Chromatin Control of Developmental Dynamics and Plasticity

Developmental Cell

Volumn 38, Issue 6, 2016, Pages 610-620

  Perino, Matteo ^a   Veenstra, Gert Jan C ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; CHROMATIN;

CELL LINE; CELL MATURATION; CELL PLASTICITY; CELLULAR DISTRIBUTION; CHROMATIN STRUCTURE; DEMETHYLATION; ENHANCER REGION; EPIGENETICS; GENE CONTROL; HISTONE MODIFICATION; MOLECULAR DYNAMICS; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; ZYGOTE; ANIMAL; CELL DIFFERENTIATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MOUSE; PROMOTER REGION;

ANIMALS; CELL DIFFERENTIATION; CELL PLASTICITY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; EMBRYONIC DEVELOPMENT; EPIGENOMICS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; PROMOTER REGIONS, GENETIC;

EID: 84991776572     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2016.08.004     Document Type: Review

References (99)

1. Acemel, R.D., Tena, J.J., Irastorza-Azcarate, I., Marletaz, F., Gomez-Marin, C., de la Calle-Mustienes, E., Bertrand, S., Diaz, S.G., Aldea, D., Aury, J.M., et al. A single three-dimensional chromatin compartment in amphioxus indicates a stepwise evolution of vertebrate Hox bimodal regulation. Nat. Genet. 48 (2016), 336–341.
2. Adam, R.C., Fuchs, E., The Yin and Yang of chromatin dynamics in stem cell fate selection. Trends Genet. 32 (2016), 89–100.
3. Adam, R.C., Yang, H., Rockowitz, S., Larsen, S.B., Nikolova, M., Oristian, D.S., Polak, L., Kadaja, M., Asare, A., Zheng, D., Fuchs, E., Pioneer factors govern super-enhancer dynamics in stem cell plasticity and lineage choice. Nature 521 (2015), 366–370.
4. Ahmed, K., Dehghani, H., Rugg-Gunn, P., Fussner, E., Rossant, J., Bazett-Jones, D.P., Global chromatin architecture reflects pluripotency and lineage commitment in the early mouse embryo. PLoS One, 5, 2010, e10531.
5. Ancelin, K., Syx, L., Borensztein, M., Ranisavljevic, N., Vassilev, I., Briseno-Roa, L., Liu, T., Metzger, E., Servant, N., Barillot, E., et al. Maternal LSD1/KDM1A is an essential regulator of chromatin and transcription landscapes during zygotic genome activation. Elife, 5, 2016, e08851.
6. Aoshima, K., Inoue, E., Sawa, H., Okada, Y., Paternal H3K4 methylation is required for minor zygotic gene activation and early mouse embryonic development. EMBO Rep. 16 (2015), 803–812.
7. Ausio, J., Dong, F., van Holde, K.E., Use of selectively trypsinized nucleosome core particles to analyze the role of the histone “tails” in the stabilization of the nucleosome. J. Mol. Biol. 206 (1989), 451–463.
8. Banaszynski, L.A., Wen, D., Dewell, S., Whitcomb, S.J., Lin, M., Diaz, N., Elsasser, S.J., Chapgier, A., Goldberg, A.D., Canaani, E., et al. Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells. Cell 155 (2013), 107–120.
9. Barutcu, A.R., Fritz, A.J., Zaidi, S.K., van Wijnen, A.J., Lian, J.B., Stein, J.L., Nickerson, J.A., Imbalzano, A.N., Stein, G.S., C-ing the genome: a compendium of chromosome conformation capture methods to study higher-order chromatin organization. J. Cell Physiol. 231 (2016), 31–35.
10. Bernier, M., Luo, Y., Nwokelo, K.C., Goodwin, M., Dreher, S.J., Zhang, P., Parthun, M.R., Fondufe-Mittendorf, Y., Ottesen, J.J., Poirier, M.G., Linker histone H1 and H3K56 acetylation are antagonistic regulators of nucleosome dynamics. Nat. Commun., 6, 2015, 10152.
11. Bertero, A., Madrigal, P., Galli, A., Hubner, N.C., Moreno, I., Burks, D., Brown, S., Pedersen, R.A., Gaffney, D., Mendjan, S., et al. Activin/nodal signaling and NANOG orchestrate human embryonic stem cell fate decisions by controlling the H3K4me3 chromatin mark. Genes Dev. 29 (2015), 702–717.
12. Biechele, S., Lin, C.J., Rinaudo, P.F., Ramalho-Santos, M., Unwind and transcribe: chromatin reprogramming in the early mammalian embryo. Curr. Opin. Genet. Dev. 34 (2015), 17–23.
13. Bogdanovic, O., Gomez-Skarmeta, J.L., Embryonic DNA methylation: insights from the genomics era. Brief. Funct. Genomics 13 (2014), 121–130.
14. Bogdanović, O., Smits, A.H., de la Mustienes, E., Tena, J.J., Ford, E., Williams, R., Senanayake, U., Schultz, M.D., Hontelez, S., van Kruijsbergen, I., et al. Active DNA demethylation at enhancers during the vertebrate phylotypic period. Nat. Genet. 48 (2016), 417–426.
15. Boija, A., Mannervik, M., A time of change: dynamics of chromatin and transcriptional regulation during nuclear programming in early Drosophila development. Mol. Reprod. Dev. 82 (2015), 735–746.
16. Boskovic, A., Eid, A., Pontabry, J., Ishiuchi, T., Spiegelhalter, C., Raghu Ram, E.V., Meshorer, E., Torres-Padilla, M.E., Higher chromatin mobility supports totipotency and precedes pluripotency in vivo. Genes Dev. 28 (2014), 1042–1047.
17. Buecker, C., Srinivasan, R., Wu, Z., Calo, E., Acampora, D., Faial, T., Simeone, A., Tan, M., Swigut, T., Wysocka, J., Reorganization of enhancer patterns in transition from naive to primed pluripotency. Cell Stem Cell 14 (2014), 838–853.
18. Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y., Greenleaf, W.J., Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10 (2013), 1213–1218.
19. Buenrostro, J.D., Wu, B., Litzenburger, U.M., Ruff, D., Gonzales, M.L., Snyder, M.P., Chang, H.Y., Greenleaf, W.J., Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523 (2015), 486–490.
20. Cheloufi, S., Elling, U., Hopfgartner, B., Jung, Y.L., Murn, J., Ninova, M., Hubmann, M., Badeaux, A.I., Euong Ang, C., Tenen, D., et al. The histone chaperone CAF-1 safeguards somatic cell identity. Nature 528 (2015), 218–224.
21. Chen, J., Zhang, Z., Li, L., Chen, B.C., Revyakin, A., Hajj, B., Legant, W., Dahan, M., Lionnet, T., Betzig, E., et al. Single-molecule dynamics of enhanceosome assembly in embryonic stem cells. Cell 156 (2014), 1274–1285.
22. Collart, C., Owens, N.D., Bhaw-Rosun, L., Cooper, B., De Domenico, E., Patrushev, I., Sesay, A.K., Smith, J.N., Smith, J.C., Gilchrist, M.J., High-resolution analysis of gene activity during the Xenopus mid-blastula transition. Development 141 (2014), 1927–1939.
23. Dawlaty, M.M., Breiling, A., Le, T., Barrasa, M.I., Raddatz, G., Gao, Q., Powell, B.E., Cheng, A.W., Faull, K.F., Lyko, F., Jaenisch, R., Loss of Tet enzymes compromises proper differentiation of embryonic stem cells. Dev. Cell 29 (2014), 102–111.
24. Dixon, J.R., Jung, I., Selvaraj, S., Shen, Y., Antosiewicz-Bourget, J.E., Lee, A.Y., Ye, Z., Kim, A., Rajagopal, N., Xie, W., et al. Chromatin architecture reorganization during stem cell differentiation. Nature 518 (2015), 331–336.
25. Domazet-Loso, T., Tautz, D., A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468 (2010), 815–818.
26. Domcke, S., Bardet, A.F., Adrian Ginno, P., Hartl, D., Burger, L., Schubeler, D., Competition between DNA methylation and transcription factors determines binding of NRF1. Nature 528 (2015), 575–579.
27. Dowen, J.M., Fan, Z.P., Hnisz, D., Ren, G., Abraham, B.J., Zhang, L.N., Weintraub, A.S., Schuijers, J., Lee, T.I., Zhao, K., Young, R.A., Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 159 (2014), 374–387.
28. Du, J., Johnson, L.M., Jacobsen, S.E., Patel, D.J., DNA methylation pathways and their crosstalk with histone methylation. Nat. Rev. Mol. Cell Biol. 16 (2015), 519–532.
29. Ea, V., Baudement, M.O., Lesne, A., Forne, T., Contribution of topological domains and loop formation to 3D chromatin organization. Genes 6 (2015), 734–750.
30. Ernst, J., Kellis, M., ChromHMM: automating chromatin-state discovery and characterization. Nat. Methods 9 (2012), 215–216.
31. Factor, D.C., Corradin, O., Zentner, G.E., Saiakhova, A., Song, L., Chenoweth, J.G., McKay, R.D., Crawford, G.E., Scacheri, P.C., Tesar, P.J., Epigenomic comparison reveals activation of “seed” enhancers during transition from naive to primed pluripotency. Cell Stem Cell 14 (2014), 854–863.
32. Grandy, R.A., Whitfield, T.W., Wu, H., Fitzgerald, M.P., VanOudenhove, J.J., Zaidi, S.K., Montecino, M.A., Lian, J.B., van Wijnen, A.J., Stein, J.L., Stein, G.S., Genome-wide studies reveal that H3K4me3 modification in bivalent genes is dynamically regulated during the pluripotent cell cycle and stabilized upon differentiation. Mol. Cell Biol. 36 (2015), 615–627.
33. Guo, H., Zhu, P., Yan, L., Li, R., Hu, B., Lian, Y., Yan, J., Ren, X., Lin, S., Li, J., et al. The DNA methylation landscape of human early embryos. Nature 511 (2014), 606–610.
34. Haberle, V., Li, N., Hadzhiev, Y., Plessy, C., Previti, C., Nepal, C., Gehrig, J., Dong, X., Akalin, A., Suzuki, A.M., et al. Two independent transcription initiation codes overlap on vertebrate core promoters. Nature 507 (2014), 381–385.
35. Hammoud, S.S., Nix, D.A., Zhang, H., Purwar, J., Carrell, D.T., Cairns, B.R., Distinctive chromatin in human sperm packages genes for embryo development. Nature 460 (2009), 473–478.
36. Harrison, M.M., Eisen, M.B., Transcriptional activation of the zygotic genome in Drosophila. Curr. Top. Dev. Biol. 113 (2015), 85–112.
37. Harrison, M.M., Li, X.Y., Kaplan, T., Botchan, M.R., Eisen, M.B., Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transition. PLoS Genet., 7, 2011, e1002266.
38. Heyn, P., Kircher, M., Dahl, A., Kelso, J., Tomancak, P., Kalinka, A.T., Neugebauer, K.M., The earliest transcribed zygotic genes are short, newly evolved, and different across species. Cell Rep. 6 (2014), 285–292.
39. Hontelez, S., van Kruijsbergen, I., Georgiou, G., van Heeringen, S.J., Bogdanovic, O., Lister, R., Veenstra, G.J., Embryonic transcription is controlled by maternally defined chromatin state. Nat. Commun., 6, 2015, 10148.
40. Hsu, H.T., Chen, H.M., Yang, Z., Wang, J., Lee, N.K., Burger, A., Zaret, K., Liu, T., Levine, E., Mango, S.E., TRANSCRIPTION. Recruitment of RNA polymerase II by the pioneer transcription factor PHA-4. Science 348 (2015), 1372–1376.
41. Inoue, A., Zhang, Y., Nucleosome assembly is required for nuclear pore complex assembly in mouse zygotes. Nat. Struct. Mol. Biol. 21 (2014), 609–616.
42. Jang, C.W., Shibata, Y., Starmer, J., Yee, D., Magnuson, T., Histone H3.3 maintains genome integrity during mammalian development. Genes Dev. 29 (2015), 1377–1392.
43. Ji, X., Dadon, D.B., Powell, B.E., Fan, Z.P., Borges-Rivera, D., Shachar, S., Weintraub, A.S., Hnisz, D., Pegoraro, G., Lee, T.I., et al. 3D chromosome regulatory landscape of human pluripotent cells. Cell Stem Cell 18 (2016), 262–275.
44. Jin, W., Tang, Q., Wan, M., Cui, K., Zhang, Y., Ren, G., Ni, B., Sklar, J., Przytycka, T.M., Childs, R., et al. Genome-wide detection of DNase I hypersensitive sites in single cells and FFPE tissue samples. Nature 528 (2015), 142–146.
45. Joshi, O., Wang, S.Y., Kuznetsova, T., Atlasi, Y., Peng, T., Fabre, P.J., Habibi, E., Shaik, J., Saeed, S., Handoko, L., et al. Dynamic reorganization of extremely long-range promoter-promoter interactions between two states of pluripotency. Cell Stem Cell 17 (2015), 748–757.
46. Kalinka, A.T., Varga, K.M., Gerrard, D.T., Preibisch, S., Corcoran, D.L., Jarrells, J., Ohler, U., Bergman, C.M., Tomancak, P., Gene expression divergence recapitulates the developmental hourglass model. Nature 468 (2010), 811–814.
47. Kamakaka, R.T., Biggins, S., Histone variants: deviants?. Genes Dev. 19 (2005), 295–310.
48. Kurimoto, K., Yabuta, Y., Hayashi, K., Ohta, H., Kiyonari, H., Mitani, T., Moritoki, Y., Kohri, K., Kimura, H., Yamamoto, T., et al. Quantitative dynamics of chromatin remodeling during germ cell specification from mouse embryonic stem cells. Cell Stem Cell 16 (2015), 517–532.
49. Lawrence, M., Daujat, S., Schneider, R., Lateral thinking: how histone modifications regulate gene expression. Trends Genet. 32 (2016), 42–56.
50. Lee, M.T., Bonneau, A.R., Takacs, C.M., Bazzini, A.A., DiVito, K.R., Fleming, E.S., Giraldez, A.J., Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition. Nature 503 (2013), 360–364.
51. Lee, H.J., Hore, T.A., Reik, W., Reprogramming the methylome: erasing memory and creating diversity. Cell Stem Cell 14 (2014), 710–719.
52. Lee, M.T., Bonneau, A.R., Giraldez, A.J., Zygotic genome activation during the maternal-to-zygotic transition. Annu. Rev. Cell Dev. Biol. 30 (2014), 581–613.
53. Lee, H.J., Lowdon, R.F., Maricque, B., Zhang, B., Stevens, M., Li, D., Johnson, S.L., Wang, T., Developmental enhancers revealed by extensive DNA methylome maps of zebrafish early embryos. Nat. Commun., 6, 2015, 6315.
54. Leichsenring, M., Maes, J., Mossner, R., Driever, W., Onichtchouk, D., Pou5f1 transcription factor controls zygotic gene activation in vertebrates. Science 341 (2013), 1005–1009.
55. Li, L., Lu, X., Dean, J., The maternal to zygotic transition in mammals. Mol. Aspects Med. 34 (2013), 919–938.
56. Liao, J., Karnik, R., Gu, H., Ziller, M.J., Clement, K., Tsankov, A.M., Akopian, V., Gifford, C.A., Donaghey, J., Galonska, C., et al. Targeted disruption of DNMT1, DNMT3A and DNMT3B in human embryonic stem cells. Nat. Genet. 47 (2015), 469–478.
57. Lin, C.J., Koh, F.M., Wong, P., Conti, M., Ramalho-Santos, M., Hira-mediated H3.3 incorporation is required for DNA replication and ribosomal RNA transcription in the mouse zygote. Dev. Cell 30 (2014), 268–279.
58. Loh, K.M., Ang, L.T., Zhang, J., Kumar, V., Ang, J., Auyeong, J.Q., Lee, K.L., Choo, S.H., Lim, C.Y., Nichane, M., et al. Efficient endoderm induction from human pluripotent stem cells by logically directing signals controlling lineage bifurcations. Cell Stem Cell 14 (2014), 237–252.
59. Long, H.K., Sims, D., Heger, A., Blackledge, N.P., Kutter, C., Wright, M.L., Grutzner, F., Odom, D.T., Patient, R., Ponting, C.P., Klose, R.J., Epigenetic conservation at gene regulatory elements revealed by non-methylated DNA profiling in seven vertebrates. Elife, 2, 2013, e00348.
60. Lowdon, R.F., Zhang, B., Bilenky, M., Mauro, T., Li, D., Gascard, P., Sigaroudinia, M., Farnham, P.J., Bastian, B.C., Tlsty, T.D., et al. Regulatory network decoded from epigenomes of surface ectoderm-derived cell types. Nat. Commun., 5, 2014, 5442.
61. Lu, F., Liu, Y., Inoue, A., Suzuki, T., Zhao, K., Zhang, Y., Establishing chromatin regulatory landscape during mouse preimplantation development. Cell 165 (2016), 1375–1388.
62. Lupianez, D.G., Kraft, K., Heinrich, V., Krawitz, P., Brancati, F., Klopocki, E., Horn, D., Kayserili, H., Opitz, J.M., Laxova, R., et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161 (2015), 1012–1025.
63. Macadangdang, B.R., Oberai, A., Spektor, T., Campos, O.A., Sheng, F., Carey, M.F., Vogelauer, M., Kurdistani, S.K., Evolution of histone 2A for chromatin compaction in eukaryotes. Elife, 3, 2014, e02792.
64. Maehara, K., Ohkawa, Y., Exploration of nucleosome positioning patterns in transcription factor function. Sci. Rep., 6, 2016, 19620.
65. Marks, H., Kalkan, T., Menafra, R., Denissov, S., Jones, K., Hofemeister, H., Nichols, J., Kranz, A., Stewart, A.F., Smith, A., Stunnenberg, H.G., The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149 (2012), 590–604.
66. Oldfield, A.J., Yang, P., Conway, A.E., Cinghu, S., Freudenberg, J.M., Yellaboina, S., Jothi, R., Histone-fold domain protein NF-Y promotes chromatin accessibility for cell type-specific master transcription factors. Mol. Cell 55 (2014), 708–722.
67. Owens, N.D., Blitz, I.L., Lane, M.A., Patrushev, I., Overton, J.D., Gilchrist, M.J., Cho, K.W., Khokha, M.K., Measuring absolute RNA copy numbers at high temporal resolution reveals transcriptome kinetics in development. Cell Rep. 14 (2016), 632–647.
68. Paranjpe, S.S., Veenstra, G.J., Establishing pluripotency in early development. Biochim. Biophys. Acta 1849 (2015), 626–636.
69. Pastor, W.A., Aravind, L., Rao, A., TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat. Rev. Mol. Cell Biol. 14 (2013), 341–356.
70. Paul, F., Arkin, Y., Giladi, A., Jaitin, D.A., Kenigsberg, E., Keren-Shaul, H., Winter, D., Lara-Astiaso, D., Gury, M., Weiner, A., et al. Transcriptional heterogeneity and lineage commitment in myeloid progenitors. Cell 163 (2015), 1663–1677.
71. Pombo, A., Dillon, N., Three-dimensional genome architecture: players and mechanisms. Nat. Rev. Mol. Cell Biol. 16 (2015), 245–257.
72. Pott, S., Lieb, J.D., What are super-enhancers?. Nat. Genet. 47 (2015), 8–12.
73. Pradhan, S.K., Su, T., Yen, L., Jacquet, K., Huang, C., Cote, J., Kurdistani, S.K., Carey, M.F., EP400 deposits H3.3 into promoters and enhancers during gene activation. Mol. Cell 61 (2016), 27–38.
74. Santenard, A., Ziegler-Birling, C., Koch, M., Tora, L., Bannister, A.J., Torres-Padilla, M.E., Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat. Cell Biol. 12 (2010), 853–862.
75. Schmidl, C., Rendeiro, A.F., Sheffield, N.C., Bock, C., ChIPmentation: fast, robust, low-input ChIP-seq for histones and transcription factors. Nat. Methods 12 (2015), 963–965.
76. Schoenfelder, S., Sugar, R., Dimond, A., Javierre, B.M., Armstrong, H., Mifsud, B., Dimitrova, E., Matheson, L., Tavares-Cadete, F., Furlan-Magaril, M., et al. Polycomb repressive complex PRC1 spatially constrains the mouse embryonic stem cell genome. Nat. Genet. 47 (2015), 1179–1186.
77. Sherwood, R.I., Hashimoto, T., O'Donnell, C.W., Lewis, S., Barkal, A.A., van Hoff, J.P., Karun, V., Jaakkola, T., Gifford, D.K., Discovery of directional and nondirectional pioneer transcription factors by modeling DNase profile magnitude and shape. Nat. Biotechnol. 32 (2014), 171–178.
78. Smith, Z.D., Meissner, A., DNA methylation: roles in mammalian development. Nat. Rev. Genet. 14 (2013), 204–220.
79. Soufi, A., Garcia, M.F., Jaroszewicz, A., Osman, N., Pellegrini, M., Zaret, K.S., Pioneer transcription factors target partial DNA motifs on nucleosomes to initiate reprogramming. Cell 161 (2015), 555–568.
80. Speranzini, V., Pilotto, S., Sixma, T.K., Mattevi, A., Touch, act and go: landing and operating on nucleosomes. EMBO J. 35 (2016), 376–388.
81. Stergachis, A.B., Neph, S., Reynolds, A., Humbert, R., Miller, B., Paige, S.L., Vernot, B., Cheng, J.B., Thurman, R.E., Sandstrom, R., et al. Developmental fate and cellular maturity encoded in human regulatory DNA landscapes. Cell 154 (2013), 888–903.
82. Sun, Y., Nien, C.Y., Chen, K., Liu, H.Y., Johnston, J., Zeitlinger, J., Rushlow, C., Zelda overcomes the high intrinsic nucleosome barrier at enhancers during Drosophila zygotic genome activation. Genome Res. 25 (2015), 1703–1714.
83. Tadros, W., Lipshitz, H.D., The maternal-to-zygotic transition: a play in two acts. Development 136 (2009), 3033–3042.
84. Tee, W.W., Shen, S.S., Oksuz, O., Narendra, V., Reinberg, D., Erk1/2 activity promotes chromatin features and RNAPII phosphorylation at developmental promoters in mouse ESCs. Cell 156 (2014), 678–690.
85. Therizols, P., Illingworth, R.S., Courilleau, C., Boyle, S., Wood, A.J., Bickmore, W.A., Chromatin decondensation is sufficient to alter nuclear organization in embryonic stem cells. Science 346 (2014), 1238–1242.
86. Torres-Padilla, M.E., Bannister, A.J., Hurd, P.J., Kouzarides, T., Zernicka-Goetz, M., Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int. J. Dev. Biol. 50 (2006), 455–461.
87. Towbin, B.D., Gonzalez-Aguilera, C., Sack, R., Gaidatzis, D., Kalck, V., Meister, P., Askjaer, P., Gasser, S.M., Step-wise methylation of histone H3K9 positions heterochromatin at the nuclear periphery. Cell 150 (2012), 934–947.
88. Tsankov, A.M., Gu, H., Akopian, V., Ziller, M.J., Donaghey, J., Amit, I., Gnirke, A., Meissner, A., Transcription factor binding dynamics during human ES cell differentiation. Nature 518 (2015), 344–349.
89. van der Heijden, G.W., Dieker, J.W., Derijck, A.A., Muller, S., Berden, J.H., Braat, D.D., van der Vlag, J., de Boer, P., Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech. Dev. 122 (2005), 1008–1022.
90. Vermeulen, M., Mulder, K.W., Denissov, S., Pijnappel, W.W., van Schaik, F.M., Varier, R.A., Baltissen, M.P., Stunnenberg, H.G., Mann, M., Timmers, H.T., Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131 (2007), 58–69.
91. Wani, A.H., Boettiger, A.N., Schorderet, P., Ergun, A., Munger, C., Sadreyev, R.I., Zhuang, X., Kingston, R.E., Francis, N.J., Chromatin topology is coupled to Polycomb group protein subnuclear organization. Nat. Commun., 7, 2016, 10291.
92. Weber, C.M., Henikoff, S., Histone variants: dynamic punctuation in transcription. Genes Dev. 28 (2014), 672–682.
93. White, M.D., Angiolini, J.F., Alvarez, Y.D., Kaur, G., Zhao, Z.W., Mocskos, E., Bruno, L., Bissiere, S., Levi, V., Plachta, N., Long-lived binding of Sox2 to DNA predicts cell fate in the four-cell mouse embryo. Cell 165 (2016), 75–87.
94. Whyte, W.A., Orlando, D.A., Hnisz, D., Abraham, B.J., Lin, C.Y., Kagey, M.H., Rahl, P.B., Lee, T.I., Young, R.A., Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153 (2013), 307–319.
95. Wu, J., Huang, B., Chen, H., Yin, Q., Liu, Y., Xiang, Y., Zhang, B., Liu, B., Wang, Q., Xia, W., et al. The landscape of accessible chromatin in mammalian preimplantation embryos. Nature 534 (2016), 652–657.
96. Xie, W., Schultz, M.D., Lister, R., Hou, Z., Rajagopal, N., Ray, P., Whitaker, J.W., Tian, S., Hawkins, R.D., Leung, D., et al. Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 153 (2013), 1134–1148.
97. Yang, S.M., Kim, B.J., Norwood Toro, L., Skoultchi, A.I., H1 linker histone promotes epigenetic silencing by regulating both DNA methylation and histone H3 methylation. Proc. Natl. Acad. Sci. USA 110 (2013), 1708–1713.
98. Zaret, K.S., Mango, S.E., Pioneer transcription factors, chromatin dynamics, and cell fate control. Curr. Opin. Genet. Dev. 37 (2016), 76–81.
99. Zhang, Y., Vastenhouw, N.L., Feng, J., Fu, K., Wang, C., Ge, Y., Pauli, A., van Hummelen, P., Schier, A.F., Liu, X.S., Canonical nucleosome organization at promoters forms during genome activation. Genome Res. 24 (2014), 260–266.