The interplay of mRNA stimulatory signals required for AUU-mediated initiation and programmed -1 ribosomal frameshifting in decoding of transposable element IS911

Journal of Bacteriology

Volumn 193, Issue 11, 2011, Pages 2735-2744

  Prère, Marie Françoise ^a   Canal, Isabelle ^a   Wills, Norma M ^b   Atkins, John F ^b,c   Fayet, Olivier ^a  

^a UMR   (France)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RNA 16S; TRANSPOSABLE ELEMENT IS911; TRANSPOSASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CODON; DNA FLANKING REGION; DNA SEQUENCE; DNA TRANSPOSITION; INSERTIONAL CHROMOSOME TRANSLOCATION; MUTAGENIC ACTIVITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN SYNTHESIS; RIBOSOMAL FRAMESHIFTING; SHINE DALGARNO REGION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSPOSON;

BINDING SITES; DNA TRANSPOSABLE ELEMENTS; FRAMESHIFTING, RIBOSOMAL; NUCLEIC ACID CONFORMATION; OPEN READING FRAMES; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; RNA, RIBOSOMAL, 16S; TRANSPOSASES;

BACTERIA (MICROORGANISMS);

EID: 79958134302     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00115-11     Document Type: Article

References (54)

1. Baranov, P. V., R. F. Gesteland, and J. F. Atkins. 2002. Recoding: translational bifurcations in gene expression. Gene 286:187-201.
2. Baranov, P. V., O. Fayet, R. W. Hendrix, and J. F. Atkins. 2006. Recoding in bacteriophages and bacterial IS elements. Trends Genet. 22:174-181.
3. Barry, J. K., and W. A. Miller. 2002. A -1 ribosomal frameshift element that requires base pairing across four kilobases suggests a mechanism of regulating ribosome and replicase traffic on a viral RNA. Proc. Natl. Acad. Sci. U. S. A. 99:11133-11138.
4. Bertrand, C., M. F. Prère, R. F. Gesteland, J. F. Atkins, and O. Fayet. 2002. Influence of the stacking potential of the base 3′ of tandem shift codons on -1 ribosomal frameshifting used for gene expression. RNA 8:16-28.
5. Bidou, L., et al. 1997. In vivo HIV-1 frameshifting efficiency is directly related to the stability of the stem-loop stimulatory signal. RNA 3:1153- 1158.
6. Binns, N., and M. Masters.V 2002. Expression of the Escherichia coli pcnB gene is translationally limited using an inefficient start codon: a second chromosomal example of translation initiated at AUU. Mol. Microbiol. 44:1287-1298.
7. Blinkowa, A. L., and J. R. Walker. 1990. Programmed ribosomal frameshifting generates the Escherichia coli DNA polymerase III gamma subunit from within the tau subunit reading frame. Nucleic Acids Res. 18:1725-1729.
8. Brierley, I., A. J. Jenner, and S. C. Inglis. 1992. Mutational analysis of the " slippery-sequence" component of a coronavirus ribosomal frameshifting ignal. J. Mol. Biol. 227:463-479.
9. Brierley, I., and S. Pennell. 2001. Structure and function of the stimulatory RNAs involved in programmed eukaryotic -1 frameshifting. Cold Spring arbor Symp. Quant. Biol. 66:233-248.
10. Chandler, M., and O. Fayet. 1993. Translational frameshifting in the control of transposition in bacteria. Mol. Microbiol. 7:497-503.
11. Chen, H., M. Bjerknees, R. Kumar, and E. Jay. 1994. Determination of the optimal aligned spacing between the Shine-Dalgarno sequence and the translation initiation codon of Escherichia coli mRNAs. Nucleic Acids Res. 22:4953-4957.
12. Dulude, D., M. Baril, and L. Brakier-Gingras. 2002. Characterization of the frameshift stimulatory signal controlling a programmed -1 ribosomal frameshift in the human immunodeficiency virus type 1. Nucleic Acids Res. 30: 5094-5102.
13. Escoubas, J. M., et al. 1991. Translational control of transposition activity of the bacterial insertion sequence IS1. EMBO J. 10:705-712.
14. Farabaugh, P. J. 1996. Programmed translational frameshifting. Microbiol. Rev. 60:103-134.
15. Fayet, O., P. Ramond, P. Polard, M. F. Prère, and M. Chandler. 1990. Functional similarities between retroviruses and the IS3 family of bacterial insertion sequences? Mol. Microbiol. 4:1771-1777.
16. Fayet, O., and M. F. Prère. 2010. Programmed ribosomal -1 frameshifting as a tradition: the bacterial transposable elements of the IS3 family, p. 259-280. In J. F. Atkins and R. F. Gesteland (ed.), Recoding: expansion of decoding rules enriches gene expression. Springer, New York, NY.
17. Flower, A. M., and C. S. McHenry. 1990. The gamma subunit of DNA polymerase III holoenzyme of Escherichia coli is produced by ribosomal rameshifting. Proc. Natl. Acad. Sci. U. S. A. 87:3713-3717.
18. Giedroc, D. P., and P. V. Cornish. 2009. Frameshifting RNA pseudoknots: structure and mechanism. Virus Res. 139:193-208.
19. Haren, L., P. Polard, B. Ton-Hoang, and M. Chandler. 1998. Multiple oligomerisation domains in the IS911 transposase: a leucine zipper motif is ssential for activity. J. Mol. Biol. 283:29-41.
20. Ivanov, N., G. Loughran, and J. F. Atkins. 2008. uORFs with unusual translational start codons autoregulate expression of eukaryotic ornithine decarboxylase homologs. Proc. Natl. Acad. Sci. U. S. A. 105:10079-10084.
21. Jacks, T., H. D. Madhani, F. R. Masiarz, and H. E. Varmus. 1988. Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region. Cell 55: 47-458.
22. Kollmus, H., A. Honigman, A. Panet, and H. Hauser. 1994. The sequences of and distance between two cis-acting signals determine the efficiency of ribosomal frameshifting in human immunodeficiency virus type 1 and human T-cell leukemia virus type II in vivo. J. Virol. 68:6087-6091.
23. Larsen, B., N. M. Wills, R. F. Gesteland, and J. F. Atkins. 1994. rRNAmRNA base pairing stimulates a programmed -1 ribosomal frameshift. J. acteriol. 176:6842-6851.
24. Larsen, B., R. F. Gesteland, and J. F. Atkins. 1997. Structural probing and mutagenic analysis of the stem-loop required for Escherichia coli dnaX ribosomal frameshifting: programmed efficiency of 50%. J. Mol. Biol. 271:47-60.
25. Levin, M. E., R. W. Hendrix, and S. R. Casjens. 1993. A programmed translational frameshift is required for the synthesis of a bacteriophage lambda tail assembly protein. J. Mol. Biol. 1993 234:124-139.
26. Liao, P. Y., Y. S. Choi, J. D. Dinman, and K. H. Lee. 2011. The many paths to frameshifting: kinetic modelling and analysis of the effects of different elongation steps on programmed -1 ribosomal frameshifting. Nucleic Acids Res. 39:300-312.
27. Licznar, P., et al. 2003. Programmed translational -1 frameshifting on hexanucleotide motifs and the wobble properties of tRNAs. EMBO J. 22: 4770-778.
28. Mahillon, J., and M. Chandler. 1998. Insertion sequences. Microbiol. Mol. Biol. Rev. 62:725-774.
29. Matsufuji, S., T. Matsufuji, N. M. Wills, R. F. Gesteland, J. F. Atkins. 1996. Reading two bases twice: mammalian antizyme frameshifting in yeast. MBO J. 15:1360-1370.
30. Mazauric, M. H., P. Licznar, M. F. Prère, I. Canal, and O. Fayet. 2008. Apical loop-internal loop RNA pseudoknots: a new type of stimulator of -1 translational frameshifting in bacteria. J. Biol. Chem. 283:20421-20432.
31. Namy, O., J. P. Rousset, S. Napthine, and I. Brierley. 2004. Reprogrammed genetic decoding in cellular gene expression. Mol. Cell 13:157-168.
32. Neidhardt, F. C., P. L. Bloch, and D. F. Smith. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
33. O'Connor, M., and A. E. Dahlberg. 2001. Enhancement of translation by the epsilon element is independent of the sequence of the 460 region of 16S RNA. Nucleic Acids Res. 29:1420-1425.
34. Olins, P. O., and S. H. Rangwala. 1989. A novel sequence element derived from bacteriophage T7 mRNA acts as an enhancer of translation of the lacZ ene in Escherichia coli. J. Biol. Chem. 264:16973-16976.
35. Paulus, M., M. Haslbeck, and M. Watzele. 2004. RNA stem-loop enhanced expression of previously non-expressible genes. Nucleic Acids Res. 32:e78.
36. Polard, P., M. F. Prère, M. Chandler, and O. Fayet. 1991. Programmed translational frameshifting and initiation at an AUU codon in gene expression of bacterial insertion sequence IS911. J. Mol. Biol. 222:465-477.
37. Polard, P., M. F. Prère, O. Fayet, and M. Chandler. 1992. Transposaseinduced excision and circularization of the bacterial insertion sequence IS911. MBO J. 11:5079-5090.
38. Prère, M. F., M. Chandler, and O. Fayet. 1990. Transposition in Shigella dysenteriae: isolation and analysis of IS911, a new member of the IS3 group of nsertion sequences. J. Bacteriol. 172:4090-4099.
39. Rettberg, C. C., M. F. Prère, R. F. Gesteland, J. F. Atkins, and O. Fayet. 1999. A three-way junction and constituent stem-loops as the stimulator for programmed -1 frameshifting in bacterial insertion sequence IS911. J. Mol. Biol. 286:1365-1378.
40. Reuter, J. S., and D. H. Mathews. 2010. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinf. 11:129-137.
41. Ringquist, S., et al. 1992. Translation initiation in Escherichia coli: sequences within the ribosome-binding site. Mol. Microbiol. 6:1219-1229.
42. Sacerdot, C., et al. 1996. The role of the AUU initiation codon in the negative feedback regulation of the gene for translation initiation factor IF3 in scherichia coli. Mol. Microbiol. 21:331-346.
43. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, Y.
44. Sekine, Y., N. Eisaki, and E. Ohtsubo. 1994. Translational control in production of transposase and in transposition of insertion sequence IS3. J. Mol. iol. 235:1406-1420.
45. Sekine, Y., K. I. Izumi, T. Mizuno, and E. Ohtsubo. 1997. Inhibition of transpositional recombination by OrfA and OrfB proteins encoded by insertion equence IS3. Genes Cells 2:547-557.
46. Simonetti, A., et al. 2008. Structure of the 30S translation initiation complex. Nature 455:416-420.
47. Skorski, P., P. Leroy, O. Fayet, M. Dreyfus, and S. Hermann-Le Denmat. 2006. The highly efficient translation initiation region from the Escherichia coli rpsA gene lacks a Shine-Dalgarno element. J. Bacteriol. 188:6277-6285.
48. Takyar, S., R. P. Hickerson, and H. F. Noller. 2005. mRNA helicase activity of the ribosome. Cell 120:49-58.
49. ten Dam, E. B., C. W. Pleij, and L. Bosch. 1990. RNA pseudoknots: translational frameshifting and readthrough on viral RNAs. Virus Genes 4:121- 36.
50. Tsuchihashi, Z., and P. O. Brown. 1992. Sequence requirements for efficient translational frameshifting in the Escherichia coli dnaX gene and the role of an unstable interaction between tRNALys and an AAG lysine codon. Genes Dev. 6:511-519.
51. Tsuchihashi, Z., and A. Kornberg. 1990. Translational frameshifting generates the gamma subunit of DNA polymerase III holoenzyme. Proc. Natl. Acad. ci. U. S. A. 87:2516-2520.
52. Vögele, K., E. Schwartz, C. Welz, E. Schiltz, and B. Rak. 1991. High-level ribosomal frameshifting directs the synthesis of IS150 gene products. ucleic Acids Res. 19:4377-4385.
53. Weiss, R. B., D. M. Dunn, M. Shuh, J. F. Atkins, and R. F. Gesteland. 1989. E. coli ribosomes re-phase on retroviral frameshift signals at rates ranging rom 2 to 50 percent. New Biol. 1:159-169.
54. Yusupova, G. Z., M. M. Yusupov, J. H. Cate, and H. F. Noller. 2001. The path of messenger RNA through the ribosome. Cell 106:233-241.