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. 2002 Feb 25;78(7):568–576. doi: 10.1016/S0300-9084(96)80003-4

Pseudoknot and translational control in the expression of the S15 ribosomal protein

L Bénard a, C Philippe b, B Ehresmann b, C Ehresmann b, C Portier a,
PMCID: PMC7131963  PMID: 8955900

Abstract

Translational autocontrol of the expression of the ribosomal protein S15 proceeds through the transitory formation of a pseudoknot. A synopsis of the known data is used to propose a molecular model of the mechanism involved and for the role of the pseudoknot. This latter structure is able to recruit 30S ribosomal subunits to initiate translation, but also to bind S15 and to stop translation by trapping the ribosome on its loading site. Information on the S15 protein recognition of the messenger RNA site was deduced from mutational analyses and chemical probinb. A comparison of this messenger site with the S15 ribosomal binding site was conducted by analysing hydroxyl radical footprintings of these two sites. The existence of two subsites in 16S RNA suggests that the ribosomal protein S15 might present either two different binding sites or at least one common subsite. Clues for the presence of a common site between the messenger and 16S RNA are given which cannot rule out that recognition specificity is linked to a few other determinants. Whether these determinants are different or not remains an open question.

Keywords: S15 / pseudoknot / autocontrol / RNA binding / translation initiation

Abbreviations: CMCT, 1-cyclohexyl-3-(2-morpholinoethyl)carbodiimide metho-p-toluene sulfonate; DEPC, diethylpyrocarbonate; DMS, dimethylsulfate; ENU, ethylnitrosourea

References

  • 1.Ten Dam EB, Verlaan PWG, Pleij CWA. Analysis of the role of the pseudoknot component in the SRV-1 gag-pro ribosomal frameshift signal: loop lengths and stability of the stem regions. RNA. 1995;1:146–154. [PMC free article] [PubMed] [Google Scholar]
  • 2.Wills NM, Gesteland RF, Atkins JF. Pseudoknot-dependent read-through of retroviral gag termination codons: importance of sequences in the spacer and loop 2. EMBO J. 1994;13:4137–4144. doi: 10.1002/j.1460-2075.1994.tb06731.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Brierley I, Rolley NJ, Jenner AJ, Inglis SC. Mutational analysis of the RNA pseudoknot component of a coronavirus ribosomal frameshifting signal. J Mol Biol. 1991;220:889–902. doi: 10.1016/0022-2836(91)90361-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Wyatt JR, Puglisi JD, Tinoco IJ. RNA pseudoknots. Stability and loop size requirements. J Mol Biol. 1990;214:455–470. doi: 10.1016/0022-2836(90)90193-P. [DOI] [PubMed] [Google Scholar]
  • 5.Puglisi JD, Wyatt JR, Tinoco I. Conformation of an RNA pseudoknot. J Mol Biol. 1990;214:437–453. doi: 10.1016/0022-2836(90)90192-O. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Shen LX, Tinoco IJ. The structure of an RNA pseudoknot that causes efficient frameshifting in mouse mammary tumor virus. J Mol Biol. 1995;247:963–978. doi: 10.1006/jmbi.1995.0193. [DOI] [PubMed] [Google Scholar]
  • 7.Sanson B, Uzan M. Post transcriptional controls in bacteriophage T4: roles of the sequence-specific endoribonuclease regB. FEMS Microbiol Rev. 1995;17:141–150. doi: 10.1111/j.1574-6976.1995.tb00196.x. [DOI] [PubMed] [Google Scholar]
  • 8.Asano K, Kato A, Moriwaki H, Hama C, Shiba K, Mizobuchi K. Positive and negative regulations of plasmid ColIb-P9 repZ gene expression at the translational level. J Biol Chem. 1991;266:3774–3781. [PubMed] [Google Scholar]
  • 9.Ma C, Simons RW. The IS10 antisense RNA blocks ribosome binding at the transposase translation initiation site. EMBO J. 1990;9:1267–1274. doi: 10.1002/j.1460-2075.1990.tb08235.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Brunel C, Romby P, Sacerdot C, de Smit M, Graffe M, Dondon J, van Duin J, Ehresmann B, Ehresmann C, Springer M. Stabilised secondary structure at the ribosomal binding site enhances translational repression in E coli. J Mol Biol. 1995;253:277–290. doi: 10.1006/jmbi.1995.0552. [DOI] [PubMed] [Google Scholar]
  • 11.Spedding GS, Gluick TC, Draper DE. Ribosome initiation complex formation with the pseudoknotted α operon messenger RNA. J Mol Biol. 1993;229:609–622. doi: 10.1006/jmbi.1993.1067. [DOI] [PubMed] [Google Scholar]
  • 12.Philippe C, Eyermann F, Bénard L, Portier C, Ehresmann B, Ehresmann C. Ribosomal protein S15 from Escherichia coli modulates its own translation by trapping the ribosome on the mRNA initiation loading site. Proc Natl Acad Sci USA. 1993;90:4394–4398. doi: 10.1073/pnas.90.10.4394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Portier C, Dondon L, Grunberg-Manago M. Translational autocontrol of the Escherichia coli ribosomal protein S15. J Mol Biol. 1990;211:407–414. doi: 10.1016/0022-2836(90)90361-O. [DOI] [PubMed] [Google Scholar]
  • 14.Portier C, Philippe C, Dondon L, Grunberg-Manago M, Ehresmann B, Ehresmann C. Translational control of ribosomal protein S15. Biochim Biophys Acta. 1990;1050:328–336. doi: 10.1016/0167-4781(90)90190-d. [DOI] [PubMed] [Google Scholar]
  • 15.Philippe C, Portier C, Mougel M, Grunberg-Manago M, Ebel J-P, Ehresmann B, Ehresmann C. Target site of Escherichia coli ribosomal protein S15 on its messenger RNA. Conformation and interaction with the protein. J Mol Biol. 1990;211:415–426. doi: 10.1016/0022-2836(90)90362-P. [DOI] [PubMed] [Google Scholar]
  • 16.Bénard L, Philippe C, Dondon L, Grunberg-Manago M, Ehresmann B, Ehresmann C, Portier C. Mutational analysis of the pseudoknot structure of the S15 translational operator from Escherichia coli. Mol Microbiol. 1994;14:31–40. doi: 10.1111/j.1365-2958.1994.tb01264.x. [DOI] [PubMed] [Google Scholar]
  • 17.Philippe C, Bénard L, Eyermann F, Cachia C, Kirillov SV, Portier C, Ehresmann B, Ehresmann C. Structural elements of rpsO mRNA involved in the modulation of translation initiation and regulation of E coli ribosomal protein S15. Nucleic Acids Res. 1994;22:2538–2546. doi: 10.1093/nar/22.13.2538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Philippe C, Bénard L, Portier C, Westhof E, Ehresmann B, Ehresmann C. Molecular dissection of the pseudoknot governing the translational regulation of Escherichia coli ribosomal protein. Nucleic Acids Res. 1995;23:18–28. doi: 10.1093/nar/23.1.18. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Draper DE. Translational regulation of ribosomalproteins in Escherichia coli. Molecular mechanisms. In: Ilan J, editor. Plenum Publishing; New-York: 1988. p. 487. (Translational regulation of gene expression). [Google Scholar]
  • 20.Wang C, Le S-Y, Ali N, Siddiqui A. An RNA pseudoknot is an essential structure element of the internal ribosome entry site located within the hepatitis C virus 5′ noncoding region. RNA. 1995;1:526–537. [PMC free article] [PubMed] [Google Scholar]
  • 21.Rinquist S, Jones T, Snyder EE, Gibson T, Boni I, Gold L. High-affinity RNA ligands to Escherichia coli ribosomes and ribosomal protein S1: comparison of natural and unnatural binding sites. Biochemistry. 1995;34:3640–3648. doi: 10.1021/bi00011a019. [DOI] [PubMed] [Google Scholar]
  • 22.Powers T, Noller HF. Hydroxyl radical footprinting of ribosomal proteins on 16S RNA. RNA. 1995;1:194–209. [PMC free article] [PubMed] [Google Scholar]
  • 23.Conrad RC, Craven GR. A cyanogen bromide fragment of S4 that specificallyrebinds 16S RNA. Nucleic Acids Res. 1987;15:10331–10343. doi: 10.1093/nar/15.24.10331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Baker AM, Draper DE. Messenger RNA recognition by fragments of ribosomal protein S4. J Biol Chem. 1995;270:22939–22945. doi: 10.1074/jbc.270.39.22939. [DOI] [PubMed] [Google Scholar]
  • 25.Groeneveld H, Thimon K, van Duin J. Translational control of maturation-protein synthesis in phage MS2: a role for the kinetics of RNA folding? RNA. 1995;1:79–88. [PMC free article] [PubMed] [Google Scholar]

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