Insights into epigenetic patterns in mammalian early embryos

Abstract

Mammalian fertilization begins with the fusion of two specialized gametes, followedbymajor epigenetic remodeling leading to the formation of a totipotent embryo. During the development of the pre-implantation embryo, precise reprogramming progress is a prerequisite for avoiding developmental defects or embryonic lethality, but the underlyingmolecularmechanisms remain elusive. For the past few years, unprecedented breakthroughs have been made in mapping the regulatory network of dynamic epigenomes during mammalian early embryo development, taking advantage ofmultiple advances and innovations in low-input genome-wide chromatin analysis technologies. The aim of this review is to highlight the most recent progress in understanding the mechanisms of epigenetic remodeling during early embryogenesis in mammals, including DNA methylation, histone modifications, chromatin accessibility and 3D chromatin organization.

Keywords

epigenetic reprogramming / DNA methylation / histone modifications / early embryo development

References

[1] Abe KI, Funaya S, Tsukioka D, Kawamura M, Suzuki Y, Suzuki MG, Schultz RM, Aoki F (2018) Minor zygotic gene activation is essential for mouse pre-implantation development. Proc Natl Acad Sci USA 115:E6780–E6788

[2] Allshire RC, Madhani HD (2018) Ten principles of heterochromatin formation and function. Nat Rev Mol Cell Biol 19:229–244

[3] Amdani SN, Yeste M, Jones C, Coward K (2015) Sperm factors and oocyte activation: current controversies and considerations. Biol Reprod 93:50

[4] Amouroux R, Nashun B, Shirane K, Nakagawa S, Hill PW, D'Souza Z, Nakayama M, Matsuda M, Turp A, Ndjetehe E (2016) De novo DNA methylation drives 5hmC accumulation in mouse zygotes. Nat Cell Biol 18:225–233

[5] Andreu-Vieyra CV, Chen R, Agno JE, Glaser S, Anastassiadis K, Stewart AF, Matzuk MM (2010) MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol. https://doi.org/10.1371/journal.pbio.1000453

[6] Atlasi Y, Stunnenberg HG (2017) The interplay of epigenetic marks during stem cell differentiation and development. Nat Rev Genet 18:643–658

[7] Au Yeung WK, Brind'Amour J, Hatano Y, Yamagata K, Feil R, Lorincz MC, Tachibana M, Shinkai Y, Sasaki H (2019) Histone H3K9 methyltransferase G9a in oocytes is essential for preimplantation development but dispensable for CG methylation protection. Cell Rep 27(282–293):e284

[8] Babaian A, Mager DL (2016) Endogenous retroviral promoter exaptation in human cancer. Mob DNA 7:24

[9] Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395

[10] Bartke T, Vermeulen M, Xhemalce B, Robson SC, Mann M, Kouzarides T (2010) Nucleosome-interacting proteins regulated by DNA and histone methylation. Cell 143:470–484

[11] Battulin N, Fishman VS, Mazur AM, Pomaznoy M, Khabarova AA, Afonnikov DA, Prokhortchouk EB, Serov OL (2015) Comparison of the three-dimensional organization of sperm and fibroblast genomes using the Hi-C approach. Genome Biol 16:77

[12] Baubec T, Colombo DF, Wirbelauer C, Schmidt J, Burger L, Krebs AR, Akalin A, Schubeler D (2015) Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature 520:243–247

[13] Beagrie RA, Scialdone A, Schueler M, Kraemer DC, Chotalia M, Xie SQ, Barbieri M, de Santiago I, Lavitas LM, Branco MR (2017) Complex multi-enhancer contacts captured by genome architecture mapping. Nature 543:519–524

[14] Becker JS, Nicetto D, Zaret KS (2016) H3K9me3-dependent heterochromatin: barrier to cell fate changes. Trends Genet 32:29–41

[15] Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315–326

[16] Bonev B, Cavalli G (2016) Organization and function of the 3D genome. Nat Rev Genet 17:772

[17] Bonte D, Reddy Guggilla R, Stamatiadis P, De Sutter P, Heindryckx B (2018) Chapter 14—unraveling the causes of failed fertilization after intracytoplasmic sperm injection due to oocyte activation deficiency. In: Horcajadas JA, Gosálvez J (eds) Reproductomics. Academic Press, London, pp 243–277

[18] Borsos M, Perricone SM, Schauer T, Pontabry J, de Luca KL, de Vries SS, Ruiz-Morales ER, Torres-Padilla ME, Kind J (2019) Genome–lamina interactions are established de novo in the early mouse embryo. Nature 569:729–733

[19] Bourque G (2009) Transposable elements in gene regulation and in the evolution of vertebrate genomes. Curr Opin Genet Dev 19:607–612

[20] Brinkman AB, Gu H, Bartels SJ, Zhang Y, Matarese F, Simmer F, Marks H, Bock C, Gnirke A, Meissner A (2012) Sequential ChIP-bisulfite sequencing enables direct genome-scale investigation of chromatin and DNA methylation cross-talk. Genome Res 22:1128–1138

[21] Buenrostro JD, Wu B, Litzenburger UM, Ruff D, Gonzales ML, Snyder MP, Chang HY, Greenleaf WJ (2015) Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523:486–490

[22] Burns KH (2017) Transposable elements in cancer. Nat Rev Cancer 17:415–424

[23] Burton A, Torres-Padilla ME (2010) Epigenetic reprogramming and development: a unique heterochromatin organization in the preimplantation mouse embryo. Brief Funct Genomics 9:444–454

[24] Burton A, Torres-Padilla ME (2014) Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis. Nat Rev Mol Cell Biol 15:723–734

[25] Canovas S, Ross PJ (2016) Epigenetics in pre-implantation mammalian development. Theriogenology 86:69–79

[26] Chen Z, Zhang Y (2019) Loss of DUX causes minor defects in zygotic genome activation and is compatible with mouse development. Nat Genet 51:947–951

[27] Chen X, Ke Y, Wu K, Zhao H, Sun Y, Gao L, Liu Z, Zhang J, Tao W, Hou Z (2019a) Key role for CTCF in establishing chromatin structure in human embryos. Nature 576:306–310

[28] Chen Z, Yin Q, Inoue A, Zhang C, Zhang Y (2019b) Allelic H3K27me3 to allelic DNA methylation switch maintains noncanonical imprinting in extraembryonic cells. Sci Adv 5:eaay7246

[29] Chen M, Zhu Q, Li C, Kou X, Zhao Y, Li Y, Xu R, Yang L, Yang L, Gu L (2020) Chromatin architecture reorganization in murine somatic cell nuclear transfer embryos. Nat Commun 11:1813

[30] Chung YG, Matoba S, Liu Y, Eum JH, Lu F, Jiang W, Lee JE, Sepilian V, Cha KY, Lee DR (2015) Histone demethylase expression enhances human somatic cell nuclear transfer efficiency and promotes derivation of pluripotent stem cells. Cell Stem Cell 17:758–766

[31] Collombet S, Ranisavljevic N, Nagano T, Varnai C, Shisode T, Leung W, Piolot T, Galupa R, Borensztein M, Servant N (2020) Parental-to-embryo switch of chromosome organization in early embryogenesis. Nature 580:142–146

[32] Cossec JC, Theurillat I, Chica C, Bua Aguin S, Gaume X, Andrieux A, Iturbide A, Jouvion G, Li H, Bossis G (2018) SUMO safeguards somatic and pluripotent cell identities by enforcing distinct chromatin states. Cell Stem Cell 23(742–757):e748

[33] Cusanovich DA, Daza R, Adey A, Pliner HA, Christiansen L, Gunderson KL, Steemers FJ, Trapnell C, Shendure J (2015) Multiplex single cell profiling of chromatin accessibility by combinatorial cellular indexing. Science 348:910–914

[34] Dahl JA, Jung I, Aanes H, Greggains GD, Manaf A, Lerdrup M, Li G, Kuan S, Li B, Lee AY (2016) Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nature 537:548–552

[35] Dean W, Santos F, Stojkovic M, Zakhartchenko V, Walter J, Wolf E, Reik W (2001) Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci USA 98:13734–13738

[36] Deaton AM, Bird A (2011) CpG islands and the regulation of transcription. Genes Dev 25:1010–1022

[37] De Iaco A, Planet E, Coluccio A, Verp S, Duc J, Trono D (2017) DUX-family transcription factors regulate zygotic genome activation in placental mammals. Nat Genet 49:941–945

[38] Deng Q, Ramskold D, Reinius B, Sandberg R (2014) Single-cell RNA-seq reveals dynamic, random monoallelic gene expression in mammalian cells. Science 343:193–196

[39] Di Croce L, Helin K (2013) Transcriptional regulation by Polycomb group proteins. Nat Struct Mol Biol 20:1147–1155

[40] Djekidel MN, Inoue A, Matoba S, Suzuki T, Zhang CX, Lu FL, Jiang L, Zhang Y (2018) Reprogramming of chromatin accessibility in somatic cell nuclear transfer is DNA replication independent. Cell Reports 23:1939–1947

[41] Du Z, Zheng H, Huang B, Ma R, Wu J, Zhang X, He J, Xiang Y, Wang Q, Li Y (2017) Allelic reprogramming of 3D chromatin architecture during early mammalian development. Nature 547:232–235

[42] Du Z, Zheng H, Kawamura YK, Zhang K, Gassler J, Powell S, Xu Q, Lin Z, Xu K, Zhou Q (2020) Polycomb group proteins regulate chromatin architecture in mouse oocytes and early embryos. Mol Cell 77(825–839):e827

[43] Eckersley-Maslin MA, Svensson V, Krueger C, Stubbs TM, Giehr P, Krueger F, Miragaia RJ, Kyriakopoulos C, Berrens RV, Milagre I (2016) MERVL/Zscan4 network activation results in transient genome-wide DNA demethylation of mESCs. Cell Rep 17:179–192

[44] Eckersley-Maslin MA, Alda-Catalinas C, Reik W (2018) Dynamics of the epigenetic landscape during the maternal-to-zygotic transition. Nat Rev Mol Cell Biol 19:436–450

[45] Eckersley-Maslin M, Alda-Catalinas C, Blotenburg M, Kreibich E, Krueger C, Reik W (2019) Dppa2 and Dppa4 directly regulate the Dux-driven zygotic transcriptional program. Genes Dev 33:194–208

[46] Edmunds JW, Mahadevan LC, Clayton AL (2008) Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation. EMBO J 27:406–420

[47] Evsikov AV, de Vries WN, Peaston AE, Radford EE, Fancher KS, Chen FH, Blake JA, Bult CJ, Latham KE, Solter D (2004) Systems biology of the 2-cell mouse embryo. Cytogenet Genome Res 105:240–250

[48] Fadloun A, Le Gras S, Jost B, Ziegler-Birling C, Takahashi H, Gorab E, Carninci P, Torres-Padilla ME (2013) Chromatin signatures and retrotransposon profiling in mouse embryos reveal regulation of LINE-1 by RNA. Nat Struct Mol Biol 20:332–338

[49] Fulka H, Mrazek M, Tepla O, Fulka J Jr (2004) DNA methylation pattern in human zygotes and developing embryos. Reproduction 128:703–708

[50] Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H, Mohamed YB, Orlov YL, Velkov S, Ho A, Mei PH (2009) An oestrogen-receptoralpha-bound human chromatin interactome. Nature 462:58–64

[51] Gabellini D, Green MR, Tupler R (2002) Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscle. Cell 110:339–348

[52] Gao L, Wu K, Liu Z, Yao X, Yuan S, Tao W, Yi L, Yu G, Hou Z, Fan D (2018a) Chromatin accessibility landscape in human early embryos and its association with evolution. Cell 173(248–259): e215

[53] Gao R, Wang C, Gao Y, Xiu W, Chen J, Kou X, Zhao Y, Liao Y, Bai D, Qiao Z (2018b) Inhibition of aberrant DNA re-methylation improves post-implantation development of somatic cell nuclear transfer embryos. Cell Stem Cell 23(426–435):e425

[54] Ginisty H, Amalric F, Bouvet P (1998) Nucleolin functions in the first step of ribosomal RNA processing. EMBO J 17:1476–1486

[55] Goolam M, Scialdone A, Graham SJL, Macaulay IC, Jedrusik A, Hupalowska A, Voet T, Marioni JC, Zernicka-Goetz M (2016) Heterogeneity in Oct4 and Sox2 targets biases cell fate in 4-cell mouse embryos. Cell 165:61–74

[56] Gorkin DU, Leung D, Ren B (2014) The 3D genome in transcriptional regulation and pluripotency. Cell Stem Cell 14:762–775

[57] Gu TP, Guo F, Yang H, Wu HP, Xu GF, Liu W, Xie ZG, Shi L, He X, Jin SG (2011) The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477:606–610

[58] Guo F, Li X, Liang D, Li T, Zhu P, Guo H, Wu X, Wen L, Gu TP, Hu B (2014a) Active and passive demethylation of male and female pronuclear DNA in the mammalian zygote. Cell Stem Cell 15:447–459

[59] Guo H, Zhu P, Yan L, Li R, Hu B, Lian Y, Yan J, Ren X, Lin S, Li J (2014b) The DNA methylation landscape of human early embryos. Nature 511:606–610

[60] Guo F, Li L, Li J, Wu X, Hu B, Zhu P, Wen L, Tang F (2017) Singlecell multi-omics sequencing of mouse early embryos and embryonic stem cells. Cell Res 27:967–988

[61] Guo M, Zhang Y, Zhou J, Bi Y, Xu J, Xu C, Kou X, Zhao Y, Li Y, Tu Z (2019) Precise temporal regulation of Dux is important for embryo development. Cell Res 29:956–959

[62] Han L, Ren C, Li L, Li X, Ge J, Wang H, Miao YL, Guo X, Moley KH, Shu W (2018) Embryonic defects induced by maternal obesity in mice derive from Stella insufficiency in oocytes. Nat Genet 50:432–442

[63] Hanna CW, Taudt A, Huang J, Gahurova L, Kranz A, Andrews S, Dean W, Stewart AF, Colome-Tatche M, Kelsey G (2018) MLL2 conveys transcription-independent H3K4 trimethylation in oocytes. Nat Struct Mol Biol 25:73–82

[64] Hatanaka Y, Inoue K, Oikawa M, Kamimura S, Ogonuki N, Kodama EN, Ohkawa Y, Tsukada Y, Ogura A (2015) Histone chaperone CAF-1 mediates repressive histone modifications to protect preimplantation mouse embryos from endogenous retrotransposons. Proc Natl Acad Sci USA 112:14641–14646

[65] Hawkins RD, Hon GC, Lee LK, Ngo Q, Lister R, Pelizzola M, Edsall LE, Kuan S, Luu Y, Klugman S (2010) Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 6:479–491

[66] Hendrickson PG, Dorais JA, Grow EJ, Whiddon JL, Lim JW, Wike CL, Weaver BD, Pflueger C, Emery BR, Wilcox AL (2017) Conserved roles of mouse DUX and human DUX4 in activating cleavage-stage genes and MERVL/HERVL retrotransposons. Nat Genet 49:925–934

[67] Huang Y, Kim JK, Do DV, Lee C, Penfold CA, Zylicz JJ, Marioni JC, Hackett JA, Surani MA (2017) Stella modulates transcriptional and endogenous retrovirus programs during maternal-to-zygotic transition. Elife. https://doi.org/10.7554/eLife.22345

[68] Huang X, Gao X, Li W, Jiang S, Li R, Hong H, Zhao C, Zhou P, Chen H, Bo X (2019) Stable H3K4me3 is associated with transcription initiation during early embryo development. Bioinformatics 35:3931–3936

[69] Hug CB, Vaquerizas JM (2018) The birth of the 3D genome during early embryonic development. Trends Genet 34:903–914

[70] Hupalowska A, Jedrusik A, Zhu M, Bedford MT, Glover DM, Zernicka-Goetz M (2018) CARM1 and paraspeckles regulate pre-implantation mouse embryo development. Cell 175(1902–1916):e1913

[71] Inoue A, Zhang Y (2011) Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 334:194–194

[72] Inoue A, Zhang Y (2014) Nucleosome assembly is required for nuclear pore complex assembly in mouse zygotes. Nat Struct Mol Biol 21:609–616

[73] Inoue K, Kohda T, Sugimoto M, Sado T, Ogonuki N, Matoba S, Shiura H, Ikeda R, Mochida K, Fujii T (2010) Impeding Xist expression from the active X chromosome improves mouse somatic cell nuclear transfer. Science 330:496–499

[74] Inoue A, Jiang L, Lu F, Suzuki T, Zhang Y (2017a) Maternal H3K27me3 controls DNA methylation-independent imprinting. Nature 547:419–424

[75] Inoue A, Jiang L, Lu F, Zhang Y (2017b) Genomic imprinting of Xist by maternal H3K27me3. Genes Dev 31:1927–1932

[76] Inoue A, Chen Z, Yin Q, Zhang Y (2018) Maternal Eed knockout causes loss of H3K27me3 imprinting and random X inactivation in the extraembryonic cells. Genes Dev 32:1525–1536

[77] Inoue K, Ogonuki N, Kamimura S, Inoue H, Matoba S, Hirose M, Honda A, Miura K, Hada M, Hasegawa A (2020) Loss of H3K27me3 imprinting in the Sfmbt2 miRNA cluster causes enlargement of cloned mouse placentas. Nat Commun 11:2150

[78] Ishiuchi T, Enriquez-Gasca R, Mizutani E, Boskovic A, Ziegler-Birling C, Rodriguez-Terrones D, Wakayama T, Vaquerizas JM, Torres-Padilla ME (2015) Early embryonic-like cells are induced by downregulating replication-dependent chromatin assembly. Nat Struct Mol Biol 22:662–671

[79] Iurlaro M, von Meyenn F, Reik W (2017) DNA methylation homeostasis in human and mouse development. Curr Opin Genet Dev 43:101–109

[80] Jachowicz JW, Bing X, Pontabry J, Boskovic A, Rando OJ, Torres-Padilla ME (2017) LINE-1 activation after fertilization regulates global chromatin accessibility in the early mouse embryo. Nat Genet 49:1502–1510

[81] Jin WF, Tang QS, Wan MM, Cui KR, Zhang Y, Ren G, Ni B, Sklar J, Przytycka TM, Childs R (2015) Genome-wide detection of DNase I hypersensitive sites in single cells and FFPE tissue samples. Nature 528:142

[82] Jukam D, Shariati SAM, Skotheim JM (2017) Zygotic genome activation in vertebrates. Dev Cell 42:316–332

[83] Karimi MM, Goyal P, Maksakova IA, Bilenky M, Leung D, Tang JX, Shinkai Y, Mager DL, Jones S, Hirst M (2011) DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 8:676–687

[84] Kasowitz SD, Ma J, Anderson SJ, Leu NA, Xu Y, Gregory BD, Schultz RM, Wang PJ (2018) Nuclear m6A reader YTHDC1 regulates alternative polyadenylation and splicing during mouse oocyte development. PLoS Genet 14:e1007412

[85] Ke Y, Xu Y, Chen X, Feng S, Liu Z, Sun Y, Yao X, Li F, Zhu W, Gao L (2017) 3D chromatin structures of mature gametes and structural reprogramming during mammalian embryogenesis. Cell 170(367–381):e320

[86] Kigami D, Minami N, Takayama H, Imai H (2003) MuERV-L is one of the earliest transcribed genes in mouse one-cell embryos. Biol Reprod 68:651–654

[87] Kizer KO, Phatnani HP, Shibata Y, Hall H, Greenleaf AL, Strahl BD (2005) A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol Cell Biol 25:3305–3316

[88] Kohli RM, Zhang Y (2013) TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502:472–479

[89] Kragesteen BK, Spielmann M, Paliou C, Heinrich V, Schopflin R, Esposito A, Annunziatella C, Bianco S, Chiariello AM, Jerkovic I (2018) Dynamic 3D chromatin architecture contributes to enhancer specificity and limb morphogenesis. Nat Genet 50:1463–1473

[90] Kraushaar DC, Jin W, Maunakea A, Abraham B, Ha M, Zhao K (2013) Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3.3. Genome Biol 14:R121

[91] Lee MT, Bonneau AR, Giraldez AJ (2014) Zygotic genome activation during the maternal-to-zygotic transition. Annu Rev Cell Dev Biol 30:581–613

[92] Legault LM, Bertrand-Lehouillier V, McGraw S (2018) Pre-implantation alcohol exposure and developmental programming of FASD: an epigenetic perspective. Biochem Cell Biol 96:117–130

[93] Leung D, Du T, Wagner U, Xie W, Lee AY, Goyal P, Li Y, Szulwach KE, Jin P, Lorincz MC (2014) Regulation of DNA methylation turnover at LTR retrotransposons and imprinted loci by the histone methyltransferase Setdb1. Proc Natl Acad Sci USA 111:6690–6695

[94] Li E, Zhang Y (2014) DNA methylation in mammals. Cold Spring Harb Perspect Biol 6:a019133

[95] Li L, Guo F, Gao Y, Ren Y, Yuan P, Yan L, Li R, Lian Y, Li J, Hu B (2018a) Single-cell multi-omics sequencing of human early embryos. Nat Cell Biol 20:847–858

[96] Li Y, Zhang Z, Chen J, Liu W, Lai W, Liu B, Li X, Liu L, Xu S, Dong Q (2018b) Stella safeguards the oocyte methylome by preventing de novo methylation mediated by DNMT1. Nature 564:136–140

[97] Lin CJ, Conti M, Ramalho-Santos M (2013) Histone variant H3.3 maintains a decondensed chromatin state essential for mouse pre-implantation development. Development 140:3624–3634

[98] Lin CJ, Koh FM, Wong P, Conti M, Ramalho-Santos M (2014) Hiramediated H3.3 incorporation is required for DNA replication and ribosomal RNA transcription in the mouse zygote. Dev Cell 30:268–279

[99] Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315–322

[100] Liu W, Liu X, Wang C, Gao Y, Gao R, Kou X, Zhao Y, Li J, Wu Y, Xiu W (2016a) Identification of key factors conquering developmental arrest of somatic cell cloned embryos by combining embryo biopsy and single-cell sequencing. Cell Discov 2:16010

[101] Liu X, Wang C, Liu W, Li J, Li C, Kou X, Chen J, Zhao Y, Gao H, Wang H (2016b) Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537:558–562

[102] Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL, Couble P (2005) The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437:1386–1390

[103] Lu F, Liu Y, Inoue A, Suzuki T, Zhao K, Zhang Y (2016) Establishing chromatin regulatory landscape during mouse preimplantation development. Cell 165:1375–1388

[104] Lubas M, Christensen MS, Kristiansen MS, Domanski M, Falkenby LG, Lykke-Andersen S, Andersen JS, Dziembowski A, Jensen TH (2011) Interaction profiling identifies the human nuclear exosome targeting complex. Mol Cell 43:624–637

[105] Ma H, Zhai J, Wan H, Jiang X, Wang X, Wang L, Xiang Y, He X, Zhao ZA, Zhao B (2019) In vitro culture of cynomolgus monkey embryos beyond early gastrulation. Science. https://doi.org/10.1126/science.aax7890

[106] Macfarlan TS, Gifford WD, Driscoll S, Lettieri K, Rowe HM, Bonanomi D, Firth A, Singer O, Trono D, Pfaff SL (2012) Embryonic stem cell potency fluctuates with endogenous retrovirus activity. Nature 487:57–63

[107] Malki S, van der Heijden GW, O'Donnell KA, Martin SL, Bortvin A (2019) A role for retrotransposon LINE-1 in fetal oocyte attrition in mice. Dev Cell 51:658

[108] Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469:343–349

[109] Matoba S, Inoue K, Kohda T, Sugimoto M, Mizutani E, Ogonuki N, Nakamura T, Abe K, Nakano T, Ishino F (2011) RNAimediated knockdown of Xist can rescue the impaired postimplantation development of cloned mouse embryos. Proc Natl Acad Sci U S A 108:20621–20626

[110] Matoba S, Liu Y, Lu F, Iwabuchi KA, Shen L, Inoue A, Zhang Y (2014) Embryonic development following somatic cell nuclear transfer impeded by persisting histone methylation. Cell 159:884–895

[111] Matoba S, Wang H, Jiang L, Lu F, Iwabuchi KA, Wu X, Inoue K, Yang L, Press W, Lee JT (2018) Loss of H3K27me3 imprinting in somatic cell nuclear transfer embryos disrupts post-implantation development. Cell Stem Cell 23(343–354):e345

[112] Messerschmidt DM, Knowles BB, Solter D (2014) DNA methylation dynamics during epigenetic reprogramming in the germline and pre-implantation embryos. Genes Dev 28:812–828

[113] Mihajlovic AI, Bruce AW (2017) The first cell-fate decision of mouse pre-implantation embryo development: integrating cell position and polarity. Open Biol. https://doi.org/10.1098/rsob.170210

[114] Minami N, Suzuki T, Tsukamoto S (2007) Zygotic gene activation and maternal factors in mammals. J Reprod Dev 53:707–715

[115] Miri K, Latham K, Panning B, Zhong Z, Andersen A, Varmuza S (2013) The imprinted polycomb group gene Sfmbt2 is required for trophoblast maintenance and placenta development. Development 140:4480–4489

[116] Molaro A, Hodges E, Fang F, Song Q, McCombie WR, Hannon GJ, Smith AD (2011) Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell 146:1028–1040

[117] Mure F, Corbin A, Benbahouche NEH, Bertrand E, Manet E, Gruffat H (2018) The splicing factor SRSF3 is functionally connected to the nuclear RNA exosome for intronless mRNA decay. Sci Rep 8:12901

[118] Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, Taniguchi H, Sekimoto T, Ikawa M, Yoneda Y, Okabe M (2007) PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol 9:64–71

[119] Nakamura T, Liu YJ, Nakashima H, Umehara H, Inoue K, Matoba S, Tachibana M, Ogura A, Shinkai Y, Nakano T (2012) PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 486:415–419

[120] Nicetto D, Donahue G, Jain T, Peng T, Sidoli S, Sheng L, Montavon T, Becker JS, Grindheim JM, Blahnik K (2019) H3K9me3-heterochromatin loss at protein-coding genes enables developmental lineage specification. Science 363:294–297

[121] Nichols J, Smith A (2009) Naive and primed pluripotent states. Cell Stem Cell 4:487–492

[122] Niu Y, Sun N, Li C, Lei Y, Huang Z, Wu J, Si C, Dai X, Liu C, Wei J (2019) Dissecting primate early post-implantation development using long-term in vitro embryo culture. Science. https://doi.org/10.1126/science.aaw5754

[123] Okae H, Chiba H, Hiura H, Hamada H, Sato A, Utsunomiya T, Kikuchi H, Yoshida H, Tanaka A, Suyama M (2014a) Genome-wide analysis of DNA methylation dynamics during early human development. PLoS Genet 10:e1004868

[124] Okae H, Matoba S, Nagashima T, Mizutani E, Inoue K, Ogonuki N, Chiba H, Funayama R, Tanaka S, Yaegashi N (2014b) RNA sequencing-based identification of aberrant imprinting in cloned mice. Hum Mol Genet 23:992–1001

[125] Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257

[126] Oswald J, Engemann S, Lane N, Mayer W, Olek A, Fundele R, Dean W, Reik W, Walter J (2000) Active demethylation of the paternal genome in the mouse zygote. Curr Biol 10:475–478

[127] Parfitt DE, Zernicka-Goetz M (2010) Epigenetic modification affecting expression of cell polarity and cell fate genes to regulate lineage specification in the early mouse embryo. Mol Biol Cell 21:2649–2660

[128] Peaston AE, Evsikov AV, Graber JH, de Vries WN, Holbrook AE, Solter D, Knowles BB (2004) Retrotransposons regulate host genes in mouse oocytes and pre-implantation embryos. Dev Cell 7:597–606

[129] Peat JR, Reik W (2012) Incomplete methylation reprogramming in SCNT embryos. Nat Genet 44:965–966

[130] Peng G, Suo S, Cui G, Yu F, Wang R, Chen J, Chen S, Liu Z, Chen G, Qian Y (2019) Molecular architecture of lineage allocation and tissue organization in early mouse embryo. Nature 572:528–532

[131] Percharde M, Lin CJ, Yin Y, Guan J, Peixoto GA, Bulut-Karslioglu A, Biechele S, Huang B, Shen X, Ramalho-Santos M (2018) A LINE1-nucleolin partnership regulates early development and ESC identity. Cell 174(391–405):e319

[132] Petropoulos S, Edsgard D, Reinius B, Deng Q, Panula SP, Codeluppi S, Reyes AP, Linnarsson S, Sandberg R, Lanner F (2016) Single-cell RNA-Seq reveals lineage and X chromosome dynamics in human preimplantation embryos. Cell 167:285

[133] Pijuan-Sala B, Griffiths JA, Guibentif C, Hiscock TW, Jawaid W, Calero-Nieto FJ, Mulas C, Ibarra-Soria X, Tyser RCV, Ho DLL (2019) A single-cell molecular map of mouse gastrulation and early organogenesis. Nature 566:490–495

[134] Ribet D, Louvet-Vallee S, Harper F, de Parseval N, Dewannieux M, Heidmann O, Pierron G, Maro B, Heidmann T (2008) Murine endogenous retrovirus MuERV-L is the progenitor of the orphan epsilon viruslike particles of the early mouse embryo. J Virol 82:1622–1625

[135] Richardson SR, Doucet AJ, Kopera HC, Moldovan JB, Garcia-Perez JL, Moran JV (2015) The influence of LINE-1 and SINE retrotransposons on mammalian genomes. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.MDNA3-0061-2014

[136] Risal S, Pei Y, Lu H, Manti M, Fornes R, Pui HP, Zhao Z, Massart J, Ohlsson C, Lindgren E (2019) Prenatal androgen exposure and transgenerational susceptibility to polycystic ovary syndrome. Nat Med 25:1894–1904

[137] Rivera RM, Ross JW (2013) Epigenetics in fertilization and preimplantation embryo development. Prog Biophys Mol Biol 113:423–432

[138] Roundtree IA, Luo GZ, Zhang Z, Wang X, Zhou T, Cui Y, Sha J, Huang X, Guerrero L, Xie P (2017) YTHDC1 mediates nuclear export of N(6)-methyladenosine methylated mRNAs. Elife. https://doi.org/10.7554/eLife.31311

[139] Rulands S, Lee HJ, Clark SJ, Angermueller C, Smallwood SA, Krueger F, Mohammed H, Dean W, Nichols J, Rugg-Gunn P (2018) Genome-scale oscillations in DNA methylation during exit from pluripotency. Cell Syst 7(63–76):e12

[140] Sachs M, Onodera C, Blaschke K, Ebata KT, Song JS, Ramalho-Santos M (2013) Bivalent chromatin marks developmental regulatory genes in the mouse embryonic germline in vivo. Cell Rep 3:1777–1784

[141] Sadakierska-Chudy A, Filip M (2015) A Comprehensive view of the epigenetic landscape. Part II: Histone post-translational modification, nucleosome level, and chromatin regulation by ncRNAs. Neurotox Res 27:172–197

[142] Saha B, Home P, Ray S, Larson M, Paul A, Rajendran G, Behr B, Paul S (2013) EED and KDM6B coordinate the first mammalian cell lineage commitment to ensure embryo implantation. Mol Cell Biol 33:2691–2705

[143] SanMiguel JM, Bartolomei MS (2018) DNA methylation dynamics of genomic imprinting in mouse development. Biol Reprod 99:252–262

[144] Santos F, Peters AH, Otte AP, Reik W, Dean W (2005) Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev Biol 280:225–236

[145] Schultz RM (2002) The molecular foundations of the maternal to zygotic transition in the pre-implantation embryo. Hum Reprod Update 8:323–331

[146] Schulz KN, Harrison MM (2019) Mechanisms regulating zygotic genome activation. Nat Rev Genet 20:221–234

[147] Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, Wagner U, Dixon J, Lee L,Lobanenkov VV (2012) A map of the cisregulatory sequences in the mouse genome. Nature 488:116–120

[148] Shen L, Inoue A, He J, Liu Y, Lu F, Zhang Y (2014) Tet3 and DNA replication mediate demethylation of both the maternal and paternal genomes in mouse zygotes. Cell Stem Cell 15:459–471

[149] Shi J, Chen Q, Li X, Zheng X, Zhang Y, Qiao J, Tang F, Tao Y, Zhou Q, Duan E (2015) Dynamic transcriptional symmetry-breaking in pre-implantation mammalian embryo development revealed by single-cell RNA-seq. Development 142:3468–3477

[150] Simon JA, Kingston RE (2009) Mechanisms of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10:697–708

[151] Skene PJ, Henikoff S (2013) Histone variants in pluripotency and disease. Development 140:2513–2524

[152] Skene PJ, Henikoff S (2017) An efficient targeted nuclease strategy for high-resolution mapping of DNA binding sites. Elife. https://doi.org/10.7554/eLife.21856

[153] Skvortsova K, Iovino N, Bogdanovic O (2018) Functions and mechanisms of epigenetic inheritance in animals. Nat Rev Mol Cell Biol 19:774–790

[154] Smith ZD, Meissner A (2013) DNA methylation: roles in mammalian development. Nat Rev Genet 14:204–220

[155] Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, Regev A, Meissner A (2012) A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484:339–344

[156] Smith ZD, Chan MM, Humm KC, Karnik R, Mekhoubad S, Regev A, Eggan K, Meissner A (2014) DNA methylation dynamics of the human pre-implantation embryo. Nature 511:611–615

[157] Smith ZD, Shi J, Gu H, Donaghey J, Clement K, Cacchiarelli D, Gnirke A, Michor F, Meissner A (2017) Epigenetic restriction of extraembryonic lineages mirrors the somatic transition to cancer. Nature 549:543–547

[158] Soufi A, Donahue G, Zaret KS (2012) Facilitators and impediments of the pluripotency reprogramming factors' initial engagement with the genome. Cell 151:994–1004

[159] Stewart KR, Veselovska L, Kim J, Huang J, Saadeh H, Tomizawa S, Smallwood SA, Chen T, Kelsey G (2015) Dynamic changes in histone modifications precede de novo DNA methylation in oocytes. Genes Dev 29:2449–2462

[160] Stewart KR, Veselovska L, Kelsey G (2016) Establishment and functions of DNA methylation in the germline. Epigenomics 8:1399–1413

[161] Stocking C, Kozak CA (2008) Murine endogenous retroviruses. Cell Mol Life Sci 65:3383–3398

[162] Svoboda P, Stein P, Anger M, Bernstein E, Hannon GJ, Schultz RM (2004) RNAi and expression of retrotransposons MuERV-L and IAP in pre-implantation mouse embryos. Dev Biol 269:276–285

[163] Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, Fukuda M, Takeda N, Niida H, Kato H (2002) G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev 16:1779–1791

[164] Tadros W, Lipshitz HD (2009) The maternal-to-zygotic transition: a play in two acts. Development 136:3033–3042

[165] Teperek M, Miyamoto K (2013) Nuclear reprogramming of sperm and somatic nuclei in eggs and oocytes. Reprod Med Biol 12:133–149

[166] Theunissen TW, Friedli M, He Y, Planet E, O'Neil RC, Markoulaki S, Pontis J, Wang H, Iouranova A, Imbeault M (2016) Molecular criteria for defining the naive human pluripotent state. Cell Stem Cell 19:502–515

[167] Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M (2007) Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445:214–218

[168] Tsompana M, Buck MJ (2014) Chromatin accessibility: a window into the genome. Epigenetics Chromatin 7:33

[169] van Steensel B, Belmont AS (2017) Lamina-associated domains: links with chromosome architecture, heterochromatin, and gene repression. Cell 169:780–791

[170] Vastenhouw NL, Schier AF (2012) Bivalent histone modifications in early embryogenesis. Curr Opin Cell Biol 24:374–386

[171] Vastenhouw NL, Zhang Y, Woods IG, Imam F, Regev A, Liu XS, Rinn J, Schier AF (2010) Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464:922–926

[172] Verma N, Pan H, Dore LC, Shukla A, Li QV, Pelham-Webb B, Teijeiro V, Gonzalez F, Krivtsov A, Chang CJ (2018) TET proteins safeguard bivalent promoters from de novo methylation in human embryonic stem cells. Nat Genet 50:83–95

[173] Wang H, Dey SK (2006) Roadmap to embryo implantation: clues from mouse models. Nat Rev Genet 7:185–199

[174] Wang F, Kou Z, Zhang Y, Gao S (2007) Dynamic reprogramming of histone acetylation and methylation in the first cell cycle of cloned mouse embryos. Biol Reprod 77:1007–1016

[175] Wang L, Zhang J, Duan J, Gao X, Zhu W, Lu X, Yang L, Zhang J, Li G, Ci W (2014) Programming and inheritance of parental DNA methylomes in mammals. Cell 157:979–991

[176] Wang C, Liu X, Gao Y, Yang L, Li C, Liu W, Chen C, Kou X, Zhao Y, Chen J (2018a) Reprogramming of H3K9me3-dependent heterochromatin during mammalian embryo development. Nat Cell Biol 20:620–631

[177] Wang J, Wang L, Feng G, Wang Y, Li Y, Li X, Liu C, Jiao G, Huang C, Shi J (2018b) Asymmetric expression of LincGET biases cell fate in two-cell mouse embryos. Cell 175(1887–1901):e1818

[178] Weinreb C, Rodriguez-Fraticelli A, Camargo FD, Klein AM (2020) Lineage tracing on transcriptional landscapes links state to fate during differentiation. Science.https://doi.org/10.1126/science. aaw3381

[179] Wen D, Banaszynski LA, Liu Y, Geng F, Noh KM, Xiang J, Elemento O, Rosenwaks Z, Allis CD, Rafii S (2014) Histone variant H3.3 isan essential maternal factor for oocyte reprogramming. Proc Natl Acad Sci USA 111:7325–7330

[180] Whiddon JL, Langford AT, Wong CJ, Zhong JW, Tapscott SJ (2017) Conservation and innovation in the DUX4-family gene network. Nat Genet 49:935–940

[181] White MD, Angiolini JF, Alvarez YD, Kaur G, Zhao ZW, Mocskos E, Bruno L, Bissiere S, Levi V, Plachta N (2016) Long-lived binding of Sox2 to DNA predicts cell fate in the four-cell mouse embryo. Cell 165:75–87

[182] Wu H, Zhang Y (2014) Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 156:45–68

[183] Wu X, Zhang Y (2017) TET-mediated active DNA demethylation: mechanism, function and beyond. Nat Rev Genet 18:517–534

[184] Wu Q, Bruce AW, Jedrusik A, Ellis PD, Andrews RM, Langford CF, Glover DM, Zernicka-Goetz M (2009) CARM1 is required in embryonic stem cells to maintain pluripotency and resist differentiation. Stem Cells 27:2637–2645

[185] Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329:444–448

[186] Wu J, Huang B, Chen H, Yin Q, Liu Y, Xiang Y, Zhang B, Liu B, Wang Q, Xia W (2016) The landscape of accessible chromatin in mammalian pre-implantation embryos. Nature 534:652–657

[187] Wu J, Xu J, Liu B, Yao G, Wang P, Lin Z, Huang B, Wang X, Li T, Shi S (2018) Chromatin analysis in human early development reveals epigenetic transition during ZGA. Nature 557:256–260

[188] Wu Y, Liu W, Chen J, Liu S, Wang M, Yang L, Chen C, Qi M, Xu Y, Qiao Z (2019) Nuclear exosome targeting complex core factor Zcchc8 regulates the degradation of LINE1 RNA in early embryos and embryonic stem cells. Cell Rep 29(2461–2472): e2466

[189] Xia W, Xu J, Yu G, Yao G, Xu K, Ma X, Zhang N, Liu B, Li T, Lin Z (2019) Resetting histone modifications during human parental-to-zygotic transition. Science 365:353–360

[190] Xiang Y, Zhang Y, Xu Q, Zhou C, Liu B, Du Z, Zhang K, Zhang B, Wang X, Gayen S (2020) Epigenomic analysis of gastrulation identifies a unique chromatin state for primed pluripotency. Nat Genet 52:95–105

[191] Xie B, Zhang H, Wei R, Li Q, Weng X, Kong Q, Liu Z (2016) Histone H3 lysine 27 trimethylation acts as an epigenetic barrier in porcine nuclear reprogramming. Reproduction 151:9–16

[192] Xu Q, Xie W (2018) Epigenome in early mammalian development: inheritance, reprogramming and establishment. Trends Cell Biol 28:237–253

[193] Xu Q, Xiang Y, Wang Q, Wang L, Brind'Amour J, Bogutz AB, Zhang Y, Zhang B, Yu G, Xia W (2019) SETD2 regulates the maternal epigenome, genomic imprinting and embryonic development. Nat Genet 51:844–856

[194] Yang X, Smith SL, Tian XC, Lewin HA, Renard JP, Wakayama T (2007) Nuclear reprogramming of cloned embryos and its implications for therapeutic cloning. Nat Genet 39:295–302

[195] Yang L, Song L, Liu X, Bai L, Li G (2018a) KDM6A and KDM6B play contrasting roles in nuclear transfer embryos revealed by MERVL reporter system. Embo Rep. https://doi.org/10.15252/embr. 201846240

[196] Yang X, Hu B, Hou Y, Qiao Y, Wang R, Chen Y, Qian Y, Feng S, Chen J, Liu C (2018b) Silencing of developmental genes by H3K27me3 and DNA methylation reflects the discrepant plasticity of embryonic and extraembryonic lineages. Cell Res 28:593–596

[197] Yang F, Huang X, Zang R, Chen J, Fidalgo M, Sanchez-Priego C, Yang J, Caichen A, Ma F, Macfarlan T (2020) DUX-miR-344-ZMYM2-mediated activation of MERVL LTRs induces a totipotent 2C-like state. Cell Stem Cell 26(234–250):e237

[198] Yao C, Zhang W, Shuai L (2019) The first cell fate decision in preimplantation mouse embryos. Cell Regen (Lond) 8:51–57

[199] Yeste M, Jones C, Amdani SN, Coward K (2017) Oocyte activation and fertilisation: crucial contributors from the sperm and oocyte. Results Probl Cell Differ 59:213–239

[200] Yu B, Smith TH, Battle SL, Ferrell S, Hawkins RD (2019) Superovulation alters global DNA methylation in early mouse embryo development. Epigenetics 14:780–790

[201] Zeng Y, Chen T (2019) DNA methylation reprogramming during mammalian development. Genes (Basel). https://doi.org/10.1126/science.aaw3381

[202] Zeng TB, Han L, Pierce N, Pfeifer GP, Szabo PE (2019) EHMT2 and SETDB1 protect the maternal pronucleus from 5mC oxidation. Proc Natl Acad Sci U S A 116:10834–10841

[203] Zenk F, Loeser E, Schiavo R, Kilpert F, Bogdanovic O, Iovino N (2017) Germ line-inherited H3K27me3 restricts enhancer function during maternal-to-zygotic transition. Science 357:212–216

[204] Zhang M, Wang F, Kou Z, Zhang Y, Gao S (2009) Defective chromatin structure in somatic cell cloned mouse embryos. J Biol Chem 284:24981–24987

[205] Zhang B, Zheng H, Huang B, Li W, Xiang Y, Peng X, Ming J, Wu X, Zhang Y, Xu Q (2016) Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature 537:553–557

[206] Zhang Y, Xiang Y, Yin Q, Du Z, Peng X, Wang Q, Fidalgo M, Xia W, Li Y, Zhao ZA(2018) Dynamic epigenomic landscapes during early lineage specification in mouse embryos. Nat Genet 50:96–105

[207] Zhang W, Chen F, Chen R, Xie D, Yang J, Zhao X, Guo R, Zhang Y, Shen Y, Goke J (2019) Zscan4c activates endogenous retrovirus MERVL and cleavage embryo genes. Nucleic Acids Res 47:8485–8501

[208] Zheng H, Xie W (2019) The role of 3D genome organization in development and cell differentiation. Nat Rev Mol Cell Biol 20:535–550

[209] Zheng H, Huang B, Zhang B, Xiang Y, Du Z, Xu Q, Li Y, Wang Q, Ma J, Peng X (2016) Resetting epigenetic memory by reprogramming of histone modifications in mammals. Mol Cell 63:1066–1079

[210] Zhu P, Guo H, Ren Y, Hou Y, Dong J, Li R, Lian Y, Fan X, Hu B, Gao Y (2018) Single-cell DNA methylome sequencing of human pre-implantation embryos. Nat Genet 50:12–19

RIGHTS & PERMISSIONS

2020 The Author(s) 2020