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Review
.2013 Sep-Oct;4(5):507-22.
doi: 10.1002/wrna.1175. Epub 2013 Jun 10.

Structure and function of the T-loop structural motif in noncoding RNAs

Affiliations
Review

Structure and function of the T-loop structural motif in noncoding RNAs

Clarence W Chan et al. Wiley Interdiscip Rev RNA.2013 Sep-Oct.

Abstract

The T-loop is a frequently occurring five-nucleotide motif found in the structure of noncoding RNAs where it is commonly assumed to play an important role in stabilizing the tertiary RNA structure by facilitating long-range interactions between different regions of the molecule. T-loops were first identified in tRNA(Phe) and a formal consensus sequence for this motif was formulated and later revised based on analyses of the crystal structures of prokaryotic ribosomal RNAs and RNase P and the corresponding primary sequence of their orthologues. In the past decade, several new structures of large RNA molecules have been added to the RCSB Protein Data Bank, including the eukaryotic ribosome, a self-splicing group II intron, numerous synthetases in complex with their cognate transfer RNAs (tRNAs), transfer-messenger RNA (tmRNA) in complex with SmpB, several riboswitches, and a complex of bacterial RNase P bound to its tRNA substrate. In this review, the search for T-loops is extended to these new RNA molecules based on the previously established structure-based criteria. The review highlights and discusses the function and additional roles of T-loops in four broad categories of RNA molecules, namely tRNAs, ribosomal RNAs (rRNAs), P RNAs, and RNA genetic elements. Additionally, the potential application for T-loops as interaction modules is also discussed.

Copyright © 2013 John Wiley & Sons, Ltd.

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Figures

Figure 1
Figure 1. Basic architecture of the T-loop RNA motif both with and without an intercalating nucleobase
In Panels A and B, the 2D and 3D representations of the prototypic T-loop of tRNA (PDB ID: 1EHZ) are shown in yellow. The T-loop acts as an intramolecular receptor for an intercalating nucleobase (IB) stacked between the fourth and fifth T-loop positions. In Panel C, the T-loop is shown with cross-eyed stereoview with a ball-and-stick representation and its nucleotides are numbered 1 to 5 in the 5′ to 3′ direction. The intercalating guanine nucleobase is depicted in red. In panels D and E, the 2D and 3D representations of one of two T-loops identified in the THI-box (thiamine pyrophosphate-sensing) riboswitch(PDB ID: 2HOP), which acts as a receptor for a small molecule ligand, are shown in grey. In Panel F, the T-loop is shown with a cross-eyed stereoview with a ball and stick representation.
Figure 2
Figure 2. Functional and structural similarities between the tRNA and tmRNA T-loops
In panel A, the overall tRNA structure(PDB ID: 1EHZ) is shown in purple as cartoon representation, whereas the T-loop in its TΨC-loop is shown in yellow with ball-and-stick representation. In panel B, the tRNA-like domain of tmRNA (tmRNA-TLD) bound to SmpB (PDB ID: 2CZJ) is shown in green, whereas the T-loop in its TΨC-like-loop is shown in yellow with ball and stick representation. Panel C depicts the two superposed molecules aligned using only the backbone atoms of the T-loops. In Panel D, the superposed T-loops from tRNA (in purple) and tmRNA (in green) are shown as ball and sticks, illustrating the high degree of structural similarity.
Figure 3
Figure 3. Structural importance of T-loops in prokaryotic and eukaryotic rRNAs
In panels A and B, the overall structure of the prokaryotic 16S (PDB ID: 3V2C) and eukaryotic 18S (PDB ID: 2XZM) small subunit rRNAs are shown in grey with T-loops colored in red. Similarly, in panels C and D, the overall structure of the prokaryotic 23S (PDB ID: 2ZJR) and eukaryotic 28S (PDB ID: 3IZ9) large subunit rRNAs are shown in grey with T-loops colored in red. T-loops appear frequently in rRNAs and serve important structural roles primarily by mediating intramolecular tertiary interactions between loop regions that are distant in primary sequence. Furthermore, most rRNA T-loops are structurally conserved across prokaryotic and eukaryotic rRNAs.
Figure 4
Figure 4. T-loops are involved in substrate recognition and tertiary interactions in bacterial RNase P
In panel A, three interacting T-loops in the ternary complex structure of a bacterial RNase P holoenzyme bound to a tRNA substrate (PDB ID: 3Q1Q) are depicted in ball-and-stick representation. The two interlocked T-loops of the P RNA are shown in magenta and green, whereas the T-loop of the tRNA is shown in yellow. Panel B depicts the key interactions that stabilize the two interlocked T-loops of the P RNA. The nucleobase at position 2 (marked with * and **) in of the P RNA T-loops plays a key stabilizing role by forming a co-planar base triple with the closing base-pair (at positions 1 and 5) of the adjacent P RNA T-loop. These position 2 nucleobases also participate in hydrogen bonding interactions with the phosphate oxygen of the fifth nucleotide of the same T-loop. The nucleobases in positions 3, 4, and 5 of both P RNA T-loops form a contiguous, crescent-shaped base-stack that stacks on the position 3 nucleobase of the tRNA T-loop.
Figure 5
Figure 5. A structural T-loop mediates a long-range tertiary interaction in a self-splicing group II intron
In panel A, the secondary structure diagram of theOceanobacillus iheyensis group II intron is shown with subdomains IA and IB and subdomain ID1 colored in in purple and in green, respectively. The T-loop (5′-UGAGA-3′) in subdomain IA mediates a long-range tertiary contact with a proximal loop region of subdomain ID1 (depicted by arrow) by serving as a receptor for an intercalating adenosine from ID1. The tertiary structure of this interaction in the context of the overall group II intron structure (PDB ID: 3EOG) is shown in panel B, and a close up view is shown in panel C. A sharp turn in the backbone directly 3′ of the T-loop mediates a continuous base-stacking interaction between the guanosine and uridine nucleobases directly following the T-loop with another nearby adenosine (not shown) in subdomain ID1.
Figure 6
Figure 6. A conserved T-loop mediates a long-range tertiary interaction in two classes of B12-sensing riboswitches
In panels A and B, the secondary structure diagrams of two classes of B12-sensing riboswitches are shown with the P4 and P6 arms colored in purple and in green, respectively. A conserved T-loop is located in the loop region of the P4 arm and is colored in yellow. Arrows depict a structurally-important, tertiary interaction between the P4 and P6 arms. The overall tertiary structure of the B12-sensing riboswitches from an ocean surface microorganism (PDB ID: 4FRN), Thermoanaerobacter tengcongensis (PDB ID: 4GMA), andSymbiobacteriumthermophilum (PDB ID: 4GXY) are depicted in panels C, E, and G, with the corresponding close up views of the T-loop mediated interaction in panels D, F, and H.
Figure 7
Figure 7. T-loops mediate two important long-range tertiary interaction in a flavin mononucleotide-sensing riboswitch
In panel A, the secondary structure diagram of a flavin mononucleotide (FMN)-sensing riboswitch is shown with the P2, P3, P5, and P6 arms colored in green, blue, magenta, and purple, respectively. T-loops located in the loop region of the P2 and P5 arms are colored in yellow. Both T-loops associate with an intercalated adenosine from the loop region of the P6 and P3 arms, respectively, to help bring together the P2:P6 and P3:P5 arms as seen in the overall tertiary structure of the FMN-sensing riboswitch depicted in panel B (PDB ID: 3F2Q). Close up views of the two T-loops and their key interactions are shown in panels C and D.
Figure 8
Figure 8. A T-loop in the THI-box (thiamine pyrophosphate-sensing) riboswitch is required for substrate recognition
Recognition of thiamine pyrophosphate (TPP) by both prokaryotic (panel A;PDB ID: 2GDI) and eukaryotic (panel B;PDB ID: 2CKY) THI-box riboswitches involves base intercalation of the 4-amino-5-hydroxymethyl-2-methylpyrimidine (HMP) moiety of the TPP ligand between the fourth and fifth nucleotides of the T-loop, as well as hydrogen bonding interactions with the guanosine at the second T-loop position.
Figure 9
Figure 9. T-loops mediate the formation of crystal lattice contacts
Panels A, C, and E show the crystal packing of symmetry related molecules for a tRNAPhe(PDB ID: 1EHZ), a FMN riboswitch(PDB ID: 3F2T), and a group II self-splicing intron(PDB ID: 3G78), respectively. The T-loops in all symmetry-related molecules are shown in yellow with ball-and-stick representation. Panels B, D, and F are the corresponding close up views showing the interactions between the T-loops and the symmetry-related molecules. In all three examples shown here, the third nucleotide of the T-loop stacks with a nucleobase in the adjacent molecule.
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