Resetting epigenetic signatures to induce somatic cell reprogramming

Cellular and Molecular Life Sciences

Volumn 70, Issue 8, 2013, Pages 1413-1424

  Lluis, Frederic ^a   Cosma, Maria Pia ^a,b,c  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^c INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

Cell fusion; Chromatin remodeling complexes; Epigenetic modifications; Histone marks; iPSCs; Nuclear transfer; Somatic cell reprogramming

Indexed keywords

CELL DIFFERENTIATION; CELL MATURATION; CELL TRANSDIFFERENTIATION; CHROMATIN STRUCTURE; DEMETHYLATION; DNA MODIFICATION; EPIGENETICS; GENE EXPRESSION; HISTONE MODIFICATION; HUMAN; NONHUMAN; PHYSIOLOGICAL PROCESS; REVIEW; SOMATIC CELL REPROGRAMMING; TRANSCRIPTION REGULATION;

ANIMALS; CELL FUSION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; HISTONES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; NUCLEAR REPROGRAMMING;

EID: 84876685920     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1137-8     Document Type: Review

References (117)

1. Cosma MP, Panizza S, Nasmyth K (2001) Cdk1 triggers association of RNA polymerase to cell cycle promoters only after recruitment of the mediator by SBF. Mol Cell 7(6):1213-1220 (Pubitemid 32607355)
2. Waddington CH (1957) The strategy of the genes. Allen & Unwin, London
3. Gurdon JB, Elsdale TR, Fischberg M (1958) Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 182(4627):64-65. doi: 10.1038/182064a0
4. Davis RL, Weintraub H, Lassar AB (1987) Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51(6):987-1000
5. Lassar AB, Paterson BM, Weintraub H (1986) Transfection of a DNA locus that mediates the conversion of 10T1/2 fibroblasts to myoblasts. Cell 47(5):649-656 (Pubitemid 17011408)
6. Tada M, Tada T, Lefebvre L, Barton SC, Surani MA (1997) Embryonic germ cells induce epigenetic reprogramming of somatic nucleus in hybrid cells. EMBO J 16(21):6510-6520 (Pubitemid 27483276)
7. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663-676 (Pubitemid 44233629)
8. Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9(6):465-476. doi: 10.1038/nrg2341 (Pubitemid 351693975)
9. Tan L, Shi YG (2012) Tet family proteins and 5-hydroxymethylcytosine in development and disease. Development 139(11):1895-1902. doi: 10.1242/dev.070771
10. Wu SC, Zhang Y (2010) Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 11(9):607-620. doi: 10.1038/nrm2950
11. Surani MA (2001) Reprogramming of genome function through epigenetic inheritance. Nature 414(6859):122-128 (Pubitemid 33041637)
12. Bestor TH, Coxon A (1993) Cytosine methylation: the pros and cons of DNA methylation. Curr Biol 3(6):384-386
13. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16(1):6-21. doi: 10.1101/gad.947102 (Pubitemid 34049633)
14. Hackett JA, Zylicz JJ, Surani MA (2012) Parallel mechanisms of epigenetic reprogramming in the germline. Trends Genet 28(4):164-174. doi: 10.1016/j.tig.2012.01.005
15. Howlett SK, Reik W (1991) Methylation levels of maternal and paternal genomes during preimplantation development. Development 113(1):119-127
16. Branco MR, Oda M, Reik W (2008) Safeguarding parental identity: Dnmt1 maintains imprints during epigenetic reprogramming in early embryogenesis. Genes Dev 22(12):1567-1571. doi: 10.1101/gad.1690508 (Pubitemid 351846836)
17. Hirasawa R, Chiba H, Kaneda M, Tajima S, Li E, Jaenisch R, Sasaki H (2008) Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev 22(12):1607-1616. doi: 10.1101/gad.1667008 (Pubitemid 351846841)
18. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T (2000) Demethylation of the zygotic paternal genome. Nature 403(6769):501-502. doi: 10.1038/35000654 (Pubitemid 30082186)
19. 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(8):475-478 (Pubitemid 30247337)
20. Santos F, Hendrich B, Reik W, Dean W (2002) Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 241(1):172-182. doi: 10.1006/dbio.2001.0501 (Pubitemid 34066770)
21. Wossidlo M, Arand J, Sebastiano V, Lepikhov K, Boiani M, Reinhardt R, Scholer H, Walter J (2010) Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes. EMBO J 29(11):1877-1888. doi: 10.1038/emboj.2010.80
22. Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, Taniguchi H, Sekimoto T, Ikawa M, Yoneda Y, Okabe M, Tanaka S, Shiota K, Nakano T (2007) PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol 9(1):64-71. doi: 10.1038/ncb1519 (Pubitemid 46024198)
23. 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. doi: 10.1038/ncomms1240
24. Gu TP, Guo F, Yang H, Wu HP, Xu GF, Liu W, Xie ZG, Shi L, He X, Jin SG, Iqbal K, Shi YG, Deng Z, Szabo PE, Pfeifer GP, Li J, Xu GL (2011) The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477(7366):606-610. doi: 10.1038/nature10443
25. 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 USA 108(9):3642-3647. doi: 10.1073/pnas.1014033108
26. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y, Chen Z, Li L, Sun Y, Li X, Dai Q, Song CX, Zhang K, He C, Xu GL (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333(6047):1303-1307. doi: 10.1126/science.1210944
27. 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(6047):1300-1303. doi: 10.1126/science.1210597
28. Nabel CS, Kohli RM (2011) Molecular biology. Demystifying DNA demethylation. Science 333(6047):1229-1230. doi: 10.1126/science.1211917
29. Pfaffeneder T, Hackner B, Truss M, Munzel M, Muller M, Deiml CA, Hagemeier C, Carell T (2011) The discovery of 5-formylcytosine in embryonic stem cell DNA. Angew Chem Int Ed Engl 50(31):7008-7012. doi: 10.1002/anie.201103899
30. Surani MA, Hayashi K, Hajkova P (2007) Genetic and epigenetic regulators of pluripotency. Cell 128(4):747-762 (Pubitemid 46273582)
31. Matsui Y, Zsebo K, Hogan BL (1992) Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70(5):841-847. doi: 0092-8674(92)90317-6
32. McLaren A, Lawson KA (2005) How is the mouse germ-cell lineage established? Differentiation 73(9-10):435-437. doi: 10.1111/j.1432-0436.2005. 00049.x
33. Ginsburg M, Snow MH, McLaren A (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110(2):521-528 (Pubitemid 20330528)
34. Ohinata Y, Ohta H, Shigeta M, Yamanaka K, Wakayama T, Saitou M (2009) A signaling principle for the specification of the germ cell lineage in mice. Cell 137(3):571-584. doi: 10.1016/j.cell.2009.03.014
35. Ohinata Y, Payer B, O'Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A, Saitou M, Surani MA (2005) Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436(7048):207-213. doi: 10.1038/nature03813 (Pubitemid 41021265)
36. Vincent SD, Dunn NR, Sciammas R, Shapiro-Shalef M, Davis MM, Calame K, Bikoff EK, Robertson EJ (2005) The zinc finger transcriptional repressor Blimp1/Prdm1 is dispensable for early axis formation but is required for specification of primordial germ cells in the mouse. Development 132(6):1315-1325. doi: 10.1242/dev.01711 (Pubitemid 40528791)
37. Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M, Shigeta M, Yamanaka K, Ohinata Y, Saitou M (2008) Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat Genet 40(8):1016-1022. doi: 10.1038/ng.186
38. Mochizuki K, Matsui Y (2010) Epigenetic profiles in primordial germ cells: global modulation and fine tuning of the epigenome for acquisition of totipotency. Dev Growth Differ 52(6):517-525. doi: 10.1111/j.1440-169X.2010. 01190.x
39. Hayashi K, Surani MA (2009) Resetting the epigenome beyond pluripotency in the germline. Cell Stem Cell 4(6):493-498. doi: 10.1016/j.stem.2009.05.007
40. Seki Y, Hayashi K, Itoh K, Mizugaki M, Saitou M, Matsui Y (2005) Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev Biol 278(2):440-458. doi: 10.1016/j.ydbio.2004.11.025 (Pubitemid 40175041)
41. Bhutani N, Brady JJ, Damian M, Sacco A, Corbel SY, Blau HM (2010) Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463(7284):1042-1047. doi: 10.1038/nature08752
42. Gehring M, Reik W, Henikoff S (2009) DNA demethylation by DNA repair. Trends Genet 25(2):82-90. doi: 10.1016/j.tig.2008.12.001
43. Morgan HD, Dean W, Coker HA, Reik W, Petersen-Mahrt SK (2004) Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: implications for epigenetic reprogramming. J Biol Chem 279(50):52353-52360. doi: 10.1074/jbc.M407695200M407695200 (Pubitemid 39656611)
44. Popp C, Dean W, Feng S, Cokus SJ, Andrews S, Pellegrini M, Jacobsen SE, Reik W (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463(7284):1101-1105. doi: 10.1038/nature08829
45. Seki Y, Yamaji M, Yabuta Y, Sano M, Shigeta M, Matsui Y, Saga Y, Tachibana M, Shinkai Y, Saitou M (2007) Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 134(14):2627-2638. doi: 10.1242/dev.005611 (Pubitemid 47225959)
46. Boyer LA, Mathur D, Jaenisch R (2006) Molecular control of pluripotency. Curr Opin Genet Dev 16(5):455-462 (Pubitemid 44345206)
47. Ringrose L, Paro R (2004) Epigenetic regulation of cellular memory by the polycomb and trithorax group proteins. Annu Rev Genet 38:413-443. doi: 10.1146/annurev.genet.38.072902.091907 (Pubitemid 40013734)
48. Yabuta Y, Kurimoto K, Ohinata Y, Seki Y, Saitou M (2006) Gene expression dynamics during germline specification in mice identified by quantitative single-cell gene expression profiling. Biol Reprod 75(5):705-716. doi: 10.1095/biolreprod.106.053686 (Pubitemid 44720390)
49. Matsui Y, Tokitake Y (2009) Primordial germ cells contain subpopulations that have greater ability to develop into pluripotential stem cells. Dev Growth Differ 51(7):657-667. doi: 10.1111/j.1440-169X.2009.01125.x
50. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861-872 (Pubitemid 350138099)
51. Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K (2008) Induced pluripotent stem cells generated without viral integration. Science 322(5903):945-949
52. Zhou H, Wu S, Joo JY, Zhu S, Han DW, Lin T, Trauger S, Bien G, Yao S, Zhu Y, Siuzdak G, Scholer HR, Duan L, Ding S (2009) Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4(5):381-384. doi: 10.1016/j.stem.2009.04.005
53. Cho HJ, Lee CS, Kwon YW, Paek JS, Lee SH, Hur J, Lee EJ, Roh TY, Chu IS, Leem SH, Kim Y, Kang HJ, Park YB, Kim HS (2010) Induction of pluripotent stem cells from adult somatic cells by protein-based reprogramming without genetic manipulation. Blood 116(3):386-395. doi: 10.1182/blood-2010-02-269589
54. Warren L, Manos PD, Ahfeldt T, Loh YH, Li H, Lau F, Ebina W, Mandal PK, Smith ZD, Meissner A, Daley GQ, Brack AS, Collins JJ, Cowan C, Schlaeger TM, Rossi DJ (2010) Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7(5):618-630. doi: 10.1016/j.stem.2010.08.012
55. Anokye-Danso F, Trivedi CM, Juhr D, Gupta M, Cui Z, Tian Y, Zhang Y, Yang W, Gruber PJ, Epstein JA, Morrisey EE (2011) Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8(4):376-388. doi: 10.1016/j.stem.2011.03.001
56. Li Z, Yang CS, Nakashima K, Rana TM (2011) Small RNA-mediated regulation of iPS cell generation. EMBO J 30(5):823-834. doi: 10.1038/emboj.2011.2
57. Miyoshi N, Ishii H, Nagano H, Haraguchi N, Dewi DL, Kano Y, Nishikawa S, Tanemura M, Mimori K, Tanaka F, Saito T, Nishimura J, Takemasa I, Mizushima T, Ikeda M, Yamamoto H, Sekimoto M, Doki Y, Mori M (2011) Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell 8(6):633-638. doi: 10.1016/j.stem.2011.05.001
58. Subramanyam D, Lamouille S, Judson RL, Liu JY, Bucay N, Derynck R, Blelloch R (2011) Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells. Nat Biotechnol 29(5):443-448. doi: 10.1038/nbt.1862
59. Yang CS, Li Z, Rana TM (2011) microRNAs modulate iPS cell generation. RNA 17(8):1451-1460. doi: 10.1261/rna.2664111
60. Loewer S, Cabili MN, Guttman M, Loh YH, Thomas K, Park IH, Garber M, Curran M, Onder T, Agarwal S, Manos PD, Datta S, Lander ES, Schlaeger TM, Daley GQ, Rinn JL (2010) Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet 42(12):1113-1117. doi: 10.1038/ng.710
61. Stadtfeld M, Hochedlinger K (2010) Induced pluripotency: history, mechanisms, and applications. Genes Dev 24(20):2239-2263. doi: 10.1101/gad.1963910
62. Bussmann LH, Schubert A, Vu Manh TP, De Andres L, Desbordes SC, Parra M, Zimmermann T, Rapino F, Rodriguez-Ubreva J, Ballestar E, Graf T (2009) A robust and highly efficient immune cell reprogramming system. Cell Stem Cell 5(5):554-566. doi: 10.1016/j.stem.2009.10.004
63. Xie H, Ye M, Feng R, Graf T (2004) Stepwise reprogramming of B cells into macrophages. Cell 117(5):663-676 (Pubitemid 38692531)
64. Marro S, Pang ZP, Yang N, Tsai MC, Qu K, Chang HY, Sudhof TC, Wernig M (2011) Direct lineage conversion of terminally differentiated hepatocytes to functional neurons. Cell Stem Cell 9(4):374-382. doi: 10.1016/j.stem.2011.09.002
65. Ambasudhan R, Talantova M, Coleman R, Yuan X, Zhu S, Lipton SA, Ding S (2011) Direct reprogramming of adult human fibroblasts to functional neurons under defined conditions. Cell Stem Cell 9(2):113-118. doi: 10.1016/j.stem.2011. 07.002
66. Broccoli V, Caiazzo M, Dell'Anno MT (2011) Setting a highway for converting skin into neurons. J Mol Cell Biol 3(6):322-323. doi: 10.1093/jmcb/mjr029
67. Caiazzo M, Dell'Anno MT, Dvoretskova E, Lazarevic D, Taverna S, Leo D, Sotnikova TD, Menegon A, Roncaglia P, Colciago G, Russo G, Carninci P, Pezzoli G, Gainetdinov RR, Gustincich S, Dityatev A, Broccoli V (2011) Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 476(7359):224-227. doi: 10.1038/nature10284
68. Pang ZP, Yang N, Vierbuchen T, Ostermeier A, Fuentes DR, Yang TQ, Citri A, Sebastiano V, Marro S, Sudhof TC, Wernig M (2011) Induction of human neuronal cells by defined transcription factors. Nature 476(7359):220-223. doi: 10.1038/nature10202
69. Pfisterer U, Kirkeby A, Torper O, Wood J, Nelander J, Dufour A, Bjorklund A, Lindvall O, Jakobsson J, Parmar M (2011) Direct conversion of human fibroblasts to dopaminergic neurons. Proc Natl Acad Sci USA 108(25):10343-10348. doi: 10.1073/pnas.1105135108
70. Qiang L, Fujita R, Yamashita T, Angulo S, Rhinn H, Rhee D, Doege C, Chau L, Aubry L, Vanti WB, Moreno H, Abeliovich A (2011) Directed conversion of Alzheimer's disease patient skin fibroblasts into functional neurons. Cell 146(3):359-371. doi: 10.1016/j.cell.2011.07.007
71. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Sudhof TC, Wernig M (2010) Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463(7284):1035-1041. doi: 10.1038/nature08797
72. Yang N, Ng YH, Pang ZP, Sudhof TC, Wernig M (2011) Induced neuronal cells: how to make and define a neuron. Cell Stem Cell 9(6):517-525. doi: 10.1016/j.stem.2011.11.015
73. Yoo AS, Sun AX, Li L, Shcheglovitov A, Portmann T, Li Y, Lee-Messer C, Dolmetsch RE, Tsien RW, Crabtree GR (2011) MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476(7359):228-231. doi: 10.1038/nature10323
74. Graf T (2011) Historical origins of transdifferentiation and reprogramming. Cell Stem Cell 9(6):504-516. doi: 10.1016/j.stem.2011.11.012
75. Ieda M, Fu JD, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau BG, Srivastava D (2010) Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142(3):375-386. doi: 10.1016/j.cell.2010.07.002
76. Kajimura S, Seale P, Kubota K, Lunsford E, Frangioni JV, Gygi SP, Spiegelman BM (2009) Initiation of myoblast to brown fat switch by a PRDM16-C/EBP-beta transcriptional complex. Nature 460(7259):1154-1158. doi: 10.1038/nature08262
77. Sekiya S, Suzuki A (2011) Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors. Nature 475(7356):390-393. doi: 10.1038/nature10263
78. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA (2008) In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455(7213):627-632. doi: 10.1038/nature07314
79. Gurdon JB (1962) The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J Embryol Exp Morphol 10:622-640
80. Blau HM, Pavlath GK, Hardeman EC, Chiu CP, Silberstein L, Webster SG, Miller SC, Webster C (1985) Plasticity of the differentiated state. Science 230(4727):758-766 (Pubitemid 16193964)
81. Eminli S, Foudi A, Stadtfeld M, Maherali N, Ahfeldt T, Mostoslavsky G, Hock H, Hochedlinger K (2009) Differentiation stage determines potential of hematopoietic cells for reprogramming into induced pluripotent stem cells. Nat Genet 41(9):968-976. doi: 10.1038/ng.428
82. Kim K, Doi A, Wen B, Ng K, Zhao R, Cahan P, Kim J, Aryee MJ, Ji H, Ehrlich LI, Yabuuchi A, Takeuchi A, Cunniff KC, Hongguang H, McKinney-Freeman S, Naveiras O, Yoon TJ, Irizarry RA, Jung N, Seita J, Hanna J, Murakami P, Jaenisch R, Weissleder R, Orkin SH, Weissman IL, Feinberg AP, Daley GQ (2010) Epigenetic memory in induced pluripotent stem cells. Nature 467(7313):285-290. doi: 10.1038/nature09342
83. Ng RK, Gurdon JB (2008) Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat Cell Biol 10(1):102-109. doi: 10.1038/ncb1674
84. Ohi Y, Qin H, Hong C, Blouin L, Polo JM, Guo T, Qi Z, Downey SL, Manos PD, Rossi DJ, Yu J, Hebrok M, Hochedlinger K, Costello JF, Song JS, Ramalho-Santos M (2011) Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat Cell Biol 13(5):541-549. doi: 10.1038/ncb2239
85. Polo JM, Liu S, Figueroa ME, Kulalert W, Eminli S, Tan KY, Apostolou E, Stadtfeld M, Li Y, Shioda T, Natesan S, Wagers AJ, Melnick A, Evans T, Hochedlinger K (2010) Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotechnol 28(8):848-855. doi: 10.1038/nbt.1667
86. 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(7336):68-73. doi: 10.1038/nature09798
87. Cho H, Wolffe AP (1994) Xenopus laevis B4, an intron-containing oocyte-specific linker histone-encoding gene. Gene 143(2):233-238 (Pubitemid 24185674)
88. Jullien J, Astrand C, Halley-Stott RP, Garrett N, Gurdon JB (2010) Characterization of somatic cell nuclear reprogramming by oocytes in which a linker histone is required for pluripotency gene reactivation. Proc Natl Acad Sci USA 107(12):5483-5488. doi: 10.1073/pnas.1000599107
89. Singhal N, Graumann J, Wu G, Aráuzo-Bravo J, Han DW, Greber B, Gentie L, Mann M, Scholer H (2010) Chromatin-remodeling components of the BAF complex facilitate reprogramming. Cell 141:943-955
90. Pasque V, Gillich A, Garrett N, Gurdon JB (2011) Histone variant macroH2A confers resistance to nuclear reprogramming. EMBO J 30(12):2373-2387. doi: 10.1038/emboj.2011.144
91. Banaszynski LA, Allis CD, Lewis PW (2010) Histone variants in metazoan development. Dev Cell 19(5):662-674. doi: 10.1016/j.devcel.2010.10.014
92. Angelov D, Molla A, Perche PY, Hans F, Cote J, Khochbin S, Bouvet P, Dimitrov S (2003) The histone variant macroH2A interferes with transcription factor binding and SWI/SNF nucleosome remodeling. Mol Cell 11(4):1033-1041 (Pubitemid 36566324)
93. Efroni S, Duttagupta R, Cheng J, Dehghani H, Hoeppner DJ, Dash C, Bazett-Jones DP, Le Grice S, McKay RD, Buetow KH, Gingeras TR, Misteli T, Meshorer E (2008) Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2(5):437-447. doi: 10.1016/j.stem.2008.03.021 (Pubitemid 351598083)
94. 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(1):105-116. doi: 10.1016/j.devcel.2005.10.017 (Pubitemid 43025681)
95. Bui HT, Wakayama S, Kishigami S, Park KK, Kim JH, Thuan NV, Wakayama T (2010) Effect of trichostatin A on chromatin remodeling, histone modifications, DNA replication, and transcriptional activity in cloned mouse embryos. Biol Reprod 83(3):454-463. doi: 10.1095/biolreprod.109.083337
96. Esteban MA, Wang T, Qin B, Yang J, Qin D, Cai J, Li W, Weng Z, Chen J, Ni S, Chen K, Li Y, Liu X, Xu J, Zhang S, Li F, He W, Labuda K, Song Y, Peterbauer A, Wolbank S, Redl H, Zhong M, Cai D, Zeng L, Pei D (2010) Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 6(1):71-79. doi: 10.1016/j.stem.2009.12.001
97. Huangfu D, Maehr R, Guo W, Eijkelenboom A, Snitow M, Chen AE, Melton DA (2008) Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat Biotechnol 26(7):795-797 (Pubitemid 351961456)
98. Kishigami S, Mizutani E, Ohta H, Hikichi T, Thuan NV, Wakayama S, Bui HT, Wakayama T (2006) Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem Biophys Res Commun 340(1):183-189. doi: 10.1016/j.bbrc.2005.11.164 (Pubitemid 41827663)
99. Liang G, Taranova O, Xia K, Zhang Y (2010) Butyrate promotes induced pluripotent stem cell generation. J Biol Chem 285(33):25516-25521. doi: 10.1074/jbc.M110.142059
100. Mali P, Chou BK, Yen J, Ye Z, Zou J, Dowey S, Brodsky RA, Ohm JE, Yu W, Baylin SB, Yusa K, Bradley A, Meyers DJ, Mukherjee C, Cole PA, Cheng L (2010) Butyrate greatly enhances derivation of human induced pluripotent stem cells by promoting epigenetic remodeling and the expression of pluripotency-Associated genes. Stem Cells 28(4):713-720. doi: 10.1002/stem.402
101. 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(6):575-587. doi: 10.1016/j.stem.2011.10.005
102. Barroso-del Jesus A, Lucena-Aguilar G, Menendez P (2009) The miR-302-367 cluster as a potential stemness regulator in ESCs. Cell Cycle 8(3):394-398
103. 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(2):183-197. doi: 10.1016/j.cell.2011.03.003
104. Epsztejn-Litman S, Feldman N, Abu-Remaileh M, Shufaro Y, Gerson A, Ueda J, Deplus R, Fuks F, Shinkai Y, Cedar H, Bergman Y (2008) De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nat Struct Mol Biol 15(11):1176-1183. doi: 10.1038/nsmb.1476
105. 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(8):2131-2141
106. Shi Y, Desponts C, Do JT, Hahm HS, Scholer HR, Ding S (2008) Induction of pluripotent stem cells from mouse embryonic fibroblasts by Oct4 and Klf4 with small-molecule compounds. Cell Stem Cell 3(5):568-574
107. 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(6):547-556
108. 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(7391):598-602. doi: 10.1038/nature10953
109. Lluis F, Ombrato L, Pedone E, Pepe S, Merrill BJ, Cosma MP (2011) T-cell factor 3 (Tcf3) deletion increases somatic cell reprogramming by inducing epigenome modifications. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1017402108
110. 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(1):96-105. doi: 10.1016/j.stem.2010.12.001
111. 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(7200):49-55 (Pubitemid 351931978)
112. 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(6):525-528 (Pubitemid 351729222)
113. Hanna J, Markoulaki S, Schorderet P, Carey BW, Beard C, Wernig M, Creyghton MP, Steine EJ, Cassady JP, Foreman R, Lengner CJ, Dausman JA, Jaenisch R (2008) Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell 133(2):250-264 (Pubitemid 351508307)
114. Vierbuchen T, Wernig M (2011) Direct lineage conversions: unnatural but useful? Nat Biotechnol 29(10):892-907. doi: 10.1038/nbt.1946
115. Yamanaka S, Blau HM (2010) Nuclear reprogramming to a pluripotent state by three approaches. Nature 465(7299):704-712. doi: 10.1038/nature09229
116. Hochedlinger K, Plath K (2009) Epigenetic reprogramming and induced pluripotency. Development 136(4):509-523. doi: 10.1242/dev.020867
117. Niwa H (2007) How is pluripotency determined and maintained? Development 134(4):635-646 (Pubitemid 46437906)