The tRNA methyltransferase Dnmt2 is required for accurate polypeptide synthesis during haematopoiesis

EMBO Journal

Volumn 34, Issue 18, 2015, Pages 2350-2362

  Tuorto, Francesca ^a   Herbst, Friederike ^b   Alerasool, Nader ^a   Bender, Sebastian ^a   Popp, Oliver ^c   Federico, Giuseppina ^b   Reitter, Sonja ^d   Liebers, Reinhard ^a   Stoecklin, Georg ^d   Gröne, Hermann Josef ^b   Dittmar, Gunnar ^c   Glimm, Hanno ^b   Lyko, Frank ^a  

^a GERMAN CANCER RESEARCH CENTER   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c MDC   (Germany)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

(cytosine 5) tRNA methylation; Dnmt2; haematopoiesis; MSCs; translation fidelity

Indexed keywords

BISULFITE; RNA BISULFITE; TRANSFER RNA METHYLTRANSFERASE; TRNA METHYLTRANSFERASE DNMT2; UNCLASSIFIED DRUG; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNMT2 PROTEIN, MOUSE; TRANSFER RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW CULTURE; BONE MARROW TRANSPLANTATION; CELL COUNT; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL MATURATION; CELL POPULATION; CODON; ENCHONDRAL OSSIFICATION; ENDOTHELIUM CELL; EPIPHYSIS PLATE; FLOW CYTOMETRY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METHYLATION; PROTEIN SYNTHESIS; RNA SEQUENCE; ANIMAL; BONE DEVELOPMENT; CYTOLOGY; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; METHYLATION; PHYSIOLOGY;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; METHYLATION; MICE; MICE, KNOCKOUT; OSTEOGENESIS; PROTEIN BIOSYNTHESIS; RNA, TRANSFER;

EID: 84941744498     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201591382     Document Type: Article

References (44)

1. Agris PF, (2004) Decoding the genome: a modified view. Nucleic Acids Res 32: 223-238
2. Agris PF, Vendeix FA, Graham WD, (2007) tRNA's wobble decoding of the genome: 40 years of modification. J Mol Biol 366: 1-13
3. Ball CR, Pilz IH, Schmidt M, Fessler S, Williams DA, von Kalle C, Glimm H, (2007) Stable differentiation and clonality of murine long-term hematopoiesis after extended reduced-intensity selection for MGMT P140K transgene expression. Blood 110: 1779-1787
4. Becker M, Muller S, Nellen W, Jurkowski TP, Jeltsch A, Ehrenhofer-Murray AE, (2012) Pmt1, a Dnmt2 homolog in Schizosaccharomyces pombe, mediates tRNA methylation in response to nutrient signaling. Nucleic Acids Res 40: 11648-11658
5. Begley U, Dyavaiah M, Patil A, Rooney JP, DiRenzo D, Young CM, Conklin DS, Zitomer RS, Begley TJ, (2007) Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol Cell 28: 860-870
6. Blanco S, Kurowski A, Nichols J, Watt FM, Benitah SA, Frye M, (2011) The RNA-methyltransferase Misu (NSun2) poises epidermal stem cells to differentiate. PLoS Genet 7: e1002403
7. Blanco S, Dietmann S, Flores JV, Hussain S, Kutter C, Humphreys P, Lukk M, Lombard P, Treps L, Popis M, Kellner S, Holter SM, Garrett L, Wurst W, Becker L, Klopstock T, Fuchs H, Gailus-Durner V, Hrabe de Angelis M, Karadottir RT, et al., (2014) Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders. EMBO J 33: 2020-2039
8. Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJ, (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 4: 484-494
9. Crick FH, (1966) Codon-anticodon pairing: the wobble hypothesis. J Mol Biol 19: 548-555
10. Drummond DA, Wilke CO, (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134: 341-352
11. Durdevic Z, Mobin MB, Hanna K, Lyko F, Schaefer M, (2013) The RNA methyltransferase Dnmt2 is required for efficient Dicer-2-dependent siRNA pathway activity in Drosophila. Cell Rep 4: 931-937
12. El Yacoubi B, Bailly M, de Crecy-Lagard V, (2012) Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu Rev Genet 46: 69-95
13. Gingold H, Tehler D, Christoffersen NR, Nielsen MM, Asmar F, Kooistra SM, Christophersen NS, Christensen LL, Borre M, Sorensen KD, Andersen LD, Andersen CL, Hulleman E, Wurdinger T, Ralfkiaer E, Helin K, Gronbaek K, Orntoft T, Waszak SM, Dahan O, et al., (2014) A dual program for translation regulation in cellular proliferation and differentiation. Cell 158: 1281-1292
14. de Godoy LM, Olsen JV, Cox J, Nielsen ML, Hubner NC, Frohlich F, Walther TC, Mann M, (2008) Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455: 1251-1254
15. Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, Zhang X, Golic KG, Jacobsen SE, Bestor TH, (2006) Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 311: 395-398
16. Grosjean H, de Crecy-Lagard V, Marck C, (2010) Deciphering synonymous codons in the three domains of life: co-evolution with specific tRNA modification enzymes. FEBS Lett 584: 252-264
17. Guy MP, Young DL, Payea MJ, Zhang X, Kon Y, Dean KM, Grayhack EJ, Mathews DH, Fields S, Phizicky EM, (2014) Identification of the determinants of tRNA function and susceptibility to rapid tRNA decay by high-throughput in vivo analysis. Genes Dev 28: 1721-1732
18. Hori H, (2014) Methylated nucleosides in tRNA and tRNA methyltransferases. Front Genet 5: 144
19. Hussain S, Tuorto F, Menon S, Blanco S, Cox C, Flores JV, Watt S, Kudo NR, Lyko F, Frye M, (2013) The mouse cytosine-5 RNA methyltransferase NSun2 is a component of the chromatoid body and required for testis differentiation. Mol Cell Biol 33: 1561-1570
20. Ikuta K, Weissman IL, (1992) Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc Natl Acad Sci USA 89: 1502-1506
21. Ingolia NT, Lareau LF, Weissman JS, (2011) Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147: 789-802
22. Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P, (2011) Angiogenin-induced tRNA fragments inhibit translation initiation. Mol Cell 43: 613-623
23. Ivanov P, O'Day E, Emara MM, Wagner G, Lieberman J, Anderson P, (2014) G-quadruplex structures contribute to the neuroprotective effects of angiogenin-induced tRNA fragments. Proc Natl Acad Sci USA 111: 18201-18206
24. Kiani J, Grandjean V, Liebers R, Tuorto F, Ghanbarian H, Lyko F, Cuzin F, Rassoulzadegan M, (2013) RNA-mediated epigenetic heredity requires the cytosine methyltransferase Dnmt2. PLoS Genet 9: e1003498
25. Lee JW, Beebe K, Nangle LA, Jang J, Longo-Guess CM, Cook SA, Davisson MT, Sundberg JP, Schimmel P, Ackerman SL, (2006) Editing-defective tRNA synthetase causes protein misfolding and neurodegeneration. Nature 443: 50-55
26. Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, Scadden DT, Ma'ayan A, Enikolopov GN, Frenette PS, (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466: 829-834
27. Motorin Y, Grosjean H, (2001) Transfer RNA modification. In Nature Encyclopedia of Life Sciences. Chichester, UK: John Wiley & Sons, Ltd
28. Motorin Y, Lyko F, Helm M, (2010) 5-methylcytosine in RNA: detection, enzymatic formation and biological functions. Nucleic Acids Res 38: 1415-1430
29. Nedialkova DD, Leidel SA, (2015) Optimization of codon translation rates via tRNA modifications maintains proteome integrity. Cell 161: 1606-1618
30. Okano M, Xie S, Li E, (1998) Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucleic Acids Res 26: 2536-2540
31. Osawa M, Hanada K, Hamada H, Nakauchi H, (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273: 242-245
32. Raddatz G, Guzzardo PM, Olova N, Fantappié MR, Rampp M, Schaefer M, Reik W, Hannon GJ, Lyko F, (2013) Dnmt2-dependent methylomes lack defined DNA methylation patterns. Proc Natl Acad Sci USA 110: 8627-8631
33. Rai K, Chidester S, Zavala CV, Manos EJ, James SR, Karpf AR, Jones DA, Cairns BR, (2007) Dnmt2 functions in the cytoplasm to promote liver, brain, and retina development in zebrafish. Genes Dev 21: 261-266
34. Rezgui VA, Tyagi K, Ranjan N, Konevega AL, Mittelstaet J, Rodnina MV, Peter M, Pedrioli PG, (2013) tRNA tKUUU, tQUUG, and tEUUC wobble position modifications fine-tune protein translation by promoting ribosome A-site binding. Proc Natl Acad Sci USA 110: 12289-12294
35. Rios H, Koushik SV, Wang H, Wang J, Zhou HM, Lindsley A, Rogers R, Chen Z, Maeda M, Kruzynska-Frejtag A, Feng JQ, Conway SJ, (2005) Periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype. Mol Cell Biol 25: 11131-11144
36. Rodnina MV, Wintermeyer W, (2001) Fidelity of aminoacyl-tRNA selection on the ribosome: kinetic and structural mechanisms. Annu Rev Biochem 70: 415-435
37. Schaefer M, Lyko F, (2010) Solving the Dnmt2 enigma. Chromosoma 119: 35-40
38. Schaefer M, Pollex T, Hanna K, Tuorto F, Meusburger M, Helm M, Lyko F, (2010) RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage. Genes Dev 24: 1590-1595
39. Schwanhausser B, Gossen M, Dittmar G, Selbach M, (2009) Global analysis of cellular protein translation by pulsed SILAC. Proteomics 9: 205-209
40. Seita J, Weissman IL, (2010) Hematopoietic stem cell: self-renewal versus differentiation. Wiley Interdiscip Rev Syst Biol Med 2: 640-653
41. Tuorto F, Liebers R, Musch T, Schaefer M, Hofmann S, Kellner S, Frye M, Helm M, Stoecklin G, Lyko F, (2012) RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis. Nat Struct Mol Biol 19: 900-905
42. Wilkinson C, Bartlett R, Nurse P, Bird A, (1995) The fission yeast gene pmt1+ encodes a DNA methyltransferase homologue. Nucleic Acids Res 23: 203-210
43. Yoder JA, Bestor TH, (1998) A candidate mammalian DNA methyltransferase related to pmt1p of fission yeast. Hum Mol Genet 7: 279-284
44. Zinshteyn B, Gilbert WV, (2013) Loss of a conserved tRNA anticodon modification perturbs cellular signaling. PLoS Genet 9: e1003675