Partially methylated domains are hypervariable in breast cancer and fuel widespread CpG island hypermethylation

Brinkman, Arie B.; Nik-Zainal, Serena; Simmer, Femke; Rodríguez-González, F. Germán; Smid, Marcel; Alexandrov, Ludmil B.; Butler, Adam; Martin, Sancha; Davies, Helen; Glodzik, Dominik; Zou, Xueqing; Ramakrishna, Manasa; Staaf, Johan; Ringnér, Markus; Sieuwerts, Anieta; Ferrari, Anthony; Morganella, Sandro; Fleischer, Thomas; Kristensen, Vessela; Gut, Marta; van de Vijver, Marc J.; Børresen-Dale, Anne-Lise; Richardson, Andrea L.; Thomas, Gilles; Gut, Ivo G.; Martens, John W.  M.; Foekens, John A.; Stratton, Michael R.; Stunnenberg, Hendrik G.

doi:10.1038/s41467-019-09828-0

Title: Partially methylated domains are hypervariable in breast cancer and fuel widespread CpG island hypermethylation

Journal Article · Mon Apr 15 00:00:00 EDT 2019 · Nature Communications

DOI:https://doi.org/10.1038/s41467-019-09828-0· OSTI ID:1624152

^[1]; Nik-Zainal, Serena ^[2]; Simmer, Femke ^[1]; Rodríguez-González, F. Germán ^[3]; Smid, Marcel ^[3]; Alexandrov, Ludmil B. ^[4]; Butler, Adam ^[5];

^[5]; Davies, Helen ^[5]; Glodzik, Dominik ^[5]; Zou, Xueqing ^[5]; Ramakrishna, Manasa ^[5];

^[6];

^[3]; Ferrari, Anthony ^[7]; Morganella, Sandro ^[8];

^[9]; Kristensen, Vessela ^[10]; Gut, Marta ^[11] more »

Radboud Univ., Nijmegen (Netherlands). Radboud Inst. for Molecular Life Sciences. Faculty of Science. Dept. of Molecular Biology
Wellcome Trust Sange Inst., Cambridge (United Kingdom); Univ. of Cambridge (United Kingdom). Academic Dept. of Medical Genetics
Erasmus Univ. Medical Center, Rotterdam (Netherlands). Erasmus MC Cancer Inst. and Cancer Genomics Netherlands
Wellcome Trust Sange Inst., Cambridge (United Kingdom); Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Biology and Biophysics; Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Center for Nonlinear Studies
Wellcome Trust Sange Inst., Cambridge (United Kingdom)
Lund Univ. (Sweden). Dept. of Clinical Sciences Lund. Division of Oncology and Pathology
Centre Léon Bérard, Lyon (France). Synergie Lyon Cancer
Wellcome Trust Genome Campus, Hinxton (United Kingdom). European Bioinformatics Inst. European Molecular Biology Lab.
The Norwegian Radium Hospital (Norway). Oslo Univ. Hospital. Inst. for Cancer Research. Dept. of Genetics
The Norwegian Radium Hospital (Norway). Oslo Univ. Hospital. Inst. for Cancer Research. Dept. of Genetics; Univ. of Oslo (Norway). Inst. for Clinical medicine. K.G. Jebsen Centre for Breast Cancer Research; Akerhus Univ. Hospital, Lørenskog (Norway). Division of Medicine. Dept. of Clinical moelcular Biology and Lab. Science (EpiGen)
Parc Cientific de Barcelona (Spain). Centro nacional de Análisis Genómico (CNAG)
Academic Medical Center, Amsterdam (Netherlands). Dept. of Pathology
The Norwegian Radium Hospital (Norway). Oslo Univ. Hospital. Inst. for Cancer Research. Dept. of Genetics; Univ. of Oslo (Norway). Inst. for Clinical medicine. K.G. Jebsen Centre for Breast Cancer Research
Brigham and Women's Hospital (Harvard Medical School), Boston, MA (United States). Dept. of Pathology; Dana-Farber Cancer Institute, Boston, MA (United States)

Global loss of DNA methylation and CpG island (CGI) hypermethylation are key epigenomic aberrations in cancer. Global loss manifests itself in partially methylated domains (PMDs) which extend up to megabases. However, the distribution of PMDs within and between tumor types, and their effects on key functional genomic elements including CGIs are poorly defined. We comprehensively show that loss of methylation in PMDs occurs in a large fraction of the genome and represents the prime source of DNA methylation variation. PMDs are hypervariable in methylation level, size and distribution, and display elevated mutation rates. They impose intermediate DNA methylation levels incognizant of functional genomic elements including CGIs, underpinning a CGI methylator phenotype (CIMP). Repression effects on tumor suppressor genes are negligible as they are generally excluded from PMDs. The genomic distribution of PMDs reports tissue-of-origin and may represent tissue-specific silent regions which tolerate instability at the epigenetic, transcriptomic and genetic level.

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Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1624152

Journal Information:: Nature Communications, Vol. 10, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (79)

Increased methylation variation in epigenetic domains across cancer types Hansen, Kasper Daniel; Timp, Winston; Bravo, Héctor Corrada Nature Genetics, Vol. 43, Issue 8 https://doi.org/10.1038/ng.865	journal	June 2011
The topography of mutational processes in breast cancer genomes Morganella, Sandro; Alexandrov, Ludmil B.; Glodzik, Dominik Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11383	journal	May 2016
DNA methylation loss in late-replicating domains is linked to mitotic cell division Zhou, Wanding; Dinh, Huy Q.; Ramjan, Zachary Nature Genetics, Vol. 50, Issue 4 https://doi.org/10.1038/s41588-018-0073-4	journal	April 2018
Repeated observation of breast tumor subtypes in independent gene expression data sets Sørlie, Therese; Tibshirani, Robert; Parker, Joel Proceedings of the National Academy of Sciences, Vol. 100, Issue 14 https://doi.org/10.1073/pnas.0932692100	journal	June 2003
Cell-of-origin chromatin organization shapes the mutational landscape of cancer Polak, Paz; Karlić, Rosa; Koren, Amnon Nature, Vol. 518, Issue 7539 https://doi.org/10.1038/nature14221	journal	February 2015
Breast cancer genome and transcriptome integration implicates specific mutational signatures with immune cell infiltration Smid, Marcel; Rodríguez-González, F. Germán; Sieuwerts, Anieta M. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12910	journal	September 2016
Chromatin organization is a major influence on regional mutation rates in human cancer cells Schuster-Böckler, Benjamin; Lehner, Ben Nature, Vol. 488, Issue 7412 https://doi.org/10.1038/nature11273	journal	July 2012
Global Epigenomic Reconfiguration During Mammalian Brain Development Lister, R.; Mukamel, E. A.; Nery, J. R. Science, Vol. 341, Issue 6146 https://doi.org/10.1126/science.1237905	journal	July 2013
Comprehensive and Integrative Genomic Characterization of Hepatocellular Carcinoma Ally, Adrian; Balasundaram, Miruna; Carlsen, Rebecca Cell, Vol. 169, Issue 7 https://doi.org/10.1016/j.cell.2017.05.046	journal	June 2017
Derivation of consensus inactivation status for X-linked genes from genome-wide studies Balaton, Bradley P.; Cotton, Allison M.; Brown, Carolyn J. Biology of Sex Differences, Vol. 6, Issue 1 https://doi.org/10.1186/s13293-015-0053-7	journal	December 2015
DNA methylation profiling in the Carolina Breast Cancer Study defines cancer subclasses differing in clinicopathologic characteristics and survival Conway, Kathleen; Edmiston, Sharon N.; May, Ryan Breast Cancer Research, Vol. 16, Issue 5 https://doi.org/10.1186/s13058-014-0450-6	journal	October 2014
Large-scale methylation domains mark a functional subset of neuronally expressed genes Schroeder, D. I.; Lott, P.; Korf, I. Genome Research, Vol. 21, Issue 10 https://doi.org/10.1101/gr.119131.110	journal	July 2011
Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells Lister, Ryan; Pelizzola, Mattia; Kida, Yasuyuki S. Nature, Vol. 471, Issue 7336 https://doi.org/10.1038/nature09798	journal	February 2011
Breast Cancer Methylomes Establish an Epigenomic Foundation for Metastasis Fang, F.; Turcan, S.; Rimner, A. Science Translational Medicine, Vol. 3, Issue 75 https://doi.org/10.1126/scitranslmed.3001875	journal	March 2011
Hypomethylation distinguishes genes of some human cancers from their normal counterparts Feinberg, Andrew P.; Vogelstein, Bert Nature, Vol. 301, Issue 5895 https://doi.org/10.1038/301089a0	journal	January 1983
FactoMineR : An R Package for Multivariate Analysis Lê, Sébastien; Josse, Julie; Husson, François Journal of Statistical Software, Vol. 25, Issue 1 https://doi.org/10.18637/jss.v025.i01	journal	January 2008
Human body epigenome maps reveal noncanonical DNA methylation variation Schultz, Matthew D.; He, Yupeng; Whitaker, John W. Nature, Vol. 523, Issue 7559 https://doi.org/10.1038/nature14465	journal	June 2015
Allele-specific copy number analysis of tumors Van Loo, P.; Nordgard, S. H.; Lingjaerde, O. C. Proceedings of the National Academy of Sciences, Vol. 107, Issue 39 https://doi.org/10.1073/pnas.1009843107	journal	September 2010
The Role of Chromosome Domains in Shaping the Functional Genome Sexton, Tom; Cavalli, Giacomo Cell, Vol. 160, Issue 6 https://doi.org/10.1016/j.cell.2015.02.040	journal	March 2015
The International Human Epigenome Consortium: A Blueprint for Scientific Collaboration and Discovery Stunnenberg, Hendrik G.; Hirst, Martin; Abrignani, Sergio Cell, Vol. 167, Issue 5 https://doi.org/10.1016/j.cell.2016.11.007	journal	November 2016
Whole-genome analysis of the methylome and hydroxymethylome in normal and malignant lung and liver Li, Xin; Liu, Yun; Salz, Tal Genome Research, Vol. 26, Issue 12 https://doi.org/10.1101/gr.211854.116	journal	October 2016
Topological domains in mammalian genomes identified by analysis of chromatin interactions Dixon, Jesse R.; Selvaraj, Siddarth; Yue, Feng Nature, Vol. 485, Issue 7398 https://doi.org/10.1038/nature11082	journal	April 2012
Absolute Assignment of Breast Cancer Intrinsic Molecular Subtype Paquet, Eric R.; Hallett, Michael T. JNCI: Journal of the National Cancer Institute, Vol. 107, Issue 1 https://doi.org/10.1093/jnci/dju357	journal	December 2014
Human DNA methylomes at base resolution show widespread epigenomic differences Lister, Ryan; Pelizzola, Mattia; Dowen, Robert H. Nature, Vol. 462, Issue 7271 https://doi.org/10.1038/nature08514	journal	October 2009
Comprehensive Mapping of Long-Range Interactions Reveals Folding Principles of the Human Genome Lieberman-Aiden, E.; van Berkum, N. L.; Williams, L. Science, Vol. 326, Issue 5950 https://doi.org/10.1126/science.1181369	journal	October 2009
Decoding the regulatory landscape of medulloblastoma using DNA methylation sequencing Hovestadt, Volker; Jones, David T. W.; Picelli, Simone Nature, Vol. 510, Issue 7506 https://doi.org/10.1038/nature13268	journal	May 2014
Regions of focal DNA hypermethylation and long-range hypomethylation in colorectal cancer coincide with nuclear lamina–associated domains Berman, Benjamin P.; Weisenberger, Daniel J.; Aman, Joseph F. Nature Genetics, Vol. 44, Issue 1 https://doi.org/10.1038/ng.969	journal	November 2011
Landscape of somatic mutations in 560 breast cancer whole-genome sequences Nik-Zainal, Serena; Davies, Helen; Staaf, Johan Nature, Vol. 534, Issue 7605 https://doi.org/10.1038/nature17676	journal	May 2016
Identification of a CpG Island Methylator Phenotype that Defines a Distinct Subgroup of Glioma Noushmehr, Houtan; Weisenberger, Daniel J.; Diefes, Kristin Cancer Cell, Vol. 17, Issue 5 https://doi.org/10.1016/j.ccr.2010.03.017	journal	May 2010
Subtypes of Breast Cancer Show Preferential Site of Relapse Smid, M.; Wang, Y.; Zhang, Y. Cancer Research, Vol. 68, Issue 9 https://doi.org/10.1158/0008-5472.CAN-07-5644	journal	May 2008
Integrated Genomic Characterization of Pancreatic Ductal Adenocarcinoma Raphael, Benjamin J.; Hruban, Ralph H.; Aguirre, Andrew J. Cancer Cell, Vol. 32, Issue 2 https://doi.org/10.1016/j.ccell.2017.07.007	journal	August 2017
‘Leveling’ the playing field for analyses of single-base resolution DNA methylomes Schultz, Matthew D.; Schmitz, Robert J.; Ecker, Joseph R. Trends in Genetics, Vol. 28, Issue 12 https://doi.org/10.1016/j.tig.2012.10.012	journal	December 2012
Whole-genome fingerprint of the DNA methylome during human B cell differentiation Kulis, Marta; Merkel, Angelika; Heath, Simon Nature Genetics, Vol. 47, Issue 7 https://doi.org/10.1038/ng.3291	journal	June 2015
The inactive X chromosome is epigenetically unstable and transcriptionally labile in breast cancer Chaligné, Ronan; Popova, Tatiana; Mendoza-Parra, Marco-Antonio Genome Research, Vol. 25, Issue 4 https://doi.org/10.1101/gr.185926.114	journal	February 2015
The biogenesis of chromosome translocations Roukos, Vassilis; Misteli, Tom Nature Cell Biology, Vol. 16, Issue 4 https://doi.org/10.1038/ncb2941	journal	April 2014
Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions Guelen, Lars; Pagie, Ludo; Brasset, Emilie Nature, Vol. 453, Issue 7197 https://doi.org/10.1038/nature06947	journal	May 2008
Global DNA hypomethylation coupled to repressive chromatin domain formation and gene silencing in breast cancer Hon, G. C.; Hawkins, R. D.; Caballero, O. L. Genome Research, Vol. 22, Issue 2 https://doi.org/10.1101/gr.125872.111	journal	December 2011
Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host Timp, Winston; Feinberg, Andrew P. Nature Reviews Cancer, Vol. 13, Issue 7 https://doi.org/10.1038/nrc3486	journal	June 2013
The human placenta methylome Schroeder, D. I.; Blair, J. D.; Lott, P. Proceedings of the National Academy of Sciences, Vol. 110, Issue 15 https://doi.org/10.1073/pnas.1215145110	journal	March 2013
Atypical Teratoid/Rhabdoid Tumors Are Comprised of Three Epigenetic Subgroups with Distinct Enhancer Landscapes Johann, Pascal D.; Erkek, Serap; Zapatka, Marc Cancer Cell, Vol. 29, Issue 3 https://doi.org/10.1016/j.ccell.2016.02.001	journal	March 2016
DNA methylome analysis in Burkitt and follicular lymphomas identifies differentially methylated regions linked to somatic mutation and transcriptional control Kretzmer, Helene; Bernhart, Stephan H.; Wang, Wei Nature Genetics, Vol. 47, Issue 11 https://doi.org/10.1038/ng.3413	journal	October 2015
The Cancer Genome Atlas Pan-Cancer analysis project Weinstein, John N.; Collisson, Eric A.; Mills, Gordon B. Nature Genetics, Vol. 45, Issue 10 https://doi.org/10.1038/ng.2764	journal	September 2013
A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping Rao, Suhas S. P.; Huntley, Miriam H.; Durand, Neva C. Cell, Vol. 159, Issue 7 https://doi.org/10.1016/j.cell.2014.11.021	journal	December 2014
Differential DNA mismatch repair underlies mutation rate variation across the human genome Supek, Fran; Lehner, Ben Nature, Vol. 521, Issue 7550 https://doi.org/10.1038/nature14173	journal	February 2015
Sequencing newly replicated DNA reveals widespread plasticity in human replication timing Hansen, R. S.; Thomas, S.; Sandstrom, R. Proceedings of the National Academy of Sciences, Vol. 107, Issue 1 https://doi.org/10.1073/pnas.0912402107	journal	December 2009
Gene Density, Transcription, and Insulators Contribute to the Partition of the Drosophila Genome into Physical Domains Hou, Chunhui; Li, Li; Qin, Zhaohui S. Molecular Cell, Vol. 48, Issue 3 https://doi.org/10.1016/j.molcel.2012.08.031	journal	November 2012
A Reference Methylome Database and Analysis Pipeline to Facilitate Integrative and Comparative Epigenomics Song, Qiang; Decato, Benjamin; Hong, Elizabeth E. PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0081148	journal	December 2013
Identification of active regulatory regions from DNA methylation data Burger, Lukas; Gaidatzis, Dimos; Schübeler, Dirk Nucleic Acids Research, Vol. 41, Issue 16 https://doi.org/10.1093/nar/gkt599	journal	July 2013
An integrated genomics analysis of epigenetic subtypes in human breast tumors links DNA methylation patterns to chromatin states in normal mammary cells Holm, Karolina; Staaf, Johan; Lauss, Martin Breast Cancer Research, Vol. 18, Issue 1 https://doi.org/10.1186/s13058-016-0685-5	journal	February 2016
Beta Regression in R Cribari-Neto, Francisco; Zeileis, Achim Journal of Statistical Software, Vol. 34, Issue 2 https://doi.org/10.18637/jss.v034.i02	journal	January 2010
Comprehensive Molecular Characterization of Muscle-Invasive Bladder Cancer Robertson, A. Gordon; Kim, Jaegil; Al-Ahmadie, Hikmat Cell, Vol. 171, Issue 3 https://doi.org/10.1016/j.cell.2017.09.007	journal	October 2017
SCISSOR: a framework for identifying structural changes in RNA transcripts Choi, Hyo Young; Jo, Heejoon; Zhao, Xiaobei Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-020-20593-3	journal	January 2021
Tracing DNA paths and RNA profiles in cultured cells and tissues with ORCA Mateo, Leslie J.; Sinnott-Armstrong, Nasa; Boettiger, Alistair N. Nature Protocols, Vol. 16, Issue 3 https://doi.org/10.1038/s41596-020-00478-x	journal	February 2021
Impact of air pollution on breast cancer incidence and mortality: a nationwide analysis in South Korea Hwang, Jeongeun; Bae, Hyunjin; Choi, Seunghyun Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-62200-x	journal	March 2020
SNHG7 is a lncRNA oncogene controlled by Insulin-like Growth Factor signaling through a negative feedback loop to tightly regulate proliferation Boone, David N.; Warburton, Andrew; Som, Sreeroopa Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-65109-7	journal	May 2020
The Case for Conducting a Randomized Clinical Trial to Assess the Efficacy of a Single Dose of Prophylactic HPV Vaccines Among Adolescents Kreimer, Aimée R.; Sherman, Mark E.; Sahasrabuddhe, Vikrant V. JNCI: Journal of the National Cancer Institute, Vol. 107, Issue 3 https://doi.org/10.1093/jnci/dju436	journal	February 2015
Derivation of consensus inactivation status for X-linked genes from genome-wide studies Balaton, Bradley P.; Cotton, Allison M.; Brown, Carolyn J. BioMed Central https://doi.org/10.14288/1.0361791	text	January 2017
Repeated observation of breast tumor subtypes in independent gene expression data sets Therese, Sørlie,; E., Lønning, Per; Janos, Demeter, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/0q49-xf75	text	January 2003
Allele-specific copy number analysis of tumors B., Naume,; W., Sun,; C., Lingjaerde, O. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/2zsb-7679	text	January 2010
The cancer genome atlas pan-cancer analysis project B., Mills, Gordon; R., Mills Shaw, Kenna; Ilya, Shmulevich, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/670y-yr53	text	January 2013
Identification of a CpG Island Methylator Phenotype that Defines a Distinct Subgroup of Glioma Jonathan, Buckley,; Li, Ding,; Fei, Pan, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/gb7y-mv12	text	January 2010
Breast cancer genome and transcriptome integration implicates specific mutational signatures with immune cell infiltration. Smid, Marcel; Rodríguez-González, F. Germán; Sieuwerts, Anieta M. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.30321	text	January 2016
Investigation of the role of typhoid toxin in acute typhoid fever in a human challenge model Gibani, Malick M.; Jones, Elizabeth; Barton, Amber Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.54588	text	January 2019
A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping Rao, Suhas S. P.; Huntley, Miriam H.; Durand, Neva C. Cell, Vol. 162, Issue 3 https://doi.org/10.1016/j.cell.2015.07.024	journal	July 2015
The International Human Epigenome Consortium: A Blueprint for Scientific Collaboration and Discovery Stunnenberg, Hendrik G.; Hirst, Martin Cell, Vol. 167, Issue 7 https://doi.org/10.1016/j.cell.2016.12.002	journal	December 2016
Comprehensive Molecular Characterization of Muscle-Invasive Bladder Cancer Robertson, A. Gordon; Kim, Jaegil; Al-Ahmadie, Hikmat Cell, Vol. 174, Issue 4 https://doi.org/10.1016/j.cell.2018.07.036	journal	August 2018
Identification of a CpG Island Methylator Phenotype that Defines a Distinct Subgroup of Glioma Hui, Shen,; G., Herman, James; B., Baylin, Stephen The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/bcyk-kr86	text	January 2010
Comprehensive molecular portraits of human breast tumours Charles, Perou, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/hyeb-c392	text	January 2012
The Molecular Taxonomy of Primary Prostate Cancer Charles, Perou, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/weaq-yt78	text	January 2015
Landscape of somatic mutations in 560 breast cancer whole-genome sequences. Nik-Zainal, Serena; Davies, Helen; Staaf, Johan Springer Science and Business Media LLC https://doi.org/10.17863/cam.31887	journalarticle	January 2016
Atypical teratoid/rhabdoid tumors are comprised of three epigenetic subgroups with distinct enhancer landscapes Johann, Pascal D.; Erkek, Serap; Zapatka, Marc Cell Press (Elsevier) https://doi.org/10.5167/uzh-131518	text	January 2016
Re: The Molecular Taxonomy of Primary Prostate Cancer Schlomm, Thorsten European Urology, Vol. 69, Issue 6 https://doi.org/10.1016/j.eururo.2016.02.024	journal	June 2016
The topography of mutational processes in breast cancer genomes. Morganella, Sandro; Alexandrov, Ludmil B.; Glodzik, Dominik Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.31875	text	January 2016
The International Human Epigenome Consortium: A Blueprint for Scientific Collaboration and Discovery. Stunnenberg, Hendrik G.; Consortium, International Human Epigenome; Hirst, Martin Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.15673	text	January 2016
Whole-Genome Bisulfite Sequencing of Two Distinct Interconvertible DNA Methylomes of Mouse Embryonic Stem Cells Habibi, Ehsan; Brinkman, Arie B.; Arand, Julia Cell Stem Cell, Vol. 13, Issue 3 https://doi.org/10.1016/j.stem.2013.06.002	journal	September 2013
Histone H2B.8 compacts flowering plant sperm through chromatin phase separation Buttress, Toby; He, Shengbo; Wang, Liang Nature, Vol. 611, Issue 7936 https://doi.org/10.1038/s41586-022-05386-6	journal	November 2022
Neutral tumor evolution? Tarabichi, Maxime; Martincorena, Iñigo Nature Genetics, Vol. 50, Issue 12 https://doi.org/10.1038/s41588-018-0258-x	journal	October 2018
Effects of elevational range shift on the morphology and physiology of a carabid beetle invading the sub-Antarctic Kerguelen Islands Ouisse, T.; Day, E.; Laville, L. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-57868-0	journal	January 2020
Partially Methylated Domains Are Hypervariable In Breast Cancer And Fuel Widespread Cpg Island Hypermethylation Brinkman, A. B.; Stunnenberg, H. G. Zenodo https://doi.org/10.5281/zenodo.1217427	dataset	January 2018

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