Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2018-0068
Animal Reproduction (AR)
Conference Paper

Epigenetic remodeling in preimplantation embryos: cows are not big mice

Pablo J. Ross, Rafael V. Sampaio

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Abstract

Epigenetic mechanisms allow the establishment and maintenance of multiple cellular phenotypes from a single genomic code. At the initiation of development, the oocyte and spermatozoa provide their fully differentiated chromatin that soon after fertilization undergo extensive remodeling, resulting in a totipotent state that can then drive cellular differentiation towards all cell types. These remodeling involves different epigenetic modifications, including DNA methylation, post-translational modifications of histones, non-coding RNAs, and large-scale chromatin conformation changes. Moreover, epigenetic remodeling is responsible for reprogramming somatic cells to totipotency upon somatic cell nuclear transfer/cloning, which is often incomplete and inefficient. Given that environmental factors, such as assisted reproductive techniques (ARTs), can affect epigenetic remodeling, there is interest in understanding the mechanisms driving these changes. We describe and discuss our current understanding of mechanisms responsible for the epigenetic remodeling that ensues during preimplantation development of mammals, presenting findings from studies of mouse embryos and when available comparing them to what is known for human and cattle embryos.

Keywords

bovine, epigenetics, embryo, preimplantation development, histone modifications, DNA methylation.

References

Abe K, Yamamoto R, Franke V, Cao M, Suzuki Y, Suzuki MG, Vlahovicek K, Svoboda P, Schultz RM, Aoki F. 2015. The first murine zygotic transcription is promiscuous and uncoupled from splicing and 3' processing. EMBO J, 34:1523-1537.

Akagi S, Matsukawa K, Mizutani E, Fukunari K, Kaneda M, Watanabe S, Takahashi S. 2011. Treatment with a histone deacetylase inhibitor after nuclear transfer improves the preimplantation development of cloned bovine embryos. J Reprod Dev, 57:120-126.

Amor DJ, Halliday J. 2008. A review of known imprinting syndromes and their association with assisted reproduction technologies. Hum Reprod, 23:2826-2834.

Ancelin K, Syx L, Borensztein M, Ranisavljevic N, Vassilev I, Briseno-Roa L, Liu T, Metzger E, Servant N, Barillot E, Chen CJ, Schule R, Heard E. 2016. Maternal LSD1/KDM1A is an essential regulator of chromatin and transcription landscapes during zygotic genome activation. Elife, 5: pii: e08851. Doi:10.7554/eLife.08851.

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, 8:pii: e1000453. Doi:10.1371/journal.pbio.1000453.

Aoshima K, Inoue E, Sawa H, Okada Y. 2015. Paternal H3K4 methylation is required for minor zygotic gene activation and early mouse embryonic development. EMBO Rep, 16:803-812.

Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG. 2006. Chromatin signatures of pluripotent cell lines. Nat Cell Biol, 8:532-538.

Bakhtari A, Ross PJ. 2014a. DPPA3 prevents cytosine hydroxymethylation of the maternal pronucleus and is required for normal development in bovine embryos. Epigenetics, 9:1271-1279.

Bakhtari A, Ross PJ. 2014b. DPPA3 prevents cytosine hydroxymethylation of the maternal pronucleus and is required for normal development in bovine embryos. Epigenetics, 9:1271-1279.

Bannister AJ, Schneider R, Kouzarides T. 2002. Histone methylation: dynamic or static? Cell, 109:801-806.

Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell, 125:315-326.

Bogliotti YS, PJ Ross. 2015. Molecular mechanisms of transcriptional and chromatin remodeling around embryonic genome activation. Anim Reprod, 12:52-61.

Bogliotti YS, Wu J, Vilarino M, Okamura D, Soto DA, Zhong C, Sakurai M, Sampaio RV, Suzuki K, Izpisua Belmonte JC, Ross PJ. 2018. Efficient derivation of stable primed pluripotent embryonic stem cells from bovine blastocysts. Proc Natl Acad Sci U S A, 115:2090-2095.

Bovine Genome Sequencing and Analysis Consortium. 2009. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science, 324:522-528.

Braude P, Bolton V, Moore S. 1988. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature, 332:459-461.

Braun RE. 2001. Packaging paternal chromosomes with protamine. Nat Genet, 28:10-12.

Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ. 2013. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods, 10:1213-1218.

Buenrostro JD, Wu B, Chang HY, Greenleaf WJ. 2015. ATAC-seq: A Method for Assaying Chromatin Accessibility Genome-Wide. Curr Protoc Mol Biol, 109:21 29 21-29.

Camous S, Kopecny V, Flechon JE. 1986. Autoradiographic detection of the earliest stage of [3H]-uridine incorporation into the cow embryo. Biol Cell, 58:195-200.

Canovas S, Cibelli JB, Ross PJ. 2012. Jumonji domain-containing protein 3 regulates histone 3 lysine 27 methylation during bovine preimplantation development. Proc Natl Acad Sci U S A, 109:2400-2405.

Chen J, Liu H, Liu J, Qi J, Wei B, Yang J, Liang H, Chen Y, Chen J, Wu Y, Guo L, Zhu J, Zhao X, Peng T, Zhang Y, Chen S, Li X, Li D, Wang T, Pei D. 2013. H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat Genet, 45:34-42.

Chung N, Bogliotti YS, Ding W, Vilarino M, Takahashi K, Chitwood JL, Schultz RM, Ross PJ. 2017. Active H3K27me3 demethylation by KDM6B is required for normal development of bovine preimplantation embryos. Epigenetics, 12:1048-1056.

Cotton AM, Avila L, Penaherrera MS, Affleck JG, Robinson WP, Brown CJ. 2009. Inactive X chromosome-specific reduction in placental DNA methylation. Hum Mol Genet, 18:3544-3552.

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.

Dahl JA, Jung I, Aanes H, Greggains GD, Manaf A, Lerdrup M, Li G, Kuan S, Li B, Lee AY, Preissl S, Jermstad I, Haugen MH, Suganthan R, Bjoras M, Hansen K, Dalen KT, Fedorcsak P, Ren B, Klungland A. 2016. Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nature, 537:548-552

Daigneault BW, Rajput S, Smith GW, Ross PJ. 2018. Embryonic POU5F1 is Required for Expanded Bovine Blastocyst Formation. Sci Rep, 8:7753. Doi: 10.1038/s41598-018-25964-x.

Daujat S, Weiss T, Mohn F, Lange UC, Ziegler-Birling C, Zeissler U, Lappe M, Schubeler D, Torres-Padilla ME, Schneider R. 2009. H3K64 trimethylation marks heterochromatin and is dynamically remodeled during developmental reprogramming. Nat Struct Mol Biol, 16:777-781.

Dobbs KB, Rodriguez M, Sudano MJ, Ortega MS, Hansen PJ. 2013. Dynamics of DNA Methylation during Early Development of the Preimplantation Bovine Embryo. PLoS ONE, 8:e66230.

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.

Flyamer IM, Gassler J, Imakaev M, Brandao HB, Ulianov SV, Abdennur N, Razin SV, Mirny LA, Tachibana-Konwalski K. 2017. Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature, 544:110-114.

Fogarty NME, McCarthy A, Snijders KE, Powell BE, Kubikova N, Blakeley P, Lea R, Elder K, Wamaitha SE, Kim D, Maciulyte V, Kleinjung J, Kim JS, Wells D, Vallier L, Bertero A, Turner JMA, Niakan KK. 2017. Genome editing reveals a role for OCT4 in human embryogenesis. Nature, 550:67-73.

Gatewood JM, Cook GR, Balhorn R, Bradbury EM, Schmid CW. 1987. Sequence-specific packaging of DNA in human sperm chromatin. Science, 236:962-964.

Gkountela S, Clark AT. 2014. A big surprise in the little zygote: the curious business of losing methylated cytosines. Cell Stem Cell, 15:393-394.

Glanzner WG, Rissi VB, de Macedo MP, Mujica LKS, Gutierrez K, Bridi A, de Souza JRM, Gonçalves PBD, Bordignon V. 2018. Histone 3 lysine 4, 9, and 27 demethylases expression profile in fertilized and cloned bovine and porcine embryos†. Biol Reprod, 98:742-751.

Golding MC, Williamson GL, Stroud TK, Westhusin ME, Long CR. 2011. Examination of DNA methyltransferase expression in cloned embryos reveals an essential role for Dnmt1 in bovine development. Mol Reprod Dev, 78:306-317.

Golding MC, Snyder M, Williamson GL, Veazey KJ, Peoples M, Pryor JH, Westhusin ME, Long CR. 2015. Histone-lysine N-methyltransferase SETDB1 is required for development of the bovine blastocyst. Theriogenology, 84:1411-1422.

Graf A, Krebs S, Zakhartchenko V, Schwalb B, Blum H, Wolf E. 2014. Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc Natl Acad Sci U S A, 111:4139-4144.

Gross DS, Garrard WT. 1988. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem, 57:159-197.

Gu T-P, Guo F, Yang H, Wu H-P, Xu G-F, Liu W, Xie Z-G, Shi L, He X, Jin S-g, Iqbal K, Shi YG, Deng Z, Szabó PE, Pfeifer GP, Li J, Xu G-L. 2011. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature, 477:606-610.

Hamatani T, Carter MG, Sharov AA, Ko MS. 2004. Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell, 6:117-131.

Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. 2009. Distinctive chromatin in human sperm packages genes for embryo development. Nature, 460:473-478.

Hellman A, Chess A. 2007. Gene body-specific methylation on the active X chromosome. Science, 315:1141-1143.

Howell CY, Bestor TH, Ding F, Latham KE, Mertineit C, Trasler JM, Chaillet JR. 2001. Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell, 104:829-838.

Huang J, Zhang H, Wang X, Dobbs KB, Yao J, Qin G, Whitworth K, Walters EM, Prather RS, Zhao J. 2015. Impairment of preimplantation porcine embryo development by histone demethylase KDM5B knockdown through disturbance of bivalent H3K4me3-H3K27me3 modifications. Biol Reprod, 92:72.

Inoue A, Zhang Y. 2011. Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science, 334:194.

Iqbal K, Jin SG, Pfeifer GP, Szabo PE. 2011. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci U S A, 108:3642-3647.

Jarrell VL, Day BN, Prather RS. 1991. The transition from maternal to zygotic control of development occurs during the 4-cell stage in the domestic pig, Sus scrofa: quantitative and qualitative aspects of protein synthesis. Biol Reprod, 44:62-68.

Jiang Z, Sun J, Dong H, Luo O, Zheng X, Obergfell C, Tang Y, Bi J, O'Neill R, Ruan Y, Chen J, Tian XC. 2014. Transcriptional profiles of bovine in vivo pre-implantation development. BMC Genomics, 15:756.

Kishigami S, Mizutani E, Ohta H, Hikichi T, Thuan NV, Wakayama S, Bui H-T, Wakayama T. 2006. Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem Biophys Res Commun, 340:183-189.

Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, Yayoi O, Sato S, Nakabayashi K, Hata K, Sotomaru Y, Suzuki Y, Kono T. 2012. Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS genetics, 8:e1002440.

Kopecny V. 1989. High-resolution autoradiographic studies of comparative nucleologenesis and genome reactivation during early embryogenesis in pig, man and cattle. Reprod Nutr Dev, 29:589-600.

Kornberg RD. 1974. Chromatin structure: a repeating unit of histones and DNA. Science, 184:868-871.

Kouzarides T. 2007. Chromatin modifications and their function. Cell, 128:693-705.

Lara-Astiaso D, Weiner A, Lorenzo-Vivas E, Zaretsky I, Jaitin DA, David E, Keren-Shaul H, Mildner A, Winter D, Jung S, Friedman N, Amit I. 2014. Immunogenetics. Chromatin state dynamics during blood formation. Science, 345:943-949.

Lavin Y, Winter D, Blecher-Gonen R, David E, Keren-Shaul H, Merad M, Jung S, Amit I. 2014. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell, 159:1312-1326.

Lepikhov K, Zakhartchenko V, Hao R, Yang F, Wrenzycki C, Niemann H, Wolf E, Walter J. 2008. Evidence for conserved DNA and histone H3 methylation reprogramming in mouse, bovine and rabbit zygotes. Epigenetics Chromatin, 1:8.

Li E, Bestor TH, Jaenisch R. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell, 69:915-926.

Li Q, Lian S, Dai Z, Xiang Q, Dai X. 2013. BGDB: a database of bivalent genes. Database (Oxford), 2013:bat057. Doi: 10.1093/database/bat057.

Liu X, Wang C, Liu W, Li J, Li C, Kou X, Chen J, Zhao Y, Gao H, Wang H, Zhang Y, Gao Y, Gao S. 2016. Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature, 537:558-562.

Liu X, Wang Y, Gao Y, Su J, Zhang J, Xing X, Zhou C, Yao K, An Q, Zhang Y. 2018a. H3K9 demethylase KDM4E is an epigenetic regulator for bovine embryonic development and a defective factor for nuclear reprogramming. Development, 145:dev158261.

Liu Z, Cai Y, Wang Y, Nie Y, Zhang C, Xu Y, Zhang X, Lu Y, Wang Z, Poo M, Sun Q. 2018b. Cloning of Macaque Monkeys by Somatic Cell Nuclear Transfer. Cell, 172:881-887 e887.

Long CR, Westhusin ME, Golding MC. 2014. Reshaping the transcriptional frontier: epigenetics and somatic cell nuclear transfer. Mol Reprod Dev, 81:183-193.

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.

Luger K, Richmond TJ. 1998. The histone tails of the nucleosome. Curr Opin Genet Dev, 8:140-146.

Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury WJ, 3rd, Voigt P, Martin SR, Taylor WR, De Marco V, Pirrotta V, Reinberg D, Gamblin SJ. 2009. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature, 461:762-767.

Martinez-Diaz MA, Che L, Albornoz M, Seneda MM, Collis D, Coutinho ARS, El-Beirouthi N, Laurin D, Zhao X, Bordignon V. 2010. Pre- and postimplantation development of swine-cloned embryos derived from fibroblasts and bone marrow cells after inhibition of histone deacetylases. Cell Reprogram, 12:85-94.

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.

Mayer W, Niveleau A, Walter J, Fundele R, Haaf T. 2000. Demethylation of the zygotic paternal genome. Nature, 403:501-502.

McGraw S, Vigneault C, Sirard MA. 2007. Temporal expression of factors involved in chromatin remodeling and in gene regulation during early bovine in vitro embryo development. Reproduction, 133:597-608.

Memili E, Dominko T, First NL. 1998. Onset of transcription in bovine oocytes and preimplantation embryos. Mol Reprod Dev, 51:36-41.

Memili E, First NL. 2000. Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote, 8:87-96.

Messerschmidt DM. 2012. Should I stay or should I go: protection and maintenance of DNA methylation at imprinted genes. Epigenetics, 7:969-975.

Messerschmidt DM, de Vries W, Ito M, Solter D, Ferguson-Smith A, Knowles BB. 2012. Trim28 is required for epigenetic stability during mouse oocyte to embryo transition. Science, 335:1499-1502.

Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature, 448:553-560.

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.

Nelissen ECM, Dumoulin JCM, Busato F, Ponger L, Eijssen LM, Evers JLH, Tost J, van Montfoort APA. 2014. Altered gene expression in human placentas after IVF/ICSI. Hum Reprod, 29:2821-2831.

Ng RK, Gurdon JB. 2014. Maintenance of Epigenetic Memory in Cloned Embryos. Cell Cycle, 4:760-763.

O'Doherty AM, O'Shea LC, Fair T. 2012. Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins. Biol Reprod, 86:67.

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

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.

Pan G, Tian S, Nie J, Yang C, Ruotti V, Wei H, Jonsdottir GA, Stewart R, Thomson JA. 2007. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell, 1:299-312.

Payer B, Saitou M, Barton SC, Thresher R, Dixon JP, Zahn D, Colledge WH, Carlton MB, Nakano T, Surani MA. 2003. Stella is a maternal effect gene required for normal early development in mice. Curr Biol, 13:2110-2117.

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.

Reik W, Dean W, Walter J. 2001. Epigenetic reprogramming in mammalian development. Science, 293:1089-1093.

Ross PJ, Ragina NP, Rodriguez RM, Iager AE, Siripattarapravat K, Lopez-Corrales N, Cibelli JB. 2008. Polycomb gene expression and histone H3 lysine 27 trimethylation changes during bovine preimplantation development. Reproduction, 136:777-785.

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.

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.

Sangalli JR, De Bem THC, Perecin F, Chiaratti MR, Oliveira LdJ, de Araújo RR, Valim Pimentel JR, Smith LC, Meirelles FV. 2012. Treatment of nuclear-donor cells or cloned zygotes with chromatin-modifying agents increases histone acetylation but does not improve full-term development of cloned cattle. Cell Reprogram, 14:235-247.

Sangalli JR, Chiaratti MR, De Bem THC, De Araújo RR, Bressan FF, Sampaio RV, Perecin F, Smith LC, King WA, Meirelles FV. 2014. Development to term of cloned cattle derived from donor cells treated with valproic acid. PLoS ONE, 9:e101022.

Santos FT, Zakhartchenko V, Stojkovic M, Peters A, Jenuwein T, Wolf E, Reik W, Dean W, Discussion R. 2003. Epigenetic Marking Correlates with Developmental Potential in Cloned Bovine Preimplantation Embryos tween epigenetic marks and developmental potential of cloned embryos. Curr Biol, 13:1116-1121.

Schep AN, Buenrostro JD, Denny SK, Schwartz K, Sherlock G, Greenleaf WJ. 2015. Structured nucleosome fingerprints enable high-resolution mapping of chromatin architecture within regulatory regions. Genome Res, 25:1757-1770.

Schroeder DL, Jayashankar K, Douglas KC, hirkill TL, York D, Dikinson PJ, Williams LE, Samollow PB, Ross PJ, Bannasch DL, Douglas GC, LaSalle JM. 2015. Early developmental and evolutionary origins of gene body DNA methylation patterns in mammalian placentas. PLoS Genet, 11(8):e1005442.

Schultz RM. 1993. Regulation of zygotic gene activation in the mouse. Bioessays, 15:531-538.

Schultz MD, He Y, Whitaker JW, Hariharan M, Mukamel EA, Leung D, Rajagopal N, Nery JR, Urich MA, Chen H, Lin S, Lin Y, Jung I, Schmitt AD, Selvaraj S, Ren B, Sejnowski TJ, Wang W, Ecker JR. 2015. Human body epigenome maps reveal noncanonical DNA methylation variation. Nature, 523:212-216.

Sharov AA, Ko MS. 2007. Human ES cell profiling broadens the reach of bivalent domains. Cell Stem Cell, 1:237-238.

Siklenka K, Erkek S, Godmann M, Lambrot R, McGraw S, Lafleur C, Cohen T, Xia J, Suderman M, Hallett M, Trasler J, Peters AH, Kimmins S. 2015. Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science, 350:aab2006.

Simmet K, Zakhartchenko V, Philippou-Massier J, Blum H, Klymiuk N, Wolf E. 2018. OCT4/POU5F1 is required for NANOG expression in bovine blastocysts. Proc Natl Acad Sci U S A, 115:2770-2775.

Simonsson S, Gurdon J. 2004. DNA demethylation is necessary for the epigenetic reprogramming of somatic cell nuclei. Nat Cell Biol, 6:984-990.

Smith LC, Suzuki J, Goff aK, Filion F, Therrien J, Murphy BD, Kohan-Ghadr HR, Lefebvre R, Brisville aC, Buczinski S, Fecteau G, Perecin F, Meirelles FV. 2012. Developmental and epigenetic anomalies in cloned cattle. Reprod Domest Anim, 47(Suppl 4):107-114.

Smith LC, Therrien J, Filion F, Bressan F, Meirelles FV. 2015. Epigenetic consequences of artificial reproductive technologies to the bovine imprinted genes SNRPN, H19/IGF2, and IGF2R. Frontiers in Genetics, 6:58. Doi: 10.3389/fgene.2015.00058.

Tadros W, Lipshitz HD. 2009. The maternal-to-zygotic transition: a play in two acts. Development, 136:3033-3042.

Tee WW, Reinberg D. 2014. Chromatin features and the epigenetic regulation of pluripotency states in ESCs. Development, 141:2376-2390.

Thelie A, Papillier P, Pennetier S, Perreau C, Traverso JM, Uzbekova S, Mermillod P, Joly C, Humblot P, Dalbies-Tran R. 2007. Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev Biol, 7:125.

van der Heijden GW, van den Berg IM, Baart EB, Derijck AA, Martini E, de Boer P. 2009. Parental origin of chromatin in human monopronuclear zygotes revealed by asymmetric histone methylation patterns, differs between IVF and ICSI. Mol Reprod Dev, 76:101-108.

Viuff D, Avery B, Greve T, King WA, Hyttel P. 1996. Transcriptional activity in in vitro produced bovine two- and four-cell embryos. Mol Reprod Dev, 43:171-179.

Wang J, Zhang M, Zhang Y, Kou Z, Han Z, Chen DY, Sun QY, Gao S. 2010. The histone demethylase JMJD2C is stage-specifically expressed in preimplantation mouse embryos and is required for embryonic development. Biol Reprod, 82:105-111.

Wongtawan T, Taylor JE, Lawson KA, Wilmut I, Pennings S. 2011. Histone H4K20me3 and HP1alpha are late heterochromatin markers in development, but present in undifferentiated embryonic stem cells. J Cell Sci, 124:1878-1890.

Wossidlo M, Nakamura T, Lepikhov K, Marques CJ, Zakhartchenko V, Boiani M, Arand J, Nakano T, Reik W, Walter J. 2011. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun, 2:241.

Wu J, Huang B, Chen H, Yin Q, Liu Y, Xiang Y, Zhang B, Liu B, Wang Q, Xia W, Li W, Li Y, Ma J, Peng X, Zheng H, Ming J, Zhang W, Zhang J, Tian G, Xu F, Chang Z, Na J, Yang X, Xie W. 2016. The landscape of accessible chromatin in mammalian preimplantation embryos. Nature, 534:652-657.

Young LE, Sinclair KD, Wilmut I. 1998. Large offspring syndrome in cattle and sheep. Rev Reprod, 3:155-163.

Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG, Carolan C, Broadbent PJ, Robinson JJ, Wilmut I, Sinclair KD. 2001. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet, 27:153-154.

Zhang B, Zheng H, Huang B, Li W, Xiang Y, Peng X, Ming J, Wu X, Zhang Y, Xu Q, Liu W, Kou X, Zhao Y, He W, Li C, Chen B, Li Y, Wang Q, Ma J, Yin Q, Kee K, Meng A, Gao S, Xu F, Na J, Xie W. 2016a. Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature, 537:553-557.

Zhang S, Wang F, Fan C, Tang B, Zhang X, Li Z. 2016b. Dynamic changes of histone H3 lysine 9 following trimethylation in bovine oocytes and pre-implantation embryos. Biotechnol Lett, 38:395-402.

Zhang J, Qu P, Zhou C, Liu X, Ma X, Wang M, Wang Y, Su J, Liu J, Zhang Y. 2017. MicroRNA-125b is a key epigenetic regulatory factor that promotes nuclear transfer reprogramming. J Biol Chem, 292:15916-15926.

Zhao J, Ross JW, Hao Y, Spate LD, Walters EM, Samuel MS, Rieke A, Murphy CN, Prather RS. 2009. Significant improvement in cloning efficiency of an inbred miniature pig by histone deacetylase inhibitor treatment after somatic cell nuclear transfer. Biol Reprod, 81:525-530.

Zhou LQ, Dean J. 2015. Reprogramming the genome to totipotency in mouse embryos. Trends Cell Biol, 25:82-91.

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