Investigation of Specificity Determinants in Bacterial tRNA-Guanine Transglycosylase Reveals Queuine, the Substrate of Its Eucaryotic Counterpart, as Inhibitor

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Biela, Inna ^a   Tidten Luksch, Naomi ^a   Immekus, Florian ^a   Glinca, Serghei ^a   Nguyen, Tran Xuan Phong ^a   Gerber, Hans Dieter ^a   Heine, Andreas ^a   Klebe, Gerhard ^a   Reuter, Klaus ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

7 AMINOMETHYL 7 DEAZAGUANINE; 7 CYANO 7 DEAZAGUANINE; CYSTEINE; GLYCINE; GLYCOSYLTRANSFERASE; QUEUINE; TRANSFER RNA GUANINEG LYCOSYLTRANSFERASE; UNCLASSIFIED DRUG; VALINE;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENE; BINDING AFFINITY; COMPUTER MODEL; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; GENETIC VARIABILITY; MOLECULAR RECOGNITION; NONHUMAN; POINT MUTATION; STRUCTURAL HOMOLOGY; TGT GENE; X RAY CRYSTALLOGRAPHY; ZYMOMONAS MOBILIS;

ANIMALS; BINDING SITES; BIOCATALYSIS; CAENORHABDITIS ELEGANS; CATALYTIC DOMAIN; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; ENZYME INHIBITORS; EUKARYOTIC CELLS; GUANINE; HUMANS; KINETICS; MODELS, MOLECULAR; MUTANT PROTEINS; PENTOSYLTRANSFERASES; POINT MUTATION; RNA, TRANSFER; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; ZYMOMONAS;

EID: 84877974861     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064240     Document Type: Article

References (60)

1. Stengl B, Reuter K, Klebe G, (2005) Mechanism and substrate specificity of tRNA-guanine transglycosylases (TGTs): tRNA-modifying enzymes from the three different kingdoms of life share a common catalytic mechanism. ChemBioChem 6: 1926-1939.
2. Oliva R, Tramontano A, Cavallo L, (2007) Mg2+ binding and archaeosine modification stabilise the G15-C48 Levitt base pair in tRNAs. RNA 13: 1427-1436.
3. Nakanishi S, Ueda T, Hori H, Yamazaki N, Okada N, et al. (1994) A UGU sequence in the anticodon loop is a minimum requirement for recognition by Escherichia coli tRNA-guanine transglycosylase. J Biol Chem 269: 32221-32227.
4. Curnow AW, Garcia GA, (1995) tRNA-guanine transglycosylase from Escherichia coli. Minimal tRNA structure and sequence requirements for recognition. J Biol Chem 270: 17264-17267.
5. Phillips G, Yacoubi BE, Lyons B, Alvarez S, Iwata-Reuyl D, et al. (2008) Biosynthesis of 7-deazaguanosine-modified tRNA nucleosides: a new role for GTP cyclohydrolase I. J Bacteriol 190: 7876-7884.
6. McCarthy RM, Somogyi A, Bandarian V, (2009) Escherichia coli QueD is a 6-carboxy-5,6,7,8-tetrahydropterin synthase. Biochemistry 48: 2301-2303.
7. McCarthy RM, Somogyi A, Lin G, Jacobsen NE, Bandarian V, (2009) The deazapurine biosynthetic pathway revealed: in vitro enzymatic synthesis of preQ0 from guanosine 5′-triphosphate in four steps. Biochemistry 48: 3847-3852.
8. Van Lanen SG, Reader JS, Swairjo MA, de Crécy-Lagard V, Lee B, et al. (2005) From cyclohydrolase to oxidoreductase: discovery of nitrile reductase activity in a common fold. Proc Natl Acad Sci USA 102: 4264-4269.
9. Lee BWK, Van Lanen SG, Iwata-Reuyl D, (2007) Mechanistic studies of Bacillus subtilis QueF, the nitrile oxidoreductase involved in queuosine biosynthesis. Biochemistry 46: 12844-12854.
10. Chikwana VM, Stec B, Lee BWK, de Crécy-Lagard V, Iwata-Reuyl D, et al. (2012) Structural basis of biological nitrile reduction. J Biol Chem 287: 30560-30570.
11. Van Lanen SG, Kinzie GS, Matthieu S, Link T, Culp J, et al. (2003) tRNA modification by S-adenosylmethionine:tRNA ribosyltransferase-isomerase. Assay development and characterisation of the recombinant enzyme. J Biol Chem 278: 10491-10499.
12. Mathews I, Schwarzenbacher R, McMullan D, Abdubek P, Ambing E, et al. (2005) Crystal structure of S-adenosylmethionine:tRNA ribosyltransferase-isomerase (QueA) from Thermotoga maritima at 2.0 Å resolution reveals a new fold. Proteins 59: 869-874.
13. Grimm C, Ficner R, Sgraja T, Haebel P, Klebe G, et al. (2006) Crystal structure of Bacillus subtilis S-adenosylmethionine:tRNA ribosyltransferase-isomerase. Biochem Biophys Res Comm 351: 695-701.
14. Frey B, McCloskey J, Kersten W, Kersten H, (1988) New function of vitamin B12: cobamide-dependent reduction of epoxyqueuosine to queuosine in tRNAs of Escherichia coli and Salmonella typhimurium. J Bacteriol 170: 2078-2082.
15. Miles ZD, McCarthy RM, Molnar G, Bandarian V, (2011) Discovery of epoxyqueuosine (oQ) reductase reveals parallels between halorespiration and tRNA modification. Proc Natl Acad Sci USA 108: 7368-7372.
16. Romier C, Reuter K, Suck D, Ficner R, (1996) Crystal structure of tRNA-guanine transglycosylase: RNA modification by base exchange. EMBO J 15: 2850-2857.
17. Ritschel T, Atmanene C, Reuter K, Van Dorsselaer A, Sanglier-Cianferani S, et al. (2009) An integrative approach combining noncovalent mass spectrometry, enzyme kinetics and X-ray crystallography to decipher Tgt protein-protein and protein-RNA interaction. J Mol Biol 393: 833-847.
18. Grädler U, Ficner R, Garcia GA, Stubbs MT, Klebe G, et al. (1999) Mutagenesis and crystallographic studies of Zymomonas mobilis tRNA-guanine transglycosylase to elucidate the role of serine 103 for enzymatic activity. FEBS Lett 454: 142-146.
19. Grädler U, Gerber H-D, Goodenough-Lashua DAM, Garcia GA, Ficner R, et al. (2001) A new target for Shigellosis: rational design and crystallographic studies of inhibitors of tRNA-guanine transglycosylase. J Mol Biol 306: 455-467.
20. Goodenough-Lashua DM, Garcia GA, (2003) tRNA-guanine transglycosylase from E. coli: a ping-pong kinetic mechanism is consistent with nucleophilic catalysis. Bioorg Chem 31: 331-344.
21. Xie W, Liu X, Huang RH, (2003) Chemical trapping and crystal structure analysis of a catalytic tRNA guanine transglycosylase covalent intermediate. Nature Struct Biol 10: 781-788.
22. Tidten N, Stengl B, Heine A, Garcia GA, Klebe G, et al. (2007) Glutamate versus glutamine exchange swaps substrate selectivity in tRNA-guanine transglycosylase: insight into the regulation of substrate selectivity by kinetic and crystallographic studies. J Mol Biol 374: 764-776.
23. Meyer EA, Donati N, Guillot M, Schweizer WB, Diederich F, et al. (2006) Synthesis, biological evaluation, and crystallographic studies of extended guanine-based (lin-benzoguanine) inhibitors for tRNA-guanine transglycosylase (TGT). Helv Chim Acta 89: 573-597.
24. Garcia GA, Chervin SM, Kittendorf JD, (2009) Identification of the rate-limiting step of tRNA-guanine transglycosylase from Escherichia coli. Biochemistry 48: 11243-11251.
25. Okada N, Nishimura S, (1979) Isolation and characterization of a guanine insertion enzyme, a specific tRNA transglycosylase, from Escherichia coli. J Biol Chem 254: 3061-3066.
26. Chen V-C, Brooks AF, Goodenough-Lashua DM, Kittendorf JD, Showwalter HD, et al. (2011) Evolution of eucaryal tRNA-guanine transglycosylase: insight gained from the heterocyclic substrate recognition by the wild-type and mutant human and Escherichia coli tRNA-guanine transglycosylases. Nucleic Acids Res 39: 2834-2844.
27. Boland C, Hayes P, Santa-Maria I, Nishimura S, Kelly VP, (2009) Queuosine formation in eucaryotic tRNA occurs via a mitochondria-localized heteromeric transglycosylase. J Biol Chem 284: 18218-18227.
28. Chen V-C, Kelly VP, Stachura SV, Garcia GA, (2010) Characterization of the human tRNA-guanine transglycosylase: confirmation of the heterodimeric subunit structure. RNA 16: 958-968.
29. Durand JM, Dagberg B, Uhlin BE, Björk GR, (2000) Transfer RNA modification, temperature and DNA superhelicity have a common target in the regulatory network of the virulence of Shigella flexneri: the expression of the virF gene. Mol Microbiol 35: 924-935.
30. Hurt JK, Olgen S, Garcia GA, (2007) Site-specific modification of Shigella flexneri virF mRNA by tRNA-guanine transglycosylase in vitro. Nucleic Acids Res 35: 4905-4913.
31. Ritschel T, Hörtner S, Heine A, Diederich F, Klebe G, (2009) Crystal structure analysis and in silico pKa calculations suggest strong pKa shifts of ligands as driving force for high-affinity binding to TGT. ChemBioChem 10: 716-727.
32. Ritschel T, Kohler PC, Neudert G, Heine A, Diederich F, et al. (2009) How to replace the residual solvation shell of polar active site residues to achieve nanomolar inhibition of tRNA-guanine transglycosylase. ChemMedChem 4: 2012-2023.
33. Kohler PC, Ritschel T, Schweizer WB, Klebe G, Diederich F, (2009) High-affinity inhibitors of tRNA-guanine transglycosylase replacing the function of a structural water cluster. Chem Eur J 15: 10809-10817.
34. Rakovich T, Boland C, Bernstein I, Chikwana VM, Iwata-Reuyl D, et al. (2011) Queuosine deficiency in eukaryotes compromises tyrosine production through increased tetrahydrobiopterin oxidation. J Biol Chem 286: 19354-19363.
35. Romier C, Meyer JE, Suck D, (1997) Slight sequence variations of a common fold explain the substrate specificities of tRNA-guanine transglycosylases from the three kingdoms. FEBS Lett 416: 93-98.
36. Deshpande KL, Katze JR, (2001) Characterization of cDNA encoding the human tRNA-guanine transglycosylase (TGT) catalytic subunit. Gene 265: 205-212.
37. Brenk R, Stubbs MT, Heine A, Reuter K, Klebe G, (2003) Flexible adaptations in the structure of the tRNA-modifying enzyme tRNA-guanine transglycosylase and their implications for substrate selectivity, reaction mechanism and structure-based drug design. ChemBioChem 4: 1066-1077.
38. Gerber H-D, Klebe G, (2012) Concise and efficient syntheses of preQ1, queuine and ent-queuine. Org Biomol Chem 10: 8660-8668.
39. Jerabek-Willemsen M, Wienken CJ, Braun D, Baaske P, Duhr S, (2011) Molecular interaction studies using microscale thermophoresis. ASSAY and Drug Development Technologies 9: 342-353.
40. Kung FL, Garcia GA, (1998) tRNA-guanine transglycosylase from Escherichia coli: recognition of full-length 'queuine-cognate' tRNAs. FEBS Lett 431: 427-432.
41. Sheriff S, Hendrickson WA, Smith JL, (1987) Structure of myohemerythrin in the azidomet state at 1.7/1.3 Å resolution. J Mol Biol 197: 273-296.
42. Thomas CE, Chen Y-C, Garcia GA, (2011) Differential heterocyclic substrate recognition by, and pteridine inhibition of E. coli tRNA-guanine transglycosylase. Biochem Biophys Res Comm 410: 34-39.
43. Lovell SC, Word JM, Richardson JS, Richardson DC, (2000) The penultimate rotamer library. Proteins 40: 389-408.
44. Boeckmann B, Bairoch A, Apweiler R, Blatter MC, Estreicher A, et al. (2003) The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res 31: 365-370.
45. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.
46. Eswar N, Marti-Renom MA, Webb B, Madhusudhan MS, Eranian D, et al. (2000) Comparative protein structure modelling with MODELLER. Current Protocols in Bioinformatics Supplement 15: 5.6.1-5.6.30.
47. Romier C, Ficner R, Reuter K, Suck D, (1996) Purification, crystallization, and preliminary X-ray diffraction studies of tRNA-guanine transglycosylase from Zymomonas mobilis. Proteins 24: 516-519.
48. Curnow AW, Kung FL, Koch KA, Garcia GA, (1993) tRNA-guanine transglycosylase from Escherichia coli: gross tRNA structural requirements for recognition. Biochemistry 32: 5239-5246.
49. Wienken CJ, Baaske P, Rothbauer U, Braun D, Duhr S, (2010) Protein-binding assays in biological liquids using microscale thermophoresis. Nat Commun 1: 100.
50. Otwinowski Z, Minor W, (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
51. Battye TGG, Kontogiannis L, Johnson O, Powell HR, Leslie AGW, (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr Sect D 67: 271-281.
52. Evans PR, (2011) An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr Sect D 67: 282-292.
53. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr Sect D 54: 905-921.
54. Sheldrick GM, Schneider TR, (1997) SHELXL: high-resolution refinement. Methods Enzymol 277b: 319-343.
55. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr Sect D 66: 213-221.
56. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr Sect D 60: 2126-2132.
57. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr Sect D 67: 235-242.
58. Painter J, Merritt EA, (2006) TLSMD web server for the generation of multi-group TLS models. J Appl Crystallogr 39: 109-111.
59. Laskowski RA, MacArthur MW, Moss DS, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: 283-291.
60. Kleywegt GJ, Zou JY, Kjeldgaard M, Jones TA, Around O (2001) In International Tables for Crystallography; Rossmann MG, Arnold E, Eds, Kluwer Academic Publishers: Dordrecht Vol F, 353-356.