Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes

Grosjean, Henri; Fiers, Walter

doi:10.1016/0378-1119(82)90157-3

Cited by 832 publications

(425 citation statements)

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“…The difference between the results obtained with the trp operon and those obtained with the ilv operon appear even more paradoxical when it is recalled that the arginine codon in the trp leader (CGC) is one that can be misread (13) and therefore could be less effective in ribosome stalling, whereas that in the ilv leader (CGA) is one for which the tRNA is less efficiently charged (21). The effect of arginine starvation on trp operon expression had been measured by formation of hybridizable message, i.e., a measure of functional transcription beyond the attenuator.…”

Section: Discussionmentioning

confidence: 96%

Specificity of attenuation control in the ilvGMEDA operon of Escherichia coli K-12

1991

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Three different approaches were used to examine the regulatory effects of the amino acids specified by the peptide-coding region of the leader transcript of the ilvGMEDA operon of Escherichia coli K-12. Gene expression was examined in strains carrying an ilvGMED'-lac operon fusion. In one approach, auxotrophic derivatives were starved of single amino acids for brief periods, and the burst of j-galactosidase synthesis upon adding the missing amino acid was determined. Auxotrophic derivatives were also grown for brief periods with a limited supply of one amino acid (derepression experiments). Finally, prototrophic strains were grown in minimal medium supplemented with single and multiple supplements of the chosen amino acids. Although codons for arginine, serine, and proline are interspersed among the codons for the three branched-chain (regulatory) amino acids, they appeared to have no effect when added in excess to prototrophs or when supplied in restricted amounts to auxotrophs. Deletions removing the terminator stem from the leader removed all ilvspecific control, indicating that the attenuation mechanism is the sole mechanism for ilv-specific control.The specific control of expression of the ilvGMEDA operon in the enteric bacteria is characterized by repression of the operon when the three branched-chain amino acids are in ample supply but derepression when the supply of any one of the three is limited (14,30). This ilv-specific regulation appears to be exclusively a consequence of an attenuation mechanism ( Fig. 1) (4,32,38). In principle, the attenuation mechanism controlling the ilv operon appears to be quite similar to that found to control operons involved in tryptophan (35), leucine (19), phenylalanine (61), histidine (3), and threonine (17) biosynthesis: the leader region specifies a short peptide containing a disproportionate frequency of the amino acids that are found to regulate the operon. Thus, the rate at which the leader can be translated serves to sense whether the regulatory amino acid is in short or ample supply.As emphasized by Landick and Yanofsky (31), an important feature of the attenuation mechanism is the pausing of RNA polymerase at a certain site in the leader region. The pause allows time for the ribosome to initiate translation, and as translation proceeds, the base pairing in the protector (1:2 stem, Fig. 2) is progressively disrupted. Should ribosome movement be retarded, presumably by stalling at a regulatory codon, long enough for the bases in the upstream arm of the terminator (bases 157 to 164) to emerge on the nascent transcript, these bases can pair with those in the downstream arm of the protector (bases 98 to 105) in the antiterminator (2:3 stem, Fig. 3). It is assumed that, in the absence of ribosome stalling (repressing conditions), translation proceeds rapidly enough that the bases in the downstream arm of the protector will also be covered by the ribosome or otherwise be sterically prevented from antiterminator formation and the terminator will be formed instead. Altho...

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Section: Discussionmentioning

confidence: 96%

Specificity of attenuation control in the ilvGMEDA operon of Escherichia coli K-12

1991

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“…This is reflected by the high specific enzyme activities determined in cell extracts. In addition to the gap, pgk, and tpi genes, two more presumably highly expressed genes of C. glutamicum have been characterized:fda (57) related to the degree of codon bias (6,19,29), it was interesting to compare the combined codon usage of gap, pgk, tpi, fda, and gdh with that of C. glutamicum genes which code for enzymes involved in amino acid (threonine, lysine, isoleucine, phenylalanine, or tryptophan) biosynthesis and which I therefore consider to be moderately expressed. As shown in Table 3, the former group of genes is in fact significantly more highly biased than the latter.…”

Section: Discussionmentioning

confidence: 99%

Identification, sequence analysis, and expression of a Corynebacterium glutamicum gene cluster encoding the three glycolytic enzymes glyceraldehyde-3-phosphate dehydrogenase, 3-phosphoglycerate kinase, and triosephosphate isomerase

Eikmanns

1992

J Bacteriol

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To investigate a possible chromosomal clustering of glycolytic enzyme genes in Corynebacterium glutamicum, a 6.4-kb DNA 27,198). The amino acid sequences of the three enzymes show up to 62% (GAPDH), 48% (PGK), and 44% (TPI) identity in comparison with respective enzymes from other organisms. The gap, pgk, tpi, and ppc genes were cloned into the C. glutamicum-Escherichia coli shuttle vector pEKO and introduced into C. glutamicum. Relative to the wild type, the recombinant strains showed up to 20-fold-higher specific activities of the respective enzymes. On the basis of codon usage analysis of gap, pgk, tpi, and previously sequenced genes from C. glutamicum, a codon preference profile for this organism which differs significantly from those of E. coli and Bacillus subtilis is presented.

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“…The speed of ribosome travel on mRNA may well depend on several parameters such as codon usage, codon-anticodon interactions (Grosjean & Fiers, 1982), codon context (Lipman & Wilbur, 1983;Yarus & Folley, 1985;Shpaer, 1986;Varenne et al, 1989), adjacent codons (Gutman & Hatfield, 1989), and second-ary structure of the mRNA region. Among these, the supposition regarding the correlation between codon usage and overall translation rate is supported by various lines of published experimental evidence, as will be described subsequently.…”

Section: Rationalementioning

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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Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes

Cited by 832 publications

References 57 publications

Specificity of attenuation control in the ilvGMEDA operon of Escherichia coli K-12

Specificity of attenuation control in the ilvGMEDA operon of Escherichia coli K-12

Identification, sequence analysis, and expression of a Corynebacterium glutamicum gene cluster encoding the three glycolytic enzymes glyceraldehyde-3-phosphate dehydrogenase, 3-phosphoglycerate kinase, and triosephosphate isomerase

Ribosome‐mediated translational pause and protein domain organization

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