The Role of Chromatin Modifications in Progression through Mouse Meiotic Prophase

Baarends, 2007, Increased phosphorylation and dimethylation of XY body histones in the Hr6b-knockout mouse is associated with derepression of the X chromosome, J. Cell Sci., 120, 1841, 10.1242/jcs.03451 Baarends, 2005, Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis, Mol. Cell. Biol., 25, 1041, 10.1128/MCB.25.3.1041-1053.2005 Baltus, 2006, In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication, Nat. Genet., 38, 1430, 10.1038/ng1919 Bannister, 2011, Regulation of chromatin by histone modifications, Cell Res., 21, 381, 10.1038/cr.2011.22 Bannister, 2001, Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain, Nature, 410, 120, 10.1038/35065138 Barski, 2007, High-resolution profiling of histone methylations in the human genome, Cell, 129, 823, 10.1016/j.cell.2007.05.009 Baudat, 2010, PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice, Science, 327, 836, 10.1126/science.1183439 Baudat, 2000, Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11, Mol. Cell, 6, 989, 10.1016/S1097-2765(00)00098-8 Baumann, 2011, Role of polycomb group protein Cbx2/M33 in meiosis onset and maintenance of chromosome stability in the mammalian germline, Genes (Basel.), 2, 59, 10.3390/genes2010059 Bellani, 2005, SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm-/- spermatocytes, J. Cell Sci., 118, 3233, 10.1242/jcs.02466 Borde, 2013, Programmed induction of DNA double strand breaks during meiosis: setting up communication between DNA and the chromosome structure, Curr. Opin. Genet. Dev., 23, 147, 10.1016/j.gde.2012.12.002 Bourc'his, 2004, Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L, Nature, 431, 96, 10.1038/nature02886 Bourc'his, 2001, Dnmt3L and the establishment of maternal genomic imprints, Science, 294, 2536, 10.1126/science.1065848 Braun, 2012, Shaping the landscape: mechanistic consequences of ubiquitin modification of chromatin, EMBO Rep., 13, 619, 10.1038/embor.2012.78 Brick, 2012, Genetic recombination is directed away from functional genomic elements in mice, Nature, 485, 642, 10.1038/nature11089 Buard, 2009, Distinct histone modifications define initiation and repair of meiotic recombination in the mouse, EMBO J., 28, 2616, 10.1038/emboj.2009.207 Cao, 2012, Histone ubiquitination and deubiquitination in transcription, DNA damage response, and cancer, Front. Oncol., 2, 26, 10.3389/fonc.2012.00026 Cao, 2005, Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing, Mol. Cell, 20, 845, 10.1016/j.molcel.2005.12.002 Cao, 2002, Role of histone H3 lysine 27 methylation in polycomb-group silencing, Science, 298, 1039, 10.1126/science.1076997 Carmell, 2007, MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline, Dev. Cell, 12, 503, 10.1016/j.devcel.2007.03.001 Cedar, 2012, Programming of DNA methylation patterns, Annu. Rev. Biochem., 81, 97, 10.1146/annurev-biochem-052610-091920 Celeste, 2002, Genomic instability in mice lacking histone H2AX, Science, 296, 922, 10.1126/science.1069398 Chicheportiche, 2007, Characterization of Spo11-dependent and independent phospho-H2AX foci during meiotic prophase I in the male mouse, J. Cell Sci., 120, 1733, 10.1242/jcs.004945 Cohen, 2006, Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals, Endocr. Rev., 27, 398, 10.1210/er.2005-0017 Crichton, 2013, Defending the genome from the enemy within: mechanisms of retrotransposon suppression in the mouse germline, Cell. Mol. Life Sci Deaton, 2011, CpG islands and the regulation of transcription, Genes Dev., 25, 1010, 10.1101/gad.2037511 De La Fuente, 2006, Lsh is required for meiotic chromosome synapsis and retrotransposon silencing in female germ cells, Nat. Cell Biol., 8, 1448, 10.1038/ncb1513 Dennis, 2001, Lsh, a member of the SNF2 family, is required for genome-wide methylation, Genes Dev., 15, 2940, 10.1101/gad.929101 Endoh, 2012, Histone H2A mono-ubiquitination is a crucial step to mediate PRC1-dependent repression of developmental genes to maintain ES cell identity, PLoS Genet., 8, e1002774, 10.1371/journal.pgen.1002774 Eskeland, 2010, Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination, Mol. Cell, 38, 452, 10.1016/j.molcel.2010.02.032 Fernandez-Capetillo, 2003, H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis, Dev. Cell, 4, 497, 10.1016/S1534-5807(03)00093-5 Gaucher, 2012, Bromodomain-dependent stage-specific male genome programming by Brdt, EMBO J., 31, 3809, 10.1038/emboj.2012.233 Grey, 2011, Mouse PRDM9 DNA-binding specificity determines sites of histone H3 lysine 4 trimethylation for initiation of meiotic recombination, PLoS Biol., 9, e1001176, 10.1371/journal.pbio.1001176 Hackett, 2012, Promoter DNA methylation couples genome-defence mechanisms to epigenetic reprogramming in the mouse germline, Development, 139, 3623, 10.1242/dev.081661 Hackett, 2013, Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine, Science, 339, 448, 10.1126/science.1229277 Hackett, 2013, DNA methylation dynamics during the mammalian life cycle, Philos. Trans. R. Soc. Lond. B Biol. Sci., 368, 20110328, 10.1098/rstb.2011.0328 Hajkova, 2002, Epigenetic reprogramming in mouse primordial germ cells, Mech. Dev., 117, 15, 10.1016/S0925-4773(02)00181-8 Handel, 2010, Genetics of mammalian meiosis: regulation, dynamics and impact on fertility, Nat. Rev. Genet., 11, 124, 10.1038/nrg2723 Hata, 2002, Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice, Development, 129, 1983, 10.1242/dev.129.8.1983 Hayashi, 2005, A histone H3 methyltransferase controls epigenetic events required for meiotic prophase, Nature, 438, 374, 10.1038/nature04112 Hendrich, 1998, Identification and characterization of a family of mammalian methyl-CpG binding proteins, Mol. Cell. Biol., 18, 6538, 10.1128/MCB.18.11.6538 Ichijima, 2011, MDC1 directs chromosome-wide silencing of the sex chromosomes in male germ cells, Genes Dev., 25, 959, 10.1101/gad.2030811 Ito, 2011, Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine, Science, 333, 1300, 10.1126/science.1210597 Kaneda, 2004, Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting, Nature, 429, 900, 10.1038/nature02633 Kato, 2007, Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse, Hum. Mol. Genet., 16, 2272, 10.1093/hmg/ddm179 Khalil, 2004, Dynamic histone modifications mark sex chromosome inactivation and reactivation during mammalian spermatogenesis, Proc. Natl. Acad. Sci. USA, 101, 16583, 10.1073/pnas.0406325101 Kouznetsova, 2009, BRCA1-mediated chromatin silencing is limited to oocytes with a small number of asynapsed chromosomes, J. Cell Sci., 122, 2446, 10.1242/jcs.049353 La Salle, 2004, Windows for sex-specific methylation marked by DNA methyltransferase expression profiles in mouse germ cells, Dev. Biol., 268, 403, 10.1016/j.ydbio.2003.12.031 Leeb, 2010, Polycomb complexes act redundantly to repress genomic repeats and genes, Genes Dev., 24, 265, 10.1101/gad.544410 Lewis, 1992, Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA, Cell, 69, 905, 10.1016/0092-8674(92)90610-O Lu, 2010, RNF8-dependent histone modifications regulate nucleosome removal during spermatogenesis, Dev. Cell, 18, 371, 10.1016/j.devcel.2010.01.010 Mahadevaiah, 2008, Extensive meiotic asynapsis in mice antagonises meiotic silencing of unsynapsed chromatin and consequently disrupts meiotic sex chromosome inactivation, J. Cell Biol., 182, 263, 10.1083/jcb.200710195 Mahadevaiah, 2001, Recombinational DNA double-strand breaks in mice precede synapsis, Nat. Genet., 27, 271, 10.1038/85830 Meissner, 2008, Genome-scale DNA methylation maps of pluripotent and differentiated cells, Nature, 454, 766, 10.1038/nature07107 Mihola, 2009, A mouse speciation gene encodes a meiotic histone H3 methyltransferase, Science, 323, 373, 10.1126/science.1163601 Musselman, 2012, Perceiving the epigenetic landscape through histone readers, Nat. Struct. Mol. Biol., 19, 1218, 10.1038/nsmb.2436 Myant, 2008, LSH cooperates with DNA methyltransferases to repress transcription, Mol. Cell. Biol., 28, 215, 10.1128/MCB.01073-07 Nickerson, 2007, Cyclin A1-deficient mice lack histone H3 serine 10 phosphorylation and exhibit altered aurora B dynamics in late prophase of male meiosis, Dev. Biol., 306, 725, 10.1016/j.ydbio.2007.04.009 Okano, 1999, DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development, Cell, 99, 247, 10.1016/S0092-8674(00)81656-6 Ollinger, 2010, Meiosis and retrotransposon silencing during germ cell development in mice, Differentiation, 79, 147, 10.1016/j.diff.2009.10.004 Peters, 2001, Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability, Cell, 107, 323, 10.1016/S0092-8674(01)00542-6 Pivot-Pajot, 2003, Acetylation-dependent chromatin reorganization by BRDT, a testis-specific bromodomain-containing protein, Mol. Cell. Biol., 23, 5354, 10.1128/MCB.23.15.5354-5365.2003 Prokhortchouk, 2001, The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor, Genes Dev., 15, 1613, 10.1101/gad.198501 Reddington, 2013, Non-canonical functions of the DNA methylome in gene regulation, Biochem. J., 451, 13, 10.1042/BJ20121585 Reddington, 2013, Redistribution of H3K27me3 upon DNA hypomethylation results in de-repression of polycomb target genes, Genome Biol., 14, R25, 10.1186/gb-2013-14-3-r25 Reichmann, 2012, Microarray analysis of LTR retrotransposon silencing identifies Hdac1 as a regulator of retrotransposon expression in mouse embryonic stem cells, PLoS Comput. Biol., 8, e1002486, 10.1371/journal.pcbi.1002486 Reichmann, 2013, The genome-defence gene Tex19.1 suppresses LINE-1 retrotransposons in the placenta and prevents intra-uterine growth retardation in mice, Hum. Mol. Genet., 22, 1791, 10.1093/hmg/ddt029 Rogakou, 1998, DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139, J. Biol. Chem., 273, 5858, 10.1074/jbc.273.10.5858 Romanienko, 2000, The mouse Spo11 gene is required for meiotic chromosome synapsis, Mol. Cell, 6, 975, 10.1016/S1097-2765(00)00097-6 Sasaki, 2009, Real-time imaging of histone H4 hyperacetylation in living cells, Proc. Natl. Acad. Sci. USA, 106, 16257, 10.1073/pnas.0902150106 Schneider, 2004, Histone H3 lysine 4 methylation patterns in higher eukaryotic genes, Nat. Cell Biol., 6, 73, 10.1038/ncb1076 Seki, 2005, Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice, Dev. Biol., 278, 440, 10.1016/j.ydbio.2004.11.025 Simon, 2013, Occupying chromatin: polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put, Mol. Cell, 49, 808, 10.1016/j.molcel.2013.02.013 Smagulova, 2011, Genome-wide analysis reveals novel molecular features of mouse recombination hotspots, Nature, 472, 375, 10.1038/nature09869 Suetake, 2004, DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction, J. Biol. Chem., 279, 27816, 10.1074/jbc.M400181200 Sun, 2004, Growth retardation and premature aging phenotypes in mice with disruption of the SNF2-like gene, PASG, Genes Dev., 18, 1035, 10.1101/gad.1176104 Tachibana, 2007, Functional dynamics of H3K9 methylation during meiotic prophase progression, EMBO J., 26, 3346, 10.1038/sj.emboj.7601767 Takada, 2011, HP1γ links histone methylation marks to meiotic synapsis in mice, Development, 138, 4207, 10.1242/dev.064444 Tan, 2011, Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification, Cell, 146, 1016, 10.1016/j.cell.2011.08.008 Tavares, 2012, RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3, Cell, 148, 664, 10.1016/j.cell.2011.12.029 Turner, 2007, Meiotic sex chromosome inactivation, Development, 134, 1823, 10.1242/dev.000018 Turner, 2005, Silencing of unsynapsed meiotic chromosomes in the mouse, Nat. Genet., 37, 41, 10.1038/ng1484 Weber, 2007, Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome, Nat. Genet., 39, 457, 10.1038/ng1990 Webster, 2005, Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis, Proc. Natl. Acad. Sci. USA, 102, 4068, 10.1073/pnas.0500702102 Wiench, 2011, DNA methylation status predicts cell type-specific enhancer activity, EMBO J., 30, 3028, 10.1038/emboj.2011.210 Yamaguchi, 2012, Tet1 controls meiosis by regulating meiotic gene expression, Nature, 492, 443, 10.1038/nature11709 Yaman, 2006, Timing of entry of meiosis depends on a mark generated by DNA methyltransferase 3a in testis, Mol. Reprod. Dev., 73, 390, 10.1002/mrd.20430 Yokobayashi, 2013, PRC1 coordinates timing of sexual differentiation of female primordial germ cells, Nature, 495, 236, 10.1038/nature11918 Zeng, 2011, Lymphoid-specific helicase (HELLS) is essential for meiotic progression in mouse spermatocytes, Biol. Reprod., 84, 1235, 10.1095/biolreprod.110.085720 Zentner, 2013, Regulation of nucleosome dynamics by histone modifications, Nat. Struct. Mol. Biol., 20, 259, 10.1038/nsmb.2470