DNA methylation dynamics during the mammalian life cycle

DNA methylation is dynamically remodelled during the mammalian life cycle through distinct phases of reprogramming and de novo methylation. These events enable the acquisition of cellular potential followed by the maintenance of lineage-restricted cell identity, respectively, a process that defines the life cycle through successive generations. DNA methylation contributes to the epigenetic regulation of many key developmental processes including genomic imprinting, X-inactivation, genome stability and gene regulation. Emerging sequencing technologies have led to recent insights into the dynamic distribution of DNA methylation during development and the role of this epigenetic mark within distinct genomic contexts, such as at promoters, exons or imprinted control regions. Additionally, there is a better understanding of the mechanistic basis of DNA demethylation during epigenetic reprogramming in primordial germ cells and during pre-implantation development. Here, we discuss our current understanding of the developmental roles and dynamics of this key epigenetic system.

[1]  M. Kaufman,et al.  Establishment in culture of pluripotential cells from mouse embryos , 1981, Nature.

[2]  Rudolf Jaenisch,et al.  Targeted mutation of the DNA methyltransferase gene results in embryonic lethality , 1992, Cell.

[3]  L. E. McDonald,et al.  A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[4]  S. Clark,et al.  Detection and measurement of PCR bias in quantitative methylation analysis of bisulphite-treated DNA. , 1997, Nucleic acids research.

[5]  C. Walsh,et al.  Cytosine methylation and the ecology of intragenomic parasites. , 1997, Trends in genetics : TIG.

[6]  C. Walsh,et al.  Transcription of IAP endogenous retroviruses is constrained by cytosine methylation , 1998, Nature Genetics.

[7]  D. Haber,et al.  DNA Methyltransferases Dnmt3a and Dnmt3b Are Essential for De Novo Methylation and Mammalian Development , 1999, Cell.

[8]  David I. K. Martin,et al.  Epigenetic inheritance at the agouti locus in the mouse , 1999, Nature Genetics.

[9]  J. Walter,et al.  Embryogenesis: Demethylation of the zygotic paternal genome , 2000, Nature.

[10]  W. Reik,et al.  Active demethylation of the paternal genome in the mouse zygote , 2000, Current Biology.

[11]  A. Bird,et al.  Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[12]  W. Reik,et al.  Genomic imprinting: parental influence on the genome , 2001, Nature Reviews Genetics.

[13]  M. Surani,et al.  Epigenetic reprogramming in mouse primordial germ cells , 2002, Mechanisms of Development.

[14]  A. Bird DNA methylation patterns and epigenetic memory. , 2002, Genes & development.

[15]  W. Reik,et al.  Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse , 2003, Genesis.

[16]  T. Bestor,et al.  Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L , 2004, Nature.

[17]  Lloyd J. Old,et al.  Cancer/testis antigens, gametogenesis and cancer , 2005, Nature Reviews Cancer.

[18]  Y. Matsui,et al.  Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. , 2005, Developmental biology.

[19]  A. Gnirke,et al.  Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis , 2005, Nucleic acids research.

[20]  E. Li,et al.  DNA methylation is a primary mechanism for silencing postmigratory primordial germ cell genes in both germ cell and somatic cell lineages , 2006, Development.

[21]  Wei Jiang,et al.  High-throughput DNA methylation profiling using universal bead arrays. , 2006, Genome research.

[22]  T. Rauch,et al.  MIRA-assisted microarray analysis, a new technology for the determination of DNA methylation patterns, identifies frequent methylation of homeodomain-containing genes in lung cancer cells. , 2006, Cancer research.

[23]  Kenny Q. Ye,et al.  Comparative isoschizomer profiling of cytosine methylation: the HELP assay. , 2006, Genome research.

[24]  Tomohiro Hayakawa,et al.  Maintenance of self‐renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b , 2006, Genes to cells : devoted to molecular & cellular mechanisms.

[25]  H. Cedar,et al.  G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis , 2006, Nature Cell Biology.

[26]  Michael B. Stadler,et al.  Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome , 2007, Nature Genetics.

[27]  Satoshi Tanaka,et al.  PGC7/Stella protects against DNA demethylation in early embryogenesis , 2007, Nature Cell Biology.

[28]  W. Reik Stability and flexibility of epigenetic gene regulation in mammalian development , 2007, Nature.

[29]  M. Surani,et al.  Genetic and Epigenetic Regulators of Pluripotency , 2007, Cell.

[30]  A. Chess,et al.  Gene Body-Specific Methylation on the Active X Chromosome , 2007, Science.

[31]  C. Allis,et al.  DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA , 2007, Nature.

[32]  R. Lister,et al.  Highly Integrated Single-Base Resolution Maps of the Epigenome in Arabidopsis , 2008, Cell.

[33]  R. Jaenisch,et al.  Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. , 2008, Genes & development.

[34]  T. Mikkelsen,et al.  Genome-scale DNA methylation maps of pluripotent and differentiated cells , 2008, Nature.

[35]  N. Gray,et al.  Deletion of the Pluripotency-Associated Tex19.1 Gene Causes Activation of Endogenous Retroviruses and Defective Spermatogenesis in Mice , 2008, PLoS genetics.

[36]  Ravi Sachidanandam,et al.  A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. , 2008, Molecular cell.

[37]  Jim Stalker,et al.  A Novel CpG Island Set Identifies Tissue-Specific Methylation at Developmental Gene Loci , 2008, PLoS biology.

[38]  Vladimir Benes,et al.  Transient cyclical methylation of promoter DNA , 2008, Nature.

[39]  A. Bird,et al.  DNA methylation landscapes: provocative insights from epigenomics , 2008, Nature Reviews Genetics.

[40]  W. Reik,et al.  Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5 , 2008, Nature Cell Biology.

[41]  R. Durbin,et al.  A Bayesian deconvolution strategy for immunoprecipitation-based DNA methylome analysis , 2008, Nature Biotechnology.

[42]  Michael B. Stadler,et al.  Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. , 2008, Molecular cell.

[43]  H. Cedar,et al.  Linking DNA methylation and histone modification: patterns and paradigms , 2009, Nature Reviews Genetics.

[44]  J. Greally,et al.  The HELP assay. , 2009, Methods in molecular biology.

[45]  David R. Liu,et al.  Conversion of 5-Methylcytosine to 5- Hydroxymethylcytosine in Mammalian DNA by the MLL Partner TET1 , 2009 .

[46]  G. Kelsey,et al.  Transcription is required for establishment of germline methylation marks at imprinted genes. , 2009, Genes & development.

[47]  E. Li,et al.  KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints , 2009, Nature.

[48]  M. Bartolomei Genomic imprinting: employing and avoiding epigenetic processes. , 2009, Genes & development.

[49]  A. Feinberg,et al.  Genome-wide methylation analysis of human colon cancer reveals similar hypo- and hypermethylation at conserved tissue-specific CpG island shores , 2008, Nature Genetics.

[50]  Michael Q. Zhang,et al.  Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications , 2010, Nature Biotechnology.

[51]  M. Surani,et al.  Genome-Wide Reprogramming in the Mouse Germ Line Entails the Base Excision Repair Pathway , 2010, Science.

[52]  D. Rossell,et al.  Ectopic Expression of Germline Genes Drives Malignant Brain Tumor Growth in Drosophila , 2010, Science.

[53]  A. Feinberg,et al.  Comprehensive High‐Throughput Arrays for Relative Methylation (CHARM) , 2010, Current protocols in human genetics.

[54]  Michael Weber,et al.  Targets and dynamics of promoter DNA methylation during early mouse development , 2010, Nature Genetics.

[55]  P. Laird Principles and challenges of genome-wide DNA methylation analysis , 2010, Nature Reviews Genetics.

[56]  Damien Neuillet,et al.  Dnmt3b recruitment through E2F6 transcriptional repressor mediates germ-line gene silencing in murine somatic tissues , 2010, Proceedings of the National Academy of Sciences.

[57]  Robert S. Illingworth,et al.  CpG islands influence chromatin structure via the CpG-binding protein Cfp1 , 2010, Nature.

[58]  David Serre,et al.  MBD-isolated Genome Sequencing provides a high-throughput and comprehensive survey of DNA methylation in the human genome , 2009, Nucleic acids research.

[59]  Irving L. Weissman,et al.  A comprehensive methylome map of lineage commitment from hematopoietic progenitors , 2010, Nature.

[60]  David R. Liu,et al.  The Behaviour of 5-Hydroxymethylcytosine in Bisulfite Sequencing , 2010, PloS one.

[61]  R. Meehan,et al.  Enzymatic approaches and bisulfite sequencing cannot distinguish between 5-methylcytosine and 5-hydroxymethylcytosine in DNA. , 2010, BioTechniques.

[62]  M. Pellegrini,et al.  Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency , 2010, Nature.

[63]  H. Schöler,et al.  Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes , 2010, The EMBO journal.

[64]  Albert Jeltsch,et al.  Cyclical DNA methylation of a transcriptionally active promoter , 2008, Nature.

[65]  R. Chatterjee,et al.  CpG methylation of half-CRE sequences creates C/EBPα binding sites that activate some tissue-specific genes , 2010, Proceedings of the National Academy of Sciences.

[66]  A. Ferguson-Smith Genomic imprinting: the emergence of an epigenetic paradigm , 2011, Nature Reviews Genetics.

[67]  K. Mitsuya,et al.  Role for piRNAs and Noncoding RNA in de Novo DNA Methylation of the Imprinted Mouse Rasgrf1 Locus , 2011, Science.

[68]  Thomas Lengauer,et al.  Genomic Distribution and Inter-Sample Variation of Non-CpG Methylation across Human Cell Types , 2011, PLoS genetics.

[69]  Poshen B. Chen,et al.  Mbd3/NURD Complex Regulates Expression of 5-Hydroxymethylcytosine Marked Genes in Embryonic Stem Cells , 2011, Cell.

[70]  Vijay K. Tiwari,et al.  DNA-binding factors shape the mouse methylome at distal regulatory regions , 2011, Nature.

[71]  A. Klein-Szanto,et al.  Thymine DNA Glycosylase Is Essential for Active DNA Demethylation by Linked Deamination-Base Excision Repair , 2011, Cell.

[72]  K. Helin,et al.  DNA methylation: TET proteins—guardians of CpG islands? , 2012, EMBO reports.

[73]  Chuan He,et al.  Tet Proteins Can Convert 5-Methylcytosine to 5-Formylcytosine and 5-Carboxylcytosine , 2011, Science.

[74]  D. Page,et al.  Tet 1 Is Dispensable for Maintaining Pluripotency and Its Loss Is Compatible with Embryonic and Postnatal Development , 2011 .

[75]  G. Pfeifer,et al.  Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine , 2011, Proceedings of the National Academy of Sciences.

[76]  Yi Zhang,et al.  Replication-Dependent Loss of 5-Hydroxymethylcytosine in Mouse Preimplantation Embryos , 2011, Science.

[77]  Juri Rappsilber,et al.  TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity , 2011, Nature.

[78]  D. Page,et al.  Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. , 2011, Cell stem cell.

[79]  F. Lienert,et al.  Identification of genetic elements that autonomously determine DNA methylation states , 2011, Nature Genetics.

[80]  S. Andrews,et al.  Dynamic CpG island methylation landscape in oocytes and preimplantation embryos , 2011, Nature Genetics.

[81]  Yang Wang,et al.  Tet-Mediated Formation of 5-Carboxylcytosine and Its Excision by TDG in Mammalian DNA , 2011, Science.

[82]  S. Andrews,et al.  Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes , 2011, Development.

[83]  Qing Dai,et al.  Generation and replication-dependent dilution of 5fC and 5caC during mouse preimplantation development , 2011, Cell Research.

[84]  Philipp Kapranov,et al.  Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells , 2011, Nature.

[85]  Z. Deng,et al.  The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes , 2011, Nature.

[86]  W. Reik,et al.  Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation , 2011, Nature.

[87]  Robert S. Illingworth,et al.  Cell type-specific DNA methylation at intragenic CpG islands in the immune system. , 2011, Genome research.

[88]  Christoph Bock,et al.  Global DNA Demethylation During Mouse Erythropoiesis in Vivo , 2011, Science.

[89]  W. Reik,et al.  5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. , 2011, Nature communications.

[90]  J. Berg,et al.  Dnmt3a is essential for hematopoietic stem cell differentiation , 2011, Nature Genetics.

[91]  Colm E. Nestor,et al.  Promoter DNA methylation couples genome-defence mechanisms to epigenetic reprogramming in the mouse germline , 2012, Development.

[92]  M. Bartolomei,et al.  Genomic imprinting: recognition and marking of imprinted loci. , 2012, Current opinion in genetics & development.

[93]  G. Kelsey,et al.  De novo DNA methylation: a germ cell perspective. , 2012, Trends in genetics : TIG.

[94]  W. Reik,et al.  Uncovering the role of 5-hydroxymethylcytosine in the epigenome , 2011, Nature Reviews Genetics.

[95]  Zachary D. Smith,et al.  A unique regulatory phase of DNA methylation in the early mammalian embryo , 2012, Nature.

[96]  M. Surani,et al.  Parallel mechanisms of epigenetic reprogramming in the germline. , 2012, Trends in genetics : TIG.

[97]  S. Balasubramanian,et al.  Quantitative Sequencing of 5-Methylcytosine and 5-Hydroxymethylcytosine at Single-Base Resolution , 2012, Science.

[98]  D. O'Gorman,et al.  Acute exercise remodels promoter methylation in human skeletal muscle. , 2012, Cell metabolism.

[99]  Stephan Beck,et al.  Methylome analysis using MeDIP-seq with low DNA concentrations , 2012, Nature Protocols.

[100]  Colm E. Nestor,et al.  Tissue type is a major modifier of the 5-hydroxymethylcytosine content of human genes. , 2012, Genome research.

[101]  J. Berg,et al.  Dnmt 3 a is essential for hematopoietic stem cell differentiation , 2013 .