Epigenetic programming and reprogramming during development (original) (raw)

• ENCODE Project Consortium et al. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57–74 (2012).
• Thurman, R.E. et al. The accessible chromatin landscape of the human genome. Nature 489, 75–82 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Lengsfeld, B.M., Berry, K.N., Ghosh, S., Takahashi, M. & Francis, N.J. A Polycomb complex remains bound through DNA replication in the absence of other eukaryotic proteins. Sci. Rep. 2, 661 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Lo, S.M. et al. A bridging model for persistence of a polycomb group protein complex through DNA replication in vitro. Mol. Cell 46, 784–796 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Petruk, S. et al. TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell 150, 922–933 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Fisher, A.G. & Brockdorff, N. Epigenetic memory and parliamentary privilege combine to evoke discussions on inheritance. Development 139, 3891–3896 (2012).
  Article CAS PubMed Google Scholar
• Bonasio, R., Tu, S. & Reinberg, D. Molecular signals of epigenetic states. Science 330, 612–616 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Braun, R.E. Packaging paternal chromosomes with protamine. Nat. Genet. 28, 10–12 (2001).
  CAS PubMed Google Scholar
• Adenot, P.G., Mercier, Y., Renard, J.P. & Thompson, E.M. Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124, 4615–4625 (1997).
  CAS PubMed Google Scholar
• Santos, F., Peters, A.H., Otte, A.P., Reik, W. & Dean, W. Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev. Biol. 280, 225–236 (2005).
  Article CAS PubMed Google Scholar
• Sobel, R.E., Cook, R.G., Perry, C.A., Annunziato, A.T. & Allis, C.D. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl. Acad. Sci. USA 92, 1237–1241 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Erhardt, S. et al. Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development. Development 130, 4235–4248 (2003).
  Article CAS PubMed Google Scholar
• Liu, H., Kim, J.M. & Aoki, F. Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos. Development 131, 2269–2280 (2004).
  Article CAS PubMed Google Scholar
• Arney, K.L., Bao, S., Bannister, A.J., Kouzarides, T. & Surani, M.A. Histone methylation defines epigenetic asymmetry in the mouse zygote. Int. J. Dev. Biol. 46, 317–320 (2002).
  CAS PubMed Google Scholar
• Puschendorf, M. et al. PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat. Genet. 40, 411–420 (2008).
  Article CAS PubMed Google Scholar
• Kourmouli, N. et al. Heterochromatin and tri-methylated lysine 20 of histone H4 in animals. J. Cell Sci. 117, 2491–2501 (2004).
  Article CAS PubMed Google Scholar
• Daujat, S. et al. H3K64 trimethylation marks heterochromatin and is dynamically remodeled during developmental reprogramming. Nat. Struct. Mol. Biol. 16, 777–781 (2009).
  Article CAS PubMed Google Scholar
• Sarmento, O.F. et al. Dynamic alterations of specific histone modifications during early murine development. J. Cell Sci. 117, 4449–4459 (2004).
  Article CAS PubMed Google Scholar
• Lepikhov, K. & Walter, J. Differential dynamics of histone H3 methylation at positions K4 and K9 in the mouse zygote. BMC Dev. Biol. 4, 12 (2004).
  Article PubMed PubMed Central CAS Google Scholar
• Mayer, W., Niveleau, A., Walter, J., Fundele, R. & Haaf, T. Embryogenesis: demethylation of the zygotic paternal genome. Nature 403, 501–502 (2000).
  Article CAS PubMed Google Scholar
• Santos, F., Hendrich, B., Reik, W. & Dean, W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol. 241, 172–182 (2002).
  Article CAS PubMed Google Scholar
• Inoue, A. & Zhang, Y. Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 334, 194 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Smith, Z.D. et al. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339–344 (2012).This is the first base-resolution, genome-wide analysis of DNA methylation during preimplantation development.
  Article CAS PubMed PubMed Central Google Scholar
• Gill, M.E., Erkek, S. & Peters, A.H.F.M. Parental epigenetic control of embryogenesis: a balance between inheritance and reprogramming? Curr. Opin. Cell Biol. 24, 387–396 (2012).
  Article CAS PubMed Google Scholar
• Bouniol, C., Nguyen, E. & Debey, P. Endogenous transcription occurs at the 1-cell stage in the mouse embryo. Exp. Cell Res. 218, 57–62 (1995).
  Article CAS PubMed Google Scholar
• Aoki, F., Worrad, D.M. & Schultz, R.M. Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev. Biol. 181, 296–307 (1997).
  Article CAS PubMed Google Scholar
• Henery, C.C., Miranda, M., Wiekowski, M., Wilmut, I. & DePamphilis, M.L. Repression of gene expression at the beginning of mouse development. Dev. Biol. 169, 448–460 (1995).
  Article CAS PubMed Google Scholar
• Latham, K.E. & Schultz, R.M. Embryonic genome activation. Front. Biosci. 6, D748–D759 (2001).
  Article CAS PubMed Google Scholar
• Gu, T.P. et al. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477, 606–610 (2011).Work in refs. 29 and 36 demonstrates that the global replication-independent loss of 5mC in the paternal genome of the zygote is due to its oxidation into 5hmC by Tet3 enzyme.
  Article CAS PubMed Google Scholar
• Oswald, J. et al. Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10, 475–478 (2000).
  Article CAS PubMed Google Scholar
• Wossidlo, M. et al. Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes. EMBO J. 29, 1877–1888 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Tahiliani, M. et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930–935 (2009).This work identifies TET proteins as mammalian homologs of trypanosome enzymes that are capable of oxidizing 5mC into 5hmC.
  Article CAS PubMed PubMed Central Google Scholar
• He, Y.F. et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303–1307 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Ito, S. et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333, 1300–1303 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Iqbal, K., Jin, S.G., Pfeifer, G.P. & Szabo, P.E. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc. Natl. Acad. Sci. USA 108, 3642–3647 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Wossidlo, M. et al. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat. Commun. 2, 241 (2011).
  Article CAS PubMed Google Scholar
• Inoue, A., Shen, L., Dai, Q., He, C. & Zhang, Y. Generation and replication-dependent dilution of 5fC and 5caC during mouse preimplantation development. Cell Res. 21, 1670–1676 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Teperek-Tkacz, M., Pasque, V., Gentsch, G. & Ferguson-Smith, A.C. Epigenetic reprogramming: is deamination key to active DNA demethylation? Reproduction 142, 621–632 (2011).
  Article CAS PubMed Google Scholar
• Hajkova, P. et al. Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329, 78–82 (2010).
  Article CAS PubMed Google Scholar
• Chan, M.M., Smith, Z.D., Egli, D., Regev, A. & Meissner, A. Mouse ooplasm confers context-specific reprogramming capacity. Nat. Genet. 44, 978–980 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Booth, M.J. et al. Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science 336, 934–937 (2012).
  Article CAS PubMed Google Scholar
• Yu, M. et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149, 1368–1380 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Branco, M.R., Oda, M. & Reik, W. Safeguarding parental identity: Dnmt1 maintains imprints during epigenetic reprogramming in early embryogenesis. Genes Dev. 22, 1567–1571 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Hirasawa, R. et al. Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev. 22, 1607–1616 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Payer, B. et al. Stella is a maternal effect gene required for normal early development in mice. Curr. Biol. 13, 2110–2117 (2003).
  Article CAS PubMed Google Scholar
• Nakamura, T. et al. PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat. Cell Biol. 9, 64–71 (2007).
  Article CAS PubMed Google Scholar
• Nakamura, T. et al. PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 486, 415–419 (2012).This work shows that Dppa3 protects the maternal genome and genomic imprints from Tet3-mediate oxidation by binding H3K9me2.
  Article CAS PubMed Google Scholar
• Lane, N. et al. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35, 88–93 (2003).
  Article CAS PubMed Google Scholar
• Olek, A. & Walter, J. The pre-implantation ontogeny of the H19 methylation imprint. Nat. Genet. 17, 275–276 (1997).
  Article CAS PubMed Google Scholar
• Tremblay, K.D., Duran, K.L. & Bartolomei, M.S. A 5′2-kilobase-pair region of the imprinted mouse H19 gene exhibits exclusive paternal methylation throughout development. Mol. Cell Biol. 17, 4322–4329 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Pittoggi, C. et al. A fraction of mouse sperm chromatin is organized in nucleosomal hypersensitive domains enriched in retroposon DNA. J. Cell Sci. 112, 3537–3548 (1999).
  CAS PubMed Google Scholar
• Wykes, S.M. & Krawetz, S.A. The structural organization of sperm chromatin. J. Biol. Chem. 278, 29471–29477 (2003).
  Article CAS PubMed Google Scholar
• van der Heijden, G.W. et al. Sperm-derived histones contribute to zygotic chromatin in humans. BMC Dev. Biol. 8, 34 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Li, X. et al. A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev. Cell 15, 547–557 (2008).Work described in refs. 54–57 demonstrates that sequence-specific DNA-binding factors Zfp57 and Trim28 can cooperate with the histone modification system to maintain DNA methylation marks at imprinted loci, thus preventing their loss during preimplantation development.
  Article CAS PubMed PubMed Central Google Scholar
• Messerschmidt, D.M. et al. Trim28 is required for epigenetic stability during mouse oocyte to embryo transition. Science 335, 1499–1502 (2012).
  Article CAS PubMed Google Scholar
• Quenneville, S. et al. The KRAB-ZFP/KAP1 system contributes to the early embryonic establishment of site-specific DNA methylation patterns maintained during development. Cell Rep. 2, 766–773 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Quenneville, S. et al. In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Mol. Cell 44, 361–372 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Zuo, X. et al. Zinc finger protein ZFP57 requires its co-factor to recruit DNA methyltransferases and maintains DNA methylation imprint in embryonic stem cells via its transcriptional repression domain. J. Biol. Chem. 287, 2107–2118 (2012).
  Article CAS PubMed Google Scholar
• Schultz, D.C., Ayyanathan, K., Negorev, D., Maul, G.G. & Rauscher, F.J. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 16, 919–932 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Lorthongpanich, C., Doris, T.P., Limviphuvadh, V., Knowles, B.B. & Solter, D. Developmental fate and lineage commitment of singled mouse blastomeres. Development 139, 3722–3731 (2012).
  Article CAS PubMed Google Scholar
• Takaoka, K. & Hamada, H. Cell fate decisions and axis determination in the early mouse embryo. Development 139, 3–14 (2012).
  Article CAS PubMed Google Scholar
• Guo, J.U., Su, Y., Zhong, C., Ming, G.L. & Song, H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145, 423–434 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Johnson, M.H. & Ziomek, C.A. The foundation of two distinct cell lineages within the mouse morula. Cell 24, 71–80 (1981).
  Article CAS PubMed Google Scholar
• Torres-Padilla, M.E., Parfitt, D.E., Kouzarides, T. & Zernicka-Goetz, M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445, 214–218 (2007).This work shows that increasing the levels of arginine methylation in individual blastomeres from 4-cell-stage embryos results in the dramatic upregulation of Oct4 and Sox2 and directs their progeny to the inner cell mass.
  Article CAS PubMed PubMed Central Google Scholar
• Fisher, C.L. & Fisher, A.G. Chromatin states in pluripotent, differentiated, and reprogrammed cells. Curr. Opin. Genet. Dev. 21, 140–146 (2011).
  Article CAS PubMed Google Scholar
• Azuara, V. et al. Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8, 532–538 (2006).
  Article CAS PubMed Google Scholar
• Bernstein, B.E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315–326 (2006).
  Article CAS PubMed Google Scholar
• Voigt, P. et al. Asymmetrically modified nucleosomes. Cell 151, 181–193 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Margueron, R. & Reinberg, D. The Polycomb complex PRC2 and its mark in life. Nature 469, 343–349 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Ballaré, C. et al. Phf19 links methylated Lys36 of histone H3 to regulation of Polycomb activity. Nat. Struct. Mol. Biol. 19, 1257–1265 (2012).Work described in refs. 70 and 71 demonstrates that the PRC2 component Phf19 binds H3K36me2 and H3K36me3 and is required both for the deposition of H3K27me3 and the recruitment of H3K36 demethylase enzymes at Polycomb target genes.
  Article PubMed PubMed Central CAS Google Scholar
• Brien, G.L. et al. Polycomb PHF19 binds H3K36me3 and recruits PRC2 and demethylase NO66 to embryonic stem cell genes during differentiation. Nat. Struct. Mol. Biol. 19, 1273–1281 (2012).
  Article CAS PubMed Google Scholar
• Blackledge, N.P. et al. CpG islands recruit a histone H3 lysine 36 demethylase. Mol. Cell 38, 179–190 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Ku, M. et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4, e1000242 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Ohinata, Y. et al. A signaling principle for the specification of the germ cell lineage in mice. Cell 137, 571–584 (2009).
  Article CAS PubMed Google Scholar
• Hajkova, P. et al. Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452, 877–881 (2008).
  Article CAS PubMed Google Scholar
• Seki, Y. et al. Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev. Biol. 278, 440–458 (2005).
  Article CAS PubMed Google Scholar
• Mansour, A.A. et al. The H3K27 demethylase Utx regulates somatic and germ cell epigenetic reprogramming. Nature 488, 409–413 (2012).
  Article CAS PubMed Google Scholar
• Tachibana, M. et al. Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3–K9. Genes Dev. 19, 815–826 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Dong, K.B. et al. DNA methylation in ES cells requires the lysine methyltransferase G9a but not its catalytic activity. EMBO J. 27, 2691–2701 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Tachibana, M., Matsumura, Y., Fukuda, M., Kimura, H. & Shinkai, Y. G9a/GLP complexes independently mediate H3K9 and DNA methylation to silence transcription. EMBO J. 27, 2681–2690 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Kurimoto, K. et al. Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev. 22, 1617–1635 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Yamaji, M. et al. Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat. Genet. 40, 1016–1022 (2008).
  Article CAS PubMed Google Scholar
• Lee, J. et al. Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development 129, 1807–1817 (2002).
  Article CAS PubMed Google Scholar
• Sato, S., Yoshimizu, T., Sato, E. & Matsui, Y. Erasure of methylation imprinting of Igf2r during mouse primordial germ-cell development. Mol. Reprod. Dev. 65, 41–50 (2003).
  Article CAS PubMed Google Scholar
• Yamazaki, Y. et al. Adult mice cloned from migrating primordial germ cells. Proc. Natl. Acad. Sci. USA 102, 11361–11366 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Hackett, J.A. et al. Promoter DNA methylation couples genome-defence mechanisms to epigenetic reprogramming in the mouse germline. Development 139, 3623–3632 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Guibert, S., Forne, T. & Weber, M. Global profiling of DNA methylation erasure in mouse primordial germ cells. Genome Res. 22, 633–641 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Popp, C. et al. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463, 1101–1105 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Chuva de Sousa Lopes, S.M. et al. X chromosome activity in mouse XX primordial germ cells. PLoS Genet. 4, e30 (2008).
  Article PubMed PubMed Central Google Scholar
• Yamaguchi, S. et al. Tet1 controls meiosis by regulating meiotic gene expression. Nature 492, 443–447 (2012).This work shows that during PGCs development Tet1 is required for the demethylation and the consequent expression of a specific functional class of genes, which are required for meiosis.
  Article CAS PubMed PubMed Central Google Scholar
• Cortellino, S. et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146, 67–79 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Hanna, J. et al. Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 462, 595–601 (2009).Work described in refs. 92 and 93 demonstrates that reprogramming of somatic cells via the forced expression of a defined set of transcriptional factors is initially triggered by a series of stochastic (epigenetic) events that subsequently lead to the hierarchical activation of the pluripotency network.
  Article CAS PubMed PubMed Central Google Scholar
• Buganim, Y. et al. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150, 1209–1222 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Bui, H.T. et al. Effect of trichostatin A on chromatin remodeling, histone modifications, DNA replication, and transcriptional activity in cloned mouse embryos. Biol. Reprod. 83, 454–463 (2010).
  Article CAS PubMed Google Scholar
• Esteban, M.A. et al. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 6, 71–79 (2010).
  Article CAS PubMed Google Scholar
• Huangfu, D. et al. Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat. Biotechnol. 26, 795–797 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Kishigami, S. et al. Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem. Biophys. Res. Commun. 340, 183–189 (2006).
  Article CAS PubMed Google Scholar
• Liang, G., Taranova, O., Xia, K. & Zhang, Y. Butyrate promotes induced pluripotent stem cell generation. J. Biol. Chem. 285, 25516–25521 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Mali, P. et al. Butyrate greatly enhances derivation of human induced pluripotent stem cells by promoting epigenetic remodeling and the expression of pluripotency–associated genes. Stem Cells 28, 713–720 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Mikkelsen, T.S. et al. Dissecting direct reprogramming through integrative genomic analysis. Nature 454, 49–55 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Sridharan, R. et al. Role of the murine reprogramming factors in the induction of pluripotency. Cell 136, 364–377 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Ang, Y.S. et al. Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 145, 183–197 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Shi, Y. et al. Induction of pluripotent stem cells from mouse embryonic fibroblasts by Oct4 and Klf4 with small-molecule compounds. Cell Stem Cell 3, 568–574 (2008).
  Article CAS PubMed Google Scholar
• Shi, Y. et al. A combined chemical and genetic approach for the generation of induced pluripotent stem cells. Cell Stem Cell 2, 525–528 (2008).
  Article CAS PubMed Google Scholar
• Epsztejn-Litman, S. et al. De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nat. Struct. Mol. Biol. 15, 1176–1183 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Ma, D.K., Chiang, C.H., Ponnusamy, K., Ming, G.L. & Song, H. G9a and Jhdm2a regulate embryonic stem cell fusion-induced reprogramming of adult neural stem cells. Stem Cells 26, 2131–2141 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Ho, L. & Crabtree, G.R. Chromatin remodelling during development. Nature 463, 474–484 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Gaspar-Maia, A. et al. Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 460, 863–868 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Ho, L. et al. An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc. Natl. Acad. Sci. USA 106, 5187–5191 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Ho, L. et al. esBAF facilitates pluripotency by conditioning the genome for LIF/STAT3 signalling and by regulating polycomb function. Nat. Cell Biol. 13, 903–913 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Singhal, N. et al. Chromatin-remodeling components of the BAF complex facilitate reprogramming. Cell 141, 943–955 (2010).
  Article CAS PubMed Google Scholar
• Banaszynski, L.A., Allis, C.D. & Lewis, P.W. Histone variants in metazoan development. Dev. Cell 19, 662–674 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Pasque, V., Gillich, A., Garrett, N. & Gurdon, J.B. Histone variant macroH2A confers resistance to nuclear reprogramming. EMBO J. 30, 2373–2387 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Koche, R.P. et al. Reprogramming factor expression initiates widespread targeted chromatin remodeling. Cell Stem Cell 8, 96–105 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Pereira, C.F. et al. Heterokaryon-based reprogramming of human B lymphocytes for pluripotency requires Oct4 but not Sox2. PLoS Genet. 4, e1000170 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Bhutani, N. et al. Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463, 1042–1047 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Simonsson, S. & Gurdon, J. DNA demethylation is necessary for the epigenetic reprogramming of somatic cell nuclei. Nat. Cell Biol. 6, 984–990 (2004).
  Article CAS PubMed Google Scholar
• Piccolo, F.M. et al. Using heterokaryons to understand pluripotency and reprogramming. Phil. Trans. R. Soc. Lond. B 366, 2260–2265 (2011).
  Article CAS Google Scholar
• Foshay, K.M. et al. Embryonic stem cells induce pluripotency in somatic cell fusion through biphasic reprogramming. Mol. Cell 46, 159–170 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Stadtfeld, M., Maherali, N., Breault, D.T. & Hochedlinger, K. Defining molecular cornerstones during fibroblast to iPS cell reprogramming in mouse. Cell Stem Cell 2, 230–240 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Doege, C.A. et al. Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature 488, 652–655 (2012).This work shows that Tet2 is required during early phases of iPSC reprogramming for remodeling the chromatin at the promoters of key pluripotency genes in a demethylation-independent manner.
  Article CAS PubMed PubMed Central Google Scholar
• Kim, K. et al. Epigenetic memory in induced pluripotent stem cells. Nature 467, 285–290 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Hackett, J.A. et al. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science advance online publication, doi:10.1126/science.1229277 (13 December 2012).
• Takagi, N. Requirement of mitoses for the reversal of X-inactivation in cell hybrids between murine embryonal carcinoma cells and normal female thymocytes. Exp. Cell Res. 175, 363–375 (1988).
  Article CAS PubMed Google Scholar
• Gurdon, J.B. The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J. Embryol. Exp. Morphol. 10, 622–640 (1962).
  CAS PubMed Google Scholar
• Wakayama, T., Perry, A.C., Zuccotti, M., Johnson, K.R. & Yanagimachi, R. Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394, 369–374 (1998).
  Article CAS PubMed Google Scholar
• Tada, M., Takahama, Y., Abe, K., Nakatsuji, N. & Tada, T. Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells. Curr. Biol. 11, 1553–1558 (2001).
  Article CAS PubMed Google Scholar
• Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–676 (2006).
  Article CAS PubMed Google Scholar