Reprogramming of cell fate: Epigenetic memory and the erasure of memories past

EMBO Journal

Volumn 34, Issue 10, 2015, Pages 1296-1308

  Nashun, Buhe ^a   Hill, Peter W S ^a   Hajkova, Petra ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

cell fate; chromatin; induced pluripotent stem cells; reprogramming; transcription factors

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; CHAPERONE; DNA METHYLTRANSFERASE; HISTONE; PROTEIN VARIANT; TRANSCRIPTION FACTOR; CHROMATIN;

CELL DIVISION; CELL FATE; CHROMATIN STRUCTURE; DNA MODIFICATION; DNA REPLICATION; ENZYME ACTIVITY; EPIGENETICS; HISTONE MODIFICATION; HUMAN; NUCLEAR REPROGRAMMING; OXIDATION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVIEW; CELL DIFFERENTIATION; CHROMATIN; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGY;

CELL DIFFERENTIATION; CHROMATIN; EPIGENESIS, GENETIC; HUMANS; INDUCED PLURIPOTENT STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84929191955     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201490649     Document Type: Review

References (124)

1. Adachi K, Scholer HR, (2012) Directing reprogramming to pluripotency by transcription factors. Curr Opin Genet Dev 22: 416-422
2. Alabert C, Groth A, (2012) Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol 13: 153-167
3. Ancelin K, Lange UC, Hajkova P, Schneider R, Bannister AJ, Kouzarides T, Surani MA, (2006) Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat Cell Biol 8: 623-630
4. Ang YS, Tsai SY, Lee DF, Monk J, Su J, Ratnakumar K, Ding J, Ge Y, Darr H, Chang B, Wang J, Rendl M, Bernstein E, Schaniel C, Lemischka IR, (2011) Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 145: 183-197
5. Apostolou E, Hochedlinger K, (2013) Chromatin dynamics during cellular reprogramming. Nature 502: 462-471
6. Banaszynski LA, Wen D, Dewell S, Whitcomb SJ, Lin M, Diaz N, Elsasser SJ, Chapgier A, Goldberg AD, Canaani E, Rafii S, Zheng D, Allis CD, (2013) Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells. Cell 155: 107-120
7. Banath JP, Banuelos CA, Klokov D, MacPhail SM, Lansdorp PM, Olive PL, (2009) Explanation for excessive DNA single-strand breaks and endogenous repair foci in pluripotent mouse embryonic stem cells. Exp Cell Res 315: 1505-1520
8. Barrero MJ, Sese B, Kuebler B, Bilic J, Boue S, Marti M, Izpisua Belmonte JC, (2013) Macrohistone variants preserve cell identity by preventing the gain of H3K4me2 during reprogramming to pluripotency. Cell Rep 3: 1005-1011
9. Bonenfant D, Towbin H, Coulot M, Schindler P, Mueller DR, van Oostrum J, (2007) Analysis of dynamic changes in post-translational modifications of human histones during cell cycle by mass spectrometry. Mol Cell Proteomics 6: 1917-1932
10. Brambrink T, Foreman R, Welstead GG, Lengner CJ, Wernig M, Suh H, Jaenisch R, (2008) Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell 2: 151-159
11. Braunschweig U, Hogan GJ, Pagie L, van Steensel B, (2009) Histone H1 binding is inhibited by histone variant H3.3. EMBO J 28: 3635-3645
12. Buganim Y, Faddah DA, Cheng AW, Itskovich E, Markoulaki S, Ganz K, Klemm SL, van Oudenaarden A, Jaenisch R, (2012) Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150: 1209-1222
13. Burgess RJ, Zhang Z, (2013) Histone chaperones in nucleosome assembly and human disease. Nat Struct Mol Biol 20: 14-22
14. Cahan P, Li H, Morris SA, Lummertz da Rocha E, Daley GQ, Collins JJ, (2014) Cell Net: network biology applied to stem cell engineering. Cell 158: 903-915
15. Chang CC, Gao S, Sung LY, Corry GN, Ma Y, Nagy ZP, Tian XC, Rasmussen TP, (2010) Rapid elimination of the histone variant MacroH2A from somatic cell heterochromatin after nuclear transfer. Cell Reprogram 12: 43-53
16. Chen J, Guo L, Zhang L, Wu H, Yang J, Liu H, Wang X, Hu X, Gu T, Zhou Z, Liu J, Liu J, Wu H, Mao SQ, Mo K, Li Y, Lai K, Qi J, Yao H, Pan G, et al, (2013a) Vitamin C modulates TET1 function during somatic cell reprogramming. Nat Genet 45: 1504-1509
17. 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, (2013b) H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat Genet 45: 34-42
18. Costa Y, Ding J, Theunissen TW, Faiola F, Hore TA, Shliaha PV, Fidalgo M, Saunders A, Lawrence M, Dietmann S, Das S, Levasseur DN, Li Z, Xu M, Reik W, Silva JC, Wang J, (2013) NANOG-dependent function of TET1 and TET2 in establishment of pluripotency. Nature 495: 370-374
19. Creppe C, Janich P, Cantarino N, Noguera M, Valero V, Musulen E, Douet J, Posavec M, Martin-Caballero J, Sumoy L, Di Croce L, Benitah SA, Buschbeck M, (2012) MacroH2A1 regulates the balance between self-renewal and differentiation commitment in embryonic and adult stem cells. Mol Cell Biol 32: 1442-1452
20. Davidson EH, Erwin DH, (2006) Gene regulatory networks and the evolution of animal body plans. Science 311: 796-800
21. Davis RL, Weintraub H, Lassar AB, (1987) Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51: 987-1000
22. Doege CA, Inoue K, Yamashita T, Rhee DB, Travis S, Fujita R, Guarnieri P, Bhagat G, Vanti WB, Shih A, Levine RL, Nik S, Chen EI, Abeliovich A, (2012) Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature 488: 652-655
23. Drouin J, (2014) Minireview: pioneer transcription factors in cell fate specification. Mol Endocrinol 28: 989-998
24. Feldmann A, Ivanek R, Murr R, Gaidatzis D, Burger L, Schubeler D, (2013) Transcription factor occupancy can mediate active turnover of DNA methylation at regulatory regions. PLoS Genet 9: e1003994
25. Ficz G, Hore TA, Santos F, Lee HJ, Dean W, Arand J, Krueger F, Oxley D, Paul YL, Walter J, Cook SJ, Andrews S, Branco MR, Reik W, (2013) FGF signaling inhibition in ESCs drives rapid genome-wide demethylation to the epigenetic ground state of pluripotency. Cell Stem Cell 13: 351-359
26. Fragola G, Germain PL, Laise P, Cuomo A, Blasimme A, Gross F, Signaroldi E, Bucci G, Sommer C, Pruneri G, Mazzarol G, Bonaldi T, Mostoslavsky G, Casola S, Testa G, (2013) Cell reprogramming requires silencing of a core subset of polycomb targets. PLoS Genet 9: e1003292
27. Gao YW, Chen JY, Li K, Wu T, Huang B, Liu WQ, Kou XC, Zhang Y, Huang H, Jiang YH, Yao C, Liu XL, Lu ZW, Xu ZJ, Kang L, Chen J, Wang HL, Cai T, Gao SR, (2013) Replacement of Oct4 by Tet1 during iPSC induction reveals an important role of DNA methylation and hydroxymethylation in reprogramming. Cell Stem Cell 12: 453-469
28. Gaspar-Maia A, Alajem A, Polesso F, Sridharan R, Mason MJ, Heidersbach A, Ramalho-Santos J, McManus MT, Plath K, Meshorer E, Ramalho-Santos M, (2009) Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 460: 863-868
29. Gaspar-Maia A, Qadeer ZA, Hasson D, Ratnakumar K, Leu NA, Leroy G, Liu S, Costanzi C, Valle-Garcia D, Schaniel C, Lemischka I, Garcia B, Pehrson JR, Bernstein E, (2013) MacroH2A histone variants act as a barrier upon reprogramming towards pluripotency. Nat Commun 4: 1565
30. Gifford CA, Ziller MJ, Gu HC, Trapnell C, Donaghey J, Tsankov A, Shalek AK, Kelley DR, Shishkin AA, Issner R, Zhang XL, Coyne M, Fostel JL, Holmes L, Meldrim J, Guttman M, Epstein C, Park H, Kohlbacher O, Rinn J, et al, (2013) Transcriptional and epigenetic dynamics during specification of human embryonic stem cells. Cell 153: 1149-1163
31. Goldberg AD, Allis CD, Bernstein E, (2007) Epigenetics: a landscape takes shape. Cell 128: 635-638
32. Gonzalez-Munoz E, Arboleda-Estudillo Y, Otu HH, Cibelli JB, (2014) Cell reprogramming. Histone chaperone ASF1A is required for maintenance of pluripotency and cellular reprogramming. Science 345: 822-825
33. Graf T, Enver T, (2009) Forcing cells to change lineages. Nature 462: 587-594
34. Gu TP, Guo F, Yang H, Wu HP, Xu GF, Liu W, Xie ZG, Shi LY, He XY, Jin SG, Iqbal K, Shi YJG, Deng ZX, Szabo PE, Pfeifer GP, Li JS, Xu GL, (2011) The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477: 606-610
35. Guo H, Zhu P, Yan L, Li R, Hu B, Lian Y, Yan J, Ren X, Lin S, Li J, Jin X, Shi X, Liu P, Wang X, Wang W, Wei Y, Li X, Guo F, Wu X, Fan X, et al, (2014) The DNA methylation landscape of human early embryos. Nature 511: 606-610
36. Gurdon JB, Elsdale TR, Fischberg M, (1958) Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 182: 64-65
37. Gurdon JB, (1960) The developmental capacity of nuclei taken from differentiating endoderm cells of Xenopus laevis. J Embryol Exp Morphol 8: 505-526
38. Gurdon JB, (1962) The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J Embryol Exp Morphol 10: 622-640
39. Habibi E, Brinkman AB, Arand J, Kroeze LI, Kerstens HH, Matarese F, Lepikhov K, Gut M, Brun-Heath I, Hubner NC, Benedetti R, Altucci L, Jansen JH, Walter J, Gut IG, Marks H, Stunnenberg HG, (2013) Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells. Cell Stem Cell 13: 360-369
40. Hanna J, Saha K, Pando B, van Zon J, Lengner CJ, Creyghton MP, van Oudenaarden A, Jaenisch R, (2009) Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 462: 595-601
41. Hayakawa K, Ohgane J, Tanaka S, Yagi S, Shiota K, (2012) Oocyte-specific linker histone H1foo is an epigenomic modulator that decondenses chromatin and impairs pluripotency. Epigenetics 7: 1029-1036
42. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang QY, Ding JP, Jia YY, Chen ZC, Li L, Sun Y, Li XX, Dai Q, Song CX, Zhang KL, He C, Xu GL, (2011) Tet-Mediated Formation of 5-Carboxylcytosine and Its Excision by TDG in Mammalian DNA. Science 333: 1303-1307
43. Hill PW, Amouroux R, Hajkova P, (2014) DNA demethylation, Tet proteins and 5-hydroxymethylcytosine in epigenetic reprogramming: an emerging complex story. Genomics 104: 324-333
44. Ho L, Jothi R, Ronan JL, Cui K, Zhao K, Crabtree GR, (2009a) 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
45. Ho L, Ronan JL, Wu J, Staahl BT, Chen L, Kuo A, Lessard J, Nesvizhskii AI, Ranish J, Crabtree GR, (2009b) An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc Natl Acad Sci USA 106: 5181-5186
46. Ho L, Miller EL, Ronan JL, Ho WQ, Jothi R, Crabtree GR, (2011) esBAF facilitates pluripotency by conditioning the genome for LIF/STAT3 signalling and by regulating polycomb function. Nat Cell Biol 13: 903-913
47. Ho JW, Jung YL, Liu T, Alver BH, Lee S, Ikegami K, Sohn KA, Minoda A, Tolstorukov MY, Appert A, Parker SC, Gu T, Kundaje A, Riddle NC, Bishop E, Egelhofer TA, Hu SS, Alekseyenko AA, Rechtsteiner A, Asker D, et al, (2014) Comparative analysis of metazoan chromatin organization. Nature 512: 449-452
48. Hou P, Li Y, Zhang X, Liu C, Guan J, Li H, Zhao T, Ye J, Yang W, Liu K, Ge J, Xu J, Zhang Q, Zhao Y, Deng H, (2013) Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science 341: 651-654
49. Hu X, Zhang L, Mao SQ, Li Z, Chen JK, Zhang RR, Wu HP, Gao J, Guo F, Liu W, Xu GF, Dai HQ, Shi YG, Li XL, Hu BQ, Tang FC, Pei DQ, Xu GL, (2014) Tet and TDG mediate DNA demethylation essential for mesenchymal-to-epithelial transition in somatic cell reprogramming. Cell Stem Cell 14: 512-522
50. Hussein SM, Puri MC, Tonge PD, Benevento M, Corso AJ, Clancy JL, Mosbergen R, Li M, Lee DS, Cloonan N, Wood DL, Munoz J, Middleton R, Korn O, Patel HR, White CA, Shin JY, Gauthier ME, Le Cao KA, Kim JI, et al, (2014) Genome-wide characterization of the routes to pluripotency. Nature 516: 198-206
51. Inoue A, Zhang Y, (2014) Nucleosome assembly is required for nuclear pore complex assembly in mouse zygotes. Nat Struct Mol Biol 21: 609-616
52. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y, (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333: 1300-1303
53. Jost D, (2014) Bifurcation in epigenetics: implications in development, proliferation, and diseases. Phys Rev E Stat Nonlin Soft Matter Phys 89: 010701
54. Jullien J, Astrand C, Szenker E, Garrett N, Almouzni G, Gurdon JB, (2012) HIRA dependent H3.3 deposition is required for transcriptional reprogramming following nuclear transfer to Xenopus oocytes. Epigenet Chromatin 5: 17-26
55. Kaji K, Caballero IM, MacLeod R, Nichols J, Wilson VA, Hendrich B, (2006) The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat Cell Biol 8: 285-292
56. Klose RJ, Kallin EM, Zhang Y, (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7: 715-727
57. Koche RP, Smith ZD, Adli M, Gu H, Ku M, Gnirke A, Bernstein BE, Meissner A, (2011) Reprogramming factor expression initiates widespread targeted chromatin remodeling. Cell Stem Cell 8: 96-105
58. Leitch HG, McEwen KR, Turp A, Encheva V, Carroll T, Grabole N, Mansfield W, Nashun B, Knezovich JG, Smith A, Surani MA, Hajkova P, (2013) Naive pluripotency is associated with global DNA hypomethylation. Nat Struct Mol Biol 20: 311-316
59. Liang G, He J, Zhang Y, (2012) Kdm2b promotes induced pluripotent stem cell generation by facilitating gene activation early in reprogramming. Nat Cell Biol 14: 457-466
60. Lin CJ, Conti M, Ramalho-Santos M, (2013) Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development. Development 140: 3624-3634
61. Lin CJ, Koh FM, Wong P, Conti M, Ramalho-Santos M, (2014) Hira-mediated H3.3 incorporation is required for DNA replication and ribosomal RNA transcription in the mouse zygote. Dev Cell 30: 268-279
62. Lister R, Pelizzola M, Kida YS, Hawkins RD, Nery JR, Hon G, Antosiewicz-Bourget J, O'Malley R, Castanon R, Klugman S, Downes M, Yu R, Stewart R, Ren B, Thomson JA, Evans RM, Ecker JR, (2011) Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471: 68-73
63. Luo M, Ling T, Xie W, Sun H, Zhou Y, Zhu Q, Shen M, Zong L, Lyu G, Zhao Y, Ye T, Gu J, Tao W, Lu Z, Grummt I, (2013) NuRD blocks reprogramming of mouse somatic cells into pluripotent stem cells. Stem Cells 31: 1278-1286
64. Ma DK, Chiang CH, Ponnusamy K, Ming GL, Song H, (2008) G9a and Jhdm2a regulate embryonic stem cell fusion-induced reprogramming of adult neural stem cells. Stem Cells 26: 2131-2141
65. Ma H, Morey R, O'Neil RC, He Y, Daughtry B, Schultz MD, Hariharan M, Nery JR, Castanon R, Sabatini K, Thiagarajan RD, Tachibana M, Kang E, Tippner-Hedges R, Ahmed R, Gutierrez NM, Van Dyken C, Polat A, Sugawara A, Sparman M, et al, (2014) Abnormalities in human pluripotent cells due to reprogramming mechanisms. Nature 511: 177-183
66. MacAlpine DM, Almouzni G, (2013) Chromatin and DNA replication. Cold Spring Harb Perspect Biol 5: a010207
67. Magnani L, Eeckhoute J, Lupien M, (2011) Pioneer factors: directing transcriptional regulators within the chromatin environment. Trends Genet 27: 465-474
68. Mal A, Harter ML, (2003) MyoD is functionally linked to the silencing of a muscle-specific regulatory gene prior to skeletal myogenesis. Proc Natl Acad Sci USA 100: 1735-1739
69. Mansour AA, Gafni O, Weinberger L, Zviran A, Ayyash M, Rais Y, Krupalnik V, Zerbib M, Amann-Zalcenstein D, Maza I, Geula S, Viukov S, Holtzman L, Pribluda A, Canaani E, Horn-Saban S, Amit I, Novershtern N, Hanna JH, (2012) The H3K27 demethylase Utx regulates somatic and germ cell epigenetic reprogramming. Nature 488: 409-413
70. Matoba S, Liu Y, Lu F, Iwabuchi Kumiko A, Shen L, Inoue A, Zhang Y, (2014) Embryonic Development following Somatic Cell Nuclear Transfer Impeded by Persisting Histone Methylation. Cell 159: 884-895
71. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T, (2000) Demethylation of the zygotic paternal genome. Nature 403: 501-502
72. Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, Misteli T, (2006) Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 10: 105-116
73. Mikkelsen TS, Hanna J, Zhang X, Ku M, Wernig M, Schorderet P, Bernstein BE, Jaenisch R, Lander ES, Meissner A, (2008) Dissecting direct reprogramming through integrative genomic analysis. Nature 454: 49-55
74. Miller RA, Ruddle FH, (1976) Pluripotent teratocarcinoma-thymus somatic cell hybrids. Cell 9: 45-55
75. Montellier E, Boussouar F, Rousseaux S, Zhang K, Buchou T, Fenaille F, Shiota H, Debernardi A, Hery P, Curtet S, Jamshidikia M, Barral S, Holota H, Bergon A, Lopez F, Guardiola P, Pernet K, Imbert J, Petosa C, Tan M, et al, (2013) Chromatin-to-nucleoprotamine transition is controlled by the histone H2B variant TH2B. Genes Dev 27: 1680-1692
76. Moon JH, Heo JS, Kim JS, Jun EK, Lee JH, Kim A, Kim J, Whang KY, Kang YK, Yeo S, Lim HJ, Han DW, Kim DW, Oh S, Yoon BS, Scholer HR, You S, (2011) Reprogramming fibroblasts into induced pluripotent stem cells with Bmi1. Cell Res 21: 1305-1315
77. Morris SA, Cahan P, Li H, Zhao AM, San Roman AK, Shivdasani RA, Collins JJ, Daley GQ, (2014) Dissecting engineered cell types and enhancing cell fate conversion via Cell Net. Cell 158: 889-902
78. Nashun B, Akiyama T, Suzuki MG, Aoki F, (2011) Dramatic replacement of histone variants during genome remodeling in nuclear-transferred embryos. Epigenetics 6: 1489-1497
79. Nguyen AT, Zhang Y, (2011) The diverse functions of Dot1 and H3K79 methylation. Genes Dev 25: 1345-1358
80. Niwa H, (2014) The pluripotency transcription factor network at work in reprogramming. Curr Opin Genet Dev 28C: 25-31
81. Onder TT, Kara N, Cherry A, Sinha AU, Zhu N, Bernt KM, Cahan P, Marcarci BO, Unternaehrer J, Gupta PB, Lander ES, Armstrong SA, Daley GQ, (2012) Chromatin-modifying enzymes as modulators of reprogramming. Nature 483: 598-602
82. Orkin SH, Hochedlinger K, (2011) Chromatin connections to pluripotency and cellular reprogramming. Cell 145: 835-850
83. 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
84. Pasque V, Radzisheuskaya A, Gillich A, Halley-Stott RP, Panamarova M, Zernicka-Goetz M, Surani MA, Silva JC, (2012) Histone variant macroH2A marks embryonic differentiation in vivo and acts as an epigenetic barrier to induced pluripotency. J Cell Sci 125: 6094-6104
85. Pawlak M, Jaenisch R, (2011) De novo DNA methylation by Dnmt3a and Dnmt3b is dispensable for nuclear reprogramming of somatic cells to a pluripotent state. Genes Dev 25: 1035-1040
86. Pereira CF, Piccolo FM, Tsubouchi T, Sauer S, Ryan NK, Bruno L, Landeira D, Santos J, Banito A, Gil J, Koseki H, Merkenschlager M, Fisher AG, (2010) ESCs require PRC2 to direct the successful reprogramming of differentiated cells toward pluripotency. Cell Stem Cell 6: 547-556
87. Piccolo FM, Bagci H, Brown KE, Landeira D, Soza-Ried J, Feytout A, Mooijman D, Hajkova P, Leitch HG, Tada T, Kriaucionis S, Dawlaty MM, Jaenisch R, Merkenschlager M, Fisher AG, (2013) Different roles for Tet1 and Tet2 proteins in reprogramming-mediated erasure of imprints induced by EGC fusion. Mol Cell 49: 1023-1033
88. Polo JM, Anderssen E, Walsh RM, Schwarz BA, Nefzger CM, Lim SM, Borkent M, Apostolou E, Alaei S, Cloutier J, Bar-Nur O, Cheloufi S, Stadtfeld M, Figueroa ME, Robinton D, Natesan S, Melnick A, Zhu JF, Ramaswamy S, Hochedlinger K, (2012) A Molecular roadmap of reprogramming somatic cells into iPS cells. Cell 151: 1617-1632
89. Rais Y, Zviran A, Geula S, Gafni O, Chomsky E, Viukov S, Mansour AA, Caspi I, Krupalnik V, Zerbib M, Maza I, Mor N, Baran D, Weinberger L, Jaitin DA, Lara-Astiaso D, Blecher-Gonen R, Shipony Z, Mukamel Z, Hagai T, et al, (2013) Deterministic direct reprogramming of somatic cells to pluripotency. Nature 502: 65-70
90. Reynolds N, Latos P, Hynes-Allen A, Loos R, Leaford D, O'Shaughnessy A, Mosaku O, Signolet J, Brennecke P, Kalkan T, Costello I, Humphreys P, Mansfield W, Nakagawa K, Strouboulis J, Behrens A, Bertone P, Hendrich B, (2012) NuRD suppresses pluripotency gene expression to promote transcriptional heterogeneity and lineage commitment. Cell Stem Cell 10: 583-594
91. dos Santos RL, Tosti L, Radzisheuskaya A, Caballero IM, Kaji K, Hendrich B, Silva JC, (2014) MBD3/NuRD facilitates induction of pluripotency in a context-dependent manner. Cell Stem Cell 15: 102-110
92. Sherwood RI, Hashimoto T, O'Donnell CW, Lewis S, Barkal AA, van Hoff JP, Karun V, Jaakkola T, Gifford DK, (2014) Discovery of directional and nondirectional pioneer transcription factors by modeling DNase profile magnitude and shape. Nat Biotechnol 32: 171-178
93. Shi Y, Do JT, Desponts C, Hahm HS, Scholer HR, Ding S, (2008) A combined chemical and genetic approach for the generation of induced pluripotent stem cells. Cell Stem Cell 2: 525-528
94. Shinagawa T, Takagi T, Tsukamoto D, Tomaru C, Huynh LM, Sivaraman P, Kumarevel T, Inoue K, Nakato R, Katou Y, Sado T, Takahashi S, Ogura A, Shirahige K, Ishii S, (2014) Histone variants enriched in oocytes enhance reprogramming to induced pluripotent stem cells. Cell Stem Cell 14: 217-227
95. Shipony Z, Mukamel Z, Cohen NM, Landan G, Chomsky E, Zeliger SR, Fried YC, Ainbinder E, Friedman N, Tanay A, (2014) Dynamic and static maintenance of epigenetic memory in pluripotent and somatic cells. Nature 513: 115
96. Singhal N, Graumann J, Wu G, Arauzo-Bravo MJ, Han DW, Greber B, Gentile L, Mann M, Scholer HR, (2010) Chromatin-Remodeling Components of the BAF Complex Facilitate Reprogramming. Cell 141: 943-955
97. 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
98. Smith ZD, Chan MM, Humm KC, Karnik R, Mekhoubad S, Regev A, Eggan K, Meissner A, (2014) DNA methylation dynamics of the human preimplantation embryo. Nature 511: 611-615
99. Soufi A, Donahue G, Zaret KS, (2012) Facilitators and impediments of the pluripotency reprogramming factors' initial engagement with the genome. Cell 151: 994-1004
100. Sridharan R, Gonzales-Cope M, Chronis C, Bonora G, McKee R, Huang C, Patel S, Lopez D, Mishra N, Pellegrini M, Carey M, Garcia BA, Plath K, (2013) Proteomic and genomic approaches reveal critical functions of H3K9 methylation and heterochromatin protein-1gamma in reprogramming to pluripotency. Nat Cell Biol 15: 872-882
101. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Scholer A, Wirbelauer C, Oakeley EJ, Gaidatzis D, Tiwari VK, Schubeler D, (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480: 490-495
102. Stadtfeld M, Maherali N, Breault DT, Hochedlinger K, (2008) Defining molecular cornerstones during fibroblast to iPS cell reprogramming in mouse. Cell Stem Cell 2: 230-240
103. Tahiliani M, Koh KP, Shen YH, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A, (2009) Conversion of 5-Methylcytosine to 5-Hydroxymethylcytosine in Mammalian DNA by MLL Partner TET1. Science 324: 930-935
104. Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676
105. Takashima Y, Guo G, Loos R, Nichols J, Ficz G, Krueger F, Oxley D, Santos F, Clarke J, Mansfield W, Reik W, Bertone P, Smith A, (2014) Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell 158: 1254-1269
106. Tonge PD, Corso AJ, Monetti C, Hussein SM, Puri MC, Michael IP, Li M, Lee DS, Mar JC, Cloonan N, Wood DL, Gauthier ME, Korn O, Clancy JL, Preiss T, Grimmond SM, Shin JY, Seo JS, Wells CA, Rogers IM, et al, (2014) Divergent reprogramming routes lead to alternative stem-cell states. Nature 516: 192-197
107. Tsubouchi T, Soza-Ried J, Brown K, Piccolo FM, Cantone I, Landeira D, Bagci H, Hochegger H, Merkenschlager M, Fisher AG, (2013) DNA synthesis is required for reprogramming mediated by stem cell fusion. Cell 152: 873-883
108. Turinetto V, Orlando L, Sanchez-Ripoll Y, Kumpfmueller B, Storm MP, Porcedda P, Minieri V, Saviozzi S, Accomasso L, Cibrario Rocchietti E, Moorwood K, Circosta P, Cignetti A, Welham MJ, Giachino C, (2012) High basal gammaH2AX levels sustain self-renewal of mouse embryonic and induced pluripotent stem cells. Stem Cells 30: 1414-1423
109. Venkatesh S, Smolle M, Li H, Gogol MM, Saint M, Kumar S, Natarajan K, Workman JL, (2012) Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature 489: 452-455
110. Voss TC, Hager GL, (2014) Dynamic regulation of transcriptional states by chromatin and transcription factors. Nat Rev Genet 15: 69-81
111. Wang T, Chen K, Zeng X, Yang J, Wu Y, Shi X, Qin B, Zeng L, Esteban MA, Pan G, Pei D, (2011) The histone demethylases Jhdm1a/1b enhance somatic cell reprogramming in a vitamin-C-dependent manner. Cell Stem Cell 9: 575-587
112. Wang B, Pfeiffer MJ, Schwarzer C, Arauzo-Bravo MJ, Boiani M, (2014a) DNA replication is an integral part of the mouse oocyte's reprogramming machinery. PLoS One 9: e97199
113. Wang L, Du Y, Ward JM, Shimbo T, Lackford B, Zheng X, Miao YL, Zhou B, Han L, Fargo DC, Jothi R, Williams CJ, Wade PA, Hu G, (2014b) INO80 facilitates pluripotency gene activation in embryonic stem cell self-renewal, reprogramming, and blastocyst development. Cell Stem Cell 14: 575-591
114. Wang L, Zhang J, Duan J, Gao X, Zhu W, Lu X, Yang L, Zhang J, Li G, Ci W, Li W, Zhou Q, Aluru N, Tang F, He C, Huang X, Liu J, (2014c) Programming and inheritance of parental DNA methylomes in mammals. Cell 157: 979-991
115. 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 is an essential maternal factor for oocyte reprogramming. Proc Natl Acad Sci USA 111: 7325-7330
116. Wu T, Liu Y, Wen D, Tseng Z, Tahmasian M, Zhong M, Rafii S, Stadtfeld M, Hochedlinger K, Xiao A, (2014) Histone variant H2A.X deposition pattern serves as a functional epigenetic mark for distinguishing the developmental potentials of iPSCs. Cell Stem Cell 15: 281-294
117. Xie HF, Ye M, Feng R, Graf T, (2004) Stepwise reprogramming of B cells into macrophages. Cell 117: 663-676
118. Xie W, Schultz MD, Lister R, Hou Z, Rajagopal N, Ray P, Whitaker JW, Tian S, Hawkins RD, Leung D, Yang H, Wang T, Lee AY, Swanson SA, Zhang J, Zhu Y, Kim A, Nery JR, Urich MA, Kuan S, et al, (2013) Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 153: 1134-1148
119. Yeap LS, Hayashi K, Surani MA, (2009) ERG-associated protein with SET domain (ESET)-Oct4 interaction regulates pluripotency and represses the trophectoderm lineage. Epigenetics Chromatin 2: 12
120. Yuan P, Han J, Guo G, Orlov YL, Huss M, Loh YH, Yaw LP, Robson P, Lim B, Ng HH, (2009) Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev 23: 2507-2520
121. Zaret KS, Carroll JS, (2011) Pioneer transcription factors: establishing competence for gene expression. Genes Dev 25: 2227-2241
122. Zhang Z, Jones A, Sun CW, Li C, Chang CW, Joo HY, Dai Q, Mysliwiec MR, Wu LC, Guo Y, Yang W, Liu K, Pawlik KM, Erdjument-Bromage H, Tempst P, Lee Y, Min J, Townes TM, Wang H, (2011) PRC2 complexes with JARID2, MTF2, and esPRC2p48 in ES cells to modulate ES cell pluripotency and somatic cell reprogramming. Stem Cells 29: 229-240
123. Zhao W, Li Q, Ayers S, Gu Y, Shi Z, Zhu Q, Chen Y, Wang HY, Wang RF, (2013) Jmjd3 inhibits reprogramming by upregulating expression of INK4a/Arf and targeting PHF20 for ubiquitination. Cell 152: 1037-1050
124. Zhu J, Adli M, Zou JY, Verstappen G, Coyne M, Zhang X, Durham T, Miri M, Deshpande V, De Jager PL, Bennett DA, Houmard JA, Muoio DM, Onder TT, Camahort R, Cowan CA, Meissner A, Epstein CB, Shoresh N, Bernstein BE, (2013) Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152: 642-654