Translation initiation factor 3 antagonizes authentic start codon selection on leaderless mRNAs

Molecular Microbiology

Volumn 31, Issue 1, 1999, Pages 67-77

  Tedin, Karsten ^a   Moll, Isabella ^a   Grill, Sonja ^a   Resch, Armin ^a   Graschopf, Anton ^a   Gualerzi, Claudio O ^b   Bläsi, Udo ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF CAMERINO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR; MESSENGER RNA;

ARTICLE; ASSAY; BACTERIOPHAGE LAMBDA; BACTERIUM MUTANT; COMPLEX FORMATION; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; RIBOSOME; START CODON; TRANSLATION INITIATION;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; CODON, INITIATOR; DNA-BINDING PROTEINS; EUKARYOTIC INITIATION FACTOR-3; GENES, REPORTER; LAC OPERON; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PEPTIDE INITIATION FACTORS; PROTEIN BIOSYNTHESIS; REPRESSOR PROTEINS; RIBOSOMES; RNA, MESSENGER; VIRAL PROTEINS;

EID: 0032896616     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01147.x     Document Type: Article

References (46)

1. Balakin, A.G., Skripkin, E.A., Shatsky, I.N., and Bogdanov, A.A. (1992) Unusual ribosome binding properties of mRNA encoding bacteriophage λ repressor. Nucleic Acids Res 20: 563-571.
2. Baumeister, R., Flache, P., Melefors, Ö., von Gabain, A., and Hillen, W. (1991) Lack of a 5′ non-coding region inTn1721 encoded tetR mRNA is associated with a low efficiency of translation and a short half-life in Escherichia coli. Nucleic Acids Res 19: 4595-4600.
3. Boni, I.V., Isaeva, D.M., Musychenko, M.L., and Tzareva, N.V. (1991) Ribosome-messenger recognition: mRNA target sites for ribosomal protein S1. Nucleic Acids Res 19: 155-162.
4. Brombach, M., and Pon, C.L. (1987) The unusual translation initiation codon AUU limits the expression of the infC (initiation factor IF3) gene of Escherichia coli. Mol Gen Genet 208: 94-100.
5. Butler, J.S., Springer, M., and Grunberg-Manago, M. (1987) AUU-to-AUG mutation in the initiator codon of the translation initiation factor IF3 abolishes translation autocontrol of its own gene (infC) in vivo. Proc Natl Acad Sci USA 84: 4022-4025.
6. Calogero, R.A., Pon, C.L., Canonaco, M.A., and Gualerzi, C.O. (1988) Selection of the mRNA translation initiation region by Escherichia coli ribosomes. Proc Natl Acad Sci USA 85: 6427-6431.
7. Canonaco, M.A., Pon, C.L., Pawlik, R.T., Calogero, R., and Guaierzi, C.O. (1987) Relationship between size of mRNA ribosomal binding site and initiation factor function. Biochemie 69: 963-967.
8. Draper, D.E., and van Hippel, P.H. (1978) Nucleic acid binding properties of Escherichia coli ribosomal protein S1. I. Structure and interactions of binding site I. J Mol Biol 122: 321-338.
9. Dreyfus, M. (1988) What constitutes the signal for the initiation of protein synthesis on Escherichia coli mRNAs? J Mol Biol 204: 79-94.
10. Ehresmann, C., Moine, H., Mougel, M., Dondon, J., Grunberg-Manago, M., Ebel, J.-P., et al. (1986) Cross-linking of initiation factor IF3 to Escherichia coli 30S ribosomal subunit by trans-diaminodichloroplatinum (II): characterization of two cross-linking sites in 16S rRNA: a possible way of functioning for IF3. Nucleic Acids Res 14: 4803-4821.
11. Gold, L. (1988) Posttranscriptional regulatory mechanisms in Escherichia coli. Annu Rev Biochem 57: 199-233.
12. Gualerzi, C.O., and Pon, C.L. (1990) Initiation of mRNA translation in prokaryotes. Biochemistry 29: 5881-5889.
13. Haggerty, T.J., and Lovett, S.T. (1997) IF3-mediated suppression of a GUA initiation codon mutation in the recJ gene of Escherichia coli. J Bacteriol 179: 6705-6713.
14. Hartz, D., McPheeters, D.S., Traut, R., and Gold, L. (1988) Extension inhibition analysis of translation initiation complexes. Methods Enzymol 164: 419-425.
15. Hartz, D., McPheeters, D.S., and Gold, L. (1991a) Influence of mRNA determinants on translation initiation in Escherichia coli. J Mol Biol 218: 83-97.
16. Hartz, D., McPheeters, D.S., Green, L., and Gold, L. (1991b) Detection of Escherichia coli ribosome binding at translation initiation sites in the absence of tRNA. J Mol Biol 218: 99-105.
17. Hüttenhofer, A., and Noller, H.F. (1994) Footprinting mRNA-ribosome complexes with chemical probes. EMBO J 13: 3892-3901.
18. Janssen, G.R. (1993) Eubacterial, archaebacterial, and eukaryotic genes that encode leaderless mRNA. In Industrial Microorganisms: Basic and Applied Molecular Genetics. Baltz, R.H., Hegeman, G.D., and Skatrud, P.L. (eds). Washington, DC: American Society for Microbiology Press, pp. 59-67.
19. Jobling, M.G., and Holmes, R.K. (1990) Construction of vectors with the p15a replicon, kanamycin resistance, inducible lacZa and pUC18 and pUC19 multiple cloning sites. Nucleic Acids Res 18: 5315.
20. Jones, III, R.L., Jaskula, C.J., and Janssen, G.R. (1992) In vivo translational start site selection on leaderless mRNA transcribed from the Streptomyces fradiae aph gene. J Bacteriol 174: 4753-4760.
21. Klock, G., and Hillen, W. (1986) Expression, purification, and operator binding of the transposon Tn 1721-encoded Tet repressor. J Mol Biol 189: 633-641.
22. Kourilsky, P. (1973) Lysogenization by bacteriophage λ. I. Multiple infection and the lysogenic response. Mol Gen Genet 122: 183-195.
23. Laemmli, U.K. (1970) Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
24. Liveris, D., Klotsky, R., and Schwartz, I. (1991) Growth rate regulation of translation initiation factor IF3 biosynthesis in Escherichia coli. J Bacteriol 173: 3888-3893.
25. Lundberg, U., von Gabain, A., and Melefors, Ö. (1990) Cleavages in the 5′ region of the ompA and bla mRNA control stability: studies with an E. coli mutant altering mRNA stability and a novel endoribonuclease. EMBO J 9: 2731-2741.
26. Melancon, P., Leclerc, D., Destroismaisons, N., and Brakier-Gingras, L. (1990) The anti-Shine-Dalgarno region in Escherichia coli 16S ribosomal RNA is not essential for the correct selection of translational starts. Biochemistry 29: 3402-3407.
27. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
28. Moazed, D., Samaha, R.R., Gualerzi, C.O., and Noller, H.F. (1995) Specific protection of 16S rRNA by translational initiation factors. J Mol Biol 248: 207-210.
29. Prescot, C.D., and Dahlberg, A.E. (1990) A single base change at 726 in 16S rRNA radically alters the pattern of protein synthesis in vivo. EMBO J 9: 289-294.
30. Resch, A., Tedin, K., Graschopf, A., Haggård-Ljungquist, E., and Bläsi, U. (1995) Ternary complex formation on leaderless phage mRNA. FEMS Microbiol Rev 17: 151-157.
31. Resch, A., Tedin, K., Gründling, A., Mündlein, A., and Bläsi, U. (1996) Downstream/anti-downstream box interactions are dispensable for translation initiation of leaderless mRNAs. EMBO J 15: 4740-4748.
32. Ruscetti, W.F., and Jacobson, A.L. (1972) Accumulation of 70S monosomes in Escherichia coli after energy source shift down. J Bacteriol 111: 142-151.
33. Santer, M., Bennett-Guerrero, E., Bzahatti, S., Czarnecki, S., O'Connell, D., Meyer, M., et al. (1990) Base changes at position 792 of Escherichia coli 16S rRNA affect assembly of 70S ribosomes. Proc Natl Acad Sci USA 87: 3700-3704.
34. Schmidt, B.F., Berkhout, B., Overbeek, G.P., van Strien, A., and van Duin, J. (1987) Determination of the RNA secondary structure that regulates lysis gene expression in bacteriophage MS2. J Mol Biol 195: 505-516.
35. Shean, C.S., and Gottesman, M.E. (1992) Translation of prophage λ cl transcript. Cell 70: 513-522.
36. Soffientini, A., Lorenzetti, R., Gastaldo, L., Parlett, J.H., Spurio, R., La-Teana, A., et al. (1994) Purification procedure for bacteria translational initiation factors IF2 and IF3. Protein Expr Purif 5: 118-124.
37. Spedding, G. (1990) Isolation and analysis of ribosomes from prokaryotes, eukaryotes and organelles. In Ribosomes and Protein Synthesis. A Practical Approach. Spedding, G. (ed.). New York: IRL Press, Oxford University Press, pp. 1-29.
38. Sprengart, M.L., Fuchs, E., and Porter, A.G. (1996) The downstream box: an efficient and independent translation initiation signal in Escherichia coli. EMBO J 15: 665-674.
39. Steiner, M., Lubitz, W., and Bläsi, U. (1993) The missing link in phage lysis of Gram-positive bacteria: gene 14 of B. subtilis phage φ29 encodes the functional homolog of λ S protein. J Bacteriol 175: 1038-1042.
40. Subramanian, A.R. (1969) The ribosome dissociation factor and the ribosome-polysome cycle. Cold Spring Harbor Symp Quant Biol 34: 223-230.
41. Sussman, J.K., Simons, E.L., and Simons, R.W. (1996) Escherichia coli translation initiation factor 3 discriminates the initiation codon in vivo. Mol Microbiol 21: 347-360.
42. Tapprich, W.E., Gross, D.J., and Dahlberg, A.E. (1989) Mutation at position 791 in Escherichia coli 16S ribosomal RNA affects processes involved in the initiation of protein synthesis. Proc Natl Acad Sci USA 86: 4927-4931.
43. Tedin, K., Resch, A., and Bläsi, U. (1997) Requirements for ribosomal protein S1 for translation initiation of mRNAs with and without a 5′ leader sequence. Mol Microbiol 25: 189-199.
44. Van Etten, W.J., and Janssen, G.R. (1998) An AUG initiation codon, not codon-anticodon complementarity, is required for the translation of unleadered mRNA in Escherichia coli. Mol Microbiol 27: 987-1001.
45. Wu, X., Iyengar, P., and RajBhandary, U. (1996) Ribosome-initiator tRNA complex as an intermediate in translation initiation in Escherichia coli revealed by use of mutant initiator tRNAs and specialized ribosomes. EMBO J 15: 4734-4739.
46. Wu, C.J., and Janssen, G.R. (1996) Translation of vph mRNA in Streptomyces lividans and Escherichia coli after removal of the 5′ untranslated leader. Mol Microbiol 22: 339-355.