Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1990 Nov;9(11):3557–3563. doi: 10.1002/j.1460-2075.1990.tb07566.x

Identification of a potential RNA intermediate for transposition of the LINE-like element I factor in Drosophila melanogaster.

M C Chaboissier 1, I Busseau 1, J Prosser 1, D J Finnegan 1, A Bucheton 1
PMCID: PMC552106  PMID: 1698618

Abstract

The I factor, a transposable element related to mammalian LINEs, controls the I-R system of hybrid dysgenesis in Drosophila melanogaster. It transposes at high frequency in the germ-line of the female progeny of crosses between females of the reactive class of strains and males of the inducer class. The structure and DNA sequence of the I factor suggest that it transposes by reverse transcription of an RNA intermediate. Northern blot and S1 mapping experiments show that a full-length RNA of the I factor is synthesized specifically in the conditions of which I factors transpose. This RNA has all characteristics of a transposition intermediate. It is only found in the ovaries of dysgenic females suggesting that I factor activity is restricted to this tissue because of regulation at the level of the initiation of transcription or RNA stability.

Full text

PDF
3557

Images in this article

3558Fig.1
on p.3558
3559Fig.2
on p.3559
3560Fig.3
on p.3560
3561Fig.4
on p.3561

Selected References

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

  1. Abad P., Vaury C., Pélisson A., Chaboissier M. C., Busseau I., Bucheton A. A long interspersed repetitive element--the I factor of Drosophila teissieri--is able to transpose in different Drosophila species. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8887–8891. doi: 10.1073/pnas.86.22.8887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Black D. M., Jackson M. S., Kidwell M. G., Dover G. A. KP elements repress P-induced hybrid dysgenesis in Drosophila melanogaster. EMBO J. 1987 Dec 20;6(13):4125–4135. doi: 10.1002/j.1460-2075.1987.tb02758.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blackman R. K., Grimaila R., Koehler M. M., Gelbart W. M. Mobilization of hobo elements residing within the decapentaplegic gene complex: suggestion of a new hybrid dysgenesis system in Drosophila melanogaster. Cell. 1987 May 22;49(4):497–505. doi: 10.1016/0092-8674(87)90452-1. [DOI] [PubMed] [Google Scholar]
  4. Bogenhagen D. F., Brown D. D. Nucleotide sequences in Xenopus 5S DNA required for transcription termination. Cell. 1981 Apr;24(1):261–270. doi: 10.1016/0092-8674(81)90522-5. [DOI] [PubMed] [Google Scholar]
  5. Bucheton A. I transposable elements and I-R hybrid dysgenesis in Drosophila. Trends Genet. 1990 Jan;6(1):16–21. doi: 10.1016/0168-9525(90)90044-7. [DOI] [PubMed] [Google Scholar]
  6. Bucheton A., Lavige J. M., Picard G., L'Heritier P. Non-mendelian female sterility in Drosophila melanogaster: quantitative variations in the efficiency of inducer and reactive strains. Heredity (Edinb) 1976 Jun;36(3):305–314. doi: 10.1038/hdy.1976.38. [DOI] [PubMed] [Google Scholar]
  7. Bucheton A. Non-Mendelian female sterility in Drosophila melanogaster: influence of ageing and thermic treatments. I. Evidence for a partly inheritable effect of these two factors. Heredity (Edinb) 1978 Dec;41(3):357–369. doi: 10.1038/hdy.1978.106. [DOI] [PubMed] [Google Scholar]
  8. Bucheton A., Paro R., Sang H. M., Pelisson A., Finnegan D. J. The molecular basis of I-R hybrid dysgenesis in Drosophila melanogaster: identification, cloning, and properties of the I factor. Cell. 1984 Aug;38(1):153–163. doi: 10.1016/0092-8674(84)90536-1. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Clare J. J., Belcourt M., Farabaugh P. J. Efficient translational frameshifting occurs within a conserved sequence of the overlap between the two genes of a yeast Ty1 transposon. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6816–6820. doi: 10.1073/pnas.85.18.6816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Clare J., Farabaugh P. Nucleotide sequence of a yeast Ty element: evidence for an unusual mechanism of gene expression. Proc Natl Acad Sci U S A. 1985 May;82(9):2829–2833. doi: 10.1073/pnas.82.9.2829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Crozatier M., Vaury C., Busseau I., Pelisson A., Bucheton A. Structure and genomic organization of I elements involved in I-R hybrid dysgenesis in Drosophila melanogaster. Nucleic Acids Res. 1988 Oct 11;16(19):9199–9213. doi: 10.1093/nar/16.19.9199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Di Nocera P. P., Casari G. Related polypeptides are encoded by Drosophila F elements, I factors, and mammalian L1 sequences. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5843–5847. doi: 10.1073/pnas.84.16.5843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fanning T. G., Singer M. F. LINE-1: a mammalian transposable element. Biochim Biophys Acta. 1987 Dec 8;910(3):203–212. doi: 10.1016/0167-4781(87)90112-6. [DOI] [PubMed] [Google Scholar]
  15. Fawcett D. H., Lister C. K., Kellett E., Finnegan D. J. Transposable elements controlling I-R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs. Cell. 1986 Dec 26;47(6):1007–1015. doi: 10.1016/0092-8674(86)90815-9. [DOI] [PubMed] [Google Scholar]
  16. Gough J. A., Murray N. E. Sequence diversity among related genes for recognition of specific targets in DNA molecules. J Mol Biol. 1983 May 5;166(1):1–19. doi: 10.1016/s0022-2836(83)80047-3. [DOI] [PubMed] [Google Scholar]
  17. Humphrey T., Proudfoot N. J. A beginning to the biochemistry of polyadenylation. Trends Genet. 1988 Sep;4(9):243–245. doi: 10.1016/0168-9525(88)90028-5. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Kazazian H. H., Jr, Wong C., Youssoufian H., Scott A. F., Phillips D. G., Antonarakis S. E. Haemophilia A resulting from de novo insertion of L1 sequences represents a novel mechanism for mutation in man. Nature. 1988 Mar 10;332(6160):164–166. doi: 10.1038/332164a0. [DOI] [PubMed] [Google Scholar]
  21. Liu C. C., Simonsen C. C., Levinson A. D. Initiation of translation at internal AUG codons in mammalian cells. Nature. 1984 May 3;309(5963):82–85. doi: 10.1038/309082a0. [DOI] [PubMed] [Google Scholar]
  22. Mellor J., Fulton S. M., Dobson M. J., Wilson W., Kingsman S. M., Kingsman A. J. A retrovirus-like strategy for expression of a fusion protein encoded by yeast transposon Ty1. Nature. 1985 Jan 17;313(5999):243–246. doi: 10.1038/313243a0. [DOI] [PubMed] [Google Scholar]
  23. Mizrokhi L. J., Georgieva S. G., Ilyin Y. V. jockey, a mobile Drosophila element similar to mammalian LINEs, is transcribed from the internal promoter by RNA polymerase II. Cell. 1988 Aug 26;54(5):685–691. doi: 10.1016/s0092-8674(88)80013-8. [DOI] [PubMed] [Google Scholar]
  24. Morse B., Rotherg P. G., South V. J., Spandorfer J. M., Astrin S. M. Insertional mutagenesis of the myc locus by a LINE-1 sequence in a human breast carcinoma. Nature. 1988 May 5;333(6168):87–90. doi: 10.1038/333087a0. [DOI] [PubMed] [Google Scholar]
  25. Nitasaka E., Mukai T., Yamazaki T. Repressor of P elements in Drosophila melanogaster: Cytotype determination by a defective P element carrying only open reading frames 0 through 2. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7605–7608. doi: 10.1073/pnas.84.21.7605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Norrander J., Kempe T., Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. doi: 10.1016/0378-1119(83)90040-9. [DOI] [PubMed] [Google Scholar]
  27. Palmiter R. D. Magnesium precipitation of ribonucleoprotein complexes. Expedient techniques for the isolation of undergraded polysomes and messenger ribonucleic acid. Biochemistry. 1974 Aug 13;13(17):3606–3615. doi: 10.1021/bi00714a032. [DOI] [PubMed] [Google Scholar]
  28. Peabody D. S., Berg P. Termination-reinitiation occurs in the translation of mammalian cell mRNAs. Mol Cell Biol. 1986 Jul;6(7):2695–2703. doi: 10.1128/mcb.6.7.2695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Picard G., Bregliano J. C., Bucheton A., Lavige J. M., Pelisson A., Kidwell M. G. Non-mendelian female sterility and hybrid dysgenesis in Drosophila melanogaster. Genet Res. 1978 Nov;32(3):275–287. doi: 10.1017/s0016672300018772. [DOI] [PubMed] [Google Scholar]
  30. Picard G. Non-mendelian female sterility in Drosophila melanogaster: hereditary transmission of I factor. Genetics. 1976 May;83(1):107–123. doi: 10.1093/genetics/83.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Priimägi A. F., Mizrokhi L. J., Ilyin Y. V. The Drosophila mobile element jockey belongs to LINEs and contains coding sequences homologous to some retroviral proteins. Gene. 1988 Oct 30;70(2):253–262. doi: 10.1016/0378-1119(88)90197-7. [DOI] [PubMed] [Google Scholar]
  32. Pritchard M. A., Dura J. M., Pélisson A., Bucheton A., Finnegan D. J. A cloned I-factor is fully functional in Drosophila melanogaster. Mol Gen Genet. 1988 Nov;214(3):533–540. doi: 10.1007/BF00330491. [DOI] [PubMed] [Google Scholar]
  33. Pélisson A. The I--R system of hybrid dysgenesis in Drosophila melanogaster: are I factor insertions responsible for the mutator effect of the I--R interaction? Mol Gen Genet. 1981;183(1):123–129. doi: 10.1007/BF00270149. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Schwarz-Sommer Z., Leclercq L., Göbel E., Saedler H. Cin4, an insert altering the structure of the A1 gene in Zea mays, exhibits properties of nonviral retrotransposons. EMBO J. 1987 Dec 20;6(13):3873–3880. doi: 10.1002/j.1460-2075.1987.tb02727.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Simonelig M., Bazin C., Pelisson A., Bucheton A. Transposable and nontransposable elements similar to the I factor involved in inducer-reactive (IR) hybrid dysgenesis in Drosophila melanogaster coexist in various Drosophila species. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1141–1145. doi: 10.1073/pnas.85.4.1141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Skowronski J., Singer M. F. Expression of a cytoplasmic LINE-1 transcript is regulated in a human teratocarcinoma cell line. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6050–6054. doi: 10.1073/pnas.82.18.6050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Yannopoulos G., Stamatis N., Monastirioti M., Hatzopoulos P., Louis C. hobo is responsible for the induction of hybrid dysgenesis by strains of Drosophila melanogaster bearing the male recombination factor 23.5MRF. Cell. 1987 May 22;49(4):487–495. doi: 10.1016/0092-8674(87)90451-x. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES