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Mechanism and Regulation of Translation Initiation in Prokaryotes*

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Post-transcriptional Control of Gene Expression

Part of the book series: NATO ASI Series ((ASIH,volume 97))

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Abstract

In this chapter we shall present a short summary of the most important concepts concerning the basic mechanism of translation initiation which are relevant for understanding the various types of regulation occurring at this particular stage of gene expression (for more extensive reviews see Gualerzi et al. 1990; Hartz et al. 1990; Gualerzi and Pon 1990; Gualerzi and Pon 1993). In addition, we shall try to summarize and/or update the information on regulation of translation initiation which has been presented in recent reviews (de Smit and van Duin 1990; Gold 1988; McCarthy and Gualerzi 1990).

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References

  • Afonina E, Chichkova N, Bogdanova S and Bogdanov A (1991) 3OS ribosomal subunits with fragmented 16S rRNA: a new approach for structure and function study of ribosomes. Biochimie 73:777–787.

    Article  PubMed  CAS  Google Scholar 

  • Altuvia S, Locker-Giladi H, Koby S, Ben-Nun O and Oppenheim AB (1987) RNase III stimulates the translation of the cIII gene of bacteriophage λ. Proc Natl Acad Sci USA 84:6511–6515.

    Article  PubMed  CAS  Google Scholar 

  • Andrake M, Guild N, Hsu T, Gold L, Tuerk C and Karam J (1988) DNA polymerase of bacteriophage T4 is an autogenous translational repressor. Proc Natl Acad Sci USA 85:7942–7946.

    Article  PubMed  CAS  Google Scholar 

  • Baumeister R, Flache P, Malefors O, Gabain Av and Hillen W (1991) Lack of a 5′ non coding region in Tnl721 encoded tetR mRNA is associated with a low efficiency of translation and short half-life in E. coli. Nucleic Acids Res 19:4595–4600.

    Article  PubMed  CAS  Google Scholar 

  • Beckett D and Uhlenbeck OC (1988) Ribonucleoprotein complexes of R17 coat protein and a translation operator analog. J Mol Biol 204:927–938.

    Article  PubMed  CAS  Google Scholar 

  • Bernardi A and Spahr PF (1972) Nucleotide sequence at the binding site for coat protein on RNA of bacteriophage R17. Proc Natl Acad Sci USA 69:3033–3037.

    Article  PubMed  CAS  Google Scholar 

  • Boni IV, Isaeva DM, Musychenko ML and Tzareva NV (1991) Ribosome messenger recognition. mRNA target sites for ribosomal protein SI. Nucleic Acids Res 19:155–162.

    Article  PubMed  CAS  Google Scholar 

  • Brombach M and Pon CL (1987) The unusual translation initiation codon AUU limits the expression of the infC (initiation factor IF3) gene of E. coli. Mol Gen Genet 208:94–100.

    Article  PubMed  CAS  Google Scholar 

  • Brunei C, Caillet J, Lasage P, Graffe M, Dondon J, Moine H, Romby P, Ehresmann C, Ehresmann B, Grunberg-Manago M and Springer M (1992) Domains of the E. Coli threonyl-tRNA synthetase translational operator and their relation to threonine tRNA isoacceptors. J Mol Biol 227:621–634.

    Google Scholar 

  • Butler JS, Springer M and Grunberg-Manago M (1987) AUU to AUG mutation in the initiator codon of the translation initiation factor IF3 abolishes translational autocontrol of its own gene infC in vivo. Proc Natl Acad Sci USA 84:4022–4025.

    Article  PubMed  CAS  Google Scholar 

  • Calogero RA, Pon CL, Canonaco MA and Gualerzi CO (1988) Selection of the mRNA translation initiation region by E. coli ribosomes. Proc Natl Acad Sci USA 85:6427–6431.

    Article  PubMed  CAS  Google Scholar 

  • Carter-Muenchau P and Wolf Jr RE (1989) Growth-dependent regulation of 6-phosphogluconate dehydrogenase level mediated by an anti-Shine-Dalgarno sequence located within the E. coli gnd structural gene. Proc Natl Acad Sci USA 86:1138–1142.

    Article  PubMed  CAS  Google Scholar 

  • Coleman J, Green PJ and Inouye M (1984) The use of RNA complementary to specific mRNAs to regulate the expression of individual bacterial genes. Cell 37:429–436.

    Article  PubMed  CAS  Google Scholar 

  • Costanzo MC and Fox TD (1988) Specific translational activation by nuclear gene products occurs in the 5′ untranslated leader of yeast mitochondrial mRNA. Proc Natl Acad Sci USA 85:2677–2681.

    Article  PubMed  CAS  Google Scholar 

  • Dempsey WB (1987) Transcript analysis of the plasmid R100 traJ and finP genes. Mol Gen Genet 209:533–544.

    Article  PubMed  CAS  Google Scholar 

  • de Smit M and van Duin J (1990) Control of prokaryotic translation initiation by mRNA secondary structure. Progr Nucl Acid Res Mol Biol 38:1–35.

    Article  Google Scholar 

  • Dunn JJ, Buzash-Pollert E and Studier FW (1978) Mutations of bacteriophage T7 that affect initiation of synthesis of the gene 0.3 protein. Proc Natl Acad Sci USA 75:2741–2745.

    Article  PubMed  CAS  Google Scholar 

  • Faxen M, Plumbridge J and Isaksson LA (1991) Codon choice and potential complementarity between mRNA downstream of the initiation codon and bases 1471–1480 in 16S rRNA affects expression of glnS. Nucleic Acids Res 19:5247–5251.

    Article  PubMed  CAS  Google Scholar 

  • Gerdes K, Helin K, Christensen OW and Loebner-Olesen A (1988) Translational control and differential RNA decay are key elements regulating postsegregational expression of the killer protein encoded by the parB locus of plasmid Rl. J Mol Biol 203:119–129.

    Article  PubMed  CAS  Google Scholar 

  • Gold L, Stormo G and Saunders R (1984) E. coli translational initiation factor 1F3: a unique case of translational regulation. Proc Natl Acad Sci USA 81:7061–7065.

    Article  PubMed  CAS  Google Scholar 

  • Gold L (1988) Posttranscriptional regulatory mechanism in Escherichia coli. Annu Rev Biochem 57:199–203.

    Article  PubMed  CAS  Google Scholar 

  • Gottesman M, Oppenheim A and Court D (1982) Retroregulation: control of gene expression from sites distal to the gene. Cell 29:727–728.

    Article  PubMed  CAS  Google Scholar 

  • Graffe M, Dondon J, Caillet J, Romby P, Ehresmann C, Ehresmann B and Springer M (1992) The specificity of translational control switched with transfer RNA identity rules. Science 255:994–999.

    Article  PubMed  CAS  Google Scholar 

  • Gualerzi CO, La Teana A, Spurio R, Canonaco MA, Severini M and Pon CL (1990) Initiation of protein biosynthesis in prokaryotes: recognition of mRNAs by ribosomes and molecular basis for the function of the initiation factors. In: Hill WE, Dahlberg A, Garrett RA, Moore PB, Schlessinger D and Warner JR (eds) The ribosome. Structure, function and evolution. Am Soc Microbiol, Washington D.C. pp 281–291.

    Google Scholar 

  • Gualerzi CO and Pon CL (1990) Initiation of mRNA translation in prokaryotes. Biochemistry 29:5881–5889.

    Article  PubMed  CAS  Google Scholar 

  • Gualerzi CO and Pon CL (1993) mRNA-ribosome interaction during initiation of protein synthesis. In: Zimmermann RA and Dahlberg AE (eds) Ribosomal RNA. CRC Press, Ine, in press.

    Google Scholar 

  • Hartz D, McPheeters DS, Traut R and Gold L (1988) Extension inhibition analysis of translation initiation complexes. Meth Enzymol 164:419–425.

    Article  PubMed  CAS  Google Scholar 

  • Hartz D, McPheeters DS and Gold L (1989) Selection of the initiator tRNA by E. coli initiation factors. Genes Dev 3:1899–1912.

    Article  PubMed  CAS  Google Scholar 

  • Hartz D, McPheeters DS and Gold L (1990) From polynucleotide to natural mRNA translation initiation: function of E. coli initiation factors. In: Hill WE, Dahlberg A, Garrett RA, Moore PB, Schlessinger D and Warner JR (eds) The ribosome. Structure, function and evolution. Am Soc Microbiol, Washington DC. pp 275–280.

    Google Scholar 

  • Hartz D, McPheeters DS and Gold L (1991) Influence of mRNA determinants on translation initiation in E. coli. J Mol Biol 218:83–97.

    Article  PubMed  CAS  Google Scholar 

  • Hattman S, Newman L, Murthy HMK and Nagaraja V (1991) Com, the phage Mu mom translational activator, is a zinc-binding protein that binds specifically to its cognate mRNA. Proc Natl Acad Sci USA 88:10027–10031.

    Article  PubMed  CAS  Google Scholar 

  • Hirashima A, Sawaki S, Inokuchi Y and Inouye M (1986) Engineering of the mRNA-interfering complementary RNA immune system against viral infection. Proc Nat Acad Sci USA83:7726–7730.

    Google Scholar 

  • Hui A and de Boer HA (1987) Specialized ribosome system: preferential translation of a single mRNA species by a subpopulation of mutated ribosomes in E. coli. Proc Natl Acad Sci USA 84:4762–4766.

    Article  PubMed  CAS  Google Scholar 

  • Ito K, Kawakami K and Nakamura Y (1993) Multiple control of E. coli lysyl-tRNA synthetase expression involves a transcriptional repressor and a translational enhancer element. Proc Natl Acad Sci USA 90:302–306.

    Article  PubMed  CAS  Google Scholar 

  • Jacob WF, Sanier M and Dahlberg AE (1987) A single base change in the Shine-Dalgarno region of 16S rRNA of E. coli affects translation of many proteins. Proc Natl Acad Sci USA 84:4757–4761.

    Article  PubMed  CAS  Google Scholar 

  • Jones RL, Jaskula JC and Janssen GR (1992) In vivo translational start site selection by prokaryotic ribosomes in the absence of a Shine-Dalgarno interaction. J Bacteriol 174:475–34760.

    Google Scholar 

  • Jinks-Robertson S and Nomura M (1987) Ribosomes and tRNA. In Neidhardt FC, Ingraham JL, Brooks Low K, Magasanik B, Schaechter M and Umbarger HE (Eds) Escherichia coli and Salmonella typhimurium. Cellular and molecular biology. Am Soc Microbiol, Washington, DC pp 1358–1385.

    Google Scholar 

  • Kamath-Loeb AS and Gross CA (1991) Translational regulation of σ32 synthesis: requirement for an internal control element. J Bacteriol 173:3904–3906.

    PubMed  CAS  Google Scholar 

  • Krinke L and Wulff DL (1987) OOP RNA, produced from multicopy plasmids, inhibits ell gene expression through an RNase Ill-dependent mechanism. Genes Dev 1:1005–1013.

    Article  PubMed  CAS  Google Scholar 

  • Kuriki Y (1990) A nucleotide sequence in the translation start signal region is involved in heat shock-induced translation arrest in E. coli. FEBS Lett 264:121–124.

    Article  PubMed  CAS  Google Scholar 

  • La Teana A, Pon CL and Gualerzi CO (1993) Translation of mRNAs with degenerate initiation triplet AUU displays high IF2 dependence and is subject to IF3 repression. Proc Natl Acad Sci USA in press.

    Google Scholar 

  • Liao SM, Wu T, Chiang CH, Susskind MM and McClure WR (1987) Control of gene expression in bacteriophage P22 by a small antisense RNA. I. Characterization in vitro of the Psar promoter and the sar RNA transcript. Genes Dev 1:197–203.

    CAS  Google Scholar 

  • Lindahl L and Zengel JM (1986) Ribosomal genes in E. coli. Annu Rev Genet 20:297–326.

    Article  PubMed  CAS  Google Scholar 

  • Mahajna J, Oppenheim AB, Rattray A and Gottesman M (1986) Translation initiation of bacteriophage λ ell requires integration host factor. J Bacteriol 165:167–174.

    PubMed  CAS  Google Scholar 

  • McCarthy JEG and Gualerzi CO (1990) Translational control of prokaryotic gene expression. Trends Genet 6:78–85.

    Article  PubMed  CAS  Google Scholar 

  • McPheeters DS, Stormo GD and Gold L (1988) Autogenous regulatory site on the bacteriophage T4 gene 32 mRNA J Mol Biol 201:517–535.

    Google Scholar 

  • McMullin TW, Hafïter P and Fox TD (1990) A novel small-subunit ribosomal protein of yeast mitochondria that interacts functionally with an mRNA-specific translation activator. Mol Cell Biol 10:4590–4595.

    PubMed  CAS  Google Scholar 

  • MelanÏ‚on P, Ledere D and Brakier-Gingras L (1990a) A deletion mutant at the 5′ end of E. coli 16S rRNA. Biochim Biophys Acta 1050:98–103.

    Google Scholar 

  • MelanÏ‚on P, Ledere D, Destroismaisons N and Brakier-Gingras L (1990b) The anti-Shine-Dalgarno region in E. coli 16S rRNA is not essential for the correct selection of translational starts. Biochemistry 29:3402–3407.

    Article  Google Scholar 

  • Mizuno T, Chou MY and Inouye M (1984) A unique mechanism regulating gene expression: Translational inhibition by a complementary RNA transcript (micRNA). Proc Natl Acad Sci USA 81:1966–1970.

    Article  PubMed  CAS  Google Scholar 

  • Nagai H, Yuzawa H and Yura T (1991) Interplay of two cis-acting mRNA regions in translational control of σ32 synthesis during the heat-shock response of E. coli. Proc Natl Acad Sci USA 88:10515–10519.

    Article  PubMed  CAS  Google Scholar 

  • Ohsawa H, Herrlich P and Gualerzi CO (1984) In vitro template activity of 0.3 mRNA from wild type and initiation mutants of bacteriophage T7. Mol Gen Genet 196:53–58.

    Article  PubMed  CAS  Google Scholar 

  • Petersen GB, Stockwell PA and Hill DF (1988) Messenger RNA recognition in E. coli, a possible second site of interaction with 16S rRNA. EMBO J 7:3957–3962.

    PubMed  CAS  Google Scholar 

  • Philippe C, Portier C, Mougel M, Grunberg-Manago M, Ebel JP, Ehresmann B and Ehresmann C (1990) Target site of E. coli ribosomal protein SI5 on its mRNA. Conformation and interaction with the protein. J Mol Biol 211:415–426.

    Article  PubMed  CAS  Google Scholar 

  • Philippe C, Eyermann F, Bernard L, Portier C, Ehresmann B and Ehresmann C (1993) Ribosomal protein S15 from E. coli modulates its own translation by trapping the ribosome on the mRNA initiation loading site. Proc Natl Acad Sci USA in press.

    Google Scholar 

  • Ringquist S, Shinedling S, Barrick D, Green L, Binkley J, Stormo GD and Gold L (1992) Translation initiation in E. coli: sequences within the ribosome-binding site. Mol Microbiol 6:1219–1229.

    Article  PubMed  CAS  Google Scholar 

  • Romby P, Brunei C, Caillet J, Springer M, Grunberg-Manago M, Westhof E, Ehresmann C and Ehresmann B (1992) Molecular mimicry in translational control of E. coli threonyl-tRNA synthetase gene. Competitive inhibition in tRNA aminoacylation and operator repressor recognition switch using tRNA identity rules. Nucleic Acids Res 20:5633–5640.

    Article  PubMed  CAS  Google Scholar 

  • Rudd KE and Schneider TD, (1992) Compilation of E. coli ribosome binding sites. In: Miller JH (ed) A short course in bacterial genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York pp 17.19–17.45.

    Google Scholar 

  • Scherer GF, Walkinshaw MD, Arnott S and Morre DJ (1980) The ribosome binding sites recognized by E. coli ribosomes have regions with signal character in both the leader and protein coding segments. Nucleic Acids Res 8:3895–3907.

    Article  PubMed  CAS  Google Scholar 

  • Schneider TD and Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18:6097–6100.

    Article  PubMed  CAS  Google Scholar 

  • Schneider TD, Stormo GD, Gold L and Ehrenfeucht A (1986) Information content of binding sites on nucleotide sequences. J Mol Biol 188:415–431.

    Article  PubMed  CAS  Google Scholar 

  • Simons RW and Kleckner N (1983) Translational control of IS10 transposition. Cell 34:683–691.

    Article  PubMed  CAS  Google Scholar 

  • Spedding G, Gluick TC and Draper DE (1993) Ribosome initiation complex formation with the pseudoknotted a operon mRNA. J Mol Biol 229:609–622.

    Article  PubMed  CAS  Google Scholar 

  • Sprengart ML, Fatscher HP and Fuchs E (1990) The initiation of translation in E. Coli apparent base pairing between the 16S rRNA and downstream sequences of the mRNA. Nucleic Acids Res 18:1719–1723.

    Article  PubMed  CAS  Google Scholar 

  • Sussman JK and Simons RW (1993) Escherichia coli translation initiation factor 3 discriminates the initiation codon in vivo. Submitted for publication.

    Google Scholar 

  • Takayama KM, Houba-Herin N and Inouye M (1987) Overproduction of an antisense RNA containing the oop RNA sequence of bacteriophage induces clear plaque formation. Mol Gen Genet 210:184–186.

    Article  PubMed  CAS  Google Scholar 

  • Tang CK and Draper DE (1989) Unusual mRNA pseudoknot structure is recognized by a protein translational repressor. Cell 57:531–536.

    Article  PubMed  CAS  Google Scholar 

  • Tang CK and Draper DE (1990) Evidence for allosteric coupling between the ribosome and repressor binding sites of a translationally regulated mRNA. Biochemistry 29:4434–4439.

    Article  PubMed  CAS  Google Scholar 

  • Vellanoweth RL and Rabinowitz JC (1992) The influence of ribosome binding-site elements on translational efficiency in B. subtilis and E. coli in vivo. Mol Microbiol 6:1105–1114.

    Article  PubMed  CAS  Google Scholar 

  • Winter RB, Morrissey L, Gauss P, Gold L, Hsu T and Karam J (1987) Bacteriophage T4 regA protein binds to mRNAs and prevents translation initiation. Proc Natl Acad Sci USA 84:7822–7826.

    Article  PubMed  CAS  Google Scholar 

  • Wulczyn FG, Boelker M and Kahmann R (1989) Translation of the bacteriophage Mu mom gene is positively regulated by the phage com gene product. Cell 57:1201–1210.

    Article  PubMed  CAS  Google Scholar 

  • Wu T, Liao SM, McClure WR and Susskind MM (1987) Control of gene expression in bacteriophage P22 by a small antisense RNA. II. Characterization of mutants defective in repression. Genes Dev 1:204–212.

    CAS  Google Scholar 

  • Wulczyn FG and Kahmann R (1991) Translational stimulation: RNA sequence and structure requirements for binding of com protein. Cell 65:259–269.

    Article  PubMed  CAS  Google Scholar 

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Pon, C.L., Gualerzi, C.O. (1996). Mechanism and Regulation of Translation Initiation in Prokaryotes*. In: Resnekov, O., von Gabain, A. (eds) Post-transcriptional Control of Gene Expression. NATO ASI Series, vol 97. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-60929-9_5

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  • DOI: https://doi.org/10.1007/978-3-642-60929-9_5

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