Major reorientation of tRNA substrates defines specificity of dihydrouridine synthases

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 19, 2015, Pages 6033-6037

  Byrne, Robert T ^a   Jenkins, Huw T ^a   Peters, Daniel T ^a   Whelan, Fiona ^a   Stowell, James ^a   Aziz, Naveed ^a,b   Kasatsky, Pavel ^c,d   Rodnina, Marina V ^e   Koonin, Eugene V ^f   Konevega, Andrey L ^c,d,e   Antson, Alfred A ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b Genome Canada   (Canada)

^c KURCHATOV INSTITUTE   (Russian Federation)

^d PETER THE GREAT ST PETERSBURG POLYTECHNIC UNIVERSITY   (Russian Federation)

^e MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^f NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Dihydrouridine synthase; Protein RNA interaction; Substrate specificity; TRNA modification; X ray crystallography

Indexed keywords

AMINO ACID; DIHYDROURIDINE SYNTHASE; NUCLEOTIDE; TRANSFER RNA; UNCLASSIFIED DRUG; URIDINE DERIVATIVE; ESCHERICHIA COLI PROTEIN; OXIDOREDUCTASE; PROTEIN BINDING; RNA; RNA BINDING PROTEIN; URIDINE;

ALPHA HELIX; ARTICLE; BINDING SITE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ESCHERICHIA COLI; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; CHEMISTRY; ENZYMOLOGY; MOLECULAR EVOLUTION; PROTEIN FOLDING; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

ESCHERICHIA COLI;

AMINO ACIDS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EVOLUTION, MOLECULAR; OXIDOREDUCTASES; PROTEIN BINDING; PROTEIN FOLDING; RNA; RNA, TRANSFER; RNA-BINDING PROTEINS; SUBSTRATE SPECIFICITY; URIDINE; X-RAY DIFFRACTION;

EID: 84929190405     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1500161112     Document Type: Article

References (36)

1. Jühling F, et al. (2009) tRNAdb 2009: Compilation of tRNA sequences and tRNA genes. Nucleic Acids Res 37(Database issue):D159-D162.
2. Chen C, Tuck S, Byström AS (2009) Defects in tRNA modification associated with neurological and developmental dysfunctions in Caenorhabditis elegans elongator mutants. PLoS Genet 5(7):e1000561.
3. Rakovich T, et al. (2011) Queuosine deficiency in eukaryotes compromises tyrosine production through increased tetrahydrobiopterin oxidation. J Biol Chem 286(22): 19354-19363.
4. Zinshteyn B, Gilbert WV (2013) Loss of a conserved tRNA anticodon modification perturbs cellular signaling. PLoS Genet 9(8):e1003675.
5. Kato T, et al. (2005) A novel human tRNA-dihydrouridine synthase involved in pulmonary carcinogenesis. Cancer Res 65(13):5638-5646.
6. Kuchino Y, Borek E (1978) Tumour-specific phenylalanine tRNA contains two supernumerary methylated bases. Nature 271(5641):126-129.
7. Begley U, et al. (2013) A human tRNA methyltransferase 9-like protein prevents tumour growth by regulating LIN9 and HIF1-α. EMBO Mol Med 5(3):366-383.
8. Spinola M, et al. (2005) Identification and functional characterization of the candidate tumor suppressor gene TRIT1 in human lung cancer. Oncogene 24(35):5502-5509.
9. Dalluge JJ, Hashizume T, Sopchik AE, McCloskey JA, Davis DR (1996) Conformational flexibility in RNA: The role of dihydrouridine. Nucleic Acids Res 24(6):1073-1079.
10. Bishop AC, Xu J, Johnson RC, Schimmel P, de Crécy-Lagard V (2002) Identification of the tRNA-dihydrouridine synthase family. J Biol Chem 277(28):25090-25095.
11. Xing F, Martzen MR, Phizicky EM (2002) A conserved family of Saccharomyces cerevisiae synthases effects dihydrouridine modification of tRNA. RNA 8(3):370-381.
12. Rider LW, Ottosen MB, Gattis SG, Palfey BA (2009) Mechanism of dihydrouridine synthase 2 from yeast and the importance of modifications for efficient tRNA reduction. J Biol Chem 284(16):10324-10333.
13. Xing F, Hiley SL, Hughes TR, Phizicky EM (2004) The specificities of four yeast dihydrouridine synthases for cytoplasmic tRNAs. J Biol Chem 279(17):17850-17860.
14. Kasprzak JM, Czerwoniec A, Bujnicki JM (2012) Molecular evolution of dihydrouridine synthases. BMC Bioinformatics 13:153.
15. Park F, et al. (2004) The 1.59 A resolution crystal structure of TM0096, a flavin mononucleotide binding protein from Thermotoga maritima. Proteins 55(3):772-774.
16. Yu F, et al. (2011) Molecular basis of dihydrouridine formation on tRNA. Proc Natl Acad Sci USA 108(49):19593-19598.
17. Chen M, et al. (2013) Structure of dihydrouridine synthase C (DusC) from Escherichia coli. Acta Crystallogr Sect F Struct Biol Cryst Commun 69(Pt 8):834-838.
18. Hoang C, Ferré-D'Amaré AR (2001) Cocrystal structure of a tRNA Ψ55 pseudouridine synthase: Nucleotide flipping by an RNA-modifying enzyme. Cell 107(7):929-939.
19. Ishitani R, et al. (2003) Alternative tertiary structure of tRNA for recognition by a posttranscriptional modification enzyme. Cell 113(3):383-394.
20. Pan H, Agarwalla S, Moustakas DT, Finer-Moore J, Stroud RM (2003) Structure of tRNA pseudouridine synthase TruB and its RNA complex: RNA recognition through a combination of rigid docking and induced fit. Proc Natl Acad Sci USA 100(22):12648-12653.
21. Savage DF, de Crécy-Lagard V, Bishop AC (2006) Molecular determinants of dihydrouridine synthase activity. FEBS Lett 580(22):5198-5202.
22. Hur S, Stroud RM (2007) How U38, 39, and 40 of many tRNAs become the targets for pseudouridylation by TruA. Mol Cell 26(2):189-203.
23. McCleverty CJ, Hornsby M, Spraggon G, Kreusch A (2007) Crystal structure of human Pus10, a novel pseudouridine synthase. J Mol Biol 373(5):1243-1254.
24. Ishitani R, et al. (2002) Crystal structure of archaeosine tRNA-guanine transglycosylase. J Mol Biol 318(3):665-677.
25. Romier C, Reuter K, Suck D, Ficner R (1996) Crystal structure of tRNA-guanine transglycosylase: RNA modification by base exchange. EMBO J 15(11):2850-2857.
26. Alian A, Lee TT, Griner SL, Stroud RM, Finer-Moore J (2008) Structure of a TrmA-RNA complex: A consensus RNA fold contributes to substrate selectivity and catalysis in m5U methyltransferases. Proc Natl Acad Sci USA 105(19):6876-6881.
27. Goto-Ito S, et al. (2008) Crystal structure of archaeal tRNA(m(1)G37)methyltransferase aTrm5. Proteins 72(4):1274-1289.
28. Walbott H, Leulliot N, Grosjean H, Golinelli-Pimpaneau B (2008) The crystal structure of Pyrococcus abyssi tRNA (uracil-54, C5)-methyltransferase provides insights into its tRNA specificity. Nucleic Acids Res 36(15):4929-4940.
29. Sheldrick GM (2008) A short history of SHELX. Acta Crystallogr A 64(Pt 1):112-122.
30. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Cryst 40(Pt 4):658-674.
31. Cowtan K (2010) Recent developments in classical density modification. Acta Crystallogr D Biol Crystallogr 66(Pt 4):470-478.
32. Cowtan K (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62(Pt 9):1002-1011.
33. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
34. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53(Pt 3):240-255.
35. Keating KS, Pyle AM (2012) RCrane: Semi-automated RNA model building. Acta Crystallogr D Biol Crystallogr 68(Pt 8):985-995.
36. Chou FC, Sripakdeevong P, Dibrov SM, Hermann T, Das R (2013) Correcting pervasive errors in RNA crystallography through enumerative structure prediction. Nat Methods 10(1):74-76.