Torsional Restraint: a New Twist on Frameshifting Pseudoknots

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2005 Apr 1

PMID 15800212

Citations 53

Authors

Ewan P Plant

Jonathan D Dinman

Affiliations

Soon will be listed here.

Abstract

mRNA pseudoknots have a stimulatory function in programmed -1 ribosomal frameshifting (-1 PRF). Though we previously presented a model for how mRNA pseudoknots might activate the mechanism for -1 PRF, it did not address the question of the role that they may play in positioning the mRNA relative to the ribosome in this process [E. P. Plant, K. L. M. Jacobs, J. W. Harger, A. Meskauskas, J. L. Jacobs, J. L. Baxter, A. N. Petrov and J. D. Dinman (2003) RNA, 9, 168-174]. A separate 'torsional restraint' model suggests that mRNA pseudoknots act to increase the fraction of ribosomes directed to pause with the upstream heptameric slippery site positioned at the ribosome's A- and P-decoding sites [J. D. Dinman (1995) Yeast, 11, 1115-1127]. Here, experiments using a series of 'pseudo-pseudoknots' having different degrees of rotational freedom were used to test this model. The results of this study support the mechanistic hypothesis that -1 ribosomal frameshifting is enhanced by torsional resistance of the mRNA pseudoknot.

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References

Howard M, Gesteland R, Atkins J . Efficient stimulation of site-specific ribosome frameshifting by antisense oligonucleotides. RNA. 2004; 10(10):1653-61. PMC: 1370650. DOI: 10.1261/rna.7810204. View

Onoa B, Tinoco Jr I . RNA folding and unfolding. Curr Opin Struct Biol. 2004; 14(3):374-9. DOI: 10.1016/j.sbi.2004.04.001. View

Jacks T, Power M, Masiarz F, Luciw P, Barr P, Varmus H . Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature. 1988; 331(6153):280-3. DOI: 10.1038/331280a0. View

Puglisi J, Wyatt J, Tinoco Jr I . A pseudoknotted RNA oligonucleotide. Nature. 1988; 331(6153):283-6. DOI: 10.1038/331283a0. View

Jacks T, Madhani H, Masiarz F, Varmus H . Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region. Cell. 1988; 55(3):447-58. PMC: 7133365. DOI: 10.1016/0092-8674(88)90031-1. View

Dinman J, Icho T, Wickner R . A -1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein. Proc Natl Acad Sci U S A. 1991; 88(1):174-8. PMC: 50772. DOI: 10.1073/pnas.88.1.174. View

Brierley I, Rolley N, Jenner A, Inglis S . Mutational analysis of the RNA pseudoknot component of a coronavirus ribosomal frameshifting signal. J Mol Biol. 1991; 220(4):889-902. PMC: 7131590. DOI: 10.1016/0022-2836(91)90361-9. View

Gallie D . The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev. 1991; 5(11):2108-16. DOI: 10.1101/gad.5.11.2108. View

Morikawa S, Bishop D . Identification and analysis of the gag-pol ribosomal frameshift site of feline immunodeficiency virus. Virology. 1992; 186(2):389-97. PMC: 7131530. DOI: 10.1016/0042-6822(92)90004-9. View

10.

Dinman J, Wickner R . Ribosomal frameshifting efficiency and gag/gag-pol ratio are critical for yeast M1 double-stranded RNA virus propagation. J Virol. 1992; 66(6):3669-76. PMC: 241150. DOI: 10.1128/JVI.66.6.3669-3676.1992. View

11.

Tu C, Tzeng T, Bruenn J . Ribosomal movement impeded at a pseudoknot required for frameshifting. Proc Natl Acad Sci U S A. 1992; 89(18):8636-40. PMC: 49975. DOI: 10.1073/pnas.89.18.8636. View

12.

ten Dam E, Brierley I, Inglis S, Pleij C . Identification and analysis of the pseudoknot-containing gag-pro ribosomal frameshift signal of simian retrovirus-1. Nucleic Acids Res. 1994; 22(12):2304-10. PMC: 523688. DOI: 10.1093/nar/22.12.2304. View

13.

Brierley I . Ribosomal frameshifting viral RNAs. J Gen Virol. 1995; 76 ( Pt 8):1885-92. DOI: 10.1099/0022-1317-76-8-1885. View

14.

Dinman J . Ribosomal frameshifting in yeast viruses. Yeast. 1995; 11(12):1115-27. PMC: 7169727. DOI: 10.1002/yea.320111202. View

15.

GESTELAND R, Atkins J . Recoding: dynamic reprogramming of translation. Annu Rev Biochem. 1996; 65:741-68. DOI: 10.1146/annurev.bi.65.070196.003521. View

16.

Napthine S, Liphardt J, Bloys A, Routledge S, Brierley I . The role of RNA pseudoknot stem 1 length in the promotion of efficient -1 ribosomal frameshifting. J Mol Biol. 1999; 288(3):305-20. PMC: 7126229. DOI: 10.1006/jmbi.1999.2688. View

17.

Liphardt J, Napthine S, Kontos H, Brierley I . Evidence for an RNA pseudoknot loop-helix interaction essential for efficient -1 ribosomal frameshifting. J Mol Biol. 1999; 288(3):321-35. PMC: 7141562. DOI: 10.1006/jmbi.1999.2689. View

18.

Takyar S, Hickerson R, Noller H . mRNA helicase activity of the ribosome. Cell. 2005; 120(1):49-58. DOI: 10.1016/j.cell.2004.11.042. View

19.

Kim Y, Su L, Maas S, ONeill A, Rich A . Specific mutations in a viral RNA pseudoknot drastically change ribosomal frameshifting efficiency. Proc Natl Acad Sci U S A. 1999; 96(25):14234-9. PMC: 24420. DOI: 10.1073/pnas.96.25.14234. View

20.

Giedroc D, Theimer C, Nixon P . Structure, stability and function of RNA pseudoknots involved in stimulating ribosomal frameshifting. J Mol Biol. 2000; 298(2):167-85. PMC: 7126452. DOI: 10.1006/jmbi.2000.3668. View