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

Abstract

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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Eric Smith, Helen M Palethorpe, +3 authors, Paul A Drew.
Sci Rep, 2017 Jun 15; 7(1). PMID: 28611465    Free PMC article.
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.
Review.
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.
TMPRSS2-ERG fusion co-opts master transcription factors and activates NOTCH signaling in primary prostate cancer.
Ken J Kron, Alexander Murison, +8 authors, Mathieu Lupien.
Nat Genet, 2017 Aug 08; 49(9). PMID: 28783165
Highly Cited.
Epigenetics and Bone Remodeling.
Ali Husain, Matlock A Jeffries.
Curr Osteoporos Rep, 2017 Aug 16; 15(5). PMID: 28808893    Free PMC article.
Review.
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.
Highly Cited.
Epigenetic response of imprinted domains during carcinogenesis.
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
Highly Cited.
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.
Highly Cited.
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.
Review.
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
Highly Cited. Review.
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
Review.
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.
Review.
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.
Marija Dmitrijeva, Stephan Ossowski, Luis Serrano, Martin H Schaefer.
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.
Elizabeth M Kennedy, George N Goehring, +6 authors, Karen N Conneely.
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.
Homa Rahnamoun, Juyeong Hong, +3 authors, Shannon M Lauberth.
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.
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Diet changes alter paternally inherited epigenetic pattern in male Wild guinea pigs.
A Weyrich, M Jeschek, +8 authors, J Fickel.
Environ Epigenet, 2018 Jul 12; 4(2). PMID: 29992049    Free PMC article.
Whole-genome bisulfite sequencing with improved accuracy and cost.
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.
Review.
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?
Raquel Ordoñez, Nicolás Martínez-Calle, Xabier Agirre, Felipe Prosper.
Cancers (Basel), 2019 Sep 27; 11(10). PMID: 31554341    Free PMC article.
Review.
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.
Ksenia Skvortsova, Clare Stirzaker, Phillippa Taberlay.
Essays Biochem, 2019 Dec 18; 63(6). PMID: 31845735    Free PMC article.
Review.
Ontology-driven integrative analysis of omics data through Onassis.
Eugenia Galeota, Kamal Kishore, Mattia Pelizzola.
Sci Rep, 2020 Jan 22; 10(1). PMID: 31959844    Free PMC article.
Novel genes exhibiting DNA methylation alterations in Korean patients with chronic lymphocytic leukaemia: a methyl-CpG-binding domain sequencing study.
Miyoung Kim, Eunyup Lee, +7 authors, Young Kyung Lee.
Sci Rep, 2020 Jan 25; 10(1). PMID: 31974418    Free PMC article.
Prediction of circRNAs Based on the DNA Methylation-Mediated Feature Sponge Function in Breast Cancer.
Yue Gu, Ce Ci, +7 authors, Yan Zhang.
Front Bioeng Biotechnol, 2020 Feb 11; 7. PMID: 32039169    Free PMC article.
Predicted Archaic 3D Genome Organization Reveals Genes Related to Head and Spinal Cord Separating Modern from Archaic Humans.
Daniel Batyrev, Elisheva Lapid, Liran Carmel, Eran Meshorer.
Cells, 2019 Dec 28; 9(1). PMID: 31878147    Free PMC article.
Glia-specific APOE epigenetic changes in the Alzheimer's disease brain.
Jessica Tulloch, Lesley Leong, +5 authors, Chang-En Yu.
Brain Res, 2018 Aug 07; 1698. PMID: 30081037    Free PMC article.
Longitudinal genome-wide DNA methylation analysis uncovers persistent early-life DNA methylation changes.
Raúl F Pérez, Pablo Santamarina, +6 authors, Empar Lurbe.
J Transl Med, 2019 Jan 11; 17(1). PMID: 30626398    Free PMC article.
Aberrant enhancer hypomethylation contributes to hepatic carcinogenesis through global transcriptional reprogramming.
Lei Xiong, Feng Wu, +27 authors, Ka-Fai To.
Nat Commun, 2019 Jan 20; 10(1). PMID: 30659195    Free PMC article.
Coordinated Dialogue between UHRF1 and DNMT1 to Ensure Faithful Inheritance of Methylated DNA Patterns.
Christian Bronner, Mahmoud Alhosin, Ali Hamiche, Marc Mousli.
Genes (Basel), 2019 Jan 24; 10(1). PMID: 30669400    Free PMC article.
Review.
Collective effects of long-range DNA methylations predict gene expressions and estimate phenotypes in cancer.
Soyeon Kim, Hyun Jung Park, Xiangqin Cui, Degui Zhi.
Sci Rep, 2020 Mar 05; 10(1). PMID: 32127627    Free PMC article.
ELMER v.2: an R/Bioconductor package to reconstruct gene regulatory networks from DNA methylation and transcriptome profiles.
Tiago C Silva, Simon G Coetzee, +5 authors, Benjamin P Berman.
Bioinformatics, 2018 Oct 27; 35(11). PMID: 30364927    Free PMC article.
Genome-wide quantification of the effects of DNA methylation on human gene regulation.
Amanda J Lea, Christopher M Vockley, +4 authors, Jenny Tung.
Elife, 2018 Dec 24; 7. PMID: 30575519    Free PMC article.
Integrative computational epigenomics to build data-driven gene regulation hypotheses.
Tyrone Chen, Sonika Tyagi.
Gigascience, 2020 Jun 17; 9(6). PMID: 32543653    Free PMC article.
Oct4-Mediated Inhibition of Lsd1 Activity Promotes the Active and Primed State of Pluripotency Enhancers.
Lama AlAbdi, Debapriya Saha, +8 authors, Humaira Gowher.
Cell Rep, 2020 Feb 06; 30(5). PMID: 32023463    Free PMC article.
A distinct epigenetic program underlies the 1;7 translocation in myelodysplastic syndromes.
Anair Graciela Lema Fernandez, Barbara Crescenzi, +9 authors, Cristina Mecucci.
Leukemia, 2019 Mar 30; 33(10). PMID: 30923319    Free PMC article.
The Role of DNA Methylation in Cancer.
Ranjani Lakshminarasimhan, Gangning Liang.
Adv Exp Med Biol, 2016 Nov 09; 945. PMID: 27826838    Free PMC article.
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Multifaceted Roles of DNA Methylation in Neoplastic Transformation, from Tumor Suppressors to EMT and Metastasis.
Laura Casalino, Pasquale Verde.
Genes (Basel), 2020 Aug 19; 11(8). PMID: 32806509    Free PMC article.
Review.
Epigenetics in the plant-virus interaction.
Chenguang Wang, Chaonan Wang, +3 authors, Shuifang Zhu.
Plant Cell Rep, 2019 May 09; 38(9). PMID: 31065780
Review.
Methylation Dynamics of RASSF1A and Its Impact on Cancer.
Giorgio Malpeli, Giulio Innamorati, +4 authors, Claudio Bassi.
Cancers (Basel), 2019 Jul 22; 11(7). PMID: 31323949    Free PMC article.
Review.
TENET 2.0: Identification of key transcriptional regulators and enhancers in lung adenocarcinoma.
Daniel J Mullen, Chunli Yan, +6 authors, Suhn Kyong Rhie.
PLoS Genet, 2020 Sep 15; 16(9). PMID: 32925947    Free PMC article.
The Genome in a Three-Dimensional Context: Deciphering the Contribution of Noncoding Mutations at Enhancers to Blood Cancer.
Llorenç Rovirosa, Alberto Ramos-Morales, Biola M Javierre.
Front Immunol, 2020 Oct 30; 11. PMID: 33117405    Free PMC article.
Review.
Quantitative epigenetic co-variation in CpG islands and co-regulation of developmental genes.
Hongbo Liu, Yanjun Chen, +6 authors, Qiong Wu.
Sci Rep, 2013 Sep 04; 3. PMID: 23999385    Free PMC article.
New guidelines for DNA methylome studies regarding 5-hydroxymethylcytosine for understanding transcriptional regulation.
Le Li, Yuwei Gao, +2 authors, Kevin Y Yip.
Genome Res, 2019 Feb 21; 29(4). PMID: 30782641    Free PMC article.
A comparative study of multi-omics integration tools for cancer driver gene identification and tumour subtyping.
Anita Sathyanarayanan, Rohit Gupta, +3 authors, Shivashankar H Nagaraj.
Brief Bioinform, 2019 Nov 28; 21(6). PMID: 31774481    Free PMC article.
Genomic retargeting of p53 and CTCF is associated with transcriptional changes during oncogenic HRas-induced transformation.
Michal Schwartz, Avital Sarusi Portugez, +8 authors, Ofir Hakim.
Commun Biol, 2020 Nov 27; 3(1). PMID: 33239721    Free PMC article.
Requirement of DNMT1 to orchestrate epigenomic reprogramming for NPM-ALK-driven lymphomagenesis.
Elisa Redl, Raheleh Sheibani-Tezerji, +18 authors, Gerda Egger.
Life Sci Alliance, 2020 Dec 15; 4(2). PMID: 33310759    Free PMC article.
Simplified MethylRAD Sequencing to Detect Changes in DNA Methylation at Enhancer Elements in Differentiating Embryonic Stem Cells.
Debapriya Saha, Allison B Norvil, Nadia A Lanman, Humaira Gowher.
Epigenomes, 2021 Apr 09; 4(4). PMID: 33828860    Free PMC article.
Genomic Uracil and Aberrant Profile of Demethylation Intermediates in Epigenetics and Hematologic Malignancies.
Ryszard Olinski, Geir Slupphaug, Marek Foksinski, Hans Einar Krokan.
Int J Mol Sci, 2021 May 01; 22(8). PMID: 33921666    Free PMC article.
Review.
STAT5 Regulation of Sex-Dependent Hepatic CpG Methylation at Distal Regulatory Elements Mapping to Sex-Biased Genes.
Pengying Hao, David J Waxman.
Mol Cell Biol, 2020 Nov 18; 41(2). PMID: 33199496    Free PMC article.
Extended-representation bisulfite sequencing of gene regulatory elements in multiplexed samples and single cells.
Sarah J Shareef, Samantha M Bevill, +4 authors, Bradley E Bernstein.
Nat Biotechnol, 2021 May 08;. PMID: 33958785
Genome-wide DNA methylation alteration in prenatally stressed Brahman heifer calves with the advancement of age.
Kubra Z Cilkiz, Emilie C Baker, +5 authors, David Greg Riley.
Epigenetics, 2020 Aug 21; 16(5). PMID: 32815760    Free PMC article.
Common DNA methylation dynamics in endometriod adenocarcinoma and glioblastoma suggest universal epigenomic alterations in tumorigenesis.
Jennifer A Karlow, Benpeng Miao, +2 authors, Bo Zhang.
Commun Biol, 2021 May 23; 4(1). PMID: 34021236    Free PMC article.
Genome-Wide Epigenetic Landscape of Lung Adenocarcinoma Links HOXB9 DNA Methylation to Intrinsic EGFR-TKI Resistance and Heterogeneous Responses.
Sheng-Fang Su, Chia-Hsin Liu, +9 authors, Ker-Chau Li.
JCO Precis Oncol, 2021 May 27; 5. PMID: 34036228    Free PMC article.
Genetic and Epigenetic Alterations of CDH1 Regulatory Regions in Hereditary and Sporadic Gastric Cancer.
Gianluca Tedaldi, Chiara Molinari, +16 authors, Paola Ulivi.
Pharmaceuticals (Basel), 2021 Jun 03; 14(5). PMID: 34066170    Free PMC article.