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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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