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Chapter 23 : Discontinuous Triplet Decoding with or without Re-Pairing by Peptidyl tRNA

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Abstract:

Virtually all tRNAs are known or predicted from their DNA sequence to have seven-base anticodon loops. If natural, functional tRNAs with eight or nine-base anticodon loops exist, they may cause frameshifting, like their mutant counterparts, whether or not they also participate in triplet decoding. Recoding due to re-pairing has only recently been discovered, and it is certain that surprises lie ahead. Nevertheless, some tentative generalization of the available data on re-pairing at overlapping sites seems warranted. The +1 frameshifting uses a single shift site and offers the opportunity for regulation. In at least one case, regulation works through competition for the downstream codon, so as to sense some biochemical state. Even when the downstream codon is not used for this purpose, tandem shift codons are not used. In contrast, efficient —1 frameshifting uses tandem shift sites. Regulation is not seen, and both pre-slip A and P sites are occupied by tRNA generating the efficient double shift mechanism. Using this mechanism, weak pre-slip A site pairing seems to be important, although there is surprising latitude in repairing. An interesting issue is whether the absence to date of tandem +1 shifts is fortuitous and, if not, the reason for their absence. Several cases of programed frameshifting use more than one stimulatory signal. The +1 frameshifting often utilizes a 5' stimulator, whereas efficient —1 frameshifting often uses a stimulator 3' to the site.

Citation: Atkins J, Gesteland R. 1995. Discontinuous Triplet Decoding with or without Re-Pairing by Peptidyl tRNA, p 471-490. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch23

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Figures

Image of Figure 1
Figure 1

Doublet decoding. In panel A, the identities of the anticodon bases shown in bold are critical for the two-base interaction with the first two bases of a zero frame alanine codon ( ). Panel B shows the effect of addition of tRNASer3 alone or with tRNAAla to an E. colt in vitro protein-synthesizing system programmed with phage MS2 RNA ( ). — 1 frameshifting due to tRNASer3 reading GCA alanine codons just before the coat gene terminator yields elongated products (6 and 7), which terminate at the first — 1 frame terminator after the zero frame terminator. Termination at the previous — 1 frame terminator yields the subcoat protein 9. Addition of tRNAAla (left lane) competes with frameshifting caused by tRNASer3. Shifting to the +1 frame just before the coat gene terminator yields a coat-lysis fusion (protein 5), and synthesis is not enhanced by the addition of tRNASer3. Shifting to the —1 frame just before the 62-kDa synthetase terminator yields an elongated form of the synthetase (66 kDa). Its synthesis is greatly enhanced by addition of tRNAThr3, which causes doublet reading of CCG and CCA proline codons. The amount of tRNA added in micrograms per 12.5 µd of reaction mix is indicated below the lanes.

Citation: Atkins J, Gesteland R. 1995. Discontinuous Triplet Decoding with or without Re-Pairing by Peptidyl tRNA, p 471-490. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch23
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Image of Figure 2
Figure 2

+1 Frameshifting in decoding yeast Ty1 ( ). The rare tRNA that decodes the zero frame AGG codon is not shown.

Citation: Atkins J, Gesteland R. 1995. Discontinuous Triplet Decoding with or without Re-Pairing by Peptidyl tRNA, p 471-490. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch23
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Image of Figure 3
Figure 3

+1 Frameshifting in decoding release factor 2. (A) The interaction between the 16S rRNA of an elongating ribosome and the Shine-Dalgarno sequence 5′ of the CUU U shift site is depicted. (B) Comparison of shift site regions ( ).

Citation: Atkins J, Gesteland R. 1995. Discontinuous Triplet Decoding with or without Re-Pairing by Peptidyl tRNA, p 471-490. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch23
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Image of Figure 4
Figure 4

Simultaneous-slippage models for frameshifting in the — 1 direction. (A) The Jacks et al. model ( ). (B) The Weiss et al. model ( ). (C) A model with E site anticodon pairing. In models B and C, the shift occurs after transpeptidation and perhaps during translocation (see text). Panels A and B were reproduced from Hatfield et al. ( ) with permission.

Citation: Atkins J, Gesteland R. 1995. Discontinuous Triplet Decoding with or without Re-Pairing by Peptidyl tRNA, p 471-490. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch23
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Image of Figure 5
Figure 5

The insertion sequences IS1 and IS911. The black boxes indicate the left (IRL) and right (IRR) terminal inverted repeats. The promoter is partially located in IRL. Open reading frame (ORF) B is in the -1 frame with respect to overlapping ORF A. ORF B is expressed as part of a fusion product AB, and in IS911 but not in IS1, it is expressed independently also. The shifty heptanucleotide in the overlap region of the mRNA is underlined, and one of the possible 3′ secondary structures is shown. The termination codon for the A frame is in bold and boxed. In IS911, the Shine-Dalgarno sequence for B is boxed, and the AUU initiator is marked with asterisks. Reproduced from Chandler and Fayet ( ) with permission.

Citation: Atkins J, Gesteland R. 1995. Discontinuous Triplet Decoding with or without Re-Pairing by Peptidyl tRNA, p 471-490. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch23
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Image of Figure 6
Figure 6

Elements important for the 50-nucleotide hop in t4 gene 60 decoding ( ).

Citation: Atkins J, Gesteland R. 1995. Discontinuous Triplet Decoding with or without Re-Pairing by Peptidyl tRNA, p 471-490. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch23
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Tables

Generic image for table
Table 1

Natural frameshifting in wild-type genes

Comparison of related viruses (SO, ), including the insect retrovirus gypsy ( ), with other insertion sequences ( ) suggests numerous additional likely occurrences. Several other putative examples are being investigated (e.g., see reference ). PS = pseudoknot.

Citation: Atkins J, Gesteland R. 1995. Discontinuous Triplet Decoding with or without Re-Pairing by Peptidyl tRNA, p 471-490. In tRNA. ASM Press, Washington, DC. doi: 10.1128/9781555818333.ch23

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