DNA methylation reprogramming and DNA repair in the mouse zygote.

Here, we summarize current knowledge about epigenetic reprogramming during mammalian preimplantation development, as well as the potential mechanisms driving these processes. We will particularly focus on changes taking place in the zygote, where the paternally derived DNA and chromatin undergo the most striking alterations, such as replacement of protamines by histones, histone modifications and active DNA demethylation. The putative mechanisms of active paternal DNA demethylation have been studied for over a decade, accumulating a lot of circumstantial evidence for enzymatic activities provided by the oocyte, protection of the maternal genome against such activities and possible involvement of DNA repair. We will discuss the various facets of dynamic epigenetic changes related to DNA methylation with an emphasis on the putative involvement of DNA repair in DNA demethylation.

[1]  H. Cedar,et al.  De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes , 2008, Nature Structural &Molecular Biology.

[2]  G. Crabtree,et al.  Chromatin remodelling during development , 2010, Nature.

[3]  E. Wolf,et al.  Methylation Reprogramming and Chromosomal Aneuploidy in In Vivo Fertilized and Cloned Rabbit Preimplantation Embryos1 , 2004, Biology of reproduction.

[4]  M Plachot,et al.  Chromosome methylation patterns during mammalian preimplantation development. , 1998, Genes & development.

[5]  J. Jiricny,et al.  The versatile thymine DNA-glycosylase: a comparative characterization of the human, Drosophila and fission yeast orthologs. , 2003, Nucleic acids research.

[6]  T. Kouzarides.  Chromatin Modifications and Their Function , 2007, Cell.

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

[8]  S. Henikoff,et al.  DNA demethylation by DNA repair. , 2009, Trends in genetics : TIG.

[9]  Bao Liu,et al.  DNA cytosine methylation in plant development. , 2010, Journal of genetics and genomics = Yi chuan xue bao.

[10]  H. Shibuya,et al.  DNA demethylation in hormone-induced transcriptional derepression , 2009, Nature.

[11]  D. Wells,et al.  Control of fertilization-independent endosperm development by the MEDEA polycomb gene in Arabidopsis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[12]  C. Allis,et al.  Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa , 2003, Nature Genetics.

[13]  Y. Uchijima,et al.  Maintenance of genomic methylation patterns during preimplantation development requires the somatic form of DNA methyltransferase 1. , 2008, Developmental biology.

[14]  N. Heintz,et al.  The Nuclear DNA Base 5-Hydroxymethylcytosine Is Present in Purkinje Neurons and the Brain , 2009, Science.

[15]  Tony Kouzarides,et al.  Histone methylation defines epigenetic asymmetry in the mouse zygote. , 2002, The International journal of developmental biology.

[16]  J. Tesarik,et al.  In vitro fertilization by intracytoplasmic sperm injection. , 1999, BioEssays : news and reviews in molecular, cellular and developmental biology.

[17]  J. Fulka,et al.  DNA methylation pattern in human zygotes and developing embryos. , 2004, Reproduction.

[18]  K. Rodenacker,et al.  Effect of IVF and laser zona dissection on DNA methylation pattern of mouse zygotes , 2009, Mammalian Genome.

[19]  J. Renard,et al.  Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. , 1997, Development.

[20]  Tony Kouzarides,et al.  The Methyl-CpG-binding Protein MeCP2 Links DNA Methylation to Histone Methylation* , 2003, The Journal of Biological Chemistry.

[21]  T. Haaf,et al.  Aberrant methylation patterns at the two‐cell stage as an indicator of early developmental failure , 2002, Molecular reproduction and development.

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

[23]  M. Szyf,et al.  Demethylase Activity Is Directed by Histone Acetylation* , 2001, The Journal of Biological Chemistry.

[24]  Albert Jeltsch,et al.  Chromatin methylation activity of Dnmt3a and Dnmt3a/3L is guided by interaction of the ADD domain with the histone H3 tail , 2010, Nucleic acids research.

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

[26]  D. Armstrong,et al.  Compromised development of calves (Bos gaurus) derived from in vitro-generated embryos and transferred interspecifically into domestic cattle (Bos taurus). , 2001, Theriogenology.

[27]  Antoine H. F. M. Peters,et al.  Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa , 2010, Nature Structural &Molecular Biology.

[28]  A. Shilatifard,et al.  An operational definition of epigenetics. , 2009, Genes & development.

[29]  D. Solter,et al.  Nuclear and cytoplasmic transfer in mammalian embryos. , 1986, Developmental biology.

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

[31]  A. Razin,et al.  Mechanistic aspects of genome-wide demethylation in the preimplantation mouse embryo. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[32]  W. Reik,et al.  Epigenetic reprogramming in mammals. , 2005, Human molecular genetics.

[33]  Jian-Kang Zhu,et al.  Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[35]  A. Bird,et al.  Methylation-Induced Repression— Belts, Braces, and Chromatin , 1999, Cell.

[36]  Yong-Mahn Han,et al.  Differential DNA methylation reprogramming of various repetitive sequences in mouse preimplantation embryos. , 2004, Biochemical and biophysical research communications.

[37]  Jon Penterman,et al.  DEMETER DNA Glycosylase Establishes MEDEA Polycomb Gene Self-Imprinting by Allele-Specific Demethylation , 2006, Cell.

[38]  T. Haaf,et al.  Quantitative methylation analysis of developmentally important genes in human pregnancy losses after ART and spontaneous conception. , 2010, Molecular human reproduction.

[39]  L. Schwarzfischer,et al.  Active DNA demethylation in human postmitotic cells correlates with activating histone modifications, but not transcription levels , 2010, Genome Biology.

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

[41]  Peter S. Harper,et al.  Human Molecular Genetics and the Human Genome Project , 2008 .

[42]  R. Ishikawa,et al.  Genomic imprinting: a balance between antagonistic roles of parental chromosomes. , 2008, Seminars in cell & developmental biology.

[43]  M. Sherman.  The culture of cells derived from mouse blastocysts , 1975, Cell.

[44]  W. Lam,et al.  Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells , 2005, Nature Genetics.

[45]  M. S. Peters,et al.  Artificial activation of porcine oocytes matured in vitro , 1991, Molecular reproduction and development.

[46]  S. Lehnert,et al.  Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. , 1987, Development.

[47]  G. Pfeifer,et al.  GADD45A Does Not Promote DNA Demethylation , 2008, PLoS genetics.

[48]  Andrew J. Bannister,et al.  Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. , 2006, The International journal of developmental biology.

[49]  Andrew J. Bannister,et al.  Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development , 2003, Development.

[50]  M. Siegmann,et al.  5-Methylcytosine DNA glycosylase activity is also present in the human MBD4 (G/T mismatch glycosylase) and in a related avian sequence. , 2000, Nucleic acids research.

[51]  Wendy Dean,et al.  Activation-induced Cytidine Deaminase Deaminates 5-Methylcytosine in DNA and Is Expressed in Pluripotent Tissues , 2004, Journal of Biological Chemistry.

[52]  M. Szyf,et al.  A mammalian protein with specific demethylase activity for mCpG DNA , 1999, Nature.

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

[54]  B. Cairns,et al.  DNA Demethylation in Zebrafish Involves the Coupling of a Deaminase, a Glycosylase, and Gadd45 , 2008, Cell.

[55]  E. Wolf,et al.  Epigenetic Marking Correlates with Developmental Potential in Cloned Bovine Preimplantation Embryos , 2003, Current Biology.

[56]  P. de Boer,et al.  DNA double-strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation. , 2008, Human molecular genetics.

[57]  T. Arányi,et al.  The constant variation: DNA methylation changes during preimplantation development , 2006, FEBS letters.

[58]  S. Muller,et al.  Asymmetry in Histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote , 2005, Mechanisms of Development.

[59]  Helen M. Blau,et al.  Reprogramming towards pluripotency requires AID-dependent DNA demethylation , 2010, Nature.

[60]  F. Ding,et al.  Dynamics of Dnmt1 methyltransferase expression and intracellular localization during oogenesis and preimplantation development. , 2002, Developmental biology.

[61]  D. Solter,et al.  Completion of mouse embryogenesis requires both the maternal and paternal genomes , 1984, Cell.

[62]  W. Dean,et al.  Epigenetic reprogramming during early development in mammals. , 2004, Reproduction.

[63]  S. C. Méo,et al.  Activation and early parthenogenesis of bovine oocytes treated with ethanol and strontium. , 2004, Animal reproduction science.

[64]  M. Fraga,et al.  The Polycomb group protein EZH2 directly controls DNA methylation , 2006, Nature.

[65]  Z. Polański,et al.  Hypomethylation of paternal DNA in the late mouse zygote is not essential for development. , 2008, The International journal of developmental biology.

[66]  Christof Niehrs,et al.  Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation , 2007, Nature.

[67]  Z. Liutkevičiūtė,et al.  Cytosine-5-methyltransferases add aldehydes to DNA. , 2009, Nature chemical biology.

[68]  P. de Boer,et al.  gammaH2AX signalling during sperm chromatin remodelling in the mouse zygote. , 2006, DNA repair.

[69]  Peter A. Jones,et al.  High frequency mutagenesis by a DNA methyltransferase , 1992, Cell.

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

[71]  M. Siegmann,et al.  5-methylcytosine-DNA glycosylase activity is present in a cloned G/T mismatch DNA glycosylase associated with the chicken embryo DNA demethylation complex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[72]  J. Walter,et al.  Differential dynamics of histone H3 methylation at positions K4 and K9 in the mouse zygote , 2004, BMC Developmental Biology.

[73]  W. Reik,et al.  Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. , 2005, Developmental biology.

[74]  Megumi Kato,et al.  Impaired active demethylation of the paternal genome in pronuclear‐stage rat zygotes produced by in vitro fertilization or intracytoplasmic sperm injection , 2009, Molecular reproduction and development.

[75]  P. Frey,et al.  S-adenosylmethionine as an oxidant: the radical SAM superfamily. , 2007, Trends in biochemical sciences.

[76]  D. Solter,et al.  Nuclear transplantation in mouse embryos. , 1983, The Journal of experimental zoology.

[77]  N. Alenina,et al.  Dynamics of DNA‐demethylation in early mouse and rat embryos developed in vivo and in vitro , 2007, Molecular reproduction and development.

[78]  C. Sapienza,et al.  DNA methylation and gene expression differences in children conceived in vitro or in vivo. , 2009, Human molecular genetics.

[79]  J. Kanka.  Gene expression and chromatin structure in the pre-implantation embryo. , 2003, Theriogenology.

[80]  Zhi-Min Yuan,et al.  p53-Dependent S-Phase Damage Checkpoint and Pronuclear Cross Talk in Mouse Zygotes with X-Irradiated Sperm , 2002, Molecular and Cellular Biology.

[81]  Cassandra R. Farthing,et al.  Global Mapping of DNA Methylation in Mouse Promoters Reveals Epigenetic Reprogramming of Pluripotency Genes , 2008, PLoS genetics.

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

[83]  N. Ogonuki,et al.  Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. , 2002, Development.

[84]  F. Ding,et al.  Preimplantation expression of the somatic form of Dnmt1 suggests a role in the inheritance of genomic imprints , 2008, BMC Developmental Biology.

[85]  E. Brooks.  The culture of the will. , 2022 .

[86]  J. Fulka,et al.  No differences in the DNA methylation pattern in mouse zygotes produced in vivo, in vitro, or by intracytoplasmic sperm injection. , 2006, Fertility and sterility.

[87]  Swati Kadam,et al.  Examination of the specificity of DNA methylation profiling techniques towards 5-methylcytosine and 5-hydroxymethylcytosine , 2010, Nucleic acids research.

[88]  C. Allis,et al.  Dynamic alterations of specific histone modifications during early murine development , 2004, Journal of Cell Science.

[89]  H. Leonhardt,et al.  Restricted mobility of Dnmt1 in preimplantation embryos: implications for epigenetic reprogramming , 2005, BMC Developmental Biology.

[90]  W. Hwang,et al.  Blastocyst formation, karyotype, and mitochondrial DNA of interspecies embryos derived from nuclear transfer of human cord fibroblasts into enucleated bovine oocytes. , 2003, Fertility and sterility.

[91]  E. Wolf,et al.  Evidence for conserved DNA and histone H3 methylation reprogramming in mouse, bovine and rabbit zygotes , 2008, Epigenetics & Chromatin.

[92]  P. Farnham,et al.  5-azacytidine treatment reorganizes genomic histone modification patterns , 2010, Epigenetics.

[93]  Wendy Dean,et al.  Dynamic reprogramming of DNA methylation in the early mouse embryo. , 2002, Developmental biology.

[94]  X. An,et al.  Epigenetic modification of histone 3 at lysine 9 in sheep zygotes and its relationship with DNA methylation , 2008, BMC Developmental Biology.

[95]  C. Sapienza,et al.  Conserved DNA methylation in Gadd45a-/- mice , 2009, Epigenetics.

[96]  L. Sowers,et al.  Endogenous cytosine damage products alter the site selectivity of human DNA maintenance methyltransferase DNMT1. , 2007, Cancer research.

[97]  P. Bates,et al.  Reversal of DNA alkylation damage by two human dioxygenases , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[98]  Yi Zhang,et al.  Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification , 2010, Nature.

[99]  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.

[100]  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.

[101]  T. Nagai.  Parthenogenetic activation of cattle follicular oocytes in vitro with ethanol. , 1987, Gamete research.

[102]  H. Bayley,et al.  Continuous base identification for single-molecule nanopore DNA sequencing. , 2009, Nature nanotechnology.

[103]  Tao Chen,et al.  Blastocysts produced by nuclear transfer between chicken blastodermal cells and rabbit oocytes , 2004, Molecular reproduction and development.

[104]  M. Bartolomei,et al.  Maintenance of Paternal Methylation and Repression of the Imprinted H19 Gene Requires MBD3 , 2007, PLoS genetics.

[105]  C. Allis,et al.  Translating the Histone Code , 2001, Science.

[106]  En Li,et al.  Suv 39 h-Mediated Histone H 3 Lysine 9 Methylation Directs DNA Methylation to Major Satellite Repeats at Pericentric Heterochromatin , 2003 .

[107]  Jahnvi Pflueger,et al.  Distinctive chromatin in human sperm packages genes for embryo development , 2009 .

[108]  M. Surani,et al.  Chromatin dynamics during epigenetic reprogramming in the mouse germ line , 2008, Nature.

[109]  F. Aoki,et al.  Changes in histone acetylation during mouse oocyte meiosis , 2003, The Journal of cell biology.

[110]  F. Aoki,et al.  Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos , 2004, Development.

[111]  Tyson A. Clark,et al.  Direct detection of DNA methylation during single-molecule, real-time sequencing , 2010, Nature Methods.

[112]  S. Henikoff,et al.  Author ' s personal copy DNA demethylation by DNA repair , 2009 .

[113]  W Dean,et al.  Conservation of methylation reprogramming in mammalian development: Aberrant reprogramming in cloned embryos , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[114]  T. Hashimshony,et al.  The role of DNA methylation in setting up chromatin structure during development , 2003, Nature Genetics.

[115]  P. Jouannet,et al.  Assisted Reproductive Technology affects developmental kinetics, H19 Imprinting Control Region methylation and H19 gene expression in individual mouse embryos , 2007, BMC Developmental Biology.

[116]  Paul Tempst,et al.  MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex , 1999, Nature Genetics.

[117]  Marilu A. Hoeppner,et al.  Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. , 1998, Science.

[118]  Yi Zhang,et al.  A role for elongator in zygotic paternal genome demethylation , 2010, Nature.

[119]  J. Walter,et al.  Assisted reproductive technologies do not enhance the variability of DNA methylation imprints in human , 2009, Journal of Medical Genetics.