Translation initiation in Escherichia coli: old and new questions

We discuss the features of Escherichia coli mRNAs which determine where and how efficiently translation is initiated. We have shown that DNA fragments comprising 60–80 nucleotides that bracket the initiation codon of real genes generally promote translation when inserted within a foreign mRNA, while those not corresponding to an authentic gene start do not do so even if they include a Shine‐Dalgarno‐like element followed by AUG or GUG. Therefore, the information that pinpoints the correct start sites, while extending beyond the mere presence of these elements, remains essentially local. The possible nature of this information is discussed. Next, we point out that, in order to remain accessible, translational starts must escape long‐range base‐pairing within large mRNAs, and we argue that the tight coupling between translation and transcription plays an important role in achieving this. Finally, we discuss two intriguing situations in which the initiation frequency should be dependent upon the rate of translation elongation.

[1]  D. Draper.  Translational Regulation of Ribosomal Proteins in Escherichia coli , 1987 .

[2]  M. C. Ganoza,et al.  Potential secondary structure at translation-initiation sites [published erratum appears in Nucleic Acids Res 1988 May 11;16(9): 4196] , 1987, Nucleic Acids Res..

[3]  M Yarus,et al.  Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. , 1989, Journal of molecular biology.

[4]  M. Chamberlin,et al.  Pausing and termination of transcription within the early region of bacteriophage T7 DNA in vitro. , 1981, The Journal of biological chemistry.

[5]  S. Arnott,et al.  The ribosome binding sites recognized by E. coli ribosomes have regions with signal character in both the leader and protein coding segments. , 1980, Nucleic acids research.

[6]  B. Berkhout,et al.  Mechanism of translational coupling between coat protein and replicase genes of RNA bacteriophage MS2. , 1985, Nucleic acids research.

[7]  C. Gualerzi,et al.  Selection of the mRNA translation initiation region by Escherichia coli ribosomes. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Jan van Duin,et al.  Control of prokaryotic translational initiation by mRNA secondary structure , 1990 .

[9]  J. Forchhammer,et al.  Growth rate of polypeptide chains as a function of the cell growth rate in a mutant of Escherichia coli 15. , 1971, Journal of molecular biology.

[10]  M. Dreyfus,et al.  What constitutes the signal for the initiation of protein synthesis on Escherichia coli mRNAs? , 1988, Journal of molecular biology.

[11]  A. C. Looman,et al.  Influence of the codon following the AUG initiation codon on the expression of a modified lacZ gene in Escherichia coli. , 1987, The EMBO journal.

[12]  L. Gold,et al.  Maximizing Gene Expression , 1986 .

[13]  P. Ray,et al.  Functional inactivation of bacteriophage λ morphogenetic gene mRNA , 1975, Nature.

[14]  D. Bedwell,et al.  Regulation of alpha operon gene expression in Escherichia coli. A novel form of translational coupling. , 1987, Journal of molecular biology.

[15]  G. Stormo.  CHAPTER 7 – Translation Initiation , 1986 .

[16]  C. A. Thomas,et al.  Visualization of Bacterial Genes in Action , 1970, Science.

[17]  E. Gren.  Recognition of messenger RNA during translational initiation in Escherichia coli. , 1984, Biochimie.

[18]  L. Gold,et al.  Selection of the initiator tRNA by Escherichia coli initiation factors. , 1989, Genes & development.

[19]  C. Petersen.  Long-range translational coupling in the rplJL-rpoBC operon of Escherichia coli. , 1989, Journal of molecular biology.

[20]  N. Sonenberg,et al.  Role of Eukaryotic Messenger RNA Cap-Binding Protein in Regulation of Translation , 1987 .

[21]  W. Sebald,et al.  Translational initiation frequency of atp genes from Escherichia coli: identification of an intercistronic sequence that enhances translation. , 1985, The EMBO journal.

[22]  George B. Petersen,et al.  Messenger RNA recognition in Escherichia coli: a possible second site of interaction with 16S ribosomal RNA. , 1988, The EMBO journal.

[23]  S. Rangwala,et al.  A novel sequence element derived from bacteriophage T7 mRNA acts as an enhancer of translation of the lacZ gene in Escherichia coli. , 1989, The Journal of biological chemistry.

[24]  G. Kramer,et al.  Structure, Function, and Genetics of Ribosomes , 1986, Springer Series in Molecular Biology.

[25]  H. D. de Boer,et al.  Specialized ribosome system: preferential translation of a single mRNA species by a subpopulation of mutated ribosomes in Escherichia coli. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[26]  J. Steitz.  Polypeptide Chain Initiation: Nucleotide Sequences of the Three Ribosomal Binding Sites in Bacteriophage R17 RNA , 1969, Nature.

[27]  S. Adhya,et al.  Control of transcription termination. , 1978, Annual review of biochemistry.

[28]  C. Kurland,et al.  Codon usage determines translation rate in Escherichia coli. , 1989, Journal of molecular biology.

[29]  J. Richardson,et al.  Identification and characterization of transcription termination sites in the Escherichia coli lacZ gene. , 1989, Journal of molecular biology.

[30]  M. Ivey-Hoyle,et al.  Translation of phage f1 gene VII occurs from an inherently defective initiation site made functional by coupling. , 1989, Journal of molecular biology.

[31]  S. Horinouchi,et al.  Posttranscriptional modification of mRNA conformation: mechanism that regulates erythromycin-induced resistance. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[32]  C. Yanofsky,et al.  Translation activates the paused transcription complex and restores transcription of the trp operon leader region. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[33]  M. Santer,et al.  A single base change in the Shine-Dalgarno region of 16S rRNA of Escherichia coli affects translation of many proteins. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[34]  P. S. Lovett,et al.  Translational attenuation as the regulator of inducible cat genes , 1990, Journal of bacteriology.

[35]  L. Gold,et al.  Posttranscriptional regulatory mechanisms in Escherichia coli. , 1988, Annual review of biochemistry.

[36]  W. Fiers,et al.  Inefficient translation initiation causes premature transcription termination in the IacZ gene , 1986, Cell.

[37]  R. E. Wolf,et al.  Growth-rate-dependent regulation of 6-phosphogluconate dehydrogenase level mediated by an anti-Shine-Dalgarno sequence located within the Escherichia coli gnd structural gene. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[38]  F. Studier,et al.  Mutations of bacteriophage T7 that affect initiation of synthesis of the gene 0.3 protein. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[39]  H. Noller,et al.  Rapid chemical probing of conformation in 16 S ribosomal RNA and 30 S ribosomal subunits using primer extension. , 1986, Journal of molecular biology.

[40]  C. Gualerzi,et al.  Ribosomal affinity and translational initiation in Escherichia coli. In vitro investigations using translational initiation regions of differing efficiencies from the atp operon. , 1989, Journal of molecular biology.

[41]  W. Fiers,et al.  Secondary structure of mRNA and efficiency of translation initiation. , 1980, Gene.

[42]  D. Dubnau,et al.  Conformational alteration of mRNA structure and the posttranscriptional regulation of erythromycin-induced drug resistance. , 1980, Nucleic acids research.

[43]  J. Shine,et al.  The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[44]  T. D. Schneider,et al.  Characterization of Translational Initiation Sites in E. Coui , 1982 .

[45]  M. Bolotin-Fukuhara,et al.  Mutational alterations of translational coupling in the L11 ribosomal protein operon of Escherichia coli , 1987, Journal of bacteriology.