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Chapter 9 : Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases

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Abstract:

Contrary to most other modified bases, queuine and archaeosine biosyntheses start outside the tRNA and require a base exchange at the tRNA level, a reaction catalyzed by enzymes known as tRNA-guanine transglycosylases (TGTs). Several groups have reported the isolation of the eukaryotic TGT, but these reports do not agree on its oligomeric state and the size of its subunits. An archaebacterial TGT has been isolated very recently. This enzyme is a 78-kDa protein that has been shown through partial sequencing to be sequence-related to the prokaryotic TGT. TGT is certainly one of the most interesting enzymes of the queuine biosynthesis pathway because it catalyzes a reaction (a base exchange) which is also observed in many other cellular processes involving DNA and RNA. The structure of TGT was solved by the well-known technique of multiple isomorphous replacement (MIR). The soaking approach employed with the small preQ, molecule cannot be used with a tRNA macromolecule and the only way to get the structure of a prokaryotic TGT-tRNA complex is by cocrystallization of the components. The three-dimensional structure of queuosine monophosphate shows that the β-configuration of the ribose is preserved. The recent occurrence in sequence databases of eukaryotic and archaebacterial proteins highly homologous to the prokaryotic TGTs defines a clear phylogenetic link and suggests that TGTs from all three kingdoms have a common fold and a common catalytic mechanism.

Citation: Romier C, Suck D, Ficner R. 1998. Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases, p 169-182. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch9

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Figures

Image of Figure 1
Figure 1

Chemical structures of guanine and the different 7-deazaguanine derivatives. The numbering scheme displayed on guanine is used throughout this chapter.

Citation: Romier C, Suck D, Ficner R. 1998. Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases, p 169-182. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch9
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Image of Figure 2
Figure 2

Ribbon representation of TGT. The eight strands forming the barrel are colored dark gray. The zinc ion is represented as a sphere. The helix following the eighth strand of the barrel (colored white) is assumed to interact with the phosphate backbone of the anticodon stem-loop of the tRNA. Highlighted in black is the helix which plays the role of the “eighth helix of the barrel.” (A) View parallel to the barrel axis; (B) view perpendicular to the barrel axis.

Citation: Romier C, Suck D, Ficner R. 1998. Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases, p 169-182. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch9
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Image of Figure 3
Figure 3

Topology scheme of the structure of TGT. β-strands are represented as triangles, and α-helices are shown as circles. The eight strands forming the barrel are linked by a dashed circle. Reprinted from ( ) with permission of the publisher.

Citation: Romier C, Suck D, Ficner R. 1998. Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases, p 169-182. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch9
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Image of Figure 4
Figure 4

Recognition of preQ by TGT. Van der Waals surfaces are represented by dots. Asp102 at the bottom of the figure is the active site nucleophile of TGT. Asp156, the amide group of G230 and the carbonyl oxygen of L231 are involved in specific recognition of preQ. Reprinted from ( ) with permission of the publisher.

Citation: Romier C, Suck D, Ficner R. 1998. Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases, p 169-182. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch9
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Image of Figure 5
Figure 5

TGT-preQ1 hydrogen bonding contacts. Distances are indicated in angstroms. Reprinted from ( ) with permission of the publisher.

Citation: Romier C, Suck D, Ficner R. 1998. Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases, p 169-182. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch9
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Image of Figure 6
Figure 6

Silver-stained SDS-PAGE of wild-type TGT [TGT(wt)] and TGT mutants D102A, D156A and D156Y, in absence or presence of tRNA,(G34). Shifted bands indicating the formation of a covalent intermediate are seen only with wild-type TGT and the D156A and D156Y mutants. The lack of a shifted band with the D102A mutant identifies D102 as the active site nucleophile of TGT. Lane a, molecular mass standards; lane b, TGT(wt); lane c, TGT(wt) plus tRNA; lane d, TGT(D102A); lane e, TGT(D102A) plus tRNA; lane f, TGT(D156A); lane g, TGT(D156A) plus tRNA; lane h, TGT(D156Y); lane i, TGT(D156Y) plus tRNA; lane j, molecular mass standards. Reprinted from ( ) with permission of the publisher.

Citation: Romier C, Suck D, Ficner R. 1998. Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases, p 169-182. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch9
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Image of Figure 7
Figure 7

Proposed catalytic mechanism of TGT. A covalent intermediate is formed following the nucleopholic attack of aspartate 102 at C1′. Subsequently the deprotonated preQ molecule attacks the C1′ atom, restoring the β-configuration and leading to the modified preQ1-tRNA. Reprinted from ( ) with permission of the publisher.

Citation: Romier C, Suck D, Ficner R. 1998. Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases, p 169-182. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch9
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Image of Figure 8
Figure 8

See following page for legend. Alignment of the Z. (Z.mobi), (E.coli), (S.flex), (H.infl), (H.pylo), sp. (S.sp.), (T.mari), (c.eleg), mouse, human, (M.jann), (A.fulg) and (M.ther) TGT sequences. Highly conserved regions together with other important regions are shaded. The human and mouse sequences are incomplete and the gaps they contain may indicate missing data. Important residues have been labeled with z. numbers. Asp102, marked with an asterisk, is the active site nucleophile of z. TGT. The four zinc ligands are marked. The amino acid marked “Additional Proline” is the proline residue found exclusively in the archaebacterial sequences. The additional c-terminal residues of these later sequences are not shown (marked as “. . .”).

Citation: Romier C, Suck D, Ficner R. 1998. Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases, p 169-182. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch9
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Image of Figure 9
Figure 9

Recognition of queuine by TGT. Van der Waals surfaces are represented with dots. Reprinted from ( ) with permission of the publisher.

Citation: Romier C, Suck D, Ficner R. 1998. Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases, p 169-182. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch9
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Image of Figure 10
Figure 10

Recognition of preQ by TGT. Van der Waals surfaces are represented with dots. Reprinted from ( ) with permission of the publisher.

Citation: Romier C, Suck D, Ficner R. 1998. Structural Basis of Base Exchange by tRNA-Guanine Transglycosylases, p 169-182. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch9
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References

/content/book/10.1128/9781555818296.chap9
1. Björk, G. R., 1995. Biosynthesis and function of modified nucleosides, p. 165205. In D. Soli, and U. RajBhandary (ed.), tRNA: Structure, Biosynthesis, and Function. American Society for Microbiology, Washington, D.C..
2. Carbon, P.,, E. Haumont,, M. Fournier,, S. de Henau,, and H. Gros-jean. 1983. Site-directed in vitro replacement of nucleosides in the anticodon loop of tRNA: application to the study of structural requirements for queuine insertase activity. EMBO J. 2: 10931097.
3. Chong, S.,, A. Curnow,, T. J. Huston,, and G. A. Garcia. 1995. tRNA-guanine transglycosylase from E. coli is a zinc metallo-protein. Site-directed mutagenesis studies to identify the zinc ligands. Biochemistry 34:36943701.
4. Curnow, A. W.,, F. L. Kung,, K. A. Koch,, and G. A. Garcia. 1993. tRNA-guanine transglycosylase from Escherichia coli: gross tRNA structural requirements for recognition. Biochemistry 32: 52395246.
5. Curnow, A. W.,, and G. A. Garcia. 1995. tRNA-guanine transglycosylase from E. coli. Minimal tRNA structure and sequence requirements for recognition. J. Biol. Chem. 270: 1726417267.
6. Deshpande, K. L.,, P. H. Seubert,, D. M. Tillman,, W. R. Farkas,, and J. R. Katze. 1996. Cloning and characterization of cDNA encoding the rabbit tRNA-guanine transglycosylase 60-kilodalton subunit. Arch. Biochem. Biophys. 326:17.
7. Farber, G. K.,, and G. A. Petsko. 1990. The evolution of α/β barrel enzymes. Trends Biochem. Sci. 15:228234.
8. Frey, B.,, J. McCloskey,, W. Kersten,, and H. Kersten. 1988. New function of vitamin B12: cobamide-dependent reduction of epoxyqueuosine in tRNAs of Escherichia coli and Salmonella typhimurium. J. Bacteriol. 170:20782082.
9. Garcia, G. A.,, K. A. Koch,, and S. Chong. 1993. tRNA-guanine transglycosylase from Escherichia coli. Overexpression, purification and quaternary structure.J. Mol. Biol. 231:489497.
10. Garcia, G. A.,, and S. Chong. 1997. Cysteine 265 is in the active site of, but is not essential for catalysis by tRNA-guanine transglycosylase (TGT) from Escherichia coli. J. Protein Chem. 16: 1118.
11. Goodman, H. M.,, J. Abelson,, A. Landy,, S. Brenner,, and J. D. Smith. 1968. Amber suppression: a nucleotide change in the anticodon of a tyrosine transfer RNA. Nature 217:10191024.
12. Goodman, H. M.,, J. N. Abelson,, A. Landy,, S. Zadrazil,, and J. D. Smith. 1970. The nucleotide sequences of tyrosine transfer RNAs of Escherichia coli. Eur. J. Biochem. 13:461483.
13. Gregson, J. M.,, P. F. Crain,, C. G. Edmonds,, R. Gupta,, T. Hashizume,, D. W. Phillipson,, and J. A. McCloskey. 1993. Structure of the archaeal tRNA nucleoside G*-15. J. Biol. Chem. 268: 1007610086.
14. Grosjean, H.,, M. Sprinzl,, and S. Steinberg. 1995. Posttranscriptionally modified nucleosides in tRNA: their locations and frequencies. Biochimie 77:139141.
15. Harada, F.,, and S. Nishimura. 1972. Possible anticodon sequences of tRNAHis, tRNAAsn, and tRNAAsp from Escherichia coli B. Universal presence of nucleoside Q in the first position of the anticodons of these tRNAs. Biochemistry 11:301308.
16. Haumont, E.,, L. Droogmans,, and H. Grosjean. 1987. Enzymatic formation of queuosine and of glycosyl queuosine in yeast tRNAs microinjected into Xenopus laevis oocytes: the effect of the anticodon loop sequence. Eur J. Biochem. 168:219225.
17. Hoops, G. C.,, L. B. Townsend,, and G. A. Garcia. 1995a. tRNA-guanine transglycosylase from E. coli: structure-activity studies investigating the role of the aminomethyl substituent of the heterocyclic substrate preQ1. Biochemistry 34:1538115387.
18. Hoops, G. C.,, L. B. Townsend,, and G. A. Garcia. 1995b. Mechanism-based inactivation of tRNA-guanine transglycosylase from E. coli by 2-amino-5-(fluoromethyl)pyrrolo[2,3-d]pyrimidin-4(3H)-one. Biochemistry 34:1553915544.
19. Howes, N. K.,, and W. R. Farkas. 1978. Studies with a homogeneous enzyme from rabbit erhthrocytes catalyzing the insertion of guanine into tRNA. J. Biol. Chem. 253:90829087.
20. Kasai, H.,, Y. Kuchino,, K. Nihei,, and S. Nishimura. 1975. Distribution of the modified nucleoside Q and its derivatives in animal and plant tRNAs. Nucleic Acids Res. 2:19311939.
21. Katze, J. R.,, B. Basile,, and J. A. McCloskey. 1982. Queuine, a modified base incorporated posttranscriptionally into eukaryotic tRNA: wide distribution in nature. Science 216:5556.
22. Kjeldgaard, M.,, J. Nyborg,, and B. F. C. Clark. 1996. The GTP binding motif: variations on a theme. FASEB J. 10:13471368.
23. Limbach, P. A.,, P. F. Crain,, and A. McCloskey. 1994. Summary: the modified nucleosides of RNA. Nucleic Acids Res. 22: 21832196.
24. Mancia, F.,, N. H. Keep,, A. Nakagawa,, P. F. Leadlay,, S. McSweeney,, B. Rasmussen,, P. Bosecke,, O. Diat,, and P. R. Evans. 1996. How coenzyme B12 radicals are generated: the crystal structure of methylmalonyl-coenzyme A mutase at 2 A resolution. Structure 4:339350.
25. McCarter, J. D.,, and S. G. Withers. 1994. Mechanisms of enzymatic glycoside hydrolysis. Curr. Opin. Struct. Biol. 4:885892.
26. Mueller, S. O.,, and R. K. Slany. 1995. Structural analysis of the interaction of the tRNA modifying enzymes Tgt and QueA with a substrate tRNA. FEBS Lett. 361:259264.
27. Nakanashi, S.,, T. Ueda,, H. Hori,, N. Yamazaki,, N. Okada,, and K. Watanabe. 1994. A UGU sequence in the anticodon loop is a minimum requirement for recognition by E. coli tRNA-guanine transglycosylase.J. Biol. Chem. 269:3222132225.
28. Noguchi, S.,, Z. Yamaizumi,, T. Ohgi,, T. Goto,, Y. Nishimura,, Y. Hirota,, and S. Nishimura. 1978. Isolation of Q nucleoside precursor present in tRNA of an E. coli mutant and its characterization as 7-(cyano)-7-deazaguanosine. Nucleic Acids Res. 5: 42154223.
29. Okada, N.,, S. Noguchi,, S. Nishimura,, T. Ohgi,, T. Goto,, P. F. Crain,, and J. A. McCloskey. 1978. Structure determination of a nucleoside Q precursor isolated from E. coli tRNA: 7-(aminomethyl)-7-deazaguanosine. Nucleic Acids Res. 5: 22892297.
30. Okada, N.,, and S. Nishimura. 1979. Isolation and characterization of a guanine insertion enzyme, a specific tRNA transglycosylase, from Escherichia coli.J. Biol. Chem. 254:30613066.
31. Okada, N.,, S. Noguchi,, H. Kasai,, N. Shindo-Okada,, T. Ohgi,, T. Goto,, and S. Nishimura. 1979. Novel mechanism of post-transcriptional modification of tRNA. J. Biol. Chem. 254: 30673073.
32. Porter, D. J. T.,, B. M. Merrill,, and S. A. Short. 1995. Identification of the active site nucleophile in nucleoside 2-deoxy-ribosyltransferase as glutamic acid 98. J. Biol. Chem. 270: 1555115556.
33. Porter, D. J. T.,, and S. A. Short. 1995. Nucleoside 2-deoxy-ribosyltransferase. Pre-steady-state kinetics analysis of native enzyme and mutant enzyme with an alanyl residue replacing Glu98.J. Biol. Chem. 270:1555715562.
34. Reardon, D.,, and G. K. Farber. 1995. The structure and evolution of α/β barrel proteins. FASEB J. 9:497502.
35. Reuter, K.,, R. Slany,, F. Ullrich,, and H. Kersten. 1991. Structure and organization of Escherichia coli genes involved in biosynthesis of the deazaguanine derivative queuine, a nutrient factor for eukaryotes.J. Bacteriol. 173:22562264.
36. Reuter, K.,, S. Chong,, F. Ullrich,, H. Kersten,, and G. A. Garcia. 1994. Serine 90 is required for enzymic activity by tRNA-guanine transglycosylase from £. coli. Biochemistry 33: 70417046.
37. Reuter, K.,, and R. Ficner. 1995. Sequence analysis and overexpression of the Zymomonas mobilis tgt gene encoding tRNA-guanine transglycosylase: purification and biochemical characterization of the enzyme.J. Bacteriol. 177:52845288.
38. Romier, C. Unpublished data.
39. Romier, C.,, R. Ficner,, K. Reuter,, and D. Suck. 1996a. Purification, crystallization, and preliminary X-ray diffraction studies of tRNA-guanine transglycosylase from Zymomonas mobilis. Proteins Struct. Fund. Genet. 24:516519.
40. Romier, C.,, K. Reuter,, D. Suck,, and R. Ficner. 1996b. Crystal structure of tRNA-guanine transglycosylase: RNA modification by base exchange. EMBO J. 15:28502857.
41. Romier, C.,, K. Reuter,, D. Suck,, and R. Ficner. 1996c. Mutagenesis and crystallographic studies of Zymomonas mobilis tRNA-guanine transglycosylase reveal aspartate 102 as active site nucleophile. Biochemistry 35:1573415739.
42. Romier, C.,, J. E. W. Meyer,, and D. Suck. 1997. Slight sequence variations of a common fold explain the substrate specificities of tRNA-guanine transglycosylases from the three kingdoms. FEBS Lett. 416:9398.
43. Rould, M. A.,, J. J. Perona,, D. Soil,, and T. A. Steitz. 1989. Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNAGln and ATP at 2.8 A resolution. Science 246:11351142.
44. Ruff, M.,, S. Krishnaswamy,, M. Boeglin,, A. Poterszman,, A. Mitschler,, A. Podjarny,, B. Rees,, J. C. Thierry,, and D. Moras. 1991. Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNAAsp. Science 252:16821689.
45. Shindo-Okada, N.,, N. Okada,, T. Ohgi,, T. Goto,, and S. Nishimura. 1980. Transfer ribonucleic acid guanine transglycosylase isolated from rat liver. Biochemistry 19:395400.
46. Short, S. A.,, S. R. Armstrong,, S. E. Ealick,, and D. J. T. Porter. 1996. Active site amino acids that participate in the catalytic mechanism of nucleoside 2'-deoxyribosyltransferase.. J. Biol. Chem. 271:49784987.
47. Slany, R. K.,, M. Bosl,, P. F. Crain,, and H. Kersten. 1993. A new function of S-adenosylmethionine: the ribosyl moiety of AdoMet is the precursor of the cyclopentenediol moiety of the tRNA wobble base queuine. Biochemistry 32:78117817.
48. Slany, R. K.,, and H. Kersten. 1994. Genes, enzymes and coenzymes of queuosine biosynthesis in procaryotes. Biochimie 76: 11781182.
49. Slany, R. K.,, and S. O. Mueller. 1995. tRNA-guanine transglycosylase from bovine liver: purification of the enzyme to homogeneity and biochemical characterization. Eur. J. Biochem. 230: 221228.
50. Walden, T. L.,, N. Howes,, and W. R Farkas. 1982. Purification and properties of guanine, queuine-tRNA transglycosylase from wheat germ.J. Biol. Chem. 257:1321813222.
51. Watanabe, M.,, M. Matsuo,, S. Tanaka,, H. Akimoto,, S. Asahi,, S. Nishimura,, J. R. Katze,, T. Hashizume,, P. F. Crain,, J. A. McCloskey,, and N. Okada. 1997. Biosynthesis of archaeosine, a novel derivative of 7-deazaguanosine specific to archaeal tRNA, proceeds via a pathway involving base replacement on the tRNA polynucleotide chain.J. Biol. Chem. 272:2014620151.
52. Yokoyama, S.,, T. Miyazawa,, Y. Iitaka,, Z. Yamaizumi,, H. Kasai,, and S. Nishimura. 1979. Three-dimensional structure of hyper-modified nucleoside Q located in the wobbling position of tRNA. Nature 282:107109.
53. Yokoyama, S.,, and S. Nishimura,. 1995. Modified nucleosides and codon recognition, p. 207223. In D. Soil, and U. RajBhandary (ed.), tRNA: Structure, Biosynthesis, and Function. American Society for Microbiology, Washington, D.C..

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