Identification of determinants for tRNA substrate recognition by Escherichia coli C/U34 2'-O-methyltransferase

RNA Biology

Volumn 12, Issue 8, 2015, Pages 900-911

  Zhou, Mi ^a   Long, Tao ^a   Fang, Zhi Peng ^a   Zhou, Xiao Long ^a   Liu, Ru Juan ^a   Wang, En Duo ^a,b  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b SHANGHAITECH UNIVERSITY   (China)

Author keywords

2' O methyltransferase; Recognition determinants; TrmL; TRNA modification; Wobble base

Indexed keywords

2' O METHYLTRANSFERASE; 6 N (3,3 DIMETHYLALLYL)ADENOSINE; METHYLTRANSFERASE; PURINE; PYRIMIDINE DERIVATIVE; TRANSFER RNA; UNCLASSIFIED DRUG; ALKENE; ANTICODON; CODON; ESCHERICHIA COLI PROTEIN; LEUCINE TRANSFER RNA; S ADENOSYLMETHIONINE; TRML PROTEIN, E COLI;

ANTICODON; ARTICLE; BINDING AFFINITY; CHEMICAL INTERACTION; CHEMICAL MODIFICATION; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; GENE DELETION; IN VITRO STUDY; MOLECULAR RECOGNITION; NONHUMAN; PROTEIN SECONDARY STRUCTURE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; RNA METHYLATION; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; STEADY STATE; BINDING SITE; BIOCATALYSIS; CHEMISTRY; CODON; CONFORMATION; ENZYME SPECIFICITY; GENETICS; KINETICS; METABOLISM; METHYLATION; MOLECULAR GENETICS; MOLECULAR MODEL; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN MULTIMERIZATION;

ALKENES; ANTICODON; BASE SEQUENCE; BINDING SITES; BIOCATALYSIS; CODON; ESCHERICHIA COLI PROTEINS; KINETICS; METHYLATION; METHYLTRANSFERASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN MULTIMERIZATION; PYRIMIDINES; RNA, TRANSFER, LEU; S-ADENOSYLMETHIONINE; SUBSTRATE SPECIFICITY;

EID: 84941582819     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.1080/15476286.2015.1050576     Document Type: Article

References (53)

1. Zhou X, Wang E. Transfer RNA: a dancer between charging and mis-charging for protein biosynthesis. Sci China Life Sci 2013; 56:921-32; PMID:23982864; http://dx.doi.org/10.1007/s11427-013-4542-9
2. El Yacoubi B, Bailly M, de Crécy-Lagard V. Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu Rev Genet 2012; 46:69-95; PMID:22905870; http://dx.doi.org/10.1146/annurevgenet-110711-155641
3. Hou YM, Perona JJ. Stereochemical mechanisms of tRNA methyltransferases. FEBS Lett 2010; 584:278-86; PMID:19944101; http://dx.doi.org/10.1016/j.febslet.2009.11.075
4. Phizicky EM, Alfonzo JD. Do all modifications benefit all tRNAs? FEBS Lett 2010; 584:265-71; PMID:19931536; http://dx.doi.org/10.1016/j.febslet.2009.11.049
5. Hori H. Methylated nucleosides in tRNA and tRNA methyltransferases. Front Genet 2014; 5:144; PMID:24904644; http://dx.doi.org/10.3389/fgene.2014.00144
6. Machnicka MA, Milanowska K, Osman Oglou O, Purta E, KurkowskaM,Olchowik A, JanuszewskiW, Kalinowski S, Dunin-Horkawicz S, Rother KM, et al.MODOMICS: a database of RNA modification pathways-2013 update. Nucleic Acids Res 2013; 41:D262-7; PMID:23118484; http://dx.doi.org/10.1093/nar/gks1007
7. Phizicky EM, Hopper AK. tRNA biology charges to the front. Genes Dev 2010; 24:1832-60; PMID:20810645; http://dx.doi.org/10.1101/gad.1956510
8. Agris PF. Bringing order to translation: the contributions of transfer RNA anticodon-domain modifications. EMBO Rep 2008; 9:629-35; PMID:18552770; http://dx.doi.org/10.1038/embor.2008.104
9. Drummond DA, Wilke CO. Mistranslation-induced protein misfolding as a dominant constraint on codingsequence evolution. Cell 2008; 134:341-52; PMID:18662548; http://dx.doi.org/10.1016/j.cell.2008.05.042
10. Gingold H, Pilpel Y. Determinants of translation efficiency and accuracy. Mol Syst Biol 2011; 7:481; PMID:21487400; http://dx.doi.org/10.1038/msb.2011.14
11. Johansson MJ, Esberg A, Huang B, Bjork GR, Bystrom AS. Eukaryotic wobble uridine modifications promote a functionally redundant decoding system. Mol Cell Biol 2008; 28:3301-12; PMID:18332122; http://dx.doi.org/10.1128/MCB.01542-07
12. Chan CT, Dyavaiah M, DeMott MS, Taghizadeh K, Dedon PC, Begley TJ. A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress. PLoS Genet 2010; 6:e1001247; PMID:21187895; http://dx.doi.org/10.1371/journal.pgen.1001247
13. Wei FY, Suzuki T, Watanabe S, Kimura S, Kaitsuka T, Fujimura A, Matsui H, Atta M, Michiue H, Fontecave M, et al. Deficit of tRNA(Lys) modification by Cdkal1 causes the development of type 2 diabetes in mice. J Clin Invest 2011; 121:3598-608; PMID:21841312; http://dx.doi.org/10.1172/JCI58056
14. Lamichhane TN, Mattijssen S, Maraia RJ. Human cells have a limited set of tRNA anticodon loop substrates of the tRNA isopentenyltransferase TRIT1 tumor suppressor. Mol Cell Biol 2013; 33:4900-8; PMID:24126054; http://dx.doi.org/10.1128/MCB.01041-13
15. Begley U, Dyavaiah M, Patil A, Rooney JP, DiRenzo D, Young CM, Conklin DS, Zitomer RS, Begley TJ. Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol Cell 2007; 28:860-70; PMID:18082610; http://dx.doi.org/10.1016/j.molcel.2007.09.021
16. Benítez-Páez A, Villarroya M, Douthwaite S, Gabaldón T, Armengod ME. YibK is the 2′-O-methyltransferase TrmL that modifies the wobble nucleotide in Escherichia coli tRNA(Leu) isoacceptors. RNA 2010; 16:2131-43; http://dx.doi.org/10.1261/rna.2245910
17. Kawai G, Yamamoto Y, Kamimura T, Masegi T, Sekine M, Hata T, Iimori T, Watanabe T, Miyazawa T, Yokoyama S. Conformational rigidity of specific pyrimidine residues in tRNA arises from posttranscriptional modifications that enhance steric interaction between the base and the 2′-hydroxyl group. Biochemistry 1992; 31:1040-6; PMID:1310418; http://dx.doi.org/10.1021/bi00119a012
18. Anantharaman V, Koonin EV, Aravind L. SPOUT: a class of methyltransferases that includes spoU and trmD RNA methylase superfamilies, and novel superfamilies of predicted prokaryotic RNA methylases. J Mol Microbiol Biotechnol 2002; 4:71-5; PMID:11763972
19. Tkaczuk KL, Dunin-Horkawicz S, Purta E, Bujnicki JM. Structural and evolutionary bioinformatics of the SPOUT superfamily of methyltransferases. BMC Bioinformatics 2007; 8:73; PMID:17338813; http://dx.doi.org/10.1186/1471-2105-8-73
20. Liu RJ, Zhou M, Fang ZP, Wang M, Zhou XL, Wang ED. The tRNA recognition mechanism of the minimalist SPOUT methyltransferase, TrmL. Nucleic Acids Res 2013; 41:7828-42; PMID:23804755; http://dx.doi.org/10.1093/nar/gkt568
21. Hori H, Yamazaki N, Matsumoto T, Watanabe Y, Ueda T, Nishikawa K, Kumagai I, Watanabe K. Substrate recognition of tRNA (Guanosine-2′-)-methyltransferase from Thermus thermophilus HB27. J Biol Chem 1998; 273:25721-7; PMID:9748240; http://dx.doi.org/10.1074/jbc.273.40.25721
22. Hori H, Suzuki T, Sugawara K, Inoue Y, Shibata T, Kuramitsu S, Yokoyama S, Oshima T, Watanabe K. Identification and characterization of tRNA (Gm18) methyltransferase from Thermus thermophilus HB8: domain structure and conserved amino acid sequence motifs. Genes Cells 2002; 7:259-72; PMID:11918670; http://dx.doi.org/10.1046/j.1365-2443.2002.00520.x
23. Persson BC, Jäger G, Gustafsson C. The spoU gene of Escherichia coli, the fourth gene of the spoT operon, is essential for tRNA (Gm18) 2′-O-methyltransferase activity. Nucleic Acids Res 1997; 25:4093-7; PMID:9321663; http://dx.doi.org/10.1093/nar/25.20.4093
24. Kumagai I, Watanabe K, Oshima T. Thermally induced biosynthesis of 2′-O-methylguanosine in tRNA from an extreme thermophile, Thermus thermophilus HB27. Proc Natl Acad Sci U S A 1980; 77:1922-6; PMID:6990416; http://dx.doi.org/10.1073/pnas.77.4.1922
25. Ochi A, Makabe K, Kuwajima K, Hori H. Flexible recognition of the tRNA G18 methylation target site by TrmH methyltransferase through first binding and induced fit processes. J Biol Chem 2010; 285:9018-29; PMID:20053984; http://dx.doi.org/10.1074/jbc.M109.065698
26. Gehrig S, Eberle ME, Botschen F, Rimbach K, Eberle F, Eigenbrod T, Kaiser S, Holmes WM, Erdmann VA, Sprinzl M, et al. Identification of modifications in microbial, native tRNA that suppress immunostimulatory activity. J Exp Med 2012; 209:225-33; PMID:22312113; http://dx.doi.org/10.1084/jem.20111044
27. Ochi A, Makabe K, Yamagami R, Hirata A, Sakaguchi R, Hou YM, Watanabe K, Nureki O, Kuwajima K, Hori H. The catalytic domain of topological knot tRNA methyltransferase (TrmH) discriminates between substrate tRNA and nonsubstrate tRNA via an induced-fit process. J Biol Chem 2013; 288:25562-74; PMID:23867454; http://dx.doi.org/10.1074/jbc.M113.485128
28. Holmes WM, Andraos-Selim C, Roberts I, Wahab SZ. Structural requirements for tRNA methylation. Action of Escherichia coli tRNA(guanosine-1)methyltransferase on tRNA(1Leu) structural variants. J Biol Chem 1992; 267:13440-5; PMID:1618846
29. Grosjean H, Droogmans L, Giegé R, Uhlenbeck OC. Guanosine modifications in runoff transcripts of synthetic transfer RNA-Phe genes microinjected into Xenopus oocytes. Biochim Biophys Acta 1990; 1050:267-73; PMID:2207154; http://dx.doi.org/10.1016/0167-4781(90)90179-6
30. Li JN, Björk GR. Structural alterations of the tRNA (m1G37)methyltransferase from Salmonella typhimurium affect tRNA substrate specificity. RNA 1999; 5:395-408; PMID:10094308; http://dx.doi.org/10.1017/S1355838299980834
31. Christian T, Hou YM. Distinct determinants of tRNA recognition by the TrmD and Trm5 methyl transferases. J Mol Biol 2007; 373:623-32; PMID:17868690; http://dx.doi.org/10.1016/j.jmb.2007.08.010
32. Björk GR, Wikström PM, Byström AS. Prevention of translational frameshifting by the modified nucleoside 1-methylguanosine. Science 1989; 244:986-9; PMID:2471265; http://dx.doi.org/10.1126/science.2471265
33. Redlak M, Andraos-Selim C, Giegé R, Florentz C, Holmes WM. Interaction of tRNA with tRNA (guanosine-1)methyltransferase: binding specificity determinants involve the dinucleotide G36pG37 and tertiary structure. Biochemistry 1997; 36:8699-709; PMID:9220956; http://dx.doi.org/10.1021/bi9701538
34. Ahn HJ, Kim HW, Yoon HJ, Lee BI, Suh SW, Yang JK. Crystal structure of tRNA(m1G37)methyltransferase: insights into tRNA recognition. EMBO J 2003; 22:2593-603; PMID:12773376; http://dx.doi.org/10.1093/emboj/cdg269
35. HolmesWM, Andraos-Selim C, Redlak M. tRNA-m1G methyltransferase interactions: touching bases with structure. Biochimie 1995; 77:62-5; PMID:7599277; http://dx.doi.org/10.1016/0300-9084(96)88105-3
36. Takeda H, Toyooka T, Ikeuchi Y, Yokobori S, Okadome K, Takano F, Oshima T, Suzuki T, Endo Y, Hori H. The substrate specificity of tRNA (m1G37) methyltransferase (TrmD) from Aquifex aeolicus. Genes Cells 2006; 11:1353-65; PMID:17121543; http://dx.doi.org/10.1111/j.1365-2443.2006.01022.x
37. Qian Q, Björk GR. Structural requirements for the formation of 1-methylguanosine in vivo in tRNA(Pro) GGG of Salmonella typhimurium. J Mol Biol 1997; 266:283-96; PMID:9047363; http://dx.doi.org/10.1006/jmbi.1996.0789
38. Purta E, van Vliet F, Tkaczuk KL, Dunin-Horkawicz S, Mori H, Droogmans L, Bujnicki JM. The yfhQ gene of Escherichia coli encodes a tRNA:Cm32/Um32 methyltransferase. BMC Mol Biol 2006; 7:23; PMID:16848900; http://dx.doi.org/10.1186/1471-2199-7-23
39. Somme J, Van Laer B, Roovers M, Steyaert J, Versées W, Droogmans L. Characterization of two homologous 2′-O-methyltransferases showing different specificities for their tRNA substrates. RNA 2014; 20:1257-71; PMID:24951554; http://dx.doi.org/10.1261/rna.044503.114
40. Soderberg T, Poulter CD. Escherichia coli dimethylallyl diphosphate:tRNA dimethylallyltransferase: essential elements for recognition of tRNA substrates within the anticodon stem-loop. Biochemistry 2000; 39:6546-53; PMID:10828971; http://dx.doi.org/10.1021/bi992775u
41. Sprinzl M, Hartmann T, Meissner F, Moll J, Vorderwülbecke T. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res 1987; 15Suppl:r53-188; PMID:3554146; http://dx.doi.org/10.1093/nar/15.suppl.r53
42. Grosjean H, Edqvist J, Stråby KB, Giegé R. Enzymatic formation of modified nucleosides in tRNA: dependence on tRNA architecture. J Mol Biol 1996; 255:67-85; PMID:8568876; http://dx.doi.org/10.1006/jmbi.1996.0007
43. Persson BC, Esberg B, Ólafsson Ó, Björk GR. Synthesis and function of isopentenyl adenosine derivatives in tRNA. Biochimie 1994; 76:1152-60; PMID:7748950; http://dx.doi.org/10.1016/0300-9084(94)90044-2
44. Yarham JW, Lamichhane TN, Pyle A, Mattijssen S, Baruffini E, Bruni F, Donnini C, Vassilev A, He L, Blakely EL, et al. Defective i6A37 modification of mitochondrial and cytosolic tRNAs results from pathogenic mutations in TRIT1 and its substrate tRNA. PLoS Genet 2014; 10:e1004424; PMID:24901367; http://dx.doi.org/10.1371/journal.pgen.1004424
45. Caillet J, Droogmans L. Molecular cloning of the Escherichia coli miaA gene involved in the formation of delta 2-isopentenyl adenosine in tRNA. J Bacteriol 1988; 170:4147-52; PMID:3045085.
46. Jühling F, Mörl M, Hartmann RK, Sprinzl M, Stadler PF, Pütz J. tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res 2009; 37:D159-62; PMID:18957446; http://dx.doi.org/10.1093/nar/gkn772
47. Quigley GJ, Rich A. Structural domains of transfer RNA molecules. Science 1976; 194:796-806; PMID:790568; http://dx.doi.org/10.1126/science.790568
48. Alexandrov A, Chernyakov I, Gu W, Hiley SL, Hughes TR, Grayhack EJ, Phizicky EM. Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell 2006; 21:87-96; PMID:16387656; http://dx.doi.org/10.1016/j.molcel.2005.10.036
49. Cabello-Villegas J, Winkler ME, Nikonowicz EP. Solution conformations of unmodified and A(37)N(6)-dimethylallyl modified anticodon stem-loops of Escherichia coli tRNA(Phe). J Mol Biol 2002; 319:1015-34; PMID:12079344; http://dx.doi.org/10.1016/S0022-2836(02)00382-0
50. Jia G, Fu Y, Zhao X, Dai Q, Zheng G, Yang Y, Yi C, Lindahl T, Pan T, Yang YG, et al. N6-methyladenosine in nuclear RNA is a major substrate of the obesityassociated FTO. Nat Chem Biol 2011; 7:885-7; PMID:22002720; http://dx.doi.org/10.1038/nchembio.687
51. Wang X, Lu Z, Gomez A, Hon GC, Yue Y, Han D, Fu Y, Parisien M, Dai Q, Jia G, et al. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature 2014; 505:117-20; PMID:24284625; http://dx.doi.org/10.1038/nature12730
52. Liu RJ, Tan M, Du DH, Xu BS, Eriani G, Wang ED. Peripheral insertion modulates the editing activity of the isolated CP1 domain of leucyl-tRNA synthetase. Biochem J 2011; 440:217-27; PMID:21819379; http://dx.doi.org/10.1042/BJ20111177
53. Li Y, Chen J, Wang E, Wang Y. T7 RNA polymerase transcription of Escherichia coli isoacceptors tRNA (Leu). Sci China C Life Sci 1999; 42:185-90; PMID:18726472; http://dx.doi.org/10.1007/BF02880055