Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1998 Apr 15;26(8):2008–2015. doi: 10.1093/nar/26.8.2008

Skipper, an LTR retrotransposon of Dictyostelium.

P Leng 1, D H Klatte 1, G Schumann 1, J D Boeke 1, T L Steck 1
PMCID: PMC147500  PMID: 9518497

Abstract

The complete sequence of a retrotransposon from Dictyostelium discoideum , named skipper , was obtained from cDNA and genomic clones. The sequence of a nearly full-length skipper cDNA was similar to that of three other partially sequenced cDNAs. The corresponding retrotransposon is represented in approximately 15-20 copies and is abundantly transcribed. Skipper contains three open reading frames (ORFs) with an unusual sequence organization, aspects of which resemble certain mammalian retroviruses. ORFs 1 and 3 correspond to gag and pol genes; the second ORF, pro, corresponding to protease, was separated from gag by a single stop codon followed shortly thereafter by a potential pseudoknot. ORF3 (pol) was separated from pro by a +1 frameshift. ORFs 2 and 3 overlapped by 32 bp. The computed amino acid sequences of the skipper ORFs contain regions resembling retrotransposon polyprotein domains, including a nucleic acid binding protein, aspartyl protease, reverse transcriptase and integrase. Skipper is the first example of a retrotransposon with a separate pro gene. Skipper is also novel in that it appears to use stop codon suppression rather than frameshifting to modulate pro expression. Finally, skipper and its components may provide useful tools for the genetic characterization of Dictyostelium.

Full Text

The Full Text of this article is available as a PDF (167.7 KB).

Selected References

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

  1. Ashworth J. M., Watts D. J. Metabolism of the cellular slime mould Dictyostelium discoideum grown in axenic culture. Biochem J. 1970 Sep;119(2):175–182. doi: 10.1042/bj1190175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Belcourt M. F., Farabaugh P. J. Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell. 1990 Jul 27;62(2):339–352. doi: 10.1016/0092-8674(90)90371-K. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Cappello J., Cohen S. M., Lodish H. F. Dictyostelium transposable element DIRS-1 preferentially inserts into DIRS-1 sequences. Mol Cell Biol. 1984 Oct;4(10):2207–2213. doi: 10.1128/mcb.4.10.2207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cappello J., Handelsman K., Lodish H. F. Sequence of Dictyostelium DIRS-1: an apparent retrotransposon with inverted terminal repeats and an internal circle junction sequence. Cell. 1985 Nov;43(1):105–115. doi: 10.1016/0092-8674(85)90016-9. [DOI] [PubMed] [Google Scholar]
  6. Chalker D. L., Sandmeyer S. B. Transfer RNA genes are genomic targets for de Novo transposition of the yeast retrotransposon Ty3. Genetics. 1990 Dec;126(4):837–850. doi: 10.1093/genetics/126.4.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Chang L. J., Pryciak P., Ganem D., Varmus H. E. Biosynthesis of the reverse transcriptase of hepatitis B viruses involves de novo translational initiation not ribosomal frameshifting. Nature. 1989 Jan 26;337(6205):364–368. doi: 10.1038/337364a0. [DOI] [PubMed] [Google Scholar]
  9. Copeland T. D., Morgan M. A., Oroszlan S. Complete amino acid sequence of the basic nucleic acid binding protein of feline leukemia virus. Virology. 1984 Feb;133(1):137–145. doi: 10.1016/0042-6822(84)90432-x. [DOI] [PubMed] [Google Scholar]
  10. Covey S. N. Amino acid sequence homology in gag region of reverse transcribing elements and the coat protein gene of cauliflower mosaic virus. Nucleic Acids Res. 1986 Jan 24;14(2):623–633. doi: 10.1093/nar/14.2.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Craigie R. Hotspots and warm spots: integration specificity of retroelements. Trends Genet. 1992 Jun;8(6):187–190. doi: 10.1016/0168-9525(92)90223-q. [DOI] [PubMed] [Google Scholar]
  12. Devine S. E., Boeke J. D. Integration of the yeast retrotransposon Ty1 is targeted to regions upstream of genes transcribed by RNA polymerase III. Genes Dev. 1996 Mar 1;10(5):620–633. doi: 10.1101/gad.10.5.620. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Doolittle R. F., Feng D. F., Johnson M. S., McClure M. A. Origins and evolutionary relationships of retroviruses. Q Rev Biol. 1989 Mar;64(1):1–30. doi: 10.1086/416128. [DOI] [PubMed] [Google Scholar]
  15. Evgen'ev M. B., Corces V. G., Lankenau D. H. Ulysses transposable element of Drosophila shows high structural similarities to functional domains of retroviruses. J Mol Biol. 1992 Jun 5;225(3):917–924. doi: 10.1016/0022-2836(92)90412-d. [DOI] [PubMed] [Google Scholar]
  16. Farabaugh P. J., Zhao H., Vimaladithan A. A novel programed frameshift expresses the POL3 gene of retrotransposon Ty3 of yeast: frameshifting without tRNA slippage. Cell. 1993 Jul 16;74(1):93–103. doi: 10.1016/0092-8674(93)90297-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  18. Feng Y. X., Yuan H., Rein A., Levin J. G. Bipartite signal for read-through suppression in murine leukemia virus mRNA: an eight-nucleotide purine-rich sequence immediately downstream of the gag termination codon followed by an RNA pseudoknot. J Virol. 1992 Aug;66(8):5127–5132. doi: 10.1128/jvi.66.8.5127-5132.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hansen L. J., Chalker D. L., Sandmeyer S. B. Ty3, a yeast retrotransposon associated with tRNA genes, has homology to animal retroviruses. Mol Cell Biol. 1988 Dec;8(12):5245–5256. doi: 10.1128/mcb.8.12.5245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Henderson L. E., Copeland T. D., Sowder R. C., Smythers G. W., Oroszlan S. Primary structure of the low molecular weight nucleic acid-binding proteins of murine leukemia viruses. J Biol Chem. 1981 Aug 25;256(16):8400–8406. [PubMed] [Google Scholar]
  21. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. Jacks T. Translational suppression in gene expression in retroviruses and retrotransposons. Curr Top Microbiol Immunol. 1990;157:93–124. doi: 10.1007/978-3-642-75218-6_4. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Johnson M. S., McClure M. A., Feng D. F., Gray J., Doolittle R. F. Computer analysis of retroviral pol genes: assignment of enzymatic functions to specific sequences and homologies with nonviral enzymes. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7648–7652. doi: 10.1073/pnas.83.20.7648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kikuchi Y., Sasaki N., Ando-Yamagami Y. Cleavage of tRNA within the mature tRNA sequence by the catalytic RNA of RNase P: implication for the formation of the primer tRNA fragment for reverse transcription in copia retrovirus-like particles. Proc Natl Acad Sci U S A. 1990 Oct;87(20):8105–8109. doi: 10.1073/pnas.87.20.8105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kozak M. A consideration of alternative models for the initiation of translation in eukaryotes. Crit Rev Biochem Mol Biol. 1992;27(4-5):385–402. doi: 10.3109/10409239209082567. [DOI] [PubMed] [Google Scholar]
  29. Kozak M. The scanning model for translation: an update. J Cell Biol. 1989 Feb;108(2):229–241. doi: 10.1083/jcb.108.2.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kulkosky J., Jones K. S., Katz R. A., Mack J. P., Skalka A. M. Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases. Mol Cell Biol. 1992 May;12(5):2331–2338. doi: 10.1128/mcb.12.5.2331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Levin H. L. A novel mechanism of self-primed reverse transcription defines a new family of retroelements. Mol Cell Biol. 1995 Jun;15(6):3310–3317. doi: 10.1128/mcb.15.6.3310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Levin H. L. An unusual mechanism of self-primed reverse transcription requires the RNase H domain of reverse transcriptase to cleave an RNA duplex. Mol Cell Biol. 1996 Oct;16(10):5645–5654. doi: 10.1128/mcb.16.10.5645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lin J. H., Levin H. L. A complex structure in the mRNA of Tf1 is recognized and cleaved to generate the primer of reverse transcription. Genes Dev. 1997 Jan 15;11(2):270–285. doi: 10.1101/gad.11.2.270. [DOI] [PubMed] [Google Scholar]
  34. Marschalek R., Borschet G., Dingermann T. Genomic organization of the transposable element Tdd-3 from Dictyostelium discoideum. Nucleic Acids Res. 1990 Oct 11;18(19):5751–5757. doi: 10.1093/nar/18.19.5751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Marschalek R., Hofmann J., Schumann G., Dingermann T. Two distinct subforms of the retrotransposable DRE element in NC4 strains of Dictyostelium discoideum. Nucleic Acids Res. 1992 Dec 11;20(23):6247–6252. doi: 10.1093/nar/20.23.6247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Marschalek R., Hofmann J., Schumann G., Gösseringer R., Dingermann T. Structure of DRE, a retrotransposable element which integrates with position specificity upstream of Dictyostelium discoideum tRNA genes. Mol Cell Biol. 1992 Jan;12(1):229–239. doi: 10.1128/mcb.12.1.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Matthews G. D., Goodwin T. J., Butler M. I., Berryman T. A., Poulter R. T. pCal, a highly unusual Ty1/copia retrotransposon from the pathogenic yeast Candida albicans. J Bacteriol. 1997 Nov;179(22):7118–7128. doi: 10.1128/jb.179.22.7118-7128.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. McMillan J. P., Singer M. F. Translation of the human LINE-1 element, L1Hs. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11533–11537. doi: 10.1073/pnas.90.24.11533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Nakamura Y., Wada K., Wada Y., Doi H., Kanaya S., Gojobori T., Ikemura T. Codon usage tabulated from the international DNA sequence databases. Nucleic Acids Res. 1996 Jan 1;24(1):214–215. doi: 10.1093/nar/24.1.214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Poole S. J., Firtel R. A. Genomic instability and mobile genetic elements in regions surrounding two discoidin I genes of Dictyostelium discoideum. Mol Cell Biol. 1984 Apr;4(4):671–680. doi: 10.1128/mcb.4.4.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Rein A., Levin J. G. Readthrough suppression in the mammalian type C retroviruses and what it has taught us. New Biol. 1992 Apr;4(4):283–289. [PubMed] [Google Scholar]
  42. Schlicht H. J., Radziwill G., Schaller H. Synthesis and encapsidation of duck hepatitis B virus reverse transcriptase do not require formation of core-polymerase fusion proteins. Cell. 1989 Jan 13;56(1):85–92. doi: 10.1016/0092-8674(89)90986-0. [DOI] [PubMed] [Google Scholar]
  43. Schwartz D. E., Tizard R., Gilbert W. Nucleotide sequence of Rous sarcoma virus. Cell. 1983 Mar;32(3):853–869. doi: 10.1016/0092-8674(83)90071-5. [DOI] [PubMed] [Google Scholar]
  44. Voytas D. F., Ausubel F. M. A copia-like transposable element family in Arabidopsis thaliana. Nature. 1988 Nov 17;336(6196):242–244. doi: 10.1038/336242a0. [DOI] [PubMed] [Google Scholar]
  45. Williamson V. M. Transposable elements in yeast. Int Rev Cytol. 1983;83:1–25. doi: 10.1016/s0074-7696(08)61684-8. [DOI] [PubMed] [Google Scholar]
  46. Xiong Y., Eickbush T. H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 1990 Oct;9(10):3353–3362. doi: 10.1002/j.1460-2075.1990.tb07536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Xiong Y., Eickbush T. H. The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons. Mol Cell Biol. 1988 Jan;8(1):114–123. doi: 10.1128/mcb.8.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Yoshinaka Y., Katoh I., Copeland T. D., Oroszlan S. Murine leukemia virus protease is encoded by the gag-pol gene and is synthesized through suppression of an amber termination codon. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1618–1622. doi: 10.1073/pnas.82.6.1618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Yoshinaka Y., Luftig R. B. Properties of a P70 proteolytic factor of murine leukemia viruses. Cell. 1977 Nov;12(3):709–719. doi: 10.1016/0092-8674(77)90271-9. [DOI] [PubMed] [Google Scholar]
  50. Yoshioka K., Honma H., Zushi M., Kondo S., Togashi S., Miyake T., Shiba T. Virus-like particle formation of Drosophila copia through autocatalytic processing. EMBO J. 1990 Feb;9(2):535–541. doi: 10.1002/j.1460-2075.1990.tb08140.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Yu S. F., Baldwin D. N., Gwynn S. R., Yendapalli S., Linial M. L. Human foamy virus replication: a pathway distinct from that of retroviruses and hepadnaviruses. Science. 1996 Mar 15;271(5255):1579–1582. doi: 10.1126/science.271.5255.1579. [DOI] [PubMed] [Google Scholar]
  52. Zou S., Ke N., Kim J. M., Voytas D. F. The Saccharomyces retrotransposon Ty5 integrates preferentially into regions of silent chromatin at the telomeres and mating loci. Genes Dev. 1996 Mar 1;10(5):634–645. doi: 10.1101/gad.10.5.634. [DOI] [PubMed] [Google Scholar]
  53. von der Helm K. Cleavage of Rous sarcoma viral polypeptide precursor into internal structural proteins in vitro involves viral protein p15. Proc Natl Acad Sci U S A. 1977 Mar;74(3):911–915. doi: 10.1073/pnas.74.3.911. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES