Tissue-specific DNA methylation loss during ageing and carcinogenesis is linked to chromosome structure, replication timing and cell division rates

Baylin, 2011, A decade of exploring the cancer epigenome — biological and translational implications, Nat. Rev. Cancer, 11, 726, 10.1038/nrc3130

You, 2012, Cancer Genetics and epigenetics: two sides of the same coin, Cancer Cell, 22, 9, 10.1016/j.ccr.2012.06.008

Shen, 2013, Interplay between the cancer genome and epigenome, Cell, 153, 38, 10.1016/j.cell.2013.03.008

Susak, 2017, Signatures of positive selection reveal a universal role of chromatin modifiers as cancer driver genes, Sci. Rep., 7, 1

Suvà, 2013, Epigenetic reprogramming in cancer, Science, 339, 1567, 10.1126/science.1230184

Massie, 2017, The importance of DNA methylation in prostate cancer development, J. Steroid Biochem. Mol. Biol., 166, 1, 10.1016/j.jsbmb.2016.04.009

Majumdar, 2011, Aberrant DNA Methylation and Prostate Cancer, Curr. Genomics, 12, 486, 10.2174/138920211797904061

Feinberg, 2004, The history of cancer epigenetics, Nat. Rev. Cancer, 4, 143, 10.1038/nrc1279

Herman, 2003, Gene silencing in cancer in association with promoter hypermethylation, N. Engl. J. Med., 349, 2042, 10.1056/NEJMra023075

Cheishvili, 2015, A common promoter hypomethylation signature in invasive breast, liver and prostate cancer cell lines reveals novel targets involved in cancer invasiveness, Oncotarget, 6, 33253, 10.18632/oncotarget.5291

Upchurch, 2016, Aberrant promoter Hypomethylation in CLL: does it matter for disease development, Front. Oncol., 6, 182, 10.3389/fonc.2016.00182

Klug, 2010, Active DNA demethylation in human postmitotic cells correlates with activating histone modifications, but not transcription levels, Genome Biol., 11, R63, 10.1186/gb-2010-11-6-r63

Calvanese, 2012, A promoter DNA demethylation landscape of human hematopoietic differentiation, Nucleic Acids Res., 40, 116, 10.1093/nar/gkr685

Bergman, 2013, DNA methylation dynamics in health and disease, Nat. Struct. Mol. Biol., 20, 274, 10.1038/nsmb.2518

Madakashira, 2017, DNA methylation, nuclear organization, and cancer, Front. Genet., 8, 76, 10.3389/fgene.2017.00076

Zhou, 2018, DNA methylation loss in late-replicating domains is linked to mitotic cell division, Nat. Genet., 50, 591, 10.1038/s41588-018-0073-4

van Steensel, 2017, Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression, Cell, 169, 780, 10.1016/j.cell.2017.04.022

Schneider, 2017, Tissue-specific tumorigenesis: context matters, Nat. Rev. Cancer, 17, 239, 10.1038/nrc.2017.5

Zane, 2014, Common features of chromatin in aging and cancer—cause or coincidence, Trends Cell Biol., 24, 686, 10.1016/j.tcb.2014.07.001

Klutstein, 2016, DNA methylation in cancer and aging, Cancer Res., 76, 3446, 10.1158/0008-5472.CAN-15-3278

Jung, 2015, Aging and DNA methylation, BMC Biol., 13, 7, 10.1186/s12915-015-0118-4

Horvath, 2013, DNA methylation age of human tissues and cell types, Genome Biol., 14, 3156, 10.1186/gb-2013-14-10-r115

Nejman, 2014, Molecular rules governing de novo methylation in cancer, Cancer Res., 74, 1475, 10.1158/0008-5472.CAN-13-3042

The Cancer Genome Atlas Research Network, 2014, Comprehensive molecular characterization of urothelial bladder carcinoma, Nature, 507, 315, 10.1038/nature12965

The Cancer Genome Atlas Network, 2012, Comprehensive molecular portraits of human breast tumours, Nature, 490, 61, 10.1038/nature11412

The Cancer Genome Atlas Network, 2012, Comprehensive molecular characterization of human colon and rectal cancer, Nature, 487, 330, 10.1038/nature11252

The Cancer Genome Atlas Research Network, 2017, Integrated genomic characterization of oesophageal carcinoma, Nature, 541, 169, 10.1038/nature20805

Brennan, 2013, The somatic genomic landscape of glioblastoma, Cell, 155, 462, 10.1016/j.cell.2013.09.034

The Cancer Genome Atlas Research Network, 2015, Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas, N. Engl. J. Med., 372, 2481, 10.1056/NEJMoa1402121

The Cancer Genome Atlas Network, 2015, Comprehensive genomic characterization of head and neck squamous cell carcinomas, Nature, 517, 576, 10.1038/nature14129

The Cancer Genome Atlas Research Network, 2013, Comprehensive molecular characterization of clear cell renal cell carcinoma, Nature, 499, 43, 10.1038/nature12222

Davis, 2014, The somatic genomic landscape of chromophobe renal cell carcinoma, Cancer Cell, 26, 319, 10.1016/j.ccr.2014.07.014

The Cancer Genome Atlas Research Network, 2016, Comprehensive molecular characterization of papillary renal-cell carcinoma, N. Engl. J. Med., 374, 135, 10.1056/NEJMoa1505917

The Cancer Genome Atlas Research Network, 2017, Comprehensive and integrative genomic characterization of hepatocellular carcinoma, Cell, 169, 1327, 10.1016/j.cell.2017.05.046

The Cancer Genome Atlas Research Network, 2014, Comprehensive molecular profiling of lung adenocarcinoma, Nature, 511, 543, 10.1038/nature13385

The Cancer Genome Atlas Research Network, 2012, Comprehensive genomic characterization of squamous cell lung cancers, Nature, 489, 519, 10.1038/nature11404

Raphael, 2017, Integrated genomic characterization of pancreatic ductal adenocarcinoma, Cancer Cell, 32, 185, 10.1016/j.ccell.2017.07.007

The Cancer Genome Atlas Network, 2015, The molecular taxonomy of primary prostate cancer, Cell, 163, 1011, 10.1016/j.cell.2015.10.025

Akbani, 2015, Genomic classification of cutaneous melanoma, Cell, 161, 1681, 10.1016/j.cell.2015.05.044

Agrawal, 2014, Integrated genomic characterization of papillary thyroid carcinoma, Cell, 159, 676, 10.1016/j.cell.2014.09.050

The Cancer Genome Atlas Research Network, 2013, Integrated genomic characterization of endometrial carcinoma, Nature, 497, 67, 10.1038/nature12113

Harris, 2014, DNA methylation-associated colonic mucosal immune and defense responses in treatment-naïve pediatric ulcerative colitis, Epigenetics, 9, 1131, 10.4161/epi.29446

Huynh, 2014, Epigenome-wide differences in pathology-free regions of multiple sclerosis–affected brains, Nat. Neurosci., 17, 121, 10.1038/nn.3588

Nones, 2014, Genome-wide DNA methylation patterns in pancreatic ductal adenocarcinoma reveal epigenetic deregulation of SLIT-ROBO, ITGA2 and MET signaling, Int. J. Cancer, 135, 1110, 10.1002/ijc.28765

Vandiver, 2015, Age and sun exposure-related widespread genomic blocks of hypomethylation in nonmalignant skin, Genome Biol., 16, 80, 10.1186/s13059-015-0644-y

Wockner, 2014, Genome-wide DNA methylation analysis of human brain tissue from schizophrenia patients, Transl. Psychiatry, 4, e339, 10.1038/tp.2013.111

Qu, 2016, Integrated genomic analysis of colorectal cancer progression reveals activation of EGFR through demethylation of the EREG promoter, Oncogene, 35, 6403, 10.1038/onc.2016.170

Murphy, 2017, Methylomic profiling of cortex samples from completed suicide cases implicates a role for PSORS1C3 in major depression and suicide, Transl. Psychiatry, 7, e989, 10.1038/tp.2016.249

Viana, 2017, Schizophrenia-associated methylomic variation: molecular signatures of disease and polygenic risk burden across multiple brain regions, Hum. Mol. Genet., 26, 210

Roos, 2017, Higher nevus count exhibits a distinct DNA methylation signature in healthy human skin: implications for melanoma, J. Invest. Dermatol., 137, 910, 10.1016/j.jid.2016.11.029

Lowe, 2015, The senescent methylome and its relationship with cancer, ageing and germline genetic variation in humans, Genome Biol., 16, 194, 10.1186/s13059-015-0748-4

Heyn, 2013, Aberrant DNA methylation profiles in the premature aging disorders Hutchinson-Gilford Progeria and Werner syndrome, Epigenetics, 8, 28, 10.4161/epi.23366

Nazor, 2012, Recurrent variations in DNA methylation in human pluripotent stem cells and their differentiated derivatives, Cell Stem Cell, 10, 620, 10.1016/j.stem.2012.02.013

Chen, 2013, Discovery of cross-reactive probes and polymorphic CpGs in the Illumina Infinium HumanMethylation450 microarray, Epigenetics, 8, 203, 10.4161/epi.23470

Du, 2008, lumi: a pipeline for processing Illumina microarray, Bioinformatics, 24, 1547, 10.1093/bioinformatics/btn224

Leek, 2012, sva: Surrogate Variable Analysis

Robinson, 2010, Evaluation of affinity-based genome-wide DNA methylation data: Effects of CpG density, amplification bias, and copy number variation, Genome Res., 20, 1719, 10.1101/gr.110601.110

Hansen, 2015, IlluminaHumanMethylation450kanno

Ritchie, 2015, limma powers differential expression analyses for RNA-sequencing and microarray studies, Nucleic Acids Res., 43, e47, 10.1093/nar/gkv007

Smedley, 2015, The BioMart community portal: an innovative alternative to large, centralized data repositories, Nucleic Acids Res., 43, W589, 10.1093/nar/gkv350

Forbes, 2017, COSMIC: somatic cancer genetics at high-resolution, Nucleic Acids Res., 45, D777, 10.1093/nar/gkw1121

Andersson, 2014, An atlas of active enhancers across human cell types and tissues, Nature, 507, 455, 10.1038/nature12787

Aran, 2013, DNA methylation of distal regulatory sites characterizes dysregulation of cancer genes, Genome Biol., 14, R21, 10.1186/gb-2013-14-3-r21

Heyn, 2016, Epigenomic analysis detects aberrant super-enhancer DNA methylation in human cancer, Genome Biol., 17, 11, 10.1186/s13059-016-0879-2

Roadmap Epigenomics Consortium, 2015, Integrative analysis of 111 reference human epigenomes, Nature, 518, 317, 10.1038/nature14248

Ernst, 2012, ChromHMM: automating chromatin state discovery and characterization, Nat. Methods, 9, 215, 10.1038/nmeth.1906

Guelen, 2008, Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions, Nature, 453, 948, 10.1038/nature06947

Meuleman, 2013, Constitutive nuclear lamina–genome interactions are highly conserved and associated with A/T-rich sequence, Genome Res., 23, 270, 10.1101/gr.141028.112

Hinrichs, 2006, The UCSC genome browser database: update 2006, Nucleic Acids Res., 34, D590, 10.1093/nar/gkj144

Hansen, 2010, Sequencing newly replicated DNA reveals widespread plasticity in human replication timing, Proc. Natl. Acad. Sci. U.S.A., 107, 139, 10.1073/pnas.0912402107

Yang, 2016, Correlation of an epigenetic mitotic clock with cancer risk, Genome Biol., 17, 205, 10.1186/s13059-016-1064-3

The GTEx Consortium, 2015, The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans, Science, 348, 648, 10.1126/science.1262110

Thienpont, 2016, Tumor hypoxia causes DNA hypermethylation by reducing TET activity, Nature, 537, 63, 10.1038/nature19081

Eustace, 2013, A 26-gene hypoxia signature predicts benefit from hypoxia-modifying therapy in laryngeal cancer but not bladder cancer, Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res., 19, 4879, 10.1158/1078-0432.CCR-13-0542

Esteller, 2001, A Gene Hypermethylation profile of human cancer, Cancer Res., 61, 3225

Gu, 2003, Role of duplicate genes in genetic robustness against null mutations, Nature, 421, 63, 10.1038/nature01198

Wang, 2015, Identification and characterization of essential genes in the human genome, Science, 350, 1096, 10.1126/science.aac7041

Zapata, 2018, Negative selection in tumor genome evolution acts on essential cellular functions and the immunopeptidome, Genome Biol., 19, 67, 10.1186/s13059-018-1434-0

Scholzen, 2000, The Ki-67 protein: from the known and the unknown, J. Cell Physiol., 182, 311, 10.1002/(SICI)1097-4652(200003)182:3<311::AID-JCP1>3.0.CO;2-9

Subramanian, 2005, Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles, Proc. Natl. Acad. Sci. U.S.A., 102, 15545, 10.1073/pnas.0506580102

Ciccarone, 2017, DNA methylation dynamics in aging: how far are we from understanding the mechanisms, Mech. Ageing Dev.

Aran, 2011, Replication timing-related and gene body-specific methylation of active human genes, Hum. Mol. Genet., 20, 670, 10.1093/hmg/ddq513

Cruickshanks, 2013, Senescent cells harbour features of the cancer epigenome, Nat. Cell Biol., 15, 1495, 10.1038/ncb2879

Bandettini, 1986, Increase of the mitotic index of colonic mucosa after cholecystectomy, Cancer, 58, 685, 10.1002/1097-0142(19860801)58:3<685::AID-CNCR2820580314>3.0.CO;2-#

Grossman, 1999, Expression and targeting of the apoptosis inhibitor, survivin, in human melanoma, J. Invest. Dermatol., 113, 1076, 10.1046/j.1523-1747.1999.00776.x

Shimi, 2011, The role of nuclear lamin B1 in cell proliferation and senescence, Genes Dev., 25, 2579, 10.1101/gad.179515.111

Freund, 2012, Lamin B1 loss is a senescence-associated biomarker, Mol. Biol. Cell, 23, 2066, 10.1091/mbc.e11-10-0884

Ivanov, 2013, Lysosome-mediated processing of chromatin in senescence, J. Cell Biol., 202, 129, 10.1083/jcb.201212110

Ahmed, 2017, Hutchinson–gilford progeria syndrome: a premature aging disease, Mol. Neurobiol., 55, 4417

Johnson, 2014, Age-related DNA methylation in normal breast tissue and its relationship with invasive breast tumor methylation, Epigenetics, 9, 268, 10.4161/epi.27015

Costello, 2000, Aberrant CpG-island methylation has non-random and tumour-type–specific patterns, Nat. Genet., 24, 132, 10.1038/72785

Sproul, 2012, Tissue of origin determines cancer-associated CpG island promoter hypermethylation patterns, Genome Biol., 13, R84, 10.1186/gb-2012-13-10-r84

Hansen, 2011, Increased methylation variation in epigenetic domains across cancer types, Nat. Genet., 43, 768, 10.1038/ng.865

Chen, 2016, Tissue-independent and tissue-specific patterns of DNA methylation alteration in cancer, Epigenet. Chromatin, 9, 10, 10.1186/s13072-016-0058-4

Schlesinger, 2007, Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer, Nat. Genet., 39, 232, 10.1038/ng1950

Widschwendter, 2007, Epigenetic stem cell signature in cancer, Nat. Genet., 39, 157, 10.1038/ng1941

Bernstein, 2006, A bivalent chromatin structure marks key developmental genes in embryonic stem cells, Cell, 125, 315, 10.1016/j.cell.2006.02.041

Smith, 2017, Epigenetic restriction of extraembryonic lineages mirrors the somatic transition to cancer, Nature, 549, 543, 10.1038/nature23891

Ross, 2010, Hypomethylation of repeated DNA sequences in cancer, Epigenomics, 2, 245, 10.2217/epi.10.2

Miousse, 2015, The fine LINE: methylation drawing the cancer landscape, BioMed Res. Int., 2015, 131547, 10.1155/2015/131547

Schuster-Böckler, 2012, Chromatin organization is a major influence on regional mutation rates in human cancer cells, Nature, 488, 504, 10.1038/nature11273

Cramer, 2016, A network of epigenetic modifiers and DNA repair genes controls tissue-specific copy number alteration preference, eLife, 5, e16519, 10.7554/eLife.16519

Berman, 2012, Regions of focal DNA hypermethylation and long-range hypomethylation in colorectal cancer coincide with nuclear lamina-associated domains, Nat. Genet., 44, 40, 10.1038/ng.969

Vandiver, 2015, DNA methylation is stable during replication and cell cycle arrest, Sci. Rep., 5, 17911, 10.1038/srep17911

Desjobert, 2015, Combined analysis of DNA methylation and cell cycle in cancer cells, Epigenetics, 10, 82, 10.1080/15592294.2014.995542

Jones, 2009, Rethinking how DNA methylation patterns are maintained, Nat. Rev. Genet., 10, 805, 10.1038/nrg2651

Ryba, 2011, Replication Timing: A Fingerprint for Cell Identity and Pluripotency, PLOS Comput. Biol., 7, e1002225, 10.1371/journal.pcbi.1002225

Ryba, 2012, Abnormal developmental control of replication-timing domains in pediatric acute lymphoblastic leukemia, Genome Res., 22, 1833, 10.1101/gr.138511.112

Tomasetti, 2015, Variation in cancer risk among tissues can be explained by the number of stem cell divisions, Science, 347, 78, 10.1126/science.1260825

Tomasetti, 2017, Stem cell divisions, somatic mutations, cancer etiology, and cancer prevention, Science, 355, 1330, 10.1126/science.aaf9011

Wu, 2016, Substantial contribution of extrinsic risk factors to cancer development, Nature, 529, 43, 10.1038/nature16166

Klutstein, 2017, Contribution of epigenetic mechanisms to variation in cancer risk among tissues, Proc. Natl. Acad. Sci. U.S.A., 114, 2230, 10.1073/pnas.1616556114

Chen, 1998, DNA hypomethylation leads to elevated mutation rates, Nature, 395, 89, 10.1038/25779

Gaudet, 2003, Induction of tumors in mice by genomic hypomethylation, Science, 300, 489, 10.1126/science.1083558

Daskalos, 2009, Hypomethylation of retrotransposable elements correlates with genomic instability in non-small cell lung cancer, Int. J. Cancer, 124, 81, 10.1002/ijc.23849