Chapter 30 : Poking a Hole in the Sanctity of the Triplet Code: Inferences for Framing

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A restrictive EF-G mutant acts as an anti-suppressor of the frameshift causing properties of the tRNA position 74 substitutions but not of the sufS or tRNA hopping mutants described in this chapter. Furthermore, extensive important work on frameshift mutant suppression in Bjork’s laboratory has also focused attention on frameshifting mediated by WT near-cognate tRNAs in the presence of mutant cognate tRNAs. Farabaugh and Bjork extended the model to include the possibility that instead of a normal near-cognate tRNA an undermodified tRNA or a cognate tRNA altered in some other way may also be prone to frameshifting (due to slippage in the P site). This model also proposed that in the absence of mutant tRNAs, nearcognate tRNAs cause frameshifting. Currently two rather different philosophical views about ribosomal frameshifting are being taken. One is to consider programmed frameshifting as amplified errors whose main interest is the insight they provide into translational errors. The other is to value the richness of nature’s exploitation of opportunities to generate high-efficiency frameshifting at particular sites for gene expression purposes.

Citation: Atkins J, Herr A, Ivanov I, Gesteland R, Massire C, O'Connor M. 2000. Poking a Hole in the Sanctity of the Triplet Code: Inferences for Framing, p 396-383. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch30
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Figure 1

Frameshifting near the end of the coat protein gene of the single-stranded RNA phage MS2 results in products larger than the coat protein. The first part of the lysis gene overlaps the end of the coat protein gene, and +1 frameshifting at an unknown site near the end of the coat protein gene yields a coat-lysis hybrid termed protein 5. Reading of the fourthto- last GCA alanine codon in the coat protein gene by math type causes a shift to the -1 frame, resulting in the synthesis of protein 6. Similar -1 frameshifting at any of the last three GCA codons yields protein 7, which, though it contains the same number of amino acids as protein 6, due to its different composition migrates faster on sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Increasing the ratio of math type (which normally reads AGC) to math type (which normally reads GCA) (the numbers under the right-hand part of the autoradiogram give the amounts in micrograms per standard 12.5-μl reaction mixture) gives increasing levels of -1 frameshifting at GCA codons. The highest concentrations shown result in termination, to yield protein 9, at the last stop codon before the zero-frame terminator is reached. With elevated levels of math type (2 μg), increasing the relative amount of math type (the amounts in micrograms are given under the left-hand part of the autoradiogram) decreases the amount of frameshifting to the point where the only obvious product is the regular coat protein. The model for how stacking of 2 bases on the 5' side and 5 bases on the 3' side of the anticodon loop of math type could mediate the shift to the -1 frame is indicated at the top left of the figure. With the normal balance of tRNAs in an extract (i.e., without tRNA addition), a -1 frameshift product, 66K, that is longer than the synthetase (the virus-encoded component of replicase) is detectable. This is due to an analogous type of noncognate decoding of a proline codon by math type.

Citation: Atkins J, Herr A, Ivanov I, Gesteland R, Massire C, O'Connor M. 2000. Poking a Hole in the Sanctity of the Triplet Code: Inferences for Framing, p 396-383. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch30
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Image of Figure 2
Figure 2

(Top) Stereographic representation of the three-dimensional modeling of the canonical interaction between a GCA codon (white) and the anticodon loop of tRNA. The anticodon loop displays the classical 2:5 stack. U33 (red) adopts a U-turn conformation. (Bottom) Stereographic representation of the three-dimensional modeling of the putative interaction between a GCA codon (white) and the anticodon loop of tRNA, involving a -1 frameshift. The anticodon loop displays an alternative 1:6 stack, with U33 flipped over to base-pair with codon base A. The trace of the GCA codon in the case of the canonical interaction is shown in gray. (These models were constructed with the MANIP modeling tool [Massire and Westhof, 1998]. The ribbon drawings were produced with DRAWNA software [ ].)

Citation: Atkins J, Herr A, Ivanov I, Gesteland R, Massire C, O'Connor M. 2000. Poking a Hole in the Sanctity of the Triplet Code: Inferences for Framing, p 396-383. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch30
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Figure 3

(A) Ribosomes bypass 50 nucleotides to decode phage T4 gene . The signals important for bypass are matched “take-off” and “landing” sites (GGA), a stop codon immediately 3' of the take-off site, a stem-loop at the beginning of the coding gap, and a critical region of the nascent peptide that acts within the ribosome. (B) An autoregulatory +1 frameshift at codon 26 is required to synthesize release factor (RF) 2, which mediates polypeptide chain release at UGA. tRNA Leu dissociates from pairing with its codon CUU to re-pair to the mRNA via the overlapping +1 frame codon UUU, which includes the first base of a zero-frame UGA stop codon. An SD sequence 3 bases 5' of the shift site is important for the efficiency of the frameshifting. (C) Two-thirds of the way through the coding sequence of , 50% of the ribosomes shift to the -1 frame to synthesize the gamma product. Gamma and the product of standard decoding are present in a 1:1 ratio as subunits of DNA polymerase III. A “slippery” heptanucleotide shift site, a 5' SD sequence sense by translating ribosomes, and a 3' stem-loop are important for frameshifting.

Citation: Atkins J, Herr A, Ivanov I, Gesteland R, Massire C, O'Connor M. 2000. Poking a Hole in the Sanctity of the Triplet Code: Inferences for Framing, p 396-383. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch30
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