M6 A RNA methylation promotes XIST-mediated transcriptional repression

Nature

Volumn 537, Issue 7620, 2016, Pages 369-373

  Patil, Deepak P ^a   Chen, Chun Kan ^b   Pickering, Brian F ^a   Chow, Amy ^b   Jackson, Constanza ^b   Guttman, Mitchell ^b   Jaffrey, Samie R ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 N METHYLADENOSINE; LONG UNTRANSLATED RNA; MEMBRANE PROTEIN; METHYLTRANSFERASE; METHYLTRANSFERASE LIKE 3; RNA; RNA BINDING MOTIF PROTEIN 15; RNA BINDING MOTIF PROTEIN 15B; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; X INACTIVE SPECIFIC TRANSCRIPT; YTH DOMAIN CONTAINING 1 PROTEIN; ADENOSINE; METTL3 PROTEIN, HUMAN; N(6)-METHYLADENOSINE; NERVE PROTEIN; NUCLEAR PROTEIN; RBM15 PROTEIN, HUMAN; RNA SPLICING FACTOR; WTAP PROTEIN, HUMAN; XIST NON-CODING RNA; YTHDC1 PROTEIN, HUMAN;

CELLS AND CELL COMPONENTS; CHROMOSOME; GENE; METHYLATION; PROTEIN; RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE; GENE FUNCTION; GENE REPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MALE; METTL3 GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; RBM15 GENE; RBM15B GENE; RNA METHYLATION; SIGNAL TRANSDUCTION; XIST GENE; ANALOGS AND DERIVATIVES; ANIMAL; CELL LINE; EMBRYONIC STEM CELL; GENETICS; HEK293 CELL LINE; METABOLISM; METHYLATION;

ADENOSINE; ANIMALS; CELL LINE; EMBRYONIC STEM CELLS; FEMALE; GENE SILENCING; HEK293 CELLS; HUMANS; MALE; METHYLATION; METHYLTRANSFERASES; MICE; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; RNA SPLICING FACTORS; RNA, LONG NONCODING; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84988329709     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature19342     Document Type: Article

References (52)

1. Penny, G. D., Kay, G. F., Sheardown, S. A., Rastan, S. & Brockdorff, N. Requirement for Xist in X-chromosome inactivation. Nature 379, 131-137 (1996).
2. Wutz, A. Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nat. Rev. Genet. 12, 542-553 (2011).
3. McHugh, C. A. et al. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 521, 232-236 (2015).
4. Minajigi, A. et al. Chromosomes. A comprehensive Xist interactome reveals cohesin repulsion and an RNA-directed chromosome conformation. Science 349, aab2276 (2015).
5. Chu, C. et al. Systematic discovery of Xist RNA binding proteins. Cell 161, 404-416 (2015).
6. Hasegawa, Y. et al. The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev. Cell 19, 469-476 (2010). 10.1016/j. devcel.2010.08.006
7. Zhao, J., Sun, B. K., Erwin, J. A., Song, J. J. & Lee, J. T. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322, 750-756 (2008).
8. Meyer, K. D. et al. Comprehensive analysis of mRNA methylation reveals enrichment in 3′ UTRs and near stop codons. Cell 149, 1635-1646 (2012).
9. Moindrot, B. et al. A pooled shRNA screen identifies Rbm15, Spen, and Wtap as factors required for Xist RNA-mediated silencing. Cell Reports 12, 562-572 (2015).
10. Kö2nig, J. et al. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat. Struct. Mol. Biol. 17, 909-915 (2010).
11. Wutz, A., Rasmussen, T. P. & Jaenisch, R. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat. Genet. 30, 167-174 (2002).
12. Horiuchi, K. et al. Identification of Wilms' tumor 1-associating protein complex and its role in alternative splicing and the cell cycle. J. Biol. Chem. 288, 33292-33302 (2013).
13. Zhong, S. et al. MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor. Plant Cell 20, 1278-1288 (2008).
14. Agarwala, S. D., Blitzblau, H. G., Hochwagen, A. & Fink, G. R. RNA methylation by the MIS complex regulates a cell fate decision in yeast. PLoS Genet. 8, e1002732 (2012).
15. Ping, X. L. et al. Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase. Cell Res. 24, 177-189 (2014).
16. 6-adenosine methyltransferase from HeLa cell nuclei. Internal mRNA methylation requires a multisubunit complex. J. Biol. Chem. 269, 17697-17704 (1994).
17. 6Am throughout the transcriptome. Nat. Methods 12, 767-772 (2015).
18. Plath, K. & Lowry, W. E. Progress in understanding reprogramming to the induced pluripotent state. Nat. Rev. Genet. 12, 253-265 (2011).
19. 6A writers reveals two distinct classes of mRNA methylation at internal and 5′ sites. Cell Reports 8, 284-296 (2014).
20. 6A-seq. Nature 485, 201-206 (2012).
21. 6-methyladenosine-dependent regulation of messenger RNA stability. Nature 505, 117-120 (2014).
22. 6-methyladenosine modulates messenger RNA translation efficiency. Cell 161, 1388-1399 (2015).
23. Morohashi, K. et al. Cyclosporin A associated helicase-like protein facilitates the association of hepatitis C virus RNA polymerase with its cellular cyclophilin B. PLoS One 6, e18285 (2011).
24. Berglund, L. et al. A genecentric Human Protein Atlas for expression profiles based on antibodies. Mol. Cell. Proteomics 7, 2019-2027 (2008).
25. 6-methyladenosine and gene expression control. Nat. Rev. Mol. Cell Biol. 15, 313-326 (2014).
26. Kwon, S. C. et al. The RNA-binding protein repertoire of embryonic stem cells. Nat. Struct. Mol. Biol. 20, 1122-1130 (2013). 10.1038/nsmb.2638
27. 6A reader YTHDC1 regulates mRNA splicing. Mol. Cell 61, 507-519 (2016). 10.1016/j.molcel.2016.01.012
28. Cowley, M. J. et al. PINA v2.0: mining interactome modules. Nucleic Acids Res. 40, D862-D865 (2012).
29. Engreitz, J. M. et al. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science 341, 1237973 (2013).
30. Huppertz, I. et al. iCLIP: protein-RNA interactions at nucleotide resolution. Methods 65, 274-287 (2014).
31. Meyer, K. D. et al. 5′ UTR m(6)A promotes cap-independent translation. Cell 163, 999-1010 (2015).
32. Weyn-Vanhentenryck, S. M. et al. HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism. Cell Reports 6, 1139-1152 (2014).
33. Ma, W., Noble, W. S. & Bailey, T. L. Motif-based analysis of large nucleotide data sets using MEME-ChIP. Nat. Protocols 9, 1428-1450 (2014).
34. Singh, G. et al. The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 151, 750-764 (2012).
35. Alarcón, C. R. et al. HNRNPA2B1 is a mediator of m(6)A-dependent nuclear RNA Processing events. Cell 162, 1299-1308 (2015).
36. Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589 (2010).
37. Ramírez, F., Dündar, F., Diehl, S., Grüning, B. A. & Manke, T. deep Tools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 42, W187-91 (2014).
38. Niranjanakumari, S., Lasda, E., Brazas, R. & Garcia-Blanco, M. A. Reversible cross-linking combined with immunoprecipitation to study RNA-protein interactions in vivo. Methods 26, 182-190 (2002).
39. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682 (2012).
40. Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (2003).
41. Link, A. J. & LaBaer, J. in Proteomics: A Cold Spring Harbor Laboratory Course Manual. Ch. 8, 117-142 (Cold Spring Harbor, 2009).
42. 6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat. Chem. Biol. 7, 885-887 (2011).
43. Kochan, J., Wawro, M. & Kasza, A. Simultaneous detection of mRNA and protein in single cells using immunofluorescence-combined single-molecule RNA-FISH. Biotechniques 59, 209-212, 214, 216 passim (2015).
44. Uranishi, H. et al. The RNA-binding motif protein 15B (RBM15B/OTT3) acts as cofactor of the nuclear export receptor NXF1. J. Biol. Chem. 284, 26106-26116 (2009).
45. 6A mRNA methylation facilitates resolution of naïve pluripotency toward differentiation. Science 347, 1002-1006 (2015).
46. 6-methyladenosine-dependent RNA structural switches regulate RNA-protein interactions. Nature 518, 560-564 (2015).
47. Wei, C. M., Gershowitz, A. & Moss, B. 5′ -Terminal and internal methylated nucleotide sequences in HeLa cell mRNA. Biochemistry 15, 397-401 (1976).
48. Bylund, L., Kytölä, S., Lui, W. O., Larsson, C. & Weber, G. Analysis of the cytogenetic stability of the human embryonal kidney cell line 293 by cytogenetic and STR profiling approaches. Cytogenet. Genome Res. 106, 28-32 (2004).
49. Lin, Y. C. et al. Genome dynamics of the human embryonic kidney 293 lineage in response to cell biology manipulations. Nat. Commun. 5, 4767 (2014).
50. Cao, Q. et al. The central role of EED in the orchestration of polycomb group complexes. Nat. Commun. 5, 3127 (2014).
51. Wilkinson, F. L. et al. Emerin interacts in vitro with the splicing-associated factor, YT521-B. Eur. J. Biochem. 270, 2459-2466 (2003).
52. Hartmann, A. M., Nayler, O., Schwaiger, F. W., Obermeier, A. & Stamm, S. The interaction and colocalization of Sam68 with the splicing-associated factor YT521-B in nuclear dots is regulated by the Src family kinase p59(fyn). Mol. Biol. Cell 10, 3909-3926 (1999).