Zscan4 Is Activated after Telomere Shortening in Mouse Embryonic Stem Cells

Stem Cell Reports

Volumn 6, Issue 4, 2016, Pages 483-495

  Nakai Futatsugi, Yoko ^a,c   Niwa, Hitoshi ^a,b,d  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; DNA BINDING PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; MESSENGER RNA; REX1 PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER AND SCAN DOMAIN CONTAINING 4 PROTEIN; GREEN FLUORESCENT PROTEIN; LUCIFERASE; REX-1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; ZSCAN4C PROTEIN, MOUSE; ZSCAN4D PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL DEATH; CELL PROLIFERATION; EMBRYO; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; MALE; MOUSE; MOUSE EMBRYONIC STEM CELL; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REJUVENATION; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING; UPREGULATION; ANIMAL; BIOLOGICAL MODEL; CELL CYCLE; CYTOLOGY; FLUORESCENCE IN SITU HYBRIDIZATION; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TELOMERE; TIME FACTOR; TIME LAPSE IMAGING;

ANIMALS; CELL CYCLE; GREEN FLUORESCENT PROTEINS; IN SITU HYBRIDIZATION, FLUORESCENCE; LUCIFERASES; MICE; MICROSCOPY, FLUORESCENCE; MODELS, GENETIC; MOUSE EMBRYONIC STEM CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TELOMERE; TELOMERE SHORTENING; TIME FACTORS; TIME-LAPSE IMAGING; TRANSCRIPTION FACTORS;

EID: 84961230921     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2016.02.010     Document Type: Article

References (43)

1. K. Adachi, I. Nikaido, H. Ohta, S. Ohtsuka, H. Ura, M. Kadota, T. Wakayama, H.R. Ueda, and H. Niwa Context-dependent wiring of Sox2 regulatory networks for self-renewal of embryonic and trophoblast stem cells Mol. Cell 52 2013 380 392
2. T. Akiyama, L. Xin, M. Oda, A.A. Sharov, M. Amano, Y. Piao, J.S. Cadet, D.B. Dudekula, Y. Qian, W. Wang, and et al. Transient bursts of Zscan4 expression are accompanied by the rapid derepression of heterochromatin in mouse embryonic stem cells DNA Res. 22 2015 307 318
3. T. Amano, T. Hirata, G. Falco, M. Monti, L.V. Sharova, M. Amano, S. Sheer, H.G. Hoang, Y. Piao, C.A. Stagg, and et al. Zscan4 restores the developmental potency of embryonic stem cells Nat. Commun. 4 2013 1966
4. G.M. Baerlocher, I. Vulto, G. de Jong, and P.M. Lansdorp Flow cytometry and FISH to measure the average length of telomeres (flow FISH) Nat. Protoc. 1 2006 2365 2376
5. E.H. Blackburn Switching and signaling at the telomere Cell 106 2001 661 673
6. R.J. Callicott, and J.E. Womack Real-time PCR assay for measurement of mouse telomeres Comp. Med. 56 2006 17 22
7. M.G. Carter, C.A. Stagg, G. Falco, T. Yoshikawa, U.C. Bassey, K. Aiba, L.V. Sharova, N. Shaik, and M.S. Ko An in situ hybridization-based screen for heterogeneously expressed genes in mouse ES cells Gene Expr. Patterns 8 2008 181 198
8. L. Cerulo, D. Tagliaferri, P. Marotta, P. Zoppoli, F. Russo, C. Mazio, M. DeFelice, M. Ceccarelli, and G. Falco Identification of a novel gene signature of ES cells self-renewal fluctuation through system-wide analysis PLoS One 9 2014 e83235
9. I. Chambers, J. Silva, D. Colby, J. Nichols, B. Nijmeijer, M. Robertson, J. Vrana, K. Jones, L. Grotewold, and A. Smith Nanog safeguards pluripotency and mediates germline development Nature 450 2007 1230 1234
10. Y. Doksani, and T. de Lange The role of double-strand break repair pathways at functional and dysfunctional telomeres Cold Spring Harb Perspect. Biol. 6 2014 a016576
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. Fujii, S. Nishikawa-Torikai, Y. Futatsugi, Y. Toyooka, M. Yamane, S. Ohtsuka, and H. Niwa Nr0b1 is a negative regulator of Zscan4c in mouse embryonic stem cells Sci. Rep. 5 2015 9146
13. F. Gutierrez-Rodrigues, B.A. Santana-Lemos, P.S. Scheucher, R.M. Alves-Paiva, and R.T. Calado Direct comparison of flow-FISH and qPCR as diagnostic tests for telomere length measurement in humans PLoS One 9 2014 e113747
14. J.W. Harper, and S.J. Elledge The DNA damage response: ten years after Mol. Cell 28 2007 739 745
15. K. Hayashi, S.M. Lopes, F. Tang, and M.A. Surani Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional epigenetic status Cell Stem Cell 3 2008 391 401
16. T. Hirata, T. Amano, Y. Nakatake, M. Amano, Y. Piao, H.G. Hoang, and M.S. Ko Zscan4 transiently reactivates early embryonic genes during the generation of induced pluripotent stem cells Sci. Rep. 2 2012 208
17. K. Hoffmeyer, A. Raggioli, S. Rudloff, R. Anton, A. Hierholzer, I. Del Valle, K. Hein, R. Vogt, and R. Kemler Wnt/β-catenin signaling regulates telomerase in stem cells and cancer cells Science 336 2012 1549 1554
18. J. Huang, F. Wang, M. Okuka, N. Liu, G. Ji, X. Ye, B. Zuo, M. Li, P. Liang, W.W. Ge, and et al. Association of telomere length with authentic pluripotency of ES/iPS cells Cell Res. 21 2011 779 792
19. M. Iyer, L. Wu, M. Carey, Y. Wang, A. Smallwood, and S.S. Gambhir Two-step transcriptional amplification as a method for imaging reporter gene expression using weak promoters Proc. Natl. Acad. Sci. USA 98 2001 14595 14600
20. T. Kunath, M.K. Saba-El-Leil, M. Almousailleakh, J. Wray, S. Meloche, and A. Smith FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment Development 134 2007 2895 2902
21. P.M. Lansdorp, N.P. Verwoerd, F.M. van de Rijke, V. Dragowska, M.T. Little, R.W. Dirks, A.K. Raap, and H.J. Tanke Heterogeneity in telomere length of human chromosomes Hum. Mol. Genet. 5 1996 685 691
22. T.S. Macfarlan, W.D. Gifford, S. Driscoll, K. Lettieri, H.M. Rowe, D. Bonanomi, A. Firth, O. Singer, D. Trono, and S.L. Pfaff Embryonic stem cell potency fluctuates with endogenous retrovirus activity Nature 487 2012 57 63
23. R.S. Maser, and R.A. DePinho Telomeres and the DNA damage response: why the fox is guarding the henhouse DNA Repair (Amst) 3 2004 979 988
24. S. Masui, D. Shimosato, Y. Toyooka, R. Yagi, K. Takahashi, and H. Niwa An efficient system to establish multiple embryonic stem cell lines carrying an inducible expression unit Nucleic Acids Res. 33 2005 e43
25. S. Masui, S. Ohtsuka, R. Yagi, K. Takahashi, M.S. Ko, and H. Niwa Rex1/Zfp42 is dispensable for pluripotency in mouse ES cells BMC Dev. Biol. 8 2008 45
26. A. Mazouzi, G. Velimezi, and J.I. Loizou DNA replication stress: causes, resolution and disease Exp. Cell Res. 329 2014 85 93
27. Y. Nakai-Futatsugi, and H. Niwa Transcription factor network in embryonic stem cells: heterogeneity under the stringency Biol. Pharm. Bull. 36 2013 166 170
28. J. Nichols, B. Zevnik, K. Anastassiadis, H. Niwa, D. Klewe-Nebenius, I. Chambers, H. Schöler, and A. Smith Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4 Cell 95 1998 379 391
29. H. Niwa, J. Miyazaki, and A.G. Smith Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells Nat. Genet. 24 2000 372 376
30. H. Niwa, K. Ogawa, D. Shimosato, and K. Adachi A parallel circuit of LIF signaling pathways maintains pluripotency of mouse ES cells Nature 460 2009 118 122
31. S. Pauklin, and L. Vallier The cell-cycle state of stem cells determines cell fate propensity Cell 155 2013 135 147
32. S. Pauklin, R.A. Pedersen, and L. Vallier Mouse pluripotent stem cells at a glance J. Cell Sci. 124 2011 3727 3732
33. F. Pucci, L. Gardano, and L. Harrington Short telomeres in ESCs lead to unstable differentiation Cell Stem Cell 12 2013 479 486
34. N. Rufer, W. Dragowska, G. Thornbury, E. Roosnek, and P.M. Lansdorp Telomere length dynamics in human lymphocyte subpopulations measured by flow cytometry Nat. Biotechnol. 16 1998 743 747
35. A. Sakaue-Sawano, H. Kurokawa, T. Morimura, A. Hanyu, H. Hama, H. Osawa, S. Kashiwagi, K. Fukami, T. Miyata, H. Miyoshi, and et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression Cell 132 2008 487 498
36. A.M. Singh, T. Hamazaki, K.E. Hankowski, and N. Terada A heterogeneous expression pattern for Nanog in embryonic stem cells Stem Cells 25 2007 2534 2542
37. M.P. Storm, B. Kumpfmueller, H.K. Bone, M. Buchholz, Y. Sanchez Ripoll, J.B. Chaudhuri, H. Niwa, D. Tosh, and M.J. Welham Zscan4 is regulated by PI3-kinase and DNA-damaging agents and directly interacts with the transcriptional repressors LSD1 and CtBP2 in mouse embryonic stem cells PLoS One 9 2014 e89821
38. Y. Toyooka, D. Shimosato, K. Murakami, K. Takahashi, and H. Niwa Identification and characterization of subpopulations in undifferentiated ES cell culture Development 135 2008 909 918
39. A. Tsakiridis, E. Tzouanacou, A. Rahman, D. Colby, R. Axton, I. Chambers, V. Wilson, L. Forrester, and J.M. Brickman Expression-independent gene trap vectors for random and targeted mutagenesis in embryonic stem cells Nucleic Acids Res. 37 2009 e129
40. J. White, and S. Dalton Cell cycle control of embryonic stem cells Stem Cell Rev. 1 2005 131 138
41. C.W. Wong, P.S. Hou, S.F. Tseng, C.L. Chien, K.J. Wu, H.F. Chen, H.N. Ho, S. Kyo, and S.C. Teng Krüppel-like transcription factor 4 contributes to maintenance of telomerase activity in stem cells Stem Cells 28 2010 1510 1517
42. Q.-L. Ying, J. Wray, J. Nichols, L. Batlle-Morera, B. Doble, J. Woodgett, P. Cohen, and A. Smith The ground state of embryonic stem cell self-renewal Nature 453 2008 519 523
43. M. Zalzman, G. Falco, L.V. Sharova, A. Nishiyama, M. Thomas, S.L. Lee, C.A. Stagg, H.G. Hoang, H.T. Yang, F.E. Indig, and et al. Zscan4 regulates telomere elongation and genomic stability in ES cells Nature 464 2010 858 863