Codon usage can affect efficiency of translation of genes in<i>Escherichia coli</i>

Robinson, Martyn K.; Lilley, R.; Little, Stephen F.; Emtage, J.S.; Yarranton, Geoffrey; Pe, Stephens; Millican, A.; Eaton, Michael A. W.; Humphreys, G. O.

doi:10.1093/nar/12.17.6663

Cited by 295 publications

(166 citation statements)

References 25 publications

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“…Consequently, we cannot exclude that codon usage could also improve the rate of elongation of protein synthesis. Moreover, several experiments conducted on E. coli show that optimal codons could increase both the accuracy and the speed of translation (Robinson et al 1984;Precup and Parker 1987;Sorensen et al 1989). Thus codon usage is possibly related to both the elongation rate and the accuracy of translation.…”

Section: Does Codon Usage Improve the Accuracy The Speed Of Translatmentioning

confidence: 99%

Synonymous Codon Usage, Accuracy of Translation, and Gene Length in Caenorhabditis elegans

2001

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Abstract. In many unicellular organisms, invertebrates, and plants, synonymous codon usage biases result from a coadaptation between codon usage and tRNAs abundance to optimize the efficiency of protein synthesis. However, it remains unclear whether natural selection acts at the level of the speed or the accuracy of mRNAs translation. Here we show that codon usage can improve the fidelity of protein synthesis in multicellular species. As predicted by the model of selection for translational accuracy, we find that the frequency of codons optimal for translation is significantly higher at codons encoding for conserved amino acids than at codons encoding for nonconserved amino acids in 548 genes compared between Caenorhabditis elegans and Homo sapiens. Although this model predicts that codon bias correlates positively with gene length, a negative correlation between codon bias and gene length has been observed in eukaryotes. This suggests that selection for fidelity of protein synthesis is not the main factor responsible for codon biases. The relationship between codon bias and gene length remains unexplained. Exploring the differences in gene expression process in eukaryotes and prokaryotes should provide new insights to understand this key question of codon usage.

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Section: Does Codon Usage Improve the Accuracy The Speed Of Translatmentioning

confidence: 99%

Synonymous Codon Usage, Accuracy of Translation, and Gene Length in Caenorhabditis elegans

2001

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“…However, we propose that these two slowly translated codons are avoided by slow regions (that occur at mRNA spans that correspond to the strategic positions on proteins such as domain ends) because they may induce dissociation of the translation complex and cause a deleterious rather an intentional pause. Many reports in the literature (Robinson et al, 1984;Bonekamp et al, 1985;Spanjaard & van Duin, 1988;Varenne et al, 1989, Chen & Inouye, 1990Spanjaard et al, 1990;Kinnaird et al, 1991;Rosenberg et al, 1993;Goldman et al, 1995) show that the introduction of cua (Leu) or agg (Arg) codon strings results in the reduction of protein yield and presumably induces dissociation of the translation complex or frameshifting and hopping (Kane et al, 1992) events. Chen and Inouye (1990) observed preferential use of such codons in the region spanning the first 25 codons of the mRNA; they suggest that such a preference for the minor codons in an early gene section may modulate gene expression by premature termination of translation, thereby avoiding unnecessary translation of a large part of the mRNA.…”

Section: Rare Codons and Their Usage In Slow Regionsmentioning

confidence: 99%

Ribosome‐mediated translational pause and protein domain organization

1996

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Because regions on the messenger ribonucleic acid differ in the rate at which they are translated by the ribosome and because proteins can fold cotranslationally on the ribosome, a question arises as to whether the kinetics of translation influence the folding events in the growing nascent polypeptide chain. Translationally slow regions were identified on mRNAs for a set of 37 multidomain proteins from Escherichia coli with known three-dimensional structures. The frequencies of individual codons in mRNAs of highly expressed genes from E. coli were taken as a measure of codon translation speed. Analysis of codon usage in slow regions showed a consistency with the experimentally determined translation rates of codons; abundant codons that are translated with faster speeds compared with their synonymous codons were found to be avoided; rare codons that are translated at an unexpectedly higher rate were also found to be avoided in slow regions. The statistical significance of the occurrence of such slow regions on mRNA spans corresponding to the oligopeptide domain termini and linking regions on the encoded proteins was assessed. The amino acid type and the solvent accessibility of the residues coded by such slow regions were also examined. The results indicated that protein domain boundaries that mark higher-order structural organization are largely coded by translationally slow regions on the RNA and are composed of such amino acids that are stickier to the ribosome channel through which the synthesized polypeptide chain emerges into the cytoplasm. The translationally slow nucleotide regions on mRNA possess the potential to form hairpin secondary structures and such structures could further slow the movement of ribosome. The results point to an intriguing correlation between protein synthesis machinery and in vivo protein folding. Examination of available mutagenic data indicated that the effects of some of the reported mutations were consistent with our hypothesis.Keywords: codon usage; domain linkers; peptide channel; protein folding; ribosome; translation The rate of protein translation is nonuniform along the mRNA (Varenne et al., 1984). Ribosomes seem to pause as well as stack at specific regions on mRNA (Chaney & Morris, 1979;Wolin &Walter, 1988;Kim et al., 1991;Kim & Hollingsworth, 1992). Two of the mRNA features that slow the ribosome during translation are the presence of slow codons (Varenne et al., 1984;Bonekamp et al., 1985;Wolin & Walter, 1988) and the formation of higher order nucleotide structures (Chaney & Morris, 1979;Tu et al., 1992). The resultant translational pause may temporally separate the adjacent regions on the growing nascent polypeptide. Given that proteins can fold cotranslationally with the possible involvement of the ribosome (Phillips, 1966;Baldwin, 1975;Yonath, 1992;Kudlicki et al., 1994;Wiedmann et al., 1994;Brimacombe, 1995), the temporal separation might exert a phenotypic effect on the structural organization of the encoded protein. We show that as much as 70% of the do...

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“…However, the presence of the rare codon AGA (codon 402 of the coding region) is the most likely reason for the temporary accumulation of the 46000-M, polypeptide. The significance of rare codons in regulatory and minor proteins has been studied before [15-201, and recently [21] it has been shown that the insertion in tandem of four of the extremely rare codon (Arg AGG) into the E. coli cut gene significantly reduces the level of expression. For some E. coli proteins the synonymous codons are used in a non-random manner and the codons preferred are those recognised by the most abundant tRNA species in the cell; the concentration of each tRNA and the frequency of usage of the synonymous codons have been listed by Ikamura [22,231.…”

Section: Discussionmentioning

confidence: 99%

Intermediates in the synthesis of TolC protein include an incomplete peptide stalled at a rare Arg codon

Misra

Reeves

1985

Eur J Biochem

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TolC is a minor outer membrane protein of Escherichia coli K 12 and is initially synthesized as a precursor. A distinct intermediate polypeptide of Mr about 46000 was consistently observed at the initial stages of biosynthesis. The further elongation of this peptide can be blocked by chloramphenicol. We have investigated the cause of the temporary accumulation of the 46000‐Mr intermediate and we postulate that the presence of a rare codon AGA (Arg) at codon 402 of the tolC mRNA halts translating ribosomes owing to a limiting amount of the tRNAArg (AGA) species in the cell. The translation of tolC mRNA can be increased by providing T4 tRNAArg(AGA), encoded on a plasmid.

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Codon usage can affect efficiency of translation of genes inEscherichia coli

Cited by 295 publications

References 25 publications

Synonymous Codon Usage, Accuracy of Translation, and Gene Length in Caenorhabditis elegans

Synonymous Codon Usage, Accuracy of Translation, and Gene Length in Caenorhabditis elegans

Ribosome‐mediated translational pause and protein domain organization

Intermediates in the synthesis of TolC protein include an incomplete peptide stalled at a rare Arg codon

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