Enhanced telomere rejuvenation in pluripotent cells reprogrammed via nuclear transfer relative to induced pluripotent stem cells

Cell Stem Cell

Volumn 14, Issue 1, 2014, Pages 27-39

  Le, Rongrong ^a,b   Kou, Zhaohui ^b   Jiang, Yonghua ^a,b   Li, Ming ^b   Huang, Bo ^b   Liu, Wenqiang ^a,b   Li, Hui ^c   Kou, Xiaochen ^b   He, Wanzhong ^b   Rudolph, Karl Lenhard ^d   Ju, Zhenyu ^e   Gao, Shaorong ^b,f  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^c INSTITUTE OF ZOOLOGY   (China)

^d FRITZ LIPMANN INSTITUTE   (Germany)

^e HANGZHOU NORMAL UNIVERSITY   (China)

^f TONGJI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

TELOMERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS TRANSPLANTATION; CELL PROLIFERATION; CELL RENEWAL; COMPARATIVE STUDY; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; MITOCHONDRION; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PREMATURE AGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; REJUVENATION; SOMATIC CELL; TELOMERE; TELOMERE HOMEOSTASIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; IN SITU HYBRIDIZATION, FLUORESCENCE; INDUCED PLURIPOTENT STEM CELLS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; NEURAL PLATE; NUCLEAR REPROGRAMMING; NUCLEAR TRANSFER TECHNIQUES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; RNA, MESSENGER; TELOMERASE; TELOMERE;

EID: 84891724275     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2013.11.005     Document Type: Article

References (42)

1. L.N. Andrade, J.L. Nathanson, G.W. Yeo, C.F. Menck, and A.R. Muotri Evidence for premature aging due to oxidative stress in iPSCs from Cockayne syndrome Hum. Mol. Genet. 21 2012 3825 3834
2. B.I. Bae, H. Xu, S. Igarashi, M. Fujimuro, N. Agrawal, Y. Taya, S.D. Hayward, T.H. Moran, C. Montell, and C.A. Ross et al. p53 mediates cellular dysfunction and behavioral abnormalities in Huntington's disease Neuron 47 2005 29 41
3. L.F. Batista, M.F. Pech, F.L. Zhong, H.N. Nguyen, K.T. Xie, A.J. Zaug, S.M. Crary, J. Choi, V. Sebastiano, and A. Cherry et al. Telomere shortening and loss of self-renewal in dyskeratosis congenita induced pluripotent stem cells Nature 474 2011 399 402
4. M.A. Blasco Telomeres and human disease: ageing, cancer and beyond Nat. Rev. Genet. 6 2005 611 622
5. R.J. Callicott, and J.E. Womack Real-time PCR assay for measurement of mouse telomeres Comp. Med. 56 2006 17 22
6. V. Costa, and L. Scorrano Shaping the role of mitochondria in the pathogenesis of Huntington's disease EMBO J. 31 2012 1853 1864
7. F. d'Adda di Fagagna, P.M. Reaper, L. Clay-Farrace, H. Fiegler, P. Carr, T. Von Zglinicki, G. Saretzki, N.P. Carter, and S.P. Jackson A DNA damage checkpoint response in telomere-initiated senescence Nature 426 2003 194 198
8. S.P. Donald, X.Y. Sun, C.A. Hu, J. Yu, J.M. Mei, D. Valle, and J.M. Phang Proline oxidase, encoded by p53-induced gene-6, catalyzes the generation of proline-dependent reactive oxygen species Cancer Res. 61 2001 1810 1815
9. N. Exner, A.K. Lutz, C. Haass, and K.F. Winklhofer Mitochondrial dysfunction in Parkinson's disease: molecular mechanisms and pathophysiological consequences EMBO J. 31 2012 3038 3062
10. J.M. Facucho-Oliveira, and J.C. St John The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation Stem Cell Rev. 5 2009 140 158
11. G. Falco, S.L. Lee, I. Stanghellini, U.C. Bassey, T. Hamatani, and M.S. Ko Zscan4: a novel gene expressed exclusively in late 2-cell embryos and embryonic stem cells Dev. Biol. 307 2007 539 550
12. S. Ferrón, H. Mira, S. Franco, M. Cano-Jaimez, E. Bellmunt, C. Ramírez, I. Fariñas, and M.A. Blasco Telomere shortening and chromosomal instability abrogates proliferation of adult but not embryonic neural stem cells Development 131 2004 4059 4070
13. C.W. Greider, and E.H. Blackburn Identification of a specific telomere terminal transferase activity in Tetrahymena extracts Cell 43 1985 405 413
14. C.W. Greider, and E.H. Blackburn The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity Cell 51 1987 887 898
15. M.P. Hande, E. Samper, P. Lansdorp, and M.A. Blasco Telomere length dynamics and chromosomal instability in cells derived from telomerase null mice J. Cell Biol. 144 1999 589 601
16. W. He, P. Cowin, and D.L. Stokes Untangling desmosomal knots with electron tomography Science 302 2003 109 113
17. E. Herrera, E. Samper, and M.A. Blasco Telomere shortening in mTR-/- embryos is associated with failure to close the neural tube EMBO J. 18 1999 1172 1181
18. E. Herrera, E. Samper, J. Martín-Caballero, J.M. Flores, H.W. Lee, and M.A. Blasco Disease states associated with telomerase deficiency appear earlier in mice with short telomeres EMBO J. 18 1999 2950 2960
19. H. Hong, K. Takahashi, T. Ichisaka, T. Aoi, O. Kanagawa, M. Nakagawa, K. Okita, and S. Yamanaka Suppression of induced pluripotent stem cell generation by the p53-p21 pathway Nature 460 2009 1132 1135
20. J. Hu, S.S. Hwang, M. Liesa, B. Gan, E. Sahin, M. Jaskelioff, Z. Ding, H. Ying, A.T. Boutin, and H. Zhang et al. Antitelomerase therapy provokes ALT and mitochondrial adaptive mechanisms in cancer Cell 148 2012 651 663
21. J. Jiang, W. Lv, X. Ye, L. Wang, M. Zhang, H. Yang, M. Okuka, C. Zhou, X. Zhang, L. Liu, and J. Li Zscan4 promotes genomic stability during reprogramming and dramatically improves the quality of iPS cells as demonstrated by tetraploid complementation Cell Res. 23 2013 92 106
22. T. Kawamura, J. Suzuki, Y.V. Wang, S. Menendez, L.B. Morera, A. Raya, G.M. Wahl, and J.C. Izpisúa Belmonte Linking the p53 tumour suppressor pathway to somatic cell reprogramming Nature 460 2009 1140 1144
23. R.P. Lanza, J.B. Cibelli, C. Blackwell, V.J. Cristofalo, M.K. Francis, G.M. Baerlocher, J. Mak, M. Schertzer, E.A. Chavez, and N. Sawyer et al. Extension of cell life-span and telomere length in animals cloned from senescent somatic cells Science 288 2000 665 669
24. H.W. Lee, M.A. Blasco, G.J. Gottlieb, J.W. Horner 2nd, C.W. Greider, and R.A. DePinho Essential role of mouse telomerase in highly proliferative organs Nature 392 1998 569 574
25. L. Liu, S.M. Bailey, M. Okuka, P. Muñoz, C. Li, L. Zhou, C. Wu, E. Czerwiec, L. Sandler, and A. Seyfang et al. Telomere lengthening early in development Nat. Cell Biol. 9 2007 1436 1441
26. R.M. Marión, K. Strati, H. Li, M. Murga, R. Blanco, S. Ortega, O. Fernandez-Capetillo, M. Serrano, and M.A. Blasco A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity Nature 460 2009 1149 1153
27. R.M. Marion, K. Strati, H. Li, A. Tejera, S. Schoeftner, S. Ortega, M. Serrano, and M.A. Blasco Telomeres acquire embryonic stem cell characteristics in induced pluripotent stem cells Cell Stem Cell 4 2009 141 154
28. S. Matoba, J.G. Kang, W.D. Patino, A. Wragg, M. Boehm, O. Gavrilova, P.J. Hurley, F. Bunz, and P.M. Hwang p53 regulates mitochondrial respiration Science 312 2006 1650 1653
29. E. Mizutani, T. Ono, C. Li, R. Maki-Suetsugu, and T. Wakayama Propagation of senescent mice using nuclear transfer embryonic stem cell lines Genesis 46 2008 478 483
30. K.L. Rudolph, S. Chang, H.W. Lee, M. Blasco, G.J. Gottlieb, C. Greider, and R.A. DePinho Longevity, stress response, and cancer in aging telomerase-deficient mice Cell 96 1999 701 712
31. E. Sahin, and R.A. Depinho Linking functional decline of telomeres, mitochondria and stem cells during ageing Nature 464 2010 520 528
32. E. Sahin, S. Colla, M. Liesa, J. Moslehi, F.L. Müller, M. Guo, M. Cooper, D. Kotton, A.J. Fabian, and C. Walkey et al. Telomere dysfunction induces metabolic and mitochondrial compromise Nature 470 2011 359 365
33. I. Sancho-Martinez, and J.C. Izpisua Belmonte Will SCNT-ESCs be better than iPSCs for personalized regenerative medicine? Cell Stem Cell 13 2013 141 142
34. A. Sfeir, S.T. Kosiyatrakul, D. Hockemeyer, S.L. MacRae, J. Karlseder, C.L. Schildkraut, and T. de Lange Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication Cell 138 2009 90 103
35. T. Sperka, Z. Song, Y. Morita, K. Nalapareddy, L.M. Guachalla, A. Lechel, Y. Begus-Nahrmann, M.D. Burkhalter, M. Mach, and F. Schlaudraff et al. Puma and p21 represent cooperating checkpoints limiting self-renewal and chromosomal instability of somatic stem cells in response to telomere dysfunction Nat. Cell Biol. 14 2012 73 79
36. M. Tachibana, P. Amato, M. Sparman, N.M. Gutierrez, R. Tippner-Hedges, H. Ma, E. Kang, A. Fulati, H.S. Lee, and H. Sritanaudomchai et al. Human embryonic stem cells derived by somatic cell nuclear transfer Cell 153 2013 1228 1238
37. H. Vaziri, K.B. Chapman, A. Guigova, J. Teichroeb, M.D. Lacher, H. Sternberg, I. Singec, L. Briggs, J. Wheeler, and J. Sampathkumar et al. Spontaneous reversal of the developmental aging of normal human cells following transcriptional reprogramming Regen. Med. 5 2010 345 363
38. T. Wakayama, Y. Shinkai, K.L. Tamashiro, H. Niida, D.C. Blanchard, R.J. Blanchard, A. Ogura, K. Tanemura, M. Tachibana, and A.C. Perry et al. Cloning of mice to six generations Nature 407 2000 318 319
39. F. Wang, Y. Yin, X. Ye, K. Liu, H. Zhu, L. Wang, M. Chiourea, M. Okuka, G. Ji, and J. Dan et al. Molecular insights into the heterogeneity of telomere reprogramming in induced pluripotent stem cells Cell Res. 22 2012 757 768
40. G.L. Yu, J.D. Bradley, L.D. Attardi, and E.H. Blackburn In vivo alteration of telomere sequences and senescence caused by mutated Tetrahymena telomerase RNAs Nature 344 1990 126 132
41. M. Zalzman, G. Falco, L.V. Sharova, A. Nishiyama, M. Thomas, S.L. Lee, C.A. Stagg, H.G. Hoang, H.T. Yang, and F.E. Indig et al. Zscan4 regulates telomere elongation and genomic stability in ES cells Nature 464 2010 858 863
42. J. Zhang, E. Nuebel, G.Q. Daley, C.M. Koehler, and M.A. Teitell Metabolic regulation in pluripotent stem cells during reprogramming and self-renewal Cell Stem Cell 11 2012 589 595