Journal Article
. 2013 Mar; 14(3):R21.
doi: 10.1186/gb-2013-14-3-r21.

DNA methylation of distal regulatory sites characterizes dysregulation of cancer genes

Dvir Aran  Sivan Sabato  Asaf Hellman  
  • PMID: 23497655
  •     40 References
  •     147 citations


Background: Abnormal epigenetic marking is well documented in gene promoters of cancer cells, but the study of distal regulatory siteshas lagged behind.We performed a systematic analysis of DNA methylation sites connected with gene expression profilesacross normal and cancerous human genomes.

Results: Utilizing methylation and expression data in 58 cell types, we developed a model for methylation-expression relationships in gene promoters and extrapolated it to the genome. We mapped numerous sites at which DNA methylation was associated with expression of distal genes. These sites bind transcription factors in a methylation-dependent manner, and carry the chromatin marks of a particular class of transcriptional enhancers. In contrast to the traditional model of one enhancer site per cell type, we found that single enhancer sites may define gradients of expression levels across many different cell types. Strikingly, the identified sites were drastically altered in cancers: hypomethylated enhancer sites associated with upregulation of cancer-related genes and hypermethylated sites with downregulation. Moreover, the association between enhancer methylation and gene deregulation in cancerwas significantly stronger than the association of promoter methylationwith gene deregulation.

Conclusions: Methylation of distal regulatory sites is closely related to gene expression levels across the genome. Single enhancers may modulate ranges of cell-specific transcription levels, from constantlyopen promoters. In contrast to the remote relationships between promoter methylation and gene dysregulation in cancer, altered methylation of enhancer sites is closely related to gene expression profiles of transformed cells.

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Genome-wide methylome and chromatin interactome identify abnormal enhancer to be risk factor of breast cancer.
Yuan Wang, Da-Peng Hao, +2 authors, Li-Jun Di.
Oncotarget, 2017 Jun 18; 8(27). PMID: 28621677    Free PMC article.
A refined DNA methylation detection method using MspJI coupled quantitative PCR.
Christopher J Petell, Gilbert Loiseau, +2 authors, Humaira Gowher.
Anal Biochem, 2017 Jun 19; 533. PMID: 28624296    Free PMC article.
Genetic Mutations and Epigenetic Modifications: Driving Cancer and Informing Precision Medicine.
Krysta Mila Coyle, Jeanette E Boudreau, Paola Marcato.
Biomed Res Int, 2017 Jul 08; 2017. PMID: 28685150    Free PMC article.
Integrin α6β4 Upregulates Amphiregulin and Epiregulin through Base Excision Repair-Mediated DNA Demethylation and Promotes Genome-wide DNA Hypomethylation.
Brittany L Carpenter, Jinpeng Liu, +2 authors, Kathleen L O'Connor.
Sci Rep, 2017 Jul 25; 7(1). PMID: 28733611    Free PMC article.
A long-range interactive DNA methylation marker panel for the promoters of HOXA9 and HOXA10 predicts survival in breast cancer patients.
Seong-Min Park, Eun-Young Choi, +2 authors, Youn-Jae Kim.
Clin Epigenetics, 2017 Jul 28; 9. PMID: 28748001    Free PMC article.
Genome-wide screen for differentially methylated long noncoding RNAs identifies Esrp2 and lncRNA Esrp2-as regulated by enhancer DNA methylation with prognostic relevance for human breast cancer.
K Heilmann, R Toth, +3 authors, C Gerhauser.
Oncogene, 2017 Aug 02; 36(46). PMID: 28759043    Free PMC article.
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Nat Genet, 2017 Aug 08; 49(9). PMID: 28783165
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Epigenetics and Bone Remodeling.
Ali Husain, Matlock A Jeffries.
Curr Osteoporos Rep, 2017 Aug 16; 15(5). PMID: 28808893    Free PMC article.
Epigenome-wide analysis of DNA methylation in lung tissue shows concordance with blood studies and identifies tobacco smoke-inducible enhancers.
Theresa Ryan Stueve, Wen-Qing Li, +14 authors, Maria Teresa Landi.
Hum Mol Genet, 2017 Sep 01; 26(15). PMID: 28854564    Free PMC article.
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Corey L Bretz, Ingeborg M Langohr, Joomyeong Kim.
Clin Epigenetics, 2017 Sep 01; 9. PMID: 28855972    Free PMC article.
Reconstruction of enhancer-target networks in 935 samples of human primary cells, tissues and cell lines.
Qin Cao, Christine Anyansi, +9 authors, Kevin Y Yip.
Nat Genet, 2017 Sep 05; 49(10). PMID: 28869592
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Chronic Cigarette Smoke-Induced Epigenomic Changes Precede Sensitization of Bronchial Epithelial Cells to Single-Step Transformation by KRAS Mutations.
Michelle Vaz, Stephen Y Hwang, +9 authors, Stephen B Baylin.
Cancer Cell, 2017 Sep 13; 32(3). PMID: 28898697    Free PMC article.
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Aging, Metabolism, and Cancer Development: from Peto's Paradox to the Warburg Effect.
Tia R Tidwell, Kjetil Søreide, Hanne R Hagland.
Aging Dis, 2017 Oct 03; 8(5). PMID: 28966808    Free PMC article.
Analysis of bladder cancer tumor CpG methylation and gene expression within The Cancer Genome Atlas identifies GRIA1 as a prognostic biomarker for basal-like bladder cancer.
Sloane K Tilley, William Y Kim, Rebecca C Fry.
Am J Cancer Res, 2017 Oct 06; 7(9). PMID: 28979808    Free PMC article.
Epigenetic mechanisms underlie the crosstalk between growth factors and a steroid hormone.
Yehoshua Enuka, Morris E Feldman, +16 authors, Yosef Yarden.
Nucleic Acids Res, 2017 Oct 17; 45(22). PMID: 29036586    Free PMC article.
Statistical and integrative system-level analysis of DNA methylation data.
Andrew E Teschendorff, Caroline L Relton.
Nat Rev Genet, 2017 Nov 14; 19(3). PMID: 29129922
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Comprehensive Whole DNA Methylome Analysis by Integrating MeDIP-seq and MRE-seq.
Xiaoyun Xing, Bo Zhang, Daofeng Li, Ting Wang.
Methods Mol Biol, 2017 Dec 11; 1708. PMID: 29224147    Free PMC article.
Genome-wide methylation analysis identifies genes silenced in non-seminoma cell lines.
Dzul Azri Mohamed Noor, Jennie N Jeyapalan, +10 authors, Paul J Scotting.
NPJ Genom Med, 2016 Jan 13; 1. PMID: 29263807    Free PMC article.
Modulation of DNA methylation by human papillomavirus E6 and E7 oncoproteins in cervical cancer.
Prakriti Sen, Pooja Ganguly, Niladri Ganguly.
Oncol Lett, 2017 Dec 30; 15(1). PMID: 29285184    Free PMC article.
Lung function discordance in monozygotic twins and associated differences in blood DNA methylation.
Anneli C S Bolund, Anna Starnawska, +7 authors, Torben Sigsgaard.
Clin Epigenetics, 2018 Jan 05; 9. PMID: 29299071    Free PMC article.
Transcriptome and DNA Methylome Analysis in a Mouse Model of Diet-Induced Obesity Predicts Increased Risk of Colorectal Cancer.
Ruifang Li, Sara A Grimm, +6 authors, Paul A Wade.
Cell Rep, 2018 Jan 19; 22(3). PMID: 29346762    Free PMC article.
The polymorphism of rs266729 in adiponectin gene and type 2 diabetes mellitus: A Meta-Analysis.
Panpan Sun, Li Liu, +9 authors, Xiaoli Fu.
Medicine (Baltimore), 2018 Feb 01; 96(47). PMID: 29381968    Free PMC article.
Conserved DNA Methylation Signatures in Early Maternal Separation and in Twins Discordant for CO2 Sensitivity.
Francesca Giannese, Alessandra Luchetti, +8 authors, Marco Battaglia.
Sci Rep, 2018 Feb 06; 8(1). PMID: 29396481    Free PMC article.
Enhancer DNA methylation in acute myeloid leukemia and myelodysplastic syndromes.
Leonidas Benetatos, George Vartholomatos.
Cell Mol Life Sci, 2018 Feb 28; 75(11). PMID: 29484447
Distinct chromatin signatures of DNA hypomethylation in aging and cancer.
Raúl F Pérez, Juan Ramón Tejedor, +2 authors, Mario F Fraga.
Aging Cell, 2018 Mar 06; 17(3). PMID: 29504244    Free PMC article.
Cell-Specific PEAR1 Methylation Studies Reveal a Locus that Coordinates Expression of Multiple Genes.
Benedetta Izzi, Fabrizia Noro, +2 authors, Marc F Hoylaerts.
Int J Mol Sci, 2018 Apr 04; 19(4). PMID: 29614055    Free PMC article.
DNA Methyltransferases, DNA Methylation, and Age-Associated Cognitive Function.
Di Cui, Xiangru Xu.
Int J Mol Sci, 2018 May 02; 19(5). PMID: 29710796    Free PMC article.
Galactic Cosmic Radiation Induces Persistent Epigenome Alterations Relevant to Human Lung Cancer.
E M Kennedy, D R Powell, +9 authors, P M Vertino.
Sci Rep, 2018 May 02; 8(1). PMID: 29712937    Free PMC article.
Postnatal DNA demethylation and its role in tissue maturation.
Yitzhak Reizel, Ofra Sabag, +12 authors, Howard Cedar.
Nat Commun, 2018 May 26; 9(1). PMID: 29795194    Free PMC article.
MICMIC: identification of DNA methylation of distal regulatory regions with causal effects on tumorigenesis.
Yin Tong, Jianlong Sun, +6 authors, Jiangwen Zhang.
Genome Biol, 2018 Jun 07; 19(1). PMID: 29871649    Free PMC article.
Tissue-specific DNA methylation loss during ageing and carcinogenesis is linked to chromosome structure, replication timing and cell division rates.
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Nucleic Acids Res, 2018 Jun 13; 46(14). PMID: 29893918    Free PMC article.
An integrated -omics analysis of the epigenetic landscape of gene expression in human blood cells.
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BMC Genomics, 2018 Jun 20; 19(1). PMID: 29914364    Free PMC article.
Mutant p53 regulates enhancer-associated H3K4 monomethylation through interactions with the methyltransferase MLL4.
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J Biol Chem, 2018 Jun 30; 293(34). PMID: 29954944    Free PMC article.
DNA methylation landscapes in the pathogenesis of type 2 diabetes mellitus.
Zheng Zhou, Bao Sun, Xiaoping Li, Chunsheng Zhu.
Nutr Metab (Lond), 2018 Jul 11; 15. PMID: 29988495    Free PMC article.
Diet changes alter paternally inherited epigenetic pattern in male Wild guinea pigs.
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Environ Epigenet, 2018 Jul 12; 4(2). PMID: 29992049    Free PMC article.
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Masako Suzuki, Will Liao, +7 authors, John M Greally.
Genome Res, 2018 Aug 11; 28(9). PMID: 30093547    Free PMC article.
DNA Methylation Predicts the Response of Triple-Negative Breast Cancers to All-Trans Retinoic Acid.
Krysta Mila Coyle, Cheryl A Dean, +4 authors, Paola Marcato.
Cancers (Basel), 2018 Oct 26; 10(11). PMID: 30352973    Free PMC article.
Epigenetic mechanisms and implications in tendon inflammation (Review).
Finosh G Thankam, Chandra S Boosani, Matthew F Dilisio, Devendra K Agrawal.
Int J Mol Med, 2018 Nov 06; 43(1). PMID: 30387824    Free PMC article.
Next-Generation Sequencing Profiles of the Methylome and Transcriptome in Peripheral Blood Mononuclear Cells of Rheumatoid Arthritis.
Chia-Chun Tseng, Yuan-Zhao Lin, +8 authors, Jeng-Hsien Yen.
J Clin Med, 2019 Aug 25; 8(9). PMID: 31443559    Free PMC article.
DNA Methylation of Enhancer Elements in Myeloid Neoplasms: Think Outside the Promoters?
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Cancers (Basel), 2019 Sep 27; 11(10). PMID: 31554341    Free PMC article.
Prenatal Glucocorticoid Exposure Results in Changes in Gene Transcription and DNA Methylation in the Female Juvenile Guinea Pig Hippocampus Across Three Generations.
Andrea Constantinof, Lisa Boureau, +3 authors, Stephen G Matthews.
Sci Rep, 2019 Dec 05; 9(1). PMID: 31796763    Free PMC article.
DNA methylation directs microRNA biogenesis in mammalian cells.
Ohad Glaich, Shivang Parikh, +11 authors, Carmit Levy.
Nat Commun, 2019 Dec 13; 10(1). PMID: 31827083    Free PMC article.
The DNA methylation landscape in cancer.
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Ontology-driven integrative analysis of omics data through Onassis.
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Novel genes exhibiting DNA methylation alterations in Korean patients with chronic lymphocytic leukaemia: a methyl-CpG-binding domain sequencing study.
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Prediction of circRNAs Based on the DNA Methylation-Mediated Feature Sponge Function in Breast Cancer.
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Predicted Archaic 3D Genome Organization Reveals Genes Related to Head and Spinal Cord Separating Modern from Archaic Humans.
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Cells, 2019 Dec 28; 9(1). PMID: 31878147    Free PMC article.
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Aberrant enhancer hypomethylation contributes to hepatic carcinogenesis through global transcriptional reprogramming.
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Coordinated Dialogue between UHRF1 and DNMT1 to Ensure Faithful Inheritance of Methylated DNA Patterns.
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TENET 2.0: Identification of key transcriptional regulators and enhancers in lung adenocarcinoma.
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The Genome in a Three-Dimensional Context: Deciphering the Contribution of Noncoding Mutations at Enhancers to Blood Cancer.
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New guidelines for DNA methylome studies regarding 5-hydroxymethylcytosine for understanding transcriptional regulation.
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A comparative study of multi-omics integration tools for cancer driver gene identification and tumour subtyping.
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Genome-Wide Epigenetic Landscape of Lung Adenocarcinoma Links HOXB9 DNA Methylation to Intrinsic EGFR-TKI Resistance and Heterogeneous Responses.
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Genetic and Epigenetic Alterations of CDH1 Regulatory Regions in Hereditary and Sporadic Gastric Cancer.
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