Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1993 Oct;67(10):6273–6277. doi: 10.1128/jvi.67.10.6273-6277.1993

Two cis-acting signals control ribosomal frameshift between human T-cell leukemia virus type II gag and pro genes.

H Falk 1, N Mador 1, R Udi 1, A Panet 1, A Honigman 1
PMCID: PMC238052  PMID: 8371359

Abstract

The open reading frame of the human T-cell leukemia virus type II pro gene is arranged at a -1 position relative to the gag gene. Synthesis of the Gag-Pro fusion polyprotein is facilitated by ribosomal frameshift into the reading frame of the pro gene. Cloning of a synthetic 41-bp oligonucleotide corresponding to the gag-pro junction within a heterologous gene (nef of human immunodeficiency virus type I) and mutation analysis revealed that two cis-acting signals, an adenosine residue stretch and a dyad symmetry sequence, flanking the UAA termination codon, are required for efficient ribosomal frameshifting between gag and pro. The stability of the stem-loop structure is crucial for frameshifting.

Full text

PDF
6273

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Brierley I., Digard P., Inglis S. C. Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell. 1989 May 19;57(4):537–547. doi: 10.1016/0092-8674(89)90124-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Chamorro M., Parkin N., Varmus H. E. 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 Jan 15;89(2):713–717. doi: 10.1073/pnas.89.2.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dinman J. D., Icho T., Wickner R. B. 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 Jan 1;88(1):174–178. doi: 10.1073/pnas.88.1.174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Freier S. M., Kierzek R., Jaeger J. A., Sugimoto N., Caruthers M. H., Neilson T., Turner D. H. Improved free-energy parameters for predictions of RNA duplex stability. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9373–9377. doi: 10.1073/pnas.83.24.9373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Honigman A., Wolf D., Yaish S., Falk H., Panet A. cis Acting RNA sequences control the gag-pol translation readthrough in murine leukemia virus. Virology. 1991 Jul;183(1):313–319. doi: 10.1016/0042-6822(91)90144-Z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Jacks T., Madhani H. D., Masiarz F. R., Varmus H. E. Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region. Cell. 1988 Nov 4;55(3):447–458. doi: 10.1016/0092-8674(88)90031-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Jacks T., Power M. D., Masiarz F. R., Luciw P. A., Barr P. J., Varmus H. E. Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature. 1988 Jan 21;331(6153):280–283. doi: 10.1038/331280a0. [DOI] [PubMed] [Google Scholar]
  8. Jacks T., Townsley K., Varmus H. E., 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 Jun;84(12):4298–4302. doi: 10.1073/pnas.84.12.4298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jacks T., Varmus H. E. Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science. 1985 Dec 13;230(4731):1237–1242. doi: 10.1126/science.2416054. [DOI] [PubMed] [Google Scholar]
  10. Kaminchik J., Bashan N., Itach A., Sarver N., Gorecki M., Panet A. Genetic characterization of human immunodeficiency virus type 1 nef gene products translated in vitro and expressed in mammalian cells. J Virol. 1991 Feb;65(2):583–588. doi: 10.1128/jvi.65.2.583-588.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Mador N., Panet A., Honigman A. Translation of gag, pro, and pol gene products of human T-cell leukemia virus type 2. J Virol. 1989 May;63(5):2400–2404. doi: 10.1128/jvi.63.5.2400-2404.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Nam S. H., Copeland T. D., Hatanaka M., Oroszlan S. Characterization of ribosomal frameshifting for expression of pol gene products of human T-cell leukemia virus type I. J Virol. 1993 Jan;67(1):196–203. doi: 10.1128/jvi.67.1.196-203.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nam S. H., Kidokoro M., Shida H., Hatanaka M. Processing of gag precursor polyprotein of human T-cell leukemia virus type I by virus-encoded protease. J Virol. 1988 Oct;62(10):3718–3728. doi: 10.1128/jvi.62.10.3718-3728.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Parkin N. T., Chamorro M., Varmus H. E. Human immunodeficiency virus type 1 gag-pol frameshifting is dependent on downstream mRNA secondary structure: demonstration by expression in vivo. J Virol. 1992 Aug;66(8):5147–5151. doi: 10.1128/jvi.66.8.5147-5151.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Shimotohno K., Takahashi Y., Shimizu N., Gojobori T., Golde D. W., Chen I. S., Miwa M., Sugimura T. Complete nucleotide sequence of an infectious clone of human T-cell leukemia virus type II: an open reading frame for the protease gene. Proc Natl Acad Sci U S A. 1985 May;82(10):3101–3105. doi: 10.1073/pnas.82.10.3101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Wills N. M., Gesteland R. F., Atkins J. F. Evidence that a downstream pseudoknot is required for translational read-through of the Moloney murine leukemia virus gag stop codon. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6991–6995. doi: 10.1073/pnas.88.16.6991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Wilson W., Braddock M., Adams S. E., Rathjen P. D., Kingsman S. M., Kingsman A. J. HIV expression strategies: ribosomal frameshifting is directed by a short sequence in both mammalian and yeast systems. Cell. 1988 Dec 23;55(6):1159–1169. doi: 10.1016/0092-8674(88)90260-7. [DOI] [PubMed] [Google Scholar]
  20. Wilson W., Malim M. H., Mellor J., Kingsman A. J., Kingsman S. M. Expression strategies of the yeast retrotransposon Ty: a short sequence directs ribosomal frameshifting. Nucleic Acids Res. 1986 Sep 11;14(17):7001–7016. doi: 10.1093/nar/14.17.7001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Zuker M., Stiegler P. Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res. 1981 Jan 10;9(1):133–148. doi: 10.1093/nar/9.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES