M6A RNA methylation is regulated by microRNAs and promotes reprogramming to pluripotency

Cell Stem Cell

Volumn 16, Issue 3, 2015, Pages 289-301

  Chen, Tong ^a,f   Hao, Ya Juan ^b,f   Zhang, Ying ^c   Li, Miao Miao ^b,f   Wang, Meng ^a   Han, Weifang ^c,f   Wu, Yongsheng ^b   Lv, Ying ^b,f   Hao, Jie ^c   Wang, Libin ^c,f   Li, Ang ^b,f   Yang, Ying ^b,f   Jin, Kang Xuan ^b,f   Zhao, Xu ^b,f   Li, Yuhuan ^c   Ping, Xiao Li ^b,f   Lai, Wei Yi ^d   Wu, Li Gang ^e   Jiang, Guibin ^d   Wang, Hai Lin ^d   Sang, Lisi ^c,f   Wang, Xiu Jie ^a   Yang, Yun Gui ^b   Zhou, Qi ^c   more..

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b Chinese Academy of Sciences and China National Center for Bioinformation   (China)

^c INSTITUTE OF ZOOLOGY   (China)

^d RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^e INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^f UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

6 N METHYLADENOSINE; MESSENGER RNA; METHYLTRANSFERASE; METHYLTRANSFERASE LIKE 3; TRANSCRIPTOME; UNCLASSIFIED DRUG; 6-METHYLADENINE; ADENINE; METTL3 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL TRANSFORMATION; CONTROLLED STUDY; FIBROBLAST; GENE TARGETING; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; REGULATORY RNA SEQUENCE; RNA METHYLATION; ANALOGS AND DERIVATIVES; ANIMAL; ANIMAL EMBRYO; CYTOLOGY; METABOLISM; METHYLATION; PHYSIOLOGY; RNA PROCESSING; TRANSGENIC MOUSE;

EUKARYOTA;

ADENINE; ANIMALS; CELLULAR REPROGRAMMING; EMBRYO, MAMMALIAN; FIBROBLASTS; METHYLATION; METHYLTRANSFERASES; MICE; MICE, TRANSGENIC; PLURIPOTENT STEM CELLS; RNA PROCESSING, POST-TRANSCRIPTIONAL;

EID: 84924283323     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2015.01.016     Document Type: Article

References (52)

1. D.P. Bartel MicroRNAs: genomics, biogenesis, mechanism, and function Cell 116 2004 281 297
2. P.J. Batista, B. Molinie, J. Wang, K. Qu, J. Zhang, L. Li, D.M. Bouley, E. Lujan, B. Haddad, and K. Daneshvar m(6)A RNA modification controls cell fate transition in mammalian embryonic stem cells Cell Stem Cell 15 2014 707 719
3. Z. Bodi, J.D. Button, D. Grierson, and R.G. Fray Yeast targets for mRNA methylation Nucleic Acids Res. 38 2010 5327 5335
4. Z. Bodi, S. Zhong, S. Mehra, J. Song, N. Graham, H. Li, S. May, and R.G. Fray Adenosine methylation in Arabidopsis mRNA is associated with the 3′ end and reduced Levels cause developmental defects Front. Plant Sci. 3 2012 48
5. Bokar, J.A. (2005). The biosynthesis and functional roles of methylated nucleosides in eukaryotic mRNA, Volume 12, H. Grosjean, ed. (New York: Springer), pp. 141-177.
6. J.A. Bokar, M.E. Shambaugh, D. Polayes, A.G. Matera, and F.M. Rottman Purification and cDNA cloning of the AdoMet-binding subunit of the human mRNA (N6-adenosine)-methyltransferase RNA 3 1997 1233 1247
7. S.A. Camper, R.J. Albers, J.K. Coward, and F.M. Rottman Effect of undermethylation on mRNA cytoplasmic appearance and half-life Mol. Cell. Biol. 4 1984 538 543
8. W.A. Cantara, P.F. Crain, J. Rozenski, J.A. McCloskey, K.A. Harris, X. Zhang, F.A. Vendeix, D. Fabris, and P.F. Agris The RNA modification database, RNAMDB: 2011 update Nucleic Acids Res. 39 2011 D195 D201
9. E.S. Cenik, and P.D. Zamore Argonaute proteins Curr. Biol. 21 2011 R446 R449
10. G.E. Crooks, G. Hon, J.M. Chandonia, and S.E. Brenner WebLogo: a sequence logo generator Genome Res. 14 2004 1188 1190
11. Q. Dai, R. Fong, M. Saikia, D. Stephenson, Y.T. Yu, T. Pan, and J.A. Piccirilli Identification of recognition residues for ligation-based detection and quantitation of pseudouridine and N6-methyladenosine Nucleic Acids Res. 35 2007 6322 6329
12. R. Desrosiers, K. Friderici, and F. Rottman Identification of methylated nucleosides in messenger RNA from Novikoff hepatoma cells Proc. Natl. Acad. Sci. USA 71 1974 3971 3975
13. D. Dominissini, S. Moshitch-Moshkovitz, S. Schwartz, M. Salmon-Divon, L. Ungar, S. Osenberg, K. Cesarkas, J. Jacob-Hirsch, N. Amariglio, and M. Kupiec Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq Nature 485 2012 201 206
14. A.J. Enright, B. John, U. Gaul, T. Tuschl, C. Sander, and D.S. Marks MicroRNA targets in Drosophila Genome Biol. 5 2003 R1
15. D. Finkel, and Y. Groner Methylations of adenosine residues (m6A) in pre-mRNA are important for formation of late simian virus 40 mRNAs Virology 131 1983 409 425
16. J.M. Fustin, M. Doi, Y. Yamaguchi, H. Hida, S. Nishimura, M. Yoshida, T. Isagawa, M.S. Morioka, H. Kakeya, I. Manabe, and H. Okamura RNA-methylation-dependent RNA processing controls the speed of the circadian clock Cell 155 2013 793 806
17. S. Geula, S. Moshitch-Moshkovitz, D. Dominissini, A.A. Mansour, N. Kol, M. Salmon-Divon, V. Hershkovitz, E. Peer, N. Mor, and Y.S. Manor m6A mRNA methylation facilitates resolution of naïve pluripotency toward differentiation Science 2015 10.1126/science.1261417 in press. Published online January 1, 2015
18. D. Globisch, D. Pearson, A. Hienzsch, T. Brückl, M. Wagner, I. Thoma, P. Thumbs, V. Reiter, A.C. Kneuttinger, and M. Müller Systems-based analysis of modified tRNA bases Angew. Chem. Int. Ed. Engl. 50 2011 9739 9742
19. J.E. Harper, S.M. Miceli, R.J. Roberts, and J.L. Manley Sequence specificity of the human mRNA N6-adenosine methylase in vitro Nucleic Acids Res. 18 1990 5735 5741
20. C. He Grand challenge commentary: RNA epigenetics? Nat. Chem. Biol. 6 2010 863 865
21. S. Heinz, C. Benner, N. Spann, E. Bertolino, Y.C. Lin, P. Laslo, J.X. Cheng, C. Murre, H. Singh, and C.K. Glass Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities Mol. Cell 38 2010 576 589
22. M.E. Hess, S. Hess, K.D. Meyer, L.A. Verhagen, L. Koch, H.S. Brönneke, M.O. Dietrich, S.D. Jordan, Y. Saletore, and O. Elemento The fat mass and obesity associated gene (Fto) regulates activity of the dopaminergic midbrain circuitry Nat. Neurosci. 16 2013 1042 1048
23. D. Huangfu, R. Maehr, W. Guo, A. Eijkelenboom, M. Snitow, A.E. Chen, and D.A. Melton Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds Nat. Biotechnol. 26 2008 795 797
24. G. Jia, Y. Fu, X. Zhao, Q. Dai, G. Zheng, Y. Yang, C. Yi, T. Lindahl, T. Pan, Y.G. Yang, and C. He N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO Nat. Chem. Biol. 7 2011 885 887
25. S.E. Kane, and K. Beemon Precise localization of m6A in Rous sarcoma virus RNA reveals clustering of methylation sites: implications for RNA processing Mol. Cell. Biol. 5 1985 2298 2306
26. D. Kim, G. Pertea, C. Trapnell, H. Pimentel, R. Kelley, and S.L. Salzberg TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions Genome Biol. 14 2013 R36
27. A. Kozomara, and S. Griffiths-Jones miRBase: integrating microRNA annotation and deep-sequencing data Nucleic Acids Res. 39 2011 D152 D157
28. J. Liu, and G. Jia Methylation modifications in eukaryotic messenger RNA J. Genet. Genomics 41 2014 21 33
29. N. Liu, M. Parisien, Q. Dai, G. Zheng, C. He, and T. Pan Probing N6-methyladenosine RNA modification status at single nucleotide resolution in mRNA and long noncoding RNA RNA 19 2013 1848 1856
30. J. Liu, Y. Yue, D. Han, X. Wang, Y. Fu, L. Zhang, G. Jia, M. Yu, Z. Lu, and X. Deng A METTL3-METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation Nat. Chem. Biol. 10 2014 93 95
31. M.A. Machnicka, K. Milanowska, O. Osman Oglou, E. Purta, M. Kurkowska, A. Olchowik, W. Januszewski, S. Kalinowski, S. Dunin-Horkawicz, and K.M. Rother MODOMICS: a database of RNA modification pathways - 2013 update Nucleic Acids Res. 41 2013 D262 D267
32. G. Meister Argonaute proteins: functional insights and emerging roles Nat. Rev. Genet. 14 2013 447 459
33. K.D. Meyer, Y. Saletore, P. Zumbo, O. Elemento, C.E. Mason, and S.R. Jaffrey Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons Cell 149 2012 1635 1646
34. Y. Niu, X. Zhao, Y.S. Wu, M.M. Li, X.J. Wang, and Y.G. Yang N6-methyl-adenosine (m6A) in RNA: an old modification with a novel epigenetic function Genomics Proteomics Bioinformatics 11 2013 8 17
35. X.L. Ping, B.F. Sun, L. Wang, W. Xiao, X. Yang, W.J. Wang, S. Adhikari, Y. Shi, Y. Lv, and Y.S. Chen Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase Cell Res. 24 2014 177 189
36. T.A. Rand, S. Petersen, F. Du, and X. Wang Argonaute2 cleaves the anti-guide strand of siRNA during RISC activation Cell 123 2005 621 629
37. S. Schwartz, S.D. Agarwala, M.R. Mumbach, M. Jovanovic, P. Mertins, A. Shishkin, Y. Tabach, T.S. Mikkelsen, R. Satija, and G. Ruvkun High-resolution mapping reveals a conserved, widespread, dynamic mRNA methylation program in yeast meiosis Cell 155 2013 1409 1421
38. S. Schwartz, M.R. Mumbach, M. Jovanovic, T. Wang, K. Maciag, G.G. Bushkin, P. Mertins, D. Ter-Ovanesyan, N. Habib, and D. Cacchiarelli Perturbation of m6A writers reveals two distinct classes of mRNA methylation at internal and 5′ sites Cell Rep. 8 2014 284 296
39. T. Sibbritt, H.R. Patel, and T. Preiss Mapping and significance of the mRNA methylome Wiley Interdiscip Rev RNA 4 2013 397 422
40. C. Trapnell, D.G. Hendrickson, M. Sauvageau, L. Goff, J.L. Rinn, and L. Pachter Differential analysis of gene regulation at transcript resolution with RNA-seq Nat. Biotechnol. 31 2013 46 53
41. M.T. Tuck, P.E. Wiehl, and T. Pan Inhibition of 6-methyladenine formation decreases the translation efficiency of dihydrofolate reductase transcripts Int. J. Biochem. Cell Biol. 31 1999 837 851
42. X. Wang, Z. Lu, A. Gomez, G.C. Hon, Y. Yue, D. Han, Y. Fu, M. Parisien, Q. Dai, and G. Jia N6-methyladenosine-dependent regulation of messenger RNA stability Nature 505 2014 117 120
43. Y. Wang, Y. Li, J.I. Toth, M.D. Petroski, Z. Zhang, and J.C. Zhao N6-methyladenosine modification destabilizes developmental regulators in embryonic stem cells Nat. Cell Biol. 16 2014 191 198
44. C.-M. Wei, and B. Moss Nucleotide sequences at the N6-methyladenosine sites of HeLa cell messenger ribonucleic acid Biochemistry 16 1977 1672 1676
45. C.M. Wei, A. Gershowitz, and B. Moss Methylated nucleotides block 5′ terminus of HeLa cell messenger RNA Cell 4 1975 379 386
46. M. Wernig, C.J. Lengner, J. Hanna, M.A. Lodato, E. Steine, R. Foreman, J. Staerk, S. Markoulaki, and R. Jaenisch A drug-inducible transgenic system for direct reprogramming of multiple somatic cell types Nat. Biotechnol. 26 2008 916 924
47. W. Xie, M.D. Schultz, R. Lister, Z. Hou, N. Rajagopal, P. Ray, J.W. Whitaker, S. Tian, R.D. Hawkins, and D. Leung Epigenomic analysis of multilineage differentiation of human embryonic stem cells Cell 153 2013 1134 1148
48. C. Xu, X. Wang, K. Liu, I.A. Roundtree, W. Tempel, Y. Li, Z. Lu, C. He, and J. Min Structural basis for selective binding of m6A RNA by the YTHDC1 YTH domain Nat. Chem. Biol. 10 2014 927 929
49. X. Zhao, Y. Yang, B.F. Sun, Y. Shi, X. Yang, W. Xiao, Y.J. Hao, X.L. Ping, Y.S. Chen, and W.J. Wang FTO-dependent demethylation of N6-methyladenosine regulates mRNA splicing and is required for adipogenesis Cell Res. 24 2014 1403 1419
50. G. Zheng, J.A. Dahl, Y. Niu, P. Fedorcsak, C.M. Huang, C.J. Li, C.B. Vågbø, Y. Shi, W.L. Wang, and S.H. Song ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility Mol. Cell 49 2013 18 29
51. S. Zhong, H. Li, Z. Bodi, J. Button, L. Vespa, M. Herzog, and R.G. Fray MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor Plant Cell 20 2008 1278 1288
52. T. Zhu, I.A. Roundtree, P. Wang, X. Wang, L. Wang, C. Sun, Y. Tian, J. Li, C. He, and Y. Xu Crystal structure of the YTH domain of YTHDF2 reveals mechanism for recognition of N6-methyladenosine Cell Res. 24 2014 1493 1496