Reprogramming of telomeric regions during the generation of human induced pluripotent stem cells and subsequent differentiation into fibroblast-like derivatives

Epigenetics

Volumn 6, Issue 1, 2011, Pages 63-75

  Yehezkel, Shiran ^a   Rebibo Sabbah, Annie ^a   Segev, Yardena ^a   Tzukerman, Maty ^a   Shaked, Rony ^a   Huber, Irit ^a   Gepstein, Lior ^a   Skorecki, Karl ^a   Selig, Sara ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

DNA methylation; Human induced pluripotent stem cells; Subtelomeres; Telomerase; Telomeres; TERRA

Indexed keywords

PROTEIN TERRA; RNA; TELOMERASE; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CHROMOSOME SIZE; DEMETHYLATION; DNA METHYLATION; ENZYME ACTIVATION; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; MOLECULAR CLONING; PLURIPOTENT STEM CELL; PREPUCE; TELOMERE;

IPS;

EID: 78651228154     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.6.1.13390     Document Type: Article

References (63)

1. Amabile G, Meissner A. Induced pluripotent stem cells: current progress and potential for regenerative medicine. Trends Mol Med 2009; 15:59-68.
2. Zhao R, Daley GQ. From fibroblasts to iPS cells: induced pluripotency by defined factors. J Cell Biochem 2008; 105:949-955.
3. Maherali N, Sridharan R, Xie W, Utikal J, Eminli S, Arnold K, et al. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 2007; 1:55-70.
4. Mikkelsen TS, Hanna J, Zhang X, Ku M, Wernig M, Schorderet P, et al. Dissecting direct reprogramming through integrative genomic analysis. Nature 2008; 454:49-55.
5. Park IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008; 451:141-146.
6. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-872.
7. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126:663-676.
8. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, et al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 2007; 448:318-324.
9. Marion RM, Strati K, Li H, Tejera A, Schoeftner S, Ortega S, et al. Telomeres acquire embryonic stem cell characteristics in induced pluripotent stem cells. Cell Stem Cell 2009; 4:141-154.
10. Suhr ST, Chang EA, Rodriguez RM, Wang K, Ross PJ, Beyhan Z, et al. Telomere dynamics in human cells reprogrammed to pluripotency. PLoS One 2009; 4:8124.
11. Hug N, Lingner J. Telomere length homeostasis. Chromosoma 2006; 115:413-425.
12. LeBel C, Wellinger RJ. Telomeres: what's new at your end? J Cell Sci 2005; 118:2785-2788.
13. Zakian VA. Telomeres: beginning to understand the end. Science 1995; 270:1601-1607.
14. Harley CB, Futcher AB, Greider CW Telomeres shorten during ageing of human fibroblasts. Nature 1990; 345:458-460.
15. Allsopp RC, Harley CB. Evidence for a critical telomere length in senescent human fibroblasts. Exp Cell Res 1995; 219:130-136.
16. Mathew R, Jia W, Sharma A, Zhao Y, Clarke LE, Cheng X, et al. Robust activation of the human but not mouse telomerase gene during the induction of pluripotency. FASEB J 2010; 24:2702-2715.
17. Carpenter MK, Rosler E, Rao MS. Characterization and differentiation of human embryonic stem cells. Cloning Stem Cells 2003; 5:79-88.
18. Vaziri H, Chapman KB, Guigova A, Teichroeb J, Lacher MD, Sternberg H, et al. Spontaneous reversal of the developmental aging of normal human cells following transcriptional reprogramming. Reg Med 2010; 5:345-363.
19. Chan SW, Blackburn EH. New ways not to make ends meet: telomerase, DNA damage proteins and hetero-chromatin. Oncogene 2002; 21:553-563.
20. Blasco MA. Telomere epigenetics: a higher-order control of telomere length in mammalian cells. Carcinogenesis 2004; 25:1083-1087.
21. Blasco MA. The epigenetic regulation of mammalian telomeres. Nat Rev Genet 2007; 8:299-309.
22. Schoeftner S, Blasco MA. A 'higher order' of telomere regulation: telomere heterochromatin and telomeric RNAs. EMBO J 2009; 28:2323-2336.
23. Azzalin CM, Reichenback P, Khoriauli L, Giulotto E, Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007; 318:798-801.
24. Schoeftner S, Blasco MA. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 2008; 10:228-236.
25. Ambrosini A, Paul S, Hu S, Riethman H. Human subtelomeric duplicon structure and organization. Genome Biol 2007; 8:1511-1513.
26. Deng Z, Campbell AE, Lieberman PM. TERRA, CpG methylation and telomere heterochromatin: lessons from ICF syndrome cells. Cell Cycle 2010; 9:69-74.
27. Lee ME, Rha SY, Jeung HC, Chung HC, Oh BK. Subtelomeric DNA methylation and telomere length in human cancer cells. Cancer Lett 2009; 281:82-91.
28. 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 2009; 37:1152-1159.
29. Tilman G, Loriot A, Van Beneden A, Arnoult N, Londono-Vallejo JA, De Smet C, et al. Subtelomeric DNA hypomethylation is not required for telomeric sister chromatid exchanges in ALT cells. Oncogene 2009; 28:1682-1693.
30. Vera E, Canela A, Fraga MF, Esteller M, Blasco MA. Epigenetic regulation of telomeres in human cancer. Oncogene 2008; 27:6817-6833.
31. 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 2008; 17:2776-2789.
32. Masutomi K, Yu EY, Khurts S, Ben-Porath I, Currier JL, Metz GB, et al. Telomerase maintains telomere structure in normal human cells. Cell 2003; 114:241-253.
33. Forsyth NR, Wright WE, Shay JW Telomerase and differentiation in multicellular organisms: turn it off, turn it on, and turn it off again. Differentiation 2002; 69:188-197.
34. Greenberg RA, Allsopp RC, Chin L, Morin GB, DePinho RA. Expression of mouse telomerase reverse transcriptase during development, differentiation and proliferation. Oncogene 1998; 16:1723-1730.
35. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318:1917-1920.
36. Liu L, Bailey SM, Okuka M, Munoz P, Li C, Zhou L, et al. Telomere lengthening early in development. Nat Cell Biol 2007; 9:1436-1441.
37. Henson JD, Neumann AA, Yeager TR, Reddel RR. Alternative lengthening of telomeres in mammalian cells. Oncogene 2002; 21:598-610.
38. Cerone MA, Londono-Vallejo JA, Bacchetti S. Telomere maintenance by telomerase and by recombination can coexist in human cells. Hum Mol Genet 2001; 10:1945-1952.
39. Chen T, Ueda Y, Dodge JE, Wang Z, Li E. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol Cell Biol 2003; 23:5594-5605.
40. Okano M, Bell DW, Haber DA, Li E. DNA methyl-transferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999; 99:247-257.
41. Ueda Y, Okano M, Williams C, Chen T, Georgopoulos K, Li E. Roles for Dnmt3b in mammalian development: a mouse model for the ICF syndrome. Development 2006; 133:1183-1192.
42. Huntriss J, Hinkins M, Oliver B, Harris SE, Beazley JC, Rutherford AJ, et al. Expression of mRNAs for DNA methyltransferases and methyl-CpG-binding proteins in the human female germ line, preimplanta-tion embryos, and embryonic stem cells. Mol Reprod Dev 2004; 67:323-336.
43. Robertson KD, Uzvolgyi E, Liang G, Talmadge C, Sumegi J, Gonzales FA, et al. The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors. Nucleic Acids Res 1999; 27:2291-2298.
44. Suetake I, Shinozaki F, Miyagawa J, Takeshima H, Tajima S. DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction. J Biol Chem 2004; 279:27816-27823.
45. Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N, Bugge M, et al. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 1999; 402:187-191.
46. Nergadze SG, Farnung BO, Wischnewski H, Khoriauli L, Vitelli V, Chawla R, et al. CpG-island promoters drive transcription of human telomeres. RNA 2009; 15:2186-2194.
47. Marion RM, Blasco MA. Telomere rejuvenation during nuclear reprogramming. Curr Opin Genet Dev 2010; 20:1-7.
48. Allen ND, Baird DM. Telomere length maintenance in stem cell populations. Biochim Biophys Acta 2009; 1792:324-328.
49. Amit M, Carpenter MK, Inokuma MS, Chiu CP, Harris CP, Waknitz MA, et al. Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 2000; 227:271-278.
50. Rosler ES, Fisk GJ, Ares X, Irving J, Miura T, Rao MS, et al. Long-term culture of human embryonic stem cells in feeder-free conditions. Dev Dyn 2004; 229:259-274.
51. Okano M, Takebayashi S, Okumura K, Li E. Assignment of cytosine-5 DNA methyltransferases Dnmt3a and Dnmt3b to mouse chromosome bands 12A2-A3 and 2H1 by in situ hybridization. Cytogenet Cell Genet 1999; 86:333-334.
52. Ooi SK, Bestor TH. The colorful history of active DNA demethylation. Cell 2008; 133:1145-1148.
53. Bhutani N, Brady JJ, Damian M, Sacco A, Corbel SY, Blau HM. Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463:1042-1047.
54. Luke B, Panza A, Redon S, Iglesias N, Li Z, Lingner J. The Rat1p 5' to 3' exonuclease degrades telomeric repeat-containing RNA and promotes telomere elongation in Saccharomyces cerevisiae. Mol Cell 2008; 32:465-477.
55. Luke B, Lingner J. TERRA: telomeric repeat-containing RNA. EMBO J 2009; 28:2503-2510.
56. Yalon M, Gal S, Segev Y, Selig S, Skorecki KL. Sister chromatid separation at human telomeric regions. J Cell Sci 2004; 117:1961-1970.
57. Naviaux RK, Costanzi E, Haas M, Verma IM. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J Virol 1996; 70:5701-5705.
58. Lowry WE, Richter L, Yachechko R, Pyle AD, Tchieu J, Sridharan R, et al. Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc Natl Acad Sci USA 2008; 105:2883-2888.
59. Huangfu D, Osafune K, Maehr R, Guo W, Eijkelenboom A, Chen S, et al. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 2008; 26:1269-1275.
60. Kehat I, Kenyagin-Karsenti D, Snir M, Segev H, Amit M, Gepstein A, et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 2001; 108:407-414.
61. Tzukerman M, Rosenberg T, Reiter I, Ben-Eliezer S, Denkberg G, Coleman R, et al. The influence of a human embryonic stem cell-derived microenvironment on targeting of human solid tumor xenografts. Cancer Res 2006; 66:3792-3801.
62. Xu C, Inokuma MS, Denham J, Golds K, Kundu P, Gold JD, et al. Feeder-free growth of undifferentiated huma'n embryonic stem cells. Nat Biotechnol 2001; 19:971-974.
63. Jiang YL, Rigolet M, Bourc'his D, Nigon F, Bokesoy I, Fryns JP, et al. DNMT3B mutations and DNA meth ylation defect define two types of ICF syndrome. Hum Mutat 2005; 25:56-63.