Epigenetic regulation of telomere chromatin integrity in pluripotent embryonic stem cells

Epigenomics

Volumn 2, Issue 5, 2010, Pages 639-655

  Wong, Lee H ^a  

^a MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

Author keywords

ATRX; H3.3; histone; iPS cell; pluripotent ES cell; telomere

Indexed keywords

DNA; RETINOBLASTOMA PROTEIN; TELOMERASE;

CELL ELONGATION; CHROMATIN STRUCTURE; DNA DAMAGE; DNA METHYLATION; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DYSKERATOSIS CONGENITA; EMBRYONIC STEM CELL; EPIGENETICS; HUMAN; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TELOMERE;

CHROMATIN; DNA METHYLATION; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; HISTONES; HUMANS; PLURIPOTENT STEM CELLS; TELOMERE; TELOMERE-BINDING PROTEINS;

IPS;

EID: 78149422436     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.10.49     Document Type: Review

References (149)

1. Makarov VL, Hirose Y, Langmore JP: Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell 88(5), 657-666 (1997).
2. Wellinger RJ, Sen D: The DNA structures at the ends of eukaryotic chromosomes. Eur J. Cancer 33(5), 735-749 (1997).
3. Wright WE, Tesmer VM, Huffman KE, Levene SD, Shay JW: Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev. 11(21), 2801-2809 (1997).
4. Griffth JD, Comeau L, Rosenfeld S et al.: Mammalian telomeres end in a large duplex loop. Cell 97(4), 503-514 (1999).
5. Greider CW: Telomeres do D-loop-T-loop. Cell 97(4), 419-422 (1999).
6. Collins K: Mammalian telomeres and telomerase. Curr. Opin Cell Biol. 12(3), 378-383 (2000).
7. Greider CW, Blackburn EH: Identifcation of a specifc telomere terminal transferase activity in Tetrahymena extracts. Cell 43(2 Pt 1), 405-413 (1985).
8. Greider CW, Blackburn EH: The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specifcity Cell 51(6), 887-898 (1987).
9. Cohen SB, Graham ME, Lovrecz GO, Bache N, Robinson PJ, Reddel RR: Protein composition of catalytically active human telomerase from immortal cells. Science 315(5820), 1850-1853 (2007).
10. Mitchell JR, Wood E, Collins K: A telomerase component is defective in the human disease dyskeratosis congenita. Nature 402(6761), 551-555 (1999).
11. Nakamura TM, Morin GB, Chapman KB et al.: Telomerase catalytic subunit homologs from fssion yeast and human. Science 277(5328), 955-959 (1997).
12. Feng J, Funk WD, Wang SS et al.: The RNA component of human telomerase. Science 269(5228), 1236-1241 (1995).
13. Pogacic V, Dragon F, Filipowicz W: Human H/ACA small nucleolar RNPs and telomerase share evolutionarily conserved proteins NHP2 and NOP10. Mol. Cell Biol. 20(23), 9028-9040 (2000).
14. Dragon F, Pogacic V, Filipowicz W: In vitro assembly of human H/ACA small nucleolar RNPs reveals unique features of U17 and telomerase RNAs. Mol. Cell Biol. 20(9), 3037-3048 (2000).
15. Mitchell JR, Collins K: Human telomerase activation requires two independent interactions between telomerase RNA and telomerase reverse transcriptase. Mol. Cell 6(2), 361-371 (2000).
16. Calado RT, Young NS: Telomere diseases. N. Engl. J. Med. 361(24), 2353-2365 (2009).
17. Vulliamy T, Marrone A, Goldman F et al.: The RNA component of telomerase is mutated in autosomal dominant dyskeratosis congenita. Nature 413(6854), 432-435 (2001). (Pubitemid 32928599)
18. Blasco MA, Lee HW, Rizen M, Hanahan D, DePinho R, Greider CW: Mouse models for the study of telomerase. Ciba Found. Symp. 211, 160-170, discussion 170-166 (1997).
19. Blasco MA, Lee HW, Hande MP et al.: Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91(1), 25-34 (1997).
20. -/- mice with short telomeres. EMBO Rep. 2(9), 800-807 (2001).
21. Leri A, Franco S, Zacheo A et al.: Ablation of telomerase and telomere loss leads to cardiac dilatation and heart failure associated with p53 upregulation. EMBO J. 22(1), 131-139 (2003).
22. Herrera E, Martinez AC, Blasco MA: Impaired germinal center reaction in mice with short telomeres. EMBO J. 19(3), 472-481 (2000).
23. -/- embryos is associated with failure to close the neural tube. EMBO J. 18(5), 1172-1181 (1999).
24. Flores I, Cayuela ML, Blasco MA: Effects of telomerase and telomere length on epidermal stem cell behavior. Science 309(5738), 1253-1256 (2005).
25. Armanios M: Syndromes of telomere shortening. Annu. Rev. Genomics Hum. Genet. 10, 45-61 (2009).
26. Calado RT, Regal JA, Kleiner DE et al.: A spectrum of severe familial liver disorders associate with telomerase mutations. PLoS ONE 4(11), e7926 (2009).
27. Calado RT, Young NS: Telomere maintenance and human bone marrow failure. Blood 111(9), 4446-4455 (2008).
28. Bryan TM, Englezou A, Dalla-Pozza L, Dunham MA, Reddel RR: Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med. 3(11), 1271-1274 (1997).
29. Bryan TM, Marusic L, Bacchetti S, Namba M, Reddel RR: The telomere lengthening mechanism in telomerase-negative immortal human cells does not involve the telomerase RNA subunit. Hum. Mol. Genet. 6(6), 921-926 (1997).
30. Bryan TM, Reddel RR: Telomere dynamics and telomerase activity in in vitro immortalised human cells. Eur. J. Cancer 33(5), 767-773 (1997).
31. Dunham MA, Neumann AA, Fasching CL, Reddel RR: Telomere maintenance by recombination in human cells. Nat. Genet. 26(4), 447-450 (2000).
32. Henson JD, Neumann AA, Yeager TR, Reddel RR: Alternative lengthening of telomeres in mammalian cells. Oncogene 21(4), 598-610 (2002).
33. Cesare AJ, Griffth JD: Telomeric DNA in ALT cells is characterized by free telomeric circles and heterogeneous T-loops. Mol. Cell Biol. 24(22), 9948-9957 (2004).
34. Tokutake Y, Matsumoto T, Watanabe T et al.: Extra-chromosomal telomere repeat DNA in telomerase-negative immortalized cell lines. Biochem. Biophys. Res. Commun. 247(3), 765-772 (1998).
35. Groff-Vindman C, Cesare AJ, Natarajan S, Griffth JD, McEachern MJ: Recombination at long mutant telomeres produces tiny single-and double-stranded telomeric circles. Mol. Cell Biol. 25(11), 4406-4412 (2005).
36. Yeager TR, Neumann AA, Englezou A, Huschtscha LI, Noble JR, Reddel RR: Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59(17), 4175-4179 (1999).
37. Grobelny JV, Godwin AK, Broccoli D: ALT-associated PML bodies are present in viable cells and are enriched in cells in the G(2)/M phase of the cell cycle. J. Cell. Sci. 113(Pt 24), 4577-4585 (2000).
38. Grobelny JV, Kulp-McEliece M, Broccoli D: Effects of reconstitution of telomerase activity on telomere maintenance by the alternative lengthening of telomeres (ALT) pathway Hum. Mol. Genet. 10(18), 1953-1961 (2001).
39. Royle NJ, Foxon J, Jeyapalan JN et al.: Telomere length maintenance-an ALTernative mechanism. Cytogenet. Genome Res. 122(3-4), 281-291 (2008).
40. Wu G, Jiang X, Lee WH, Chen PL: Assembly of functional ALT-associated promyelocytic leukemia bodies requires Nijmegen Breakage Syndrome 1. Cancer Res. 63(10), 2589-2595 (2003).
41. Wu G, Lee WH, Chen PL: NBS1 and TRF1 colocalize at promyelocytic leukemia bodies during late S/G2 phases in immortalized telomerase-negative cells. Implication of NBS1 in alternative lengthening of telomeres. J. Biol. Chem. 275(39), 30618-30622 (2000).
42. Molenaar C, Wiesmeijer K, Verwoerd NP et al.: Visualizing telomere dynamics in living mammalian cells using PNA probes. EMBO J. 22(24), 6631-6641 (2003).
43. Jiang WQ, Zhong ZH, Nguyen A et al.: Induction of alternative lengthening of telomeres-associated PML bodies by p53/p21 requires HP1 proteins. J. Cell Biol. 185(5), 797-810 (2009).
44. Zhong ZH, Jiang WQ, Cesare AJ, Neumann AA, Wadhwa R, Reddel RR: Disruption of telomere maintenance by depletion of the MRE11/RAD50/NBS1 complex in cells that use alternative lengthening of telomeres. J. Biol. Chem. 282(40), 29314-29322 (2007).
45. van Steensel B, Smogorzewska A, de Lange T: TRF2 protects human telomeres from end-to-end fusions. Cell 92(3), 401-413 (1998).
46. de Lange T: Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19(18), 2100-2110 (2005).
47. Baumann P, Cech TR: Pot1, the putative telomere end-binding protein in fssion yeast and humans. Science 292(5519), 1171-1175 (2001).
48. van Steensel B, de Lange T: Control of telomere length by the human telomeric protein TRF1. Nature 385(6618), 740-743 (1997).
49. Smogorzewska A, van Steensel B, Bianchi A et al.: Control of human telomere length by TRF1 and TRF2. Mol. Cell Biol. 20(5), 1659-1668 (2000).
50. Smith S, Giriat I, Schmitt A, de Lange T: Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 282(5393), 1484-1487 (1998).
51. Smith S, de Lange T: Tankyrase promotes telomere elongation in human cells. Curr. Biol. 10(20), 1299-1302 (2000).
52. Chang W, Dynek JN, Smith S: TRF1 is degraded by ubiquitin-mediated proteolysis after release from telomeres. Genes Dev. 17(11), 1328-1333 (2003).
53. Kaminker PG, Kim SH, Taylor RD et al.: TANK2, a new TRF1-associated poly(ADP-ribose) polymerase, causes rapid induction of cell death upon overexpression. J. Biol. Chem. 276(38), 35891-35899 (2001).
54. Cook BD, Dynek JN, Chang W, Shostak G, Smith S: Role for the related poly(ADP-Ribose) polymerases tankyrase 1 and 2 at human telomeres. Mol. Cell Biol. 22(1), 332-342 (2002).
55. Hsiao SJ, Poitras MF, Cook BD, Liu Y, Smith S: Tankyrase 2 poly(ADP-ribose) polymerase domain-deleted mice exhibit growth defects but have normal telomere length and capping. Mol. Cell Biol. 26(6), 2044-2054 (2006).
56. Karlseder J, Smogorzewska A, de Lange T: Senescence induced by altered telomere state, not telomere loss. Science 295(5564), 2446-2449 (2002).
57. Stansel RM, de Lange T, Griffth JD: T-loop assembly in vitro involves binding of TRF2 near the 3́ telomeric overhang. EMBO J. 20(19), 5532-5540 (2001).
58. Loayza D, De Lange T: POT1 as a terminal transducer of TRF1 telomere length control. Nature 423(6943), 1013-1018 (2003).
59. Veldman T, Etheridge KT, Counter CM: Loss of hPot1 function leads to telomere instability and a cut-like phenotype. Curr. Biol. 14(24), 2264-2270 (2004).
60. Ye JZ, Hockemeyer D, Krutchinsky AN et al.: POT1-interacting protein PIP1: a telomere length regulator that recruits POT1 to the TIN2/TRF1 complex. Genes Dev. 18(14), 1649-1654 (2004).
61. Hockemeyer D, Daniels JP, Takai H, de Lange T: Recent expansion of the telomeric complex in rodents: two distinct POT1 proteins protect mouse telomeres. Cell 126(1), 63-77 (2006).
62. Baumann P, Podell E, Cech TR: Human Pot1 (protection of telomeres) protein: cytolocalization, gene structure, and alternative splicing. Mol. Cell Biol. 22(22), 8079-8087 (2002).
63. Denchi EL, de Lange T: Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 448(7157), 1068-1071 (2007).
64. Ye JZ, de Lange T: TIN2 is a tankyrase 1 PARP modulator in the TRF1 telomere length control complex. Nat. Genet. 36(6), 618-623 (2004).
65. Ye JZ, Donigian JR, van Overbeek M et al: TIN2 binds TRF1 and TRF2 simultaneously and stabilizes the TRF2 complex on telomeres. J. Biol. Chem. 279(45), 47264-47271 (2004).
66. Hockemeyer D, Palm W, Else T et al.: Telomere protection by mammalian Pot1 requires interaction with Tpp1. Nat. Struct. Mol. Biol. 14(8), 754-761 (2007).
67. Liu D, O'Connor MS, Qin J, Songyang Z: Telosome, a mammalian telomere-associated complex formed by multiple telomeric proteins. J. Biol. Chem. 279(49), 338-51342 (2004).
68. Liu D, Safari A, O'Connor MS et al.: PTOP interacts with POT1 and regulates its localization to telomeres. Nat. Cell Biol. 6(7), 673-680 (2004).
69. Wang F, Podell ER, Zaug AJ et al.: The POT1-TPP1 telomere complex is a telomerase processivity factor. Nature 445(7127), 506-510 (2007).
70. Li B, Oestreich S, de Lange T: Identifcation of human Rap1: implications for telomere evolution. Cell 101(5), 471-483 (2000).
71. O'Connor MS, Safari A, Liu D, Qin J, Songyang Z: The human Rap1 protein complex and modulation of telomere length. J. Biol. Chem. 279(27), 28585-28591 (2004).
72. Verdun RE, Crabbe L, Haggblom C, Karlseder J: Functional human telomeres are recognized as DNA damage in G2 of the cell cycle. Mol. Cell 20(4), 551-561 (2005).
73. Verdun RE, Karlseder J: The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 127(4), 709-720 (2006).
74. Verdun RE, Karlseder J: Replication and protection of telomeres. Nature 447(7147), 924-931 (2007).
75. Zhu XD, Kuster B, Mann M, Petrini JH, de Lange T: Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25(3), 347-352 (2000). (Pubitemid 30437327)
76. Crabbe L, Verdun RE, Haggblom CI, Karlseder J: Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 306(5703), 1951-1953 (2004).
77. Yankiwski V, Marciniak RA, Guarente L, Neff NF: Nuclear structure in normal and Bloom syndrome cells. Proc. Natl Acad. Sci. USA 97(10), 5214-5219 (2000).
78. Crabbe L, Jauch A, Naeger CM, Holtgreve-Grez H, Karlseder J: Telomere dysfunction as a cause of genomic instability in Werner syndrome. Proc. Natl Acad. Sci. USA 104(7), 2205-2210 (2007).
79. Karlseder J: Telomeric proteins: clearing the way for the replication fork. Nat. Struct. Mol. Biol. 13(5), 386-387 (2006).
80. Garcia-Cao M, O'Sullivan R, Peters AH, Jenuwein T, Blasco MA: Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat. Genet. 36(1), 94-99 (2004).
81. Peters AH, Kubicek S, Mechtler K et al.: Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 12(6), 1577-1589 (2003).
82. Peters AH, O'Carroll D, Scherthan H et al.: Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability Cell 107(3), 323-337 (2001).
83. Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T: Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410(6824), 116-120 (2001).
84. Schotta G, Lachner M, Sarma K et al.: A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18(11), 1251-1262 (2004).
85. Lachner M, Jenuwein T: The many faces of histone lysine methylation. Curr. Opin Cell Biol. 14(3), 286-298 (2002).
86. Benetti R, Gonzalo S, Jaco I et al.: Suv4-20h defciency results in telomere elongation and derepression of telomere recombination. J. Cell Biol. 178(6), 925-936 (2007).
87. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI: Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292(5514), 110-113 (2001).
88. Bannister AJ, Zegerman P, Partridge JF et al.: Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410(6824), 120-124 (2001).
89. Schotta G, Sengupta R, Kubicek S et al.: A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev. 22(15), 2048-2061 (2008).
90. Gonzalo S, Jaco I, Fraga MF et al.: DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat. Cell Biol. 8(4), 416-424 (2006).
91. Garcia-Cao M, Gonzalo S, Dean D, Blasco MA: A role for the Rb family of proteins in controlling telomere length. Nat. Genet. 32(3), 415-419 (2002).
92. Gonzalo S, Blasco MA: Role of Rb family in the epigenetic defnition of chromatin. Cell Cycle 4(6), 752-755 (2005).
93. Shanower GA, Muller M, Blanton JL, Honti V, Gyurkovics H, Schedl P: Characterization of the grappa gene, the Drosophila histone H3 lysine 79 methyltransferase. Genetics 169(1), 173-184 (2005).
94. San-Segundo PA, Roeder GS: Role for the silencing protein Dot1 in meiotic checkpoint control. Mol. Biol. Cell 11(10), 3601-3615 (2000).
95. Jones B, Su H, Bhat A et al.: The histone H3K79 methyltransferase Dot1L is essential for mammalian development and heterochromatin structure. PLoS Genet. 4(9), e1000190 (2008).
96. Benetti R, Garcia-Cao M, Blasco MA: Telomere length regulates the epigenetic status of mammalian telomeres and subtelomeres. Nat. Genet. 39(2), 243-250 (2007).
97. Michishita E, McCord RA, Berber E et al.: SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 452(7186), 492-496 (2008).
98. Benetti R, Gonzalo S, Jaco I et al.: A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nat. Struct. Mol. Biol. 15(3), 268-279 (2008).
99. Vera E, Canela A, Fraga MF, Esteller M, Blasco MA: Epigenetic regulation of telomeres in human cancer. Oncogene 27(54), 6817-6833 (2008).
100. Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J: Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318(5851), 798-801 (2007).
101. Schoeftner S, Blasco MA. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat. Cell Biol. 10(2), 228-236 (2008).
102. Luke B, Lingner J: TERRA: telomeric repeat-containing RNA. EMBO J. 28(17), 2503-2510 (2009).
103. Azzalin CM, Lingner J: Telomeres: the silence is broken. Cell Cycle 7(9), 1161-1165 (2008).
104. Yehezkel S, Segev Y, Viegas-Pequignot E, Skorecki K, Selig S: Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions. Hum. Mol. Genet. 17(18), 2776-2789 (2008).
105. Deng Z, Campbell AE, Lieberman PM: TERRA, CpG methylation and telomere heterochromatin: lessons from ICF syndrome cells. Cell Cycle 9(1), 69-74 (2010).
106. Kanoh J, Francesconi S, Collura A et al.: The fssion yeast spSet1p is a histone H3-K4 methyltransferase that functions in telomere maintenance and DNA repair in an ATM kinase Rad3-dependent pathway. J. Mol. Biol. 326(4), 1081-1094 (2003).
107. Krogan NJ, Dover J, Khorrami S et al.: COMPASS, a histone H3 (lysine 4) methyltransferase required for telomeric silencing of gene expression. J. Biol. Chem. 277(13), 10753-10755 (2002).
108. Caslini C, Connelly JA, Serna A, Broccoli D, Hess JL: MLL associates with telomeres and regulates telomeric repeat-containing RNA transcription. Mol. Cell Biol. 29(16), 4519-4526 (2009).
109. Ng LJ, Cropley JE, Pickett HA, Reddel RR, Suter CM: Telomerase activity is associated with an increase in DNA methylation at the proximal subtelomere and a reduction in telomeric transcription. Nucleic Acids Res. 37(4), 1152-1159 (2009).
110. Deng Z, Norseen J, Wiedmer A, Riethman H, Lieberman PM: TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres. Mol. Cell 35(4), 403-413 (2009).
111. Hande MP, Samper E, Lansdorp P, Blasco MA: Telomere length dynamics and chromosomal instability in cells derived from telomerase null mice. J. Cell Biol. 144(4), 589-601 (1999).
112. Rudolph KL, Chang S, Lee HW et al.: Longevity, stress response, and cancer in aging telomerase-defcient mice. Cell 96(5), 701-712 (1999).
113. Niida H, Shinkai Y, Hande MP et al.: Telomere maintenance in telomerase-defcient mouse embryonic stem cells: characterization of an amplifed telomeric DNA. Mol. Cell Biol. 20(11), 4115-4127 (2000).
114. Tilman G, Loriot A, van Beneden A et al.: Subtelomeric DNA hypomethylation is not required for telomeric sister chromatid exchanges in ALT cells. Oncogene 28(14), 1682-1693 (2009).
115. Benetti R, Schoeftner S, Munoz P, Blasco MA: Role of TRF2 in the assembly of telomeric chromatin. Cell Cycle 7(21), 3461-3468 (2008).
116. Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, Misteli T: Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev. Cell 10(1), 105-116 (2006). (Pubitemid 43025681)
117. Meshorer E, Misteli T: Chromatin in pluripotent embryonic stem cells and differentiation. Nat. Rev. Mol. Cell Biol. 7(7), 540-546 (2006). (Pubitemid 44036459)
118. Azuara V, Perry P, Sauer S et al.: Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8(5), 532-538 (2006).
119. Bibikova M, Laurent LC, Ren B, Loring JF, Fan JB: Unraveling epigenetic regulation in embryonic stem cells. Cell Stem Cell 2(2), 123-134 (2008).
120. Bernstein BE, Mikkelsen TS, Xie X et al.: A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125(2), 315-326 (2006).
121. Boyer LA, Plath K, Zeitlinger J et al.: Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441(7091), 349-353 (2006).
122. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K: Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 20(9), 1123-1136 (2006).
123. Takahashi K, Tanabe K, Ohnuki M et al.: Induction of pluripotent stem cells from adult human fbroblasts by defned factors. Cell 131(5), 861-872 (2007).
124. Takahashi K, Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fbroblast cultures by defned factors. Cell 126(4), 663-676 (2006).
125. Maherali N, Hochedlinger K: Induced pluripotency of mouse and human somatic cells. Cold Spring Harb. Symp. Quant. Biol. 73, 157-162 (2008).
126. Blasco MA: Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. 6(8), 611-622 (2005).
127. Blasco MA: Telomere length, stem cells and aging. Nat. Chem. Biol. 3(10), 640-649 (2007).
128. Hiyama E, Hiyama K: Telomere and telomerase in stem cells. Br. J. Cancer 96(7), 1020-1024 (2007).
129. Sarin KY, Cheung P, Gilison D et al.: Conditional telomerase induction causes proliferation of hair follicle stem cells. Nature 436(7053), 1048-1052 (2005).
130. Flores I, Canela A, Vera E, Tejera A, Cotsarelis G, Blasco MA: The longest telomeres: a general signature of adult stem cell compartments. Genes Dev. 22(5), 654-667 (2008).
131. Siegl-Cachedenier I, Flores I, Klatt P, Blasco MA: Telomerase reverses epidermal hair follicle stem cell defects and loss of long-term survival associated with critically short telomeres. J. Cell Biol. 179(2), 277-290 (2007).
132. Liu L, Bailey SM, Okuka M et al.: Telomere lengthening early in development. Nat. Cell Biol. 9(12), 1436-1441 (2007).
133. Marion RM, Strati K, Li H et al.: Telomeres acquire embryonic stem cell characteristics in induced pluripotent stem cells. Cell Stem Cell 4(2), 141-154 (2009).
134. Wong LH, Ren H, Williams E et al.: Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res. 19(3), 404-414 (2009).
135. Ishov AM, Vladimirova OV, Maul GG: Heterochromatin and ND10 are cell-cycle regulated and phosphorylation-dependent alternate nuclear sites of the transcription repressor Daxx and SWI/SNF protein ATRX. J. Cell. Sci. 117(Pt 17), 3807-3820 (2004).
136. Kourmouli N, Sun YM, van der Sar S, Singh PB, Brown JP: Epigenetic regulation of mammalian pericentric heterochromatin in vivo by HP1. Biochem. Biophys. Res. Commun. 337(3), 901-907 (2005).
137. McDowell TL, Gibbons RJ, Sutherland H et al.: Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes. Proc. Natl Acad. Sci. USA 96(24), 13983-13988 (1999).
138. Nan X, Hou J, Maclean A et al.: Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc. Natl Acad. Sci. USA 104(8), 2709-2714 (2007).
139. Xue Y, Gibbons R, Yan Z et al.: The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc. Natl Acad. Sci. USA 100(19), 10635-10640 (2003).
140. Wong LH, McGhie JD, Sim M et al.: ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res. 20(3), 351-360 (2010).
141. Goldberg AD, Banaszynski LA, Noh KM et al.: Distinct factors control histone variant H3.3 localization at specifc genomic regions. Cell 140(5), 678-691 (2010).
142. Wakayama T, Rodriguez I, Perry AC, Yanagimachi R, Mombaerts P: Mice cloned from embryonic stem cells. Proc. Natl Acad. Sci. USA 96(26), 14984-14989 (1999).
143. Lanza RP, Cibelli JB, Blackwell C et al.: Extension of cell life-span and telomere length in animals cloned from senescent somatic cells. Science 288(5466), 665-669 (2000).
144. Betts D, Bordignon V, Hill J et al.: Reprogramming of telomerase activity and rebuilding of telomere length in cloned cattle. Proc. Natl Acad. Sci. USA 98(3), 1077-1082 (2001).
145. Tian XC, Xu J, Yang X: Normal telomere lengths found in cloned cattle. Nat. Genet. 26(3), 272-273 (2000).
146. Shiels PG, Kind AJ, Campbell KH et al.: Analysis of telomere lengths in cloned sheep. Nature 399(6734), 1316-1317 (1999).
147. Agarwal S, Loh YH, McLoughlin EM et al.: Telomere elongation in induced pluripotent stem cells from dyskeratosis congenita patients. Nature 464(7286), 292-296 (2010).
148. Marion RM, Strati K, Li H et al.: A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 460(7259), 1149-1153 (2009)
149. Nakano M, Cardinale S, Noskov VN et al.: Inactivation of a human kinetochore by specifc targeting of chromatin modifers. Dev. Cell 14(4), 507-522 (2008).