PRDM14 promotes active DNA demethylation through the Teneleven translocation (TET)-mediated base excision repair pathway in embryonic stem cells

Development (Cambridge)

Volumn 141, Issue 2, 2014, Pages 269-280

  Okashita, Naoki ^a   Kumaki, Yuichi ^b   Ebi, Kuniaki ^a   Nishi, Miyuki ^a   Okamoto, Yoshinori ^c   Nakayama, Megumi ^a   Hashimoto, Shota ^a   Nakamura, Tomohumi ^d   Sugasawa, Kaoru ^d   Kojima, Nakao ^c   Takada, Tatsuyuki ^e   Okano, Masaki ^b   Seki, Yoshiyuki ^a  

^a KWANSEI GAKUIN UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c MEIJO UNIVERSITY   (Japan)

^d KOBE UNIVERSITY   (Japan)

^e RITSUMEIKAN UNIVERSITY   (Japan)

Author keywords

Base excision repair (BER); DNA demethylation; Embryonic stem cells; Mouse; Ten eleven translocation (TET)

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; DNA METHYLTRANSFERASE 3B; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PRDM14 PROTEIN; PROTEIN; TEN ELEVEN TRANSLOCATION PROTEIN; TEN ELEVEN TRANSLOCATION PROTEIN 1; TEN ELEVEN TRANSLOCATION PROTEIN 2; THYMINE DNA GLYCOSYLASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; EMBRYONIC STEM CELL; EXCISION REPAIR; GENE EXPRESSION; GENE LOCUS; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

EID: 84891523954     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.099622     Document Type: Article

References (48)

1. Cortellino, S., Xu, J., Sannai, M., Moore, R., Caretti, E., Cigliano, A., Le Coz, M., Devarajan, K., Wessels, A., Soprano, D. et al. (2011). Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146, 67-79.
2. Dawlaty, M. M., Breiling, A., Le, T., Raddatz, G., Barrasa, M. I., Cheng, A. W., Gao, Q., Powell, B. E., Li, Z., Xu, M. et al. (2013). Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev. Cell 24, 310-323.
3. Ficz, G., Branco, M. R., Seisenberger, S., Santos, F., Krueger, F., Hore, T. A., Marques, C. J., Andrews, S. and Reik, W. (2011). Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473, 398-402.
4. Ficz, G., Hore, T. A., Santos, F., Lee, H. J., Dean, W., Arand, J., Krueger, F., Oxley, D., Paul, Y. L., Walter, J. et al. (2013). FGF signaling inhibition in ESCs drives rapid genome-wide demethylation to the epigenetic ground state of pluripotency. Cell Stem Cell 13, 351-359.
5. Grabole, N., Tischler, J., Hackett, J. A., Kim, S., Tang, F., Leitch, H. G., Magnúsdóttir, E. and Surani, M. A. (2013). Prdm14 promotes germline fate and naive pluripotency by repressing FGF signalling and DNA methylation. EMBO Rep. 14, 629-637.
6. Guibert, S., Forné, T. and Weber, M. (2012). Global profiling of DNA methylation erasure in mouse primordial germ cells. Genome Res. 22, 633-641.
7. Guo, G., Yang, J., Nichols, J., Hall, J. S., Eyres, I., Mansfield, W. and Smith, A. (2009). Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136, 1063-1069.
8. Guo, J. U., Su, Y., Zhong, C., Ming, G. L. and Song, H. (2011). Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145, 423-434.
9. Hackett, J. A., Sengupta, R., Zylicz, J. J., Murakami, K., Lee, C., Down, T. A. and Surani, M. A. (2012a). Germline DNA demethylation dynamics and imprint erasure through 5-Hydroxymethylcytosine. Science 339, 448-452.
10. Hackett, J. A., Zylicz, J. J. and Surani, M. A. (2012b). Parallel mechanisms of epigenetic reprogramming in the germline. Trends Genet. 28, 164-174.
11. Hashimoto, H., Hong, S., Bhagwat, A. S., Zhang, X. and Cheng, X. (2012). Excision of 5-hydroxymethyluracil and 5-carboxylcytosine by the thymine DNA glycosylase domain: its structural basis and implications for active DNA demethylation. Nucleic Acids Res. 40, 10203-10214.
12. He, Y. F., Li, B. Z., Li, Z., Liu, P., Wang, Y., Tang, Q., Ding, J., Jia, Y., Chen, Z., Li, L. et al. (2011). Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307.
13. Ito, S., D'Alessio, A. C., Taranova, O. V., Hong, K., Sowers, L. C. and Zhang, Y. (2010). Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466, 1129-1133.
14. Ito, S., Shen, L., Dai, Q., Wu, S. C., Collins, L. B., Swenberg, J. A., He, C. and Zhang, Y. (2011). Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333, 1300-1303.
15. Kagiwada, S., Kurimoto, K., Hirota, T., Yamaji, M. and Saitou, M. (2013). Replication-coupled passive DNA demethylation for the erasure of genome imprints in mice. EMBO J. 32, 340-353.
16. Kurimoto, K., Yabuta, Y., Ohinata, Y., Shigeta, M., Yamanaka, K. and Saitou, M. (2008a). Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev. 22, 1617-1635.
17. Kurimoto, K., Yamaji, M., Seki, Y. and Saitou, M. (2008b). Specification of the germ cell lineage in mice: a process orchestrated by the PR-domain proteins, Blimp1 and Prdm14. Cell Cycle 7, 3514-3518.
18. Langmead, B. and Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359.
19. Leitch, H. G., McEwen, K. R., Turp, A., Encheva, V., Carroll, T., Grabole, N., Mansfield, W., Nashun, B., Knezovich, J. G., Smith, A. et al. (2013). Naive pluripotency is associated with global DNA hypomethylation. Nat. Struct. Mol. Biol. 20, 311-316.
20. Li, E., Bestor, T. H. and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926.
21. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R.; 1000 Genome Project Data Processing Subgroup (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079.
22. Ma, Z., Swigut, T., Valouev, A., Rada-Iglesias, A. and Wysocka, J. (2011). Sequence-specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat. Struct. Mol. Biol. 18, 120-127.
23. Maison, C., Bailly, D., Peters, A. H., Quivy, J. P., Roche, D., Taddei, A., Lachner, M., Jenuwein, T. and Almouzni, G. (2002). Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat. Genet. 30, 329-334.
24. Marks, H., Kalkan, T., Menafra, R., Denissov, S., Jones, K., Hofemeister, H., Nichols, J., Kranz, A., Stewart, A. F., Smith, A. et al. (2012). The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149, 590-604.
25. Nabel, C. S., Jia, H., Ye, Y., Shen, L., Goldschmidt, H. L., Stivers, J. T., Zhang, Y. and Kohli, R. M. (2012). AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat. Chem. Biol. 8, 751-758.
26. Ohi, Y., Qin, H., Hong, C., Blouin, L., Polo, J. M., Guo, T., Qi, Z., Downey, S. L., Manos, P. D., Rossi, D. J. et al. (2011). Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat. Cell Biol. 13, 541-549.
27. Ohinata, Y., Payer, B., O'Carroll, D., Ancelin, K., Ono, Y., Sano, M., Barton, S. C., Obukhanych, T., Nussenzweig, M., Tarakhovsky, A. et al. (2005). Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436, 207-213.
28. Ohno, R., Nakayama, M., Naruse, C., Okashita, N., Takano, O., Tachibana, M., Asano, M., Saitou, M. and Seki, Y. (2013). A replication-dependent passive mechanism modulates DNA demethylation in mouse primordial germ cells. Development 140, 2892-2903.
29. Okano, M., Bell, D. W., Haber, D. A. and Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257.
30. Seisenberger, S., Andrews, S., Krueger, F., Arand, J., Walter, J., Santos, F., Popp, C., Thienpont, B., Dean, W. and Reik, W. (2012). The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol. Cell 48, 849-862.
31. Seki, Y., Hayashi, K., Itoh, K., Mizugaki, M., Saitou, M. and 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, 440-458.
32. Seki, Y., Yamaji, M., Yabuta, Y., Sano, M., Shigeta, M., Matsui, Y., Saga, Y., Tachibana, M., Shinkai, Y. and Saitou, M. (2007). Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 134, 2627-2638.
33. Sharif, J., Muto, M., Takebayashi, S., Suetake, I., Iwamatsu, A., Endo, T. A., Shinga, J., Mizutani-Koseki, Y., Toyoda, T., Okamura, K. et al. (2007). The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450, 908-912.
34. Shen, L., Wu, H., Diep, D., Yamaguchi, S., D'Alessio, A. C., Fung, H. L., Zhang, K. and Zhang, Y. (2013). Genome-wide analysis reveals TET-and TDG-dependent 5-methylcytosine oxidation dynamics. Cell 153, 692-706.
35. Smyth, G., Gentleman, R., Carey, V. J., Huber, W., Irizarry, R. A. and Dudoit, S. (2005). limma: Linear Models for Microarray Data Bioinformatics and Computational Biology Solutions Using R and Bioconductor (ed. M. Gail, J. M. Samet, A. Tsiatis and W. Wong), pp. 397-420. New York, NY: Springer.
36. Song, C. X., Szulwach, K. E., Dai, Q., Fu, Y., Mao, S. Q., Lin, L., Street, C., Li, Y., Poidevin, M., Wu, H. et al. (2013). Genome-wide profiling of 5-formylcytosine reveals its roles in epigenetic priming. Cell 153, 678-691.
37. Spruijt, C. G., Gnerlich, F., Smits, A. H., Pfaffeneder, T., Jansen, P. W., Bauer, C., Münzel, M., Wagner, M., Müller, M., Khan, F. et al. (2013). Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 152, 1146-1159.
38. Stadtfeld, M., Apostolou, E., Akutsu, H., Fukuda, A., Follett, P., Natesan, S., Kono, T., Shioda, T. and Hochedlinger, K. (2010). Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 465, 175-181.
39. Suzuki, M. M. and Bird, A. (2008). DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9, 465-476.
40. Thorvaldsdóttir, H., Robinson, J. T. and Mesirov, J. P. (2013). Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14, 178-192.
41. Wang, W., Lin, C., Lu, D., Ning, Z., Cox, T., Melvin, D., Wang, X., Bradley, A. and Liu, P. (2008). Chromosomal transposition of PiggyBac in mouse embryonic stem cells. Proc. Natl. Acad. Sci. USA 105, 9290-9295.
42. Williams, K., Christensen, J., Pedersen, M. T., Johansen, J. V., Cloos, P. A., Rappsilber, J. and Helin, K. (2011). TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473, 343-348.
43. Woltjen, K., Michael, I. P., Mohseni, P., Desai, R., Mileikovsky, M., Hämäläinen, R., Cowling, R., Wang, W., Liu, P., Gertsenstein, M. et al. (2009). piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458, 766-770.
44. Wu, S. C. and Zhang, Y. (2010). Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 11, 607-620.
45. Wu, H., D'Alessio, A. C., Ito, S., Xia, K., Wang, Z., Cui, K., Zhao, K., Sun, Y. E. and Zhang, Y. (2011). Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 473, 389-393.
46. Yamaguchi, S., Hong, K., Liu, R., Shen, L., Inoue, A., Diep, D., Zhang, K. and Zhang, Y. (2012). Tet1 controls meiosis by regulating meiotic gene expression. Nature 492, 443-447.
47. Yamaji, M., Seki, Y., Kurimoto, K., Yabuta, Y., Yuasa, M., Shigeta, M., Yamanaka, K., Ohinata, Y. and Saitou, M. (2008). Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat. Genet. 40, 1016-1022.
48. Yamaji, M., Ueda, J., Hayashi, K., Ohta, H., Yabuta, Y., Kurimoto, K., Nakato, R., Yamada, Y., Shirahige, K. and Saitou, M. (2013). PRDM14 ensures naive pluripotency through dual regulation of signaling and epigenetic pathways in mouse embryonic stem cells. Cell Stem Cell 12, 368-382.