Cytosine methylation of tRNA-Asp by DNMT2 has a role in translation of proteins containing poly-Asp sequences

Cell Discovery

Volumn 1, Issue , 2015, Pages

  Shanmugam, Raghuvaran ^a   Fierer, Jacob ^b   Kaiser, Steffen ^c   Helm, Mark ^c   Jurkowski, Tomasz P ^a   Jeltsch, Albert ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

^b JACOBS UNIVERSITY BREMEN   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Aminoacylation; Asp rich proteins; Dnmt2; Regulation of translation; TRNA methylation

Indexed keywords

ASPARTATE TRANSFER RNA LIGASE; CYTOSINE; DNA METHYLTRANSFERASE; DNMT2 PROTEIN; UNCLASSIFIED DRUG;

AMINOACYLATION; ANIMAL EXPERIMENT; ARTICLE; FIBROBLAST; GENE EXPRESSION PROFILING; GENE ONTOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; RNA METHYLATION; RNA PROCESSING;

EID: 84964479843     PISSN: None     EISSN: 20565968     Source Type: Journal    
DOI: 10.1038/celldisc.2015.10     Document Type: Article

References (44)

1. Czerwoniec A, Dunin-Horkawicz S, Purta E et al. MODOMICS: a database of RNA modification pathways. 2008 update. Nucleic Acids Res 2009; 37: D118-D121.
2. Motorin Y, Lyko F, Helm M. 5-methylcytosine in RNA: detection, enzymatic formation and biological functions. Nucleic Acids Res 2010; 38: 1415-1430.
3. Cantara WA, Crain PF, Rozenski J et al. The RNA Modification Database, RNAMDB: 2011 update. Nucleic Acids Res 2011; 39: D195-D201.
4. Motorin Y, Helm M. RNA nucleotide methylation. Wiley Interdisciplinary Rev RNA 2011; 2: 611-631.
5. Khoddami V, Cairns BR. Identification of direct targets and modified bases of RNA cytosine methyltransferases. Nat Biotechnol 2013; 31: 458-464.
6. Jeltsch A, Nellen W, Lyko F. Two substrates are better than one: dual specificities for Dnmt2 methyltransferases. Trends Biochemic Sci 2006; 31: 306-308.
7. Goll MG, Kirpekar F, Maggert KA et al. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 2006; 311: 395-398.
8. Jurkowski TP, Meusburger M, Phalke S et al. Human DNMT2 methylates tRNA(Asp) molecules using a DNA methyltransferase-like catalytic mechanism. RNA 2008; 14: 1663-1670.
9. Schaefer M, Pollex T, Hanna K et al. RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage. Genes Dev 2010; 24: 1590-1595.
10. Tovy A, Siman Tov R, Gaentzsch R, Helm M, Ankri S. A new nuclear function of the Entamoeba histolytica glycolytic enzyme enolase: the metabolic regulation of cytosine-5 methyltransferase 2 (Dnmt2) activity. PLoS Pathog 2010; 6: e1000775.
11. Becker M, Muller S, Nellen W, Jurkowski TP, Jeltsch A, Ehrenhofer-Murray AE. Pmt1, a Dnmt2 homolog in Schizosaccharomyces pombe, mediates tRNA methylation in response to nutrient signaling. Nucleic Acids Res 2012; 40: 11648-11658.
12. Muller S, Windhof IM, Maximov V et al. Target recognition, RNA methylation activity and transcriptional regulation of the Dictyostelium discoideum Dnmt2-homologue (DnmA). Nucleic Acids Res 2013; 41: 8615-8627.
13. Tuorto F, Liebers R, Musch T et al. RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis. Nat Struct Mol Biol 2012; 19: 900-905.
14. Shanmugam R, Aklujkar M, Schafer M et al. The Dnmt2 RNA methyltransferase homolog of Geobacter sulfurreducens specifically methylates tRNA-Glu. Nucleic Acids Res 2014; 42: 6487-6496.
15. Jurkowski TP, Jeltsch A. On the evolutionary origin of eukaryotic DNA methyltransferases and Dnmt2. PLoS One 2011; 6: e28104.
16. EMBL-EBI Expression atlas data for mouse DNMT2. Available at http://www.ebi.ac.uk/gxa/genes/ ENSG00000107614.
17. Brawand D, Soumillon M, Necsulea A et al. The evolution of gene expression levels in mammalian organs. Nature 2011; 478: 343-348.
18. EMBL-EBI Expression atlas data for human DNMT2. Available at http://www.ebi.ac.uk/gxa/genes/ ENSMUSG00000026723.
19. Forbes SA, Beare D, Gunasekaran P et al. COSMIC: exploring the world's knowledge of somatic mutations in human cancer. Nucleic Acids Res 2014; 43: D805-D811.
20. Tang LY, Reddy MN, Rasheva V et al. The eukaryotic DNMT2 genes encode a new class of cytosine-5 DNA methyltransferases. J Biol Chem 2003; 278: 33613-33616.
21. Durdevic Z, Mobin MB, Hanna K, Lyko F, Schaefer M. The RNA methyltransferase Dnmt2 is required for efficient Dicer-2-dependent siRNA pathway activity in Drosophila. Cell Rep 2013; 4: 931-937.
22. Durdevic Z, Hanna K, Gold B et al. Efficient RNA virus control in Drosophila requires the RNA methyltransferase Dnmt2. EMBO Rep 2013; 14: 269-275.
23. Giege R, Sissler M, Florentz C. Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res 1998; 26: 5017-5035.
24. Ruff M, Krishnaswamy S, Boeglin M et al. Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNA (Asp). Science 1991; 252: 1682-1689.
25. Rudinger J, Puglisi JD, Putz J et al. Determinant nucleotides of yeast tRNA(Asp) interact directly with aspartyltRNA synthetase. Proc Natl Acad Sci USA 1992; 89: 5882-5886.
26. Martin F, Barends S, Eriani G. Single amino acid changes in AspRS reveal alternative routes for expanding its tRNA repertoire in vivo. Nucleic Acids Res 2004; 32: 4081-4089.
27. Escalante C, Yang DC. Expression of human aspartyltRNA synthetase in Escherichia coli. Functional analysis of the N-terminal putative amphiphilic helix. J Biol Chem 1993; 268: 6014-6023.
28. Reed VS, Wastney ME, Yang DC. Mechanisms of the transfer of aminoacyl-tRNA from aminoacyl-tRNA synthetase to the elongation factor 1 alpha. J Biol Chem 1994; 269: 32932-32936.
29. Ryckelynck M, Giege R, Frugier M. Yeast tRNA(Asp) charging accuracy is threatened by the N-terminal extension of aspartyl-tRNA synthetase. J Biol Chem 2003; 278: 9683-9690.
30. Cavarelli J, Eriani G, Rees B et al. The active site of yeast aspartyl-tRNA synthetase: structural and functional aspects of the aminoacylation reaction.EMBO J 1994; 13: 327-337.
31. Varshney U, Lee CP, RajBhandary UL. Direct analysis of aminoacylation levels of tRNAs in vivo. Application to studying recognition of Escherichia coli initiator tRNA mutants by glutaminyl-tRNA synthetase. J Biol Chem 1991; 266: 24712-24718.
32. Zaborske J, Pan T. Genome-wide analysis of aminoacylation (charging) levels of tRNA using microarrays. J Vis Exp 2010; 40: pii: 2007.
33. Goss DJ, Parkhurst LJ. Rapid solid phase isolation of 20 specific tRNAs from Escherichia coli. J Biol Chem 1978; 253: 7804-7806.
34. Obenauer JC, Cantley LC, Yaffe MB. Scansite 2.0: proteomewide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 2003; 31: 3635-3641.
35. Madore E, Florentz C, Giege R, Sekine S, Yokoyama S, Lapointe J. Effect of modified nucleotides on Escherichia coli tRNAGlu structure and on its aminoacylation by glutamyl-tRNA synthetase. Predominant and distinct roles of the mnm5 and s2 modifications of U34. Eur J Biochem 1999; 266: 1128-1135.
36. Alexandrov A, Chernyakov I, Gu W et al. Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell 2006; 21: 87-96.
37. Putz J, Florentz C, Benseler F, Giege R. A single methyl group prevents the mischarging of a tRNA. Nat Struct Biol 1994; 1: 580-582.
38. Bjork GR, Jacobsson K, Nilsson K, Johansson MJ, Bystrom AS, Persson OP. A primordial tRNA modification required for the evolution of life?. EMBO J 2001; 20: 231-239.
39. Begley U, Dyavaiah M, Patil A et al. Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol Cell 2007; 28: 860-870.
40. Chan CT, Pang YL, Deng W et al. Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins. Nat Commun 2012; 3: 937.
41. Fu L, Guerrero CR, Zhong N et al. Tet-mediated formation of 5-hydroxymethylcytosine in RNA. J Am Chem Soc 2014; 136: 11582-11585.
42. Buchan JR, Aucott LS, Stansfield I. tRNA properties help shape codon pair preferences in open reading frames. Nucleic Acids Res 2006; 34: 1015-1027.
43. Kurschat WC, Muller J, Wombacher R, Helm M. Optimizing splinted ligation of highly structured small RNAs. RNA 2005; 11: 1909-1914.
44. Hengesbach M, Kobitski A, Voigts-Hoffmann F, Frauer C, Nienhaus GU, Helm M. RNA intramolecular dynamics by single-molecule FRET. In: Serge L Beaucage et al (eds). Current protocols in nucleic acid chemistry, Chapter 11: Unit 11,12, 2008.