A long-range RNA-RNA interaction forms a pseudoknot required for translational control of the IF3-L35-L20 ribosomal protein operon in Escherichia coli

EMBO Journal

Volumn 15, Issue 16, 1996, Pages 4402-4413

  Chiaruttini, C ^a   Milet, M ^a   Springer, M ^a  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

Feedback regulation; Ribosomes; Tertiary RNA interaction; Translation

Indexed keywords

BACTERIAL RNA; INITIATION FACTOR; RIBOSOME PROTEIN;

ARTICLE; ESCHERICHIA COLI; GENE MUTATION; MOLECULAR INTERACTION; NONHUMAN; OPERON; PRIORITY JOURNAL; RNA STRUCTURE; TRANSLATION REGULATION;

EID: 0029757619     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00813.x     Document Type: Article

References (48)

1. Brunel, C. et al. (1992) The domains of the E.coli threonyl-tRNA synthetase translational operator and their relation to threonine tRNA isoacceptors. J. Mol. Biol., 227, 621-634.
2. Burke, J.M. Belfort, M., Cech, T.R., Davies, R.W., Schweyen, R.J., Shub, D.A., Szostak, J.W. and Tabak, H.F. (1987) Structural conventions for group I introns. Nucleic Acids Res., 15, 7217-7221.
3. Butler, J.S., Springer, M., Dondon, J., Graffe, M. and Grunberg-Manago, M. (1986) Escherichia coli protein synthesis initiation factor IF3 controls its own gene expression at the translational level in vivo. J. Mol. Biol., 192, 767-780.
4. 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 translational autocontrol of its own gene (infC) in vivo. Proc. Natl Acad. Sci. USA, 84, 4022-4025.
5. Christensen, T., Johnsen, M., Fiil, N.P. and Friesen, J.D. (1984) RNA secondary structure and translation inhibition: analysis of mutants in the rplJ leader. EMBO J., 3, 1609-1612.
6. Coetzee, T., Herschlag, D. and Belfort, M. (1994) Escherichia coli proteins, including ribosomal protein S12, facilitate in vitro splicing of phage T4 introns by acting as RNA chaperones. Genes Dev., 8, 1575-1588.
7. Das, A. (1993) Control of transcription termination by RNA-binding proteins. Annu. Rev. Biochem., 62, 893-930.
8. Davis, R.W., Botstein, D. and Roth, J.R. (1980) Advanced Bacterial Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
9. Freier, S.M., Kierzeck, R., Jaeger, J.A., Sugimoto, N., Caruthers, M.H., Neilson, T. and Turner, D.H. (1986) Improved free-energy parameters for RNA duplex stability. Proc. Natl Acad. Sci. USA, 83, 9373-9377.
10. Friesen, J.D., Tropak, M. and An, G. (1983) Mutations in the rplJ leader of Escherichia coli that abolish feedback regulation. Cell, 32, 361-369.
11. Gallinaro, H., Domenjoud, L. and Jacob, M. (1994) Structural study of the 5′ end of a synthetic premessenger RNA from adenovirus. J. Mol. Biol., 240, 205-225.
12. Gutell, R.R. (1993) Comparative studies of RNA: inferring higher-order structure from patterns of sequence variation. Curr. Opin. Struct. Biol., 3, 313-322.
13. Haas, E., Morse, S.D.P., Brown, J.W., Schmidt, F.J. and Pace, N.R. (1991) Long-range structure in ribonuclease P RNA. Science, 254, 853-856.
14. Hartz, D., McPheeters, D.S. and Gold, L. (1989) Selection of the initiator tRNA by E.coli initiation factors. Genes Dev., 3, 1899-1912.
15. Inoue, T. and Cech, T.R. (1985) Secondary structure of the circular form of the Tetrahymena rRNA intervening sequence: a technique for RNA structure analysis using chemical probes and reverse transcriptase. Proc. Natl Acad. Sci. USA, 82, 648-652.
16. Jack, A., Ladner, J.E. and Klug, A. (1976) Crystallographic refinement of yeast phenylalanine transfer RNA at 2.5 Å resolution. J. Mol. Biol., 108, 619-649.
17. Jacquier, A. and Michel, F. (1987) Multiple exon-binding sites in class II self-splicing introns. Cell, 50, 17-29.
18. Kunkel, T.A., Roberts, J.D. and Zakour, R.A. (1987) Methods Enzymol., 154, 367-382.
19. Landick, R. and Yanofsky, C. (1987) Transcription attenuation. In Ingraham, J.L., Low, K.B., Magasanik, B., Schaechter, M., Umbarger, H.E. and Neidhardt, F.C. (eds), Escherichia coli and Salmonella lyphimurium. Cellular and Molecular Biology. American Society for Microbiology, Washington DC, Vol. 2, pp. 1276-1301.
20. Lesage, P. (1991) Regulation de l'Expression Génétique au Niveau de la Traduction dans l'Opéron infC-rpml-rplT chez E.coli. Université de Paris XI.
21. Lesage, P., Truong, H.N., Graffe, M., Dondon, J. and Springer, M. (1990) Translated translational operator in Escherichia coli: autoregulation in the infC-rpml-rplT operon. J. Mol. Biol., 213, 465-475.
22. Lesage, P., Chiaruttini, C., Dondon, J., Graffe, M., Milet, M. and Springer, M. (1992) Messenger RNA secondary structure and translational coupling in the E.coli operon encoding translation initiation factor IF3 and the ribosomal proteins, L35 and L20. J Mol. Biol., 228, 366-386.
23. Michel, F. and Westhof, E. (1990) Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J. Mol. Biol., 216, 585-610.
24. Miller, E.S., Karam, J.D. and Spicer, E. (1994) Control of translation initiation: mRNA structure and protein repressors. In Karam, J.D. (ed.), The Molecular Biology of Bacteriophage T4. American Society for Microbiology. Washington DC, pp. 193-205.
25. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
26. Moazed, D., Stern, S. and Noller, H.F. (1986) Rapid chemical probing of conformation in 16S ribosomal RNA and 30S ribosomal subunits using primer extension. J. Mol. Biol., 187, 399-416.
27. Thr modulate the binding of the ribosome to the translation initiation site of the thrS mRNA. J. Mol. Biol., 216, 299-310.
28. Peattie, D.A. (1979) Direct chemical method for sequencing RNA. Proc. Natl Acad. Sci. USA, 76, 1760-1764.
29. Philippe, C., Portier, C., Mougel, M., Grunberg-Manago, M., Ebel, J.P. Ehresmann, B. and Ehresmann, C. (1990) Target site of E.coli ribosomal protein S15 on its mRNA. Conformation and interaction with the protein. J. Mol. Biol. 211, 415-426.
30. Philippe, C., Eyermann, F., Bénard, 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. Prroc. Natl Acad. Sci. USA, 90, 4394-4398.
31. Pleij, C.W.A. and Bosch, L. (1989) Methods Enzymol., 180, 289-303.
32. Pleij, C.W.A., Rietweld, K. and Bosch, L. (1985) A new principle of RNA folding based on pseudoknotting. Nucleic Acids Res., 13, 1717-1731.
33. Quigley, G.J., Wang, A.H.J., Seeman, N.C., Suddath, F.L., Rich, A., Sussman, J.L. and Kim, S.H. (1975) Hydrogen bonding in yeast phenylalanine transfer RNA. Proc. Natl Acad. Sci. USA, 72, 4866-4870.
34. Sacerdot, C., Chiaruttini, C., Engst, K., Graffe, M., Milet, M., Mathy, N., Dondon, J. and Springer, M. (1996) The role of the AUU initiation codon in the negative feedback regulation of the gene for translation initiation factor IF3 in E.coli. Mol. Microbiol., in press.
35. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Sanger, F., Nicklen, S. and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA, 74, 5463-5467.
37. Spedding, G., Gluick, T.C. and Draper, D. (1993) Ribosome initiation complex formation with the pseudoknotted α operon mRNA. J. Mol. Biol., 229, 609-622.
38. Springer, M. (1996) Translational control of gene expression in E.coli and bacteriophage. In Lin, E.C.C. and Simon Lynch, A. (eds). Regulation of Gene Expression in E.coli and Bacteriophage, R.G. Landes Company, Austin, TX, pp. 85-126.
39. Springer, M. et al. (1985) Autogenous control of Escherichia coli threonyl-tRNA synthetase expression in vivo. J. Mol. Biol., 185, 93-104.
40. Springer, M., Graffe, M., Butler, J.S. and Grunberg-Manago, M. (1986) Genetic definition of the translational operator of the threonine tRNA ligase gene in Escherichia coli. Proc. Natl Acad. Sci. USA, 83, 4384-4388.
41. Tang, C.K. and Draper, D.E. (1989) Unusual mRNA pseudoknot structure is recognized by a translational repressor. Cell, 57, 531-536.
42. van Himbergen, J., van Geffen, B. and van Duin, J. (1993) Translational control by a long range RNA-RNA interaction: a basepair substitution analysis. Nucleic Acids Res., 21, 1713-1717.
43. Wertheimer, S.J., Klotsky, R.-A. and Schwartz, I. (1988) Transcriptional patterns for the thrS-infC-rplT operon of Escherichia coli. Gene, 63, 309-320.
44. Westhof, E., Dumas, P. and Moras, D. (1985) Cristallographic refinement of yeast aspartic acid transfer RNA. J. Mol. Biol., 184, 119-145.
45. Winter, R.B., Morrissey, L., Gauss, P., Gold, L., Hsu, T. and Karam, J. (1987) Bacteriophage T4 regA proteins binds to mRNAs and prevents translation initiation. Proc. Natl Acad. Sci. USA, 84, 7822-7826.
46. Witherell, G.W., Gott, J.M. and Uhlenbeck, O.C. (1991) Specific interaction between RNA phage coat proteins and RNA. Prog. Nucleic Acid Res. Mol. Biol., 40, 185-220.
47. Zengel, J.M. and Lindahl, L. (1994) Diverse mechanisms for regulating ribosomal protein synthesis in E.coli. Prog. Nucleic Acid Res. Mol. Biol., 47, 331-369.
48. Zuker, M. (1989) On finding all suboptimal foldings of an RNA molecule. Science, 244, 48-52.