Skip to main content
NCBI home page
RNA logoLink to RNA
. 1998 Oct;4(10):1230–1238. doi: 10.1017/s1355838298980864

Programmed frameshifting in the synthesis of mammalian antizyme is +1 in mammals, predominantly +1 in fission yeast, but -2 in budding yeast.

I P Ivanov 1, R F Gesteland 1, S Matsufuji 1, J F Atkins 1
PMCID: PMC1369695  PMID: 9769097

Abstract

The coding sequence for mammalian ornithine decarboxylase antizyme is in two different partially overlapping reading frames with no independent ribosome entry to the second ORF. Immediately before the stop codon of the first ORF, a proportion of ribosomes undergo a quadruplet translocation event to shift to the +1 reading frame of the second and main ORF. The proportion that frameshifts is dependent on the polyamine level and, because the product antizyme is a negative regulator of intracellular polyamine levels, the frameshifting acts to complete an autoregulatory circuit by sensing polyamine levels. An mRNA element just 5' of the shift site and a 3' pseudoknot are important for efficient frameshifting. Previous work has shown that a cassette with the mammalian shift site and associated signals directs efficient shifting in the budding yeast Saccharomyces cerevisiae at the same codon to the correct frame, but that the shift is -2 instead of +1. The product contains an extra amino acid corresponding to the shift site. The present work shows efficient frameshifting also occurs in the fission yeast, Schizosaccharomyces pombe. This frameshifting is 80% +1 and 20% -2. The response of S. pombe translation apparatus to the mammalian antizyme recoding signals is more similar to that of the mammalian system than to that of S. cerevisiae. S. pombe provides a good model system for genetic studies on the mechanism of at least this type of programmed mammalian frameshifting.

Full Text

The Full Text of this article is available as a PDF (686.4 KB).

Selected References

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

  1. Cui Y., Dinman J. D., Kinzy T. G., Peltz S. W. The Mof2/Sui1 protein is a general monitor of translational accuracy. Mol Cell Biol. 1998 Mar;18(3):1506–1516. doi: 10.1128/mcb.18.3.1506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cui Y., Dinman J. D., Peltz S. W. Mof4-1 is an allele of the UPF1/IFS2 gene which affects both mRNA turnover and -1 ribosomal frameshifting efficiency. EMBO J. 1996 Oct 15;15(20):5726–5736. doi: 10.1002/j.1460-2075.1996.tb00956.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dinman J. D. Ribosomal frameshifting in yeast viruses. Yeast. 1995 Sep 30;11(12):1115–1127. doi: 10.1002/yea.320111202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dinman J. D., Wickner R. B. 5 S rRNA is involved in fidelity of translational reading frame. Genetics. 1995 Sep;141(1):95–105. doi: 10.1093/genetics/141.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dinman J. D., Wickner R. B. Translational maintenance of frame: mutants of Saccharomyces cerevisiae with altered -1 ribosomal frameshifting efficiencies. Genetics. 1994 Jan;136(1):75–86. doi: 10.1093/genetics/136.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Farabaugh P. J. Programmed translational frameshifting. Microbiol Rev. 1996 Mar;60(1):103–134. doi: 10.1128/mr.60.1.103-134.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gesteland R. F., Weiss R. B., Atkins J. F. Recoding: reprogrammed genetic decoding. Science. 1992 Sep 18;257(5077):1640–1641. doi: 10.1126/science.1529352. [DOI] [PubMed] [Google Scholar]
  8. Grey M., Brendel M. A ten-minute protocol for transforming Saccharomyces cerevisiae by electroporation. Curr Genet. 1992 Oct;22(4):335–336. doi: 10.1007/BF00317931. [DOI] [PubMed] [Google Scholar]
  9. Guarente L. Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol. 1983;101:181–191. doi: 10.1016/0076-6879(83)01013-7. [DOI] [PubMed] [Google Scholar]
  10. Hayashi S., Murakami Y., Matsufuji S. Ornithine decarboxylase antizyme: a novel type of regulatory protein. Trends Biochem Sci. 1996 Jan;21(1):27–30. [PubMed] [Google Scholar]
  11. Hayles J., Nurse P. Genetics of the fission yeast Schizosaccharomyces pombe. Annu Rev Genet. 1992;26:373–402. doi: 10.1146/annurev.ge.26.120192.002105. [DOI] [PubMed] [Google Scholar]
  12. Ivanov I. P., Simin K., Letsou A., Atkins J. F., Gesteland R. F. The Drosophila gene for antizyme requires ribosomal frameshifting for expression and contains an intronic gene for snRNP Sm D3 on the opposite strand. Mol Cell Biol. 1998 Mar;18(3):1553–1561. doi: 10.1128/mcb.18.3.1553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lee S. I., Umen J. G., Varmus H. E. A genetic screen identifies cellular factors involved in retroviral -1 frameshifting. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6587–6591. doi: 10.1073/pnas.92.14.6587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Li X., Coffino P. Distinct domains of antizyme required for binding and proteolysis of ornithine decarboxylase. Mol Cell Biol. 1994 Jan;14(1):87–92. doi: 10.1128/mcb.14.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Matsufuji S., Matsufuji T., Miyazaki Y., Murakami Y., Atkins J. F., Gesteland R. F., Hayashi S. Autoregulatory frameshifting in decoding mammalian ornithine decarboxylase antizyme. Cell. 1995 Jan 13;80(1):51–60. doi: 10.1016/0092-8674(95)90450-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Matsufuji S., Matsufuji T., Wills N. M., Gesteland R. F., Atkins J. F. Reading two bases twice: mammalian antizyme frameshifting in yeast. EMBO J. 1996 Mar 15;15(6):1360–1370. [PMC free article] [PubMed] [Google Scholar]
  17. Matsufuji S., Miyazaki Y., Kanamoto R., Kameji T., Murakami Y., Baby T. G., Fujita K., Ohno T., Hayashi S. Analyses of ornithine decarboxylase antizyme mRNA with a cDNA cloned from rat liver. J Biochem. 1990 Sep;108(3):365–371. doi: 10.1093/oxfordjournals.jbchem.a123207. [DOI] [PubMed] [Google Scholar]
  18. Rom E., Kahana C. Polyamines regulate the expression of ornithine decarboxylase antizyme in vitro by inducing ribosomal frame-shifting. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3959–3963. doi: 10.1073/pnas.91.9.3959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Xu H., Boeke J. D. Host genes that influence transposition in yeast: the abundance of a rare tRNA regulates Ty1 transposition frequency. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8360–8364. doi: 10.1073/pnas.87.21.8360. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from RNA are provided here courtesy of The RNA Society

RESOURCES