A critical role for AID in the initiation of reprogramming to induced pluripotent stem cells

FASEB Journal

Volumn 27, Issue 3, 2013, Pages 1107-1113

  Bhutani, Nidhi ^a   Decker, Matthew N ^a   Brady, Jennifer J ^a   Bussat, Rose T ^a   Burns, David M ^a   Corbel, Stephane Y ^a   Blau, Helen M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Activation induced deaminase; DNA demethylation; Early events in iPSC generation

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; SHORT HAIRPIN RNA;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DEMETHYLATION; EMBRYO; ENZYME ACTIVITY; FIBROBLAST; HETEROKARYON; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL DEDIFFERENTIATION; CELL LINE; CYTIDINE DEAMINASE; FIBROBLASTS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; TIME FACTORS;

EID: 84874590585     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-222125     Document Type: Article

References (33)

1. Wernig, M., Lengner, C. J., Hanna, J., Lodato, M. A., Steine, E., Foreman, R., Staerk, J., Markoulaki, S., and Jaenisch, R. (2008) A drug-inducible transgenic system for direct reprogramming of multiple somatic cell types. Nat. Biotechnol. 26, 916-924
2. Takahashi, K., and Yamanaka, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (Pubitemid 44233629)
3. Yamanaka, S., and Blau, H. M. (2010) Nuclear reprogramming to a pluripotent state by three approaches. Nature 465, 704-712
4. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872 (Pubitemid 350138099)
5. Wernig, M., Meissner, A., Foreman, R., Brambrink, T., Ku, M., Hochedlinger, K., Bernstein, B. E., and Jaenisch, R. (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-celllike state. Nature 448, 318-324 (Pubitemid 47080337)
6. Marion, R. M., Strati, K., Li, H., Murga, M., Blanco, R., Ortega, S., Fernandez-Capetillo, O., Serrano, M., and Blasco, M. A. (2009) A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 460, 1149-1153
7. Li, H., Collado, M., Villasante, A., Strati, K., Ortega, S., Canamero, M., Blasco, M. A., and Serrano, M. (2009) The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 460, 1136-1139
8. Utikal, J., Polo, J. M., Stadtfeld, M., Maherali, N., Kulalert, W., Walsh, R. M., Khalil, A., Rheinwald, J. G., and Hochedlinger, K. (2009) Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 460, 1145-1148
9. Hong, H., Takahashi, K., Ichisaka, T., Aoi, T., Kanagawa, O., Nakagawa, M., Okita, K., and Yamanaka, S. (2009) Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 460, 1132-1135
10. Maekawa, M., Yamaguchi, K., Nakamura, T., Shibukawa, R., Kodanaka, I., Ichisaka, T., Kawamura, Y., Mochizuki, H., Goshima, N., and Yamanaka, S. (2011) Direct reprogramming of somatic cells is promoted by maternal transcription factor Glis1. Nature 474, 225-229
11. Onder, T. T., Kara, N., Cherry, A., Sinha, A. U., Zhu, N., Bernt, K. M., Cahan, P., Marcarci, B. O., Unternaehrer, J., Gupta, P. B., Lander, E. S., Armstrong, S. A., and Daley, G. Q. (2012) Chromatin-modifying enzymes as modulators of reprogramming. Nature 483, 598-602
12. Buganim, Y., Faddah, D. A., Cheng, A. W., Itskovich, E., Markoulaki, S., Ganz, K., Klemm, S. L., van Oudenaarden, A., and Jaenisch, R. (2012) Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150, 1209-1222
13. Blau, H. M., Pavlath, G. K., Hardeman, E. C., Chiu, C. P., Silberstein, L., Webster, S. G., Miller, S. C., and Webster, C. (1985) Plasticity of the differentiated state. Science 230, 758-766 (Pubitemid 16193964)
14. Bhutani, N., Brady, J. J., Damian, M., Sacco, A., Corbel, S. Y., and Blau, H. M. (2010) Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463, 1042-1047
15. 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
16. Cortellino, S., Xu, J., Sannai, M., Moore, R., Caretti, E., Cigliano, A., Le Coz, M., Devarajan, K., Wessels, A., Soprano, D., Abramowitz, L. K., Bartolomei, M. S., Rambow, F., Bassi, M. R., Bruno, T., Fanciulli, M., Renner, C., Klein-Szanto, A. J., Matsumoto, Y., Kobi, D., Davidson, I., Alberti, C., Larue, L., and Bellacosa, A. (2011) Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146, 67-79
17. Tahiliani, M., Koh, K. P., Shen, Y., Pastor, W. A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L. M., Liu, D. R., Aravind, L., and Rao, A. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935
18. 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
19. 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
20. Mikkelsen, T. S., Hanna, J., Zhang, X., Ku, M., Wernig, M., Schorderet, P., Bernstein, B. E., Jaenisch, R., Lander, E. S., and Meissner, A. (2008) Dissecting direct reprogramming through integrative genomic analysis. Nature 454, 49-55 (Pubitemid 351931978)
21. Jaenisch, R., and Bird, A. (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33(Suppl.), 245-254 (Pubitemid 36278835)
22. Pavri, R., Gazumyan, A., Jankovic, M., Di Virgilio, M., Klein, I., Ansarah-Sobrinho, C., Resch, W., Yamane, A., Reina San-Martin, B., Barreto, V., Nieland, T. J., Root, D. E., Casellas, R., and Nussenzweig, M. C. (2010) Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell 143, 122-133
23. Sommer, C. A., Stadtfeld, M., Murphy, G. J., Hochedlinger, K., Kotton, D. N., and Mostoslavsky, G. (2009) Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 27, 543-549
24. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., and Honjo, T. (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102, 553-563
25. Popp, C., Dean, W., Feng, S., Cokus, S. J., Andrews, S., Pellegrini, M., Jacobsen, S. E., and Reik, W. (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463, 1101-1105
26. Bashir, T., and Pagano, M. (2005) Cdk1: the dominant sibling of Cdk2. Nat. Cell Biol. 7, 779-781 (Pubitemid 41079049)
27. Paik, J. H., Kollipara, R., Chu, G., Ji, H., Xiao, Y., Ding, Z., Miao, L., Tothova, Z., Horner, J. W., Carrasco, D. R., Jiang, S., Gilliland, D. G., Chin, L., Wong, W. H., Castrillon, D. H., and DePinho, R. A. (2007) FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128, 309-323 (Pubitemid 46123514)
28. Sage, J., Miller, A. L., Perez-Mancera, P. A., Wysocki, J. M., and Jacks, T. (2003) Acute mutation of retinoblastoma gene function is sufficient for cell cycle re-entry. Nature 424, 223-228 (Pubitemid 36858693)
29. Ramiro, A. R., Jankovic, M., Callen, E., Difilippantonio, S., Chen, H. T., McBride, K. M., Eisenreich, T. R., Chen, J., Dickins, R. A., Lowe, S. W., Nussenzweig, A., and Nussenzweig, M. C. (2006) Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature 440, 105-109 (Pubitemid 43336276)
30. 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
31. Conticello, S. G. (2008) The AID/APOBEC family of nucleic acid mutators. Genome Biol. 9, 229
32. Bhutani, N., Burns, D. M., and Blau, H. M. (2011) DNA demethylation dynamics. Cell 146, 866-872
33. Branco, M. R., Ficz, G., and Reik, W. (2012) Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat. Rev. Genet. 13, 7-13