanghai Changfeng Study (discovery, n = 407 and replication, n = 126). LFC and peripheral blood DNAm were repeatedly measured using quantitative hepatic ultrasonography and the 850 K Illumina EPIC BeadChip, respectively. Longitudinal and cross-sectional epigenome-wide association studies (EWASs) were conducted with linear mixed model and linear regression model, respectively. Meta-analysis was performed using METAL. Cross-lagged panel analysis (CLPA) was carried out to infer temporal relationships between the significant CpGs and LFC. Results Longitudinal EWAS identified cg11024682 (SREBF1), cg06500161 (ABCG1), cg16740586 (ABCG1), cg15659943 (ABCA1) and cg00163198 (SNX19) significantly associated with LFC with P < 1e-7. Another 6 of the 22 previously reported CpGs were replicated in the present longitudinal EWAS. CLPA showed longitudinal effects of cg11024682 (SREBF1) (β = 0.14 [0.06, 0.23]), cg16740586 (ABCG1) (β = 0.17 [0.08, 0.25]), cg06500161 (ABCG1) (β = 0.12 [0.03, 0.20]), cg17901584 (DHCR24) (β = -0.10 [-0.18, -0.02]), cg00574958 (CPT1A) (β = -0.09 [-0.17, -0.01]), cg08309687 (LINC00649) (β = -0.11 [-0.19, -0.03]), and cg27243685 (ABCG1) (β = 0.09 [0.01, 0.18]) on subsequent LFC. The effects were attenuated when further adjusting for body mass index. High levels of LFC led to alterations in DNAm of cg15659943 (ABCA1) (β = 0.13 [0.04, 0.21]), cg07162647 (β = -0.11 [-0.19, -0.03]), cg06500161 (ABCG1) (β = 0.10 [0.02, 0.18]), and cg27243685 (ABCG1) (β = 0.10 [0.02, 0.18]). Conclusions Blood DNAm at SREBF1, ABCG1, DHCR24, CPT1A, and LINC00649 may be predictors of subsequent LFC change. The effects of DNAm at SREBF1 and ABCG1 on LFC were partially influenced by obesity. The findings have potential implications in understanding disease pathogenesis and highlight the potential of DNAm for early detection or intervention of fatty liver.https://doi.org/10.1186/s12944-024-02304-9Liver fat contentDNA methylationCross-lagged panel analysisLongitudinal study
spellingShingle Hailuan Zeng
Wenran Li
Mingfeng Xia
Jieyu Ge
Hui Ma
Lingyan Chen
Baishen Pan
Huandong Lin
Sijia Wang
Xin Gao
Longitudinal association of peripheral blood DNA methylation with liver fat content: distinguishing between predictors and biomarkers
Lipids in Health and Disease
Liver fat content
DNA methylation
Cross-lagged panel analysis
Longitudinal study
title Longitudinal association of peripheral blood DNA methylation with liver fat content: distinguishing between predictors and biomarkers
title_full Longitudinal association of peripheral blood DNA methylation with liver fat content: distinguishing between predictors and biomarkers
title_fullStr Longitudinal association of peripheral blood DNA methylation with liver fat content: distinguishing between predictors and biomarkers
title_full_unstemmed Longitudinal association of peripheral blood DNA methylation with liver fat content: distinguishing between predictors and biomarkers
title_short Longitudinal association of peripheral blood DNA methylation with liver fat content: distinguishing between predictors and biomarkers
title_sort longitudinal association of peripheral blood dna methylation with liver fat content distinguishing between predictors and biomarkers
topic Liver fat content
DNA methylation
Cross-lagged panel analysis
Longitudinal study
url https://doi.org/10.1186/s12944-024-02304-9
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