Ribosomal Movement Impeded at a Pseudoknot Required for Frameshifting

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1992 Sep 15

PMID 1528874

Citations 107

Authors

C Tu

T H Tzeng

J A Bruenn

Affiliations

Soon will be listed here.

Abstract

Translational frameshifting sometimes occurs when ribosomes encounter a "shift" site preceding a region of unusual secondary structure, which in at least three cases is known to be a pseudoknot. We provide evidence that ribosomes have a decreased rate of movement through a pseudoknot required for frameshifting. These paused ribosomes are directly situated over the shift sequence. Ribosomal pausing appears to be necessary but not sufficient for frameshifting.

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References

Vieira J, Messing J . Production of single-stranded plasmid DNA. Methods Enzymol. 1987; 153:3-11. DOI: 10.1016/0076-6879(87)53044-0. View

Craigen W, Caskey C . Translational frameshifting: where will it stop?. Cell. 1987; 50(1):1-2. DOI: 10.1016/0092-8674(87)90652-0. View

Chamorro M, Parkin N, Varmus H . An RNA pseudoknot and an optimal heptameric shift site are required for highly efficient ribosomal frameshifting on a retroviral messenger RNA. Proc Natl Acad Sci U S A. 1992; 89(2):713-7. PMC: 48309. DOI: 10.1073/pnas.89.2.713. View

Krupp G, Gross H . Rapid RNA sequencing: nucleases from Staphylococcus aureus and Neurospora crassa discriminate between uridine and cytidine. Nucleic Acids Res. 1979; 6(11):3481-90. PMC: 327950. DOI: 10.1093/nar/6.11.3481. View

Melton D, Krieg P, Rebagliati M, Maniatis T, Zinn K, Green M . Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984; 12(18):7035-56. PMC: 320141. DOI: 10.1093/nar/12.18.7035. View

Tzeng T, Tu C, Bruenn J . Ribosomal frameshifting requires a pseudoknot in the Saccharomyces cerevisiae double-stranded RNA virus. J Virol. 1992; 66(2):999-1006. PMC: 240802. DOI: 10.1128/JVI.66.2.999-1006.1992. View

Doohan J, Samuel C . Biosynthesis of reovirus-specified polypeptides: ribosome pausing during the translation of reovirus S1 mRNA. Virology. 1992; 186(2):409-25. DOI: 10.1016/0042-6822(92)90006-b. 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

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

10.

Belcourt M, Farabaugh P . Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell. 1990; 62(2):339-52. PMC: 7133245. DOI: 10.1016/0092-8674(90)90371-k. View

11.

Atkins J, Weiss R, GESTELAND R . Ribosome gymnastics--degree of difficulty 9.5, style 10.0. Cell. 1990; 62(3):413-23. PMC: 7133308. DOI: 10.1016/0092-8674(90)90007-2. View

12.

ten Dam E, Pleij C, Bosch L . RNA pseudoknots: translational frameshifting and readthrough on viral RNAs. Virus Genes. 1990; 4(2):121-36. PMC: 7089070. DOI: 10.1007/BF00678404. View

13.

Jacks T, Varmus H . Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science. 1985; 230(4731):1237-42. DOI: 10.1126/science.2416054. View

14.

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

15.

Weiss R, Dunn D, Shuh M, Atkins J, GESTELAND R . E. coli ribosomes re-phase on retroviral frameshift signals at rates ranging from 2 to 50 percent. New Biol. 1989; 1(2):159-69. View

16.

Diamond M, Dowhanick J, Nemeroff M, Pietras D, Tu C, Bruenn J . Overlapping genes in a yeast double-stranded RNA virus. J Virol. 1989; 63(9):3983-90. PMC: 250995. DOI: 10.1128/JVI.63.9.3983-3990.1989. View

17.

Brierley I, Digard P, Inglis S . Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell. 1989; 57(4):537-47. PMC: 7133225. DOI: 10.1016/0092-8674(89)90124-4. View

18.

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

19.

Wolin S, Walter P . Ribosome pausing and stacking during translation of a eukaryotic mRNA. EMBO J. 1988; 7(11):3559-69. PMC: 454858. DOI: 10.1002/j.1460-2075.1988.tb03233.x. View

20.

Jacks T, Townsley K, Varmus H, Majors J . Two efficient ribosomal frameshifting events are required for synthesis of mouse mammary tumor virus gag-related polyproteins. Proc Natl Acad Sci U S A. 1987; 84(12):4298-302. PMC: 305072. DOI: 10.1073/pnas.84.12.4298. View