T. Amano, T. Hirata, G. Falco, M. Monti, L. V. Sharova et al., Zscan4 restores the developmental potency of embryonic stem cells, Nat. Commun, vol.4, 1966.

R. Amouroux, B. Nashun, K. Shirane, S. Nakagawa, P. W. Hill et al., , 2016.

, De novo DNA methylation drives 5hmC accumulation in mouse zygotes, Nat. Cell Biol, vol.18, pp.225-233

G. Auclair, J. Borgel, L. A. Sanz, J. Vallet, S. Guibert et al., EHMT2 directs DNA methylation for efficient gene silencing in mouse embryos, Genome Res, vol.26, pp.192-202, 2016.
URL : https://hal.archives-ouvertes.fr/hal-02187322

W. Bao, K. K. Kojima, O. Kohany, A. Bonnet-garnier, P. Feuerstein et al., Genome organization and epigenetic marks in mouse germinal vesicle oocytes, Int. J. Dev. Biol, vol.6, pp.877-887, 2012.

C. Bouniol-baly, L. Hamraoui, J. Guibert, N. Beaujean, M. S. Szö-llö-si et al., Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes, Biol. Reprod, vol.60, pp.580-587, 1999.

J. Brind'amour, S. Liu, M. Hudson, C. Chen, M. M. Karimi et al.,

, An ultra-low-input native ChIP-seq protocol for genome-wide profiling of rare cell populations, Nat. Commun, vol.6, p.6033

J. Brind'amour, H. Kobayashi, J. Richard-albert, K. Shirane, A. Sakashita et al., LTR retrotransposons transcribed in oocytes drive species-specific and heritable changes in DNA methylation, Nat. Commun, vol.9, p.3331, 2018.

C. C. Chen, P. Goyal, M. M. Karimi, M. H. Abildgaard, H. Kimura et al., , 2018.

R. E. Collins, M. Tachibana, H. Tamaru, K. M. Smith, D. Jia et al., In vitro and in vivo analyses of a Phe/Tyr switch controlling product specificity of histone lysine methyltransferases, J. Biol. Chem, vol.280, pp.5563-5570, 2005.

W. N. De-vries, L. T. Binns, K. S. Fancher, J. Dean, R. Moore et al., Expression of Cre recombinase in mouse oocytes: a means to study maternal effect genes, Genesis, vol.26, pp.110-112, 2000.

Q. Deng, D. Ramskö-ld, B. Reinius, and R. Sandberg, Single-cell RNAseq reveals dynamic, random monoallelic gene expression in mammalian cells, Science, vol.343, pp.193-196, 2014.

K. B. Dong, I. A. Maksakova, F. Mohn, D. Leung, R. Appanah et al., DNA methylation in ES cells requires the lysine methyltransferase G9a but not its catalytic activity, 2008.

, EMBO J, vol.27, pp.2691-2701

S. Epsztejn-litman, N. Feldman, M. Abu-remaileh, Y. Shufaro, A. Gerson et al., , 2008.

, De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes, Nat. Struct. Mol. Biol, vol.15, pp.1176-1183

G. Falco, S. L. Lee, I. Stanghellini, U. C. Bassey, T. Hamatani et al., Zscan4: a novel gene expressed exclusively in late 2-cell embryos and embryonic stem cells, Dev. Biol, vol.307, pp.539-550, 2007.

I. M. Flyamer, J. Gassler, M. Imakaev, H. B. Brandão, S. V. Ulianov et al., Singlenucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition, Nature, vol.544, pp.110-114, 2017.

E. Habibi, A. B. Brinkman, J. Arand, L. I. Kroeze, H. H. Kerstens et al., Wholegenome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells, Cell Stem Cell, vol.13, pp.360-369, 2013.

S. Heinz, C. Benner, N. Spann, E. Bertolino, Y. C. Lin et al., Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities, Mol. Cell, vol.38, pp.576-589, 2010.

Y. Ho, K. Wigglesworth, J. J. Eppig, and R. M. Schultz, Preimplantation development of mouse embryos in KSOM: augmentation by amino acids and analysis of gene expression, Mol. Reprod. Dev, vol.41, pp.232-238, 1995.

G. C. Hon, N. Rajagopal, Y. Shen, D. F. Mccleary, F. Yue et al., Epigenetic memory at embryonic enhancers identified in DNA methylation maps from adult mouse tissues, Nat. Genet, vol.45, pp.1198-1206, 2013.

K. Ikegami, M. Iwatani, M. Suzuki, M. Tachibana, Y. Shinkai et al., Genome-wide and locus-specific DNA hypomethylation in G9a deficient mouse embryonic stem cells, Genes Cells, vol.12, pp.1-11, 2007.

K. I. Ishiguro, M. Monti, T. Akiyama, H. Kimura, N. Chikazawa-nohtomi et al., Zscan4 is expressed specifically during late meiotic prophase in both spermatogenesis and oogenesis, In Vitro Cell. Dev. Biol. Anim, vol.53, pp.167-178, 2017.

S. Kageyama, H. Liu, N. Kaneko, M. Ooga, M. Nagata et al., , 2007.

D. Karolchik, G. P. Barber, J. Casper, H. Clawson, M. S. Cline et al., The UCSC Genome Browser database: 2014 update, Nucleic Acids Res, vol.42, pp.764-770, 2014.

D. Kim, B. Langmead, and S. L. Salzberg, HISAT: a fast spliced aligner with low memory requirements, Nat. Methods, vol.12, pp.357-360, 2015.

J. Kind, L. Pagie, H. Ortabozkoyun, S. Boyle, S. S. De-vries et al., Single-cell dynamics of genome-nuclear lamina interactions, Cell, vol.153, pp.178-192, 2013.

H. Kobayashi, T. Sakurai, M. Imai, N. Takahashi, A. Fukuda et al., Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks, PLoS Genet, vol.8, p.1002440, 2012.

F. Krueger and S. R. Andrews, Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications, Bioinformatics, vol.27, pp.1571-1572, 2011.

Z. J. Lan, X. Xu, and A. J. Cooney, Differential oocyte-specific expression of Cre recombinase activity in GDF-9-iCre, Zp3cre, and Msx2Cre transgenic mice, Biol. Reprod, vol.71, pp.1469-1474, 2004.

B. Langmead and S. L. Salzberg, Fast gapped-read alignment with Bowtie 2, Nat. Methods, vol.9, pp.357-359, 2012.

D. C. Leung, K. B. Dong, I. A. Maksakova, P. Goyal, R. Appanah et al., Lysine methyltransferase G9a is required for de novo DNA methylation and the establishment, but not the maintenance, of proviral silencing, Proc. Natl. Acad. Sci. USA, vol.108, pp.5718-5723, 2011.

B. C. Lewis, D. S. Klimstra, N. D. Socci, S. Xu, J. A. Koutcher et al., The absence of p53 promotes metastasis in a novel somatic mouse model for hepatocellular carcinoma, Mol. Cell. Biol, vol.25, pp.1228-1237, 2005.

Y. Li, Z. Zhang, J. Chen, W. Liu, W. Lai et al., Stella safeguards the oocyte methylome by preventing de novo methylation mediated by DNMT1, Nature, vol.564, pp.136-140, 2018.

H. Liu and F. Aoki, Transcriptional activity associated with meiotic competence in fully grown mouse GV oocytes, Zygote, vol.10, pp.327-332, 2002.

H. Liu, J. M. Kim, and F. Aoki, Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos, Development, vol.131, pp.2269-2280, 2004.

J. Y. Ma, M. Li, Y. B. Luo, S. Song, D. Tian et al., Maternal factors required for oocyte developmental competence in mice: transcriptome analysis of non-surrounded nucleolus (NSN) and surrounded nucleolus (SN) oocytes, Cell Cycle, vol.12, pp.1928-1938, 2013.

X. S. Ma, S. B. Chao, X. J. Huang, F. Lin, L. Qin et al., The dynamics and regulatory mechanism of pronuclear H3K9me2 asymmetry in mouse zygotes, Sci. Rep, vol.5, p.17924, 2015.

T. S. Macfarlan, W. D. Gifford, S. Driscoll, K. Lettieri, H. M. Rowe et al., Embryonic stem cell potency fluctuates with endogenous retrovirus activity, Nature, vol.487, pp.57-63, 2012.

S. Maenohara, M. Unoki, H. Toh, H. Ohishi, J. Sharif et al., Role of UHRF1 in de novo DNA methylation in oocytes and maintenance methylation in preimplantation embryos, PLoS Genet, vol.13, p.1007042, 2017.

I. A. Maksakova, P. J. Thompson, P. Goyal, S. J. Jones, P. B. Singh et al., Distinct roles of KAP1, HP1 and G9a/GLP in silencing of the two-cell-specific retrotransposon MERVL in mouse ES cells, Epigenetics Chromatin, vol.6, p.15, 2013.

K. Matsumoto, M. Anzai, N. Nakagata, A. Takahashi, Y. Takahashi et al., Onset of paternal gene activation in early mouse embryos fertilized with transgenic mouse sperm, Mol. Reprod. Dev, vol.39, pp.136-140, 1994.

W. Meuleman, D. Peric-hupkes, J. Kind, J. B. Beaudry, L. Pagie et al., Constitutive nuclear lamina-genome interactions are highly conserved and associated with A/T-rich sequence, Genome Res, vol.23, pp.270-280, 2013.

F. Miura, Y. Enomoto, R. Dairiki, and T. Ito, Amplification-free wholegenome bisulfite sequencing by post-bisulfite adaptor tagging, Nucleic Acids Res, vol.40, p.136, 2012.

K. Myant, A. Termanis, A. Y. Sundaram, T. Boe, C. Li et al., LSH and G9a/GLP complex are required for developmentally programmed DNA methylation, Genome Res, vol.21, pp.83-94, 2011.

T. Nakamura, Y. Arai, H. Umehara, M. Masuhara, T. Kimura et al., PGC7/Stella protects against DNA demethylation in early embryogenesis, Nat. Cell Biol, vol.9, pp.64-71, 2007.

T. Nakamura, Y. J. Liu, H. Nakashima, H. Umehara, K. Inoue et al., PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos, Nature, vol.486, pp.415-419, 2012.

A. E. Peaston, A. V. Evsikov, J. H. Graber, W. N. De-vries, A. E. Holbrook et al., Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos, Dev. Cell, vol.7, pp.597-606, 2004.

D. Peric-hupkes, W. Meuleman, L. Pagie, S. W. Bruggeman, I. Solovei et al., Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation, Mol. Cell, vol.38, pp.603-613, 2010.

M. Pertea, G. M. Pertea, C. M. Antonescu, T. C. Chang, J. T. Mendell et al., StringTie enables improved reconstruction of a transcriptome from RNA-seq reads, Nat. Biotechnol, vol.33, pp.290-295, 2015.

M. Pertea, D. Kim, G. M. Pertea, J. T. Leek, and S. L. Salzberg, Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown, Nat. Protoc, vol.11, pp.1650-1667, 2016.

A. H. Peters, S. Kubicek, K. Mechtler, R. J. O'sullivan, A. A. Derijck et al., Partitioning and plasticity of repressive histone methylation states in mammalian chromatin, Mol. Cell, vol.12, pp.1577-1589, 2003.

F. Santos, A. H. Peters, A. P. Otte, W. Reik, and W. Dean, Dynamic chromatin modifications characterise the first cell cycle in mouse embryos, 2005.

, Dev. Biol, vol.280, pp.225-236

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, NIH Image to ImageJ: 25 years of image analysis, Nat. Methods, vol.9, pp.671-675, 2012.

K. Shirane, H. Toh, H. Kobayashi, F. Miura, H. Chiba et al., Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases, PLoS Genet, vol.9, p.1003439, 2013.

S. A. Smallwood, S. Tomizawa, F. Krueger, N. Ruf, N. Carli et al., Dynamic CpG island methylation landscape in oocytes and preimplantation embryos, 2011.

, Nat. Genet, vol.43, pp.811-814

K. R. Stewart, L. Veselovska, J. Kim, J. Huang, H. Saadeh et al., Dynamic changes in histone modifications precede de novo DNA methylation in oocytes, Genes Dev, vol.29, pp.2449-2462, 2015.

M. Tachibana, K. Sugimoto, T. Fukushima, and Y. Shinkai, Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3, J. Biol. Chem, vol.276, pp.25309-25317, 2001.

M. Tachibana, K. Sugimoto, M. Nozaki, J. Ueda, T. Ohta et al., , vol.16, pp.1779-1791, 2002.

M. Tachibana, J. Ueda, M. Fukuda, N. Takeda, T. Ohta et al., Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9, Genes Dev, vol.19, pp.815-826, 2005.

M. Tachibana, M. Nozaki, N. Takeda, and Y. Shinkai, Functional dynamics of H3K9 methylation during meiotic prophase progression, EMBO J, vol.26, pp.3346-3359, 2007.

M. Tachibana, Y. Matsumura, M. Fukuda, H. Kimura, and Y. Shinkai, , 2008.

, G9a/GLP complexes independently mediate H3K9 and DNA methylation to silence transcription, EMBO J, vol.27, pp.2681-2690

T. Takada, T. Ebata, H. Noguchi, T. M. Keane, D. J. Adams et al., The ancestor of extant Jap, 2013.

, Genome Res, vol.23, pp.1329-1338

H. Toh, K. Shirane, F. Miura, N. Kubo, K. Ichiyanagi et al., Software updates in the Illumina HiSeq platform affect whole-genome bisulfite sequencing, BMC Genomics, vol.18, p.31, 2017.

S. Tomizawa, H. Kobayashi, T. Watanabe, S. Andrews, K. Hata et al., Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes, Development, vol.138, pp.811-820, 2011.

L. Veselovska, S. A. Smallwood, H. Saadeh, K. R. Stewart, F. Krueger et al., Deep sequencing and de novo assembly of the mouse oocyte transcriptome define the contribution of transcription to the DNA methylation landscape, Genome Biol, vol.16, p.209, 2015.
URL : https://hal.archives-ouvertes.fr/hal-01917300

A. Wagschal, H. G. Sutherland, K. Woodfine, A. Henckel, K. Chebli et al., G9a histone methyltransferase contributes to imprinting in the mouse placenta, Mol. Cell. Biol, vol.28, pp.1104-1113, 2008.

L. Wang, J. Zhang, J. Duan, X. Gao, W. Zhu et al., Programming and inheritance of parental DNA methylomes in mammals, Cell, vol.157, pp.979-991, 2014.

B. Wen, H. Wu, Y. Shinkai, R. A. Irizarry, and A. P. Feinberg, Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells, Nat. Genet, vol.41, pp.246-250, 2009.

K. Yamagata and J. Ueda, Long-term live-cell imaging of mammalian preimplantation development and derivation process of pluripotent stem cells from the embryos, Dev. Growth Differ, vol.55, pp.378-389, 2013.

K. Yamagata, R. Suetsugu, and T. Wakayama, Long-term, six-dimensional live-cell imaging for the mouse preimplantation embryo that does not affect full-term development, J. Reprod. Dev, vol.55, pp.343-350, 2009.

H. Younesy, T. Mö-ller, M. C. Lorincz, M. M. Karimi, and S. J. Jones, VisRseq: R-based visual framework for analysis of sequencing data, BMC Bioinformatics, vol.16, issue.11, p.2, 2015.

M. Zalzman, G. Falco, L. V. Sharova, A. Nishiyama, M. Thomas et al., Zscan4 regulates telomere elongation and genomic stability in ES cells, Nature, vol.464, pp.858-863, 2010.

T. Zhang, A. Termanis, B. Ö-zkan, X. X. Bao, J. Culley et al., G9a/GLP complex maintains imprinted DNA methylation in embryonic stem cells, Cell Rep, vol.15, pp.77-85, 2016.

M. Zuccotti, P. Giorgi-rossi, A. Martinez, S. Garagna, A. Forabosco et al., Meiotic and developmental competence of mouse antral oocytes, Biol. Reprod, vol.58, pp.700-704, 1998.

J. J. Zylicz, S. Dietmann, U. G?-unesdogan, J. A. Hackett, D. Cougot et al., Chromatin dynamics and the role of G9a in gene regulation and enhancer silencing during early mouse development, vol.4, p.9571, 2015.

J. J. Zylicz, M. Borensztein, F. C. Wong, Y. Huang, C. Lee et al., G9a regulates temporal preimplantation developmental program and lineage segregation in blastocyst. eLife 7, e33361. CONTACT FOR REAGENT AND RESOURCE SHARING Further information and requests for resources and reagents should be directed to and will be fulfilled by the Lead Contact, 2018.

. Tachibana, Genotyping was performed by PCR using the previously described primers for the G9a alleles (Tachibana et al., 2007) and GCAGAACCTGAAGATGTTCGCGAT and AGGTATCTCTGACCAGAGTCATCC for the Zp3-Cre transgene. JF1 mice were described previously (Takada et al., 2013). mice of 10 weeks or older were placed together with males in the same cage. Vaginal plugs were checked the next morning. Males were removed after a plug was observed and females were maintained for 20 days, 2000.

, FGOs were harvested from P15 or adult (10 weeks or older) ovaries by needle puncture. Superovulation was induced by injecting females sequentially with pregnant mare serum gonadotrophin and human chorionic gonadotropin. Cumulus-oocyte complexes were collected from the oviducts and fertilized with C57BL/6J or JF1 sperm for assessment of preimplantation development, WGBS, and RNA-seq. MII oocytes were harvested by digestion in hyaluronidase (H4272, Sigma-Aldrich). Cumulus cells were removed by capillary washing in PBS and zygotes were cultured in EmbryoMax KSOM Medium (1X) w/ 1/2 Amino Acids (Merck Millipore) or KSOM AA (Ho et al., 1995) at 37 C and 5% CO 2 . Two-cell embryos were harvested within 2 hours after the completion of the first mitotic division for WGBS and at 24 hours for RNA-seq, Oocyte Collection, IVF and Embryo Culture GOs were harvested by sequential digestion of P10 ovaries in 1 mg/ml collagenase, vol.5147, pp.34-10533

. Rt-pcr, Total RNA was extracted from pooled oocytes using Trizol reagent (Thermo Fisher Scientific). cDNA was synthesized using PrimeScript RT reagent Kit with gDNA Eraser (Perfect Real Time) (Takara Bio Inc.) and subjected to PCR using KAPA HiFi HotStart ReadyMix PCR Kit (Kapa Biosystems) and TaKaRa PCR Thermal Cycler Diceâ

G. Actb and C. Western, Proteins were separated on a 12%-15% SDS-polyacrylamide gel and transferred to a polyvinylidene difluoride membrane by wet blotting. The blot was blocked by 5% skimmed milk or 5% BSA in TBS with Tween-20

. Hrp-conjugated-igg, Signals were detected using Chemi-Lumi One Ultra (Nacalai Tesque) on ImageQuant LAS4000 mini (GE Healthcare Life Sciences). Can Get Signal Immunoreaction Enhancer Solution (TOYOBO) was used to detect H3K9me2

, Ovary Sectioning and Hematoxylin-Eosin Staining Ovaries were embedded in OCT and flash frozen. Frozen sections were prepared using CM3050 S Research Cryostat (Leica)

, BioAcademia) were used. Alexa Flour 488-, 555-, or 647-conjugated IgG (Thermo Fisher Scientific) was used as the secondary antibody. Oocytes and embryos were mounted in VECTASHEILD medium with DAPI (Vector Laboratory) and observed under LSM700 confocal laser scanning microscope (Carl Zeiss). The different anti-H3K9me2 antibodies displayed similar results, Active motif), H3K9me3 (MABI0318, MBL), CDX2 (ab157524, abcam), SOX2 (ab92494, abcam), SOX17 (AF1924, R&D Systems), and HP1b, vol.39239, pp.70-223, 2012.

. Wgbs, C. Rna-seq, and . Miura, Zona pellucida was removed by acid Tyrode's solution. ChIP was performed with anti-H3K9me2 antibody (abcam ab1220) in 200 mL NChIP buffer. WGBS libraries were sequenced on HiSeq 1500 or HiSeq 2500 (Illumina) (FGOs and blastocysts: HCS v2.0.5 and RTA v1.17.20; MII oocytes and 2-cell embryos: HCS v2.2.68 and RTA v1, p.2500, 2012.

. Yamagata, Microinjection and Live-cell Imaging Zygotes were injected with 5 ng/ml mRNAs encoding EGFP-a-tubulin and H2B-mCherry at 5 hours post fertilization, Raw images were stacked and projected by CV1000 Software, 2009.

. Bao, QUANTIFICATION AND STATISTICAL ANALYSIS Reference Sequences RefSeq transcript coordinates (RefFlat) and assemblies (GTF) of mouse genome mm10 were obtained from iGenomes (Illumina), The repeat masker track of mm10 was downloaded from UCSC Table Browser, 2011.

. Takada, Windows with less than 5 informative CG (or non-CG) sites were excluded. To study CG methylation at ERVs, reads were mapped to the Repbase annotations. For allelic-specific analysis, reads were mapped to N-masked mm10 genome using published SNP data of JF1, WGBS Data Analysis Reads were trimmed to remove low quality bases and adaptor sequences using Trim-Galore! v0, vol.3, 2011.

. Kim, ERVs with R 100 copies in the genome and at least 2-fold increase in all replicates were defined as derepressed. RefSeq transcripts containing an extra ERV sequence at their 5 0 ends were identified as additional chimeric transcripts. For allelic-specific analysis, reads were mapped to N-masked mm10 genome using published SNP data of JF1, RNA-seq Data Analysis Reads were trimmed and mapped to mouse genome mm10 by HISAT2, vol.1, 2012.