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. 1987 Aug;84(16):5843–5847. doi: 10.1073/pnas.84.16.5843

Related polypeptides are encoded by Drosophila F elements, I factors, and mammalian L1 sequences.

P P Di Nocera, G Casari
PMCID: PMC298959  PMID: 2441397

Abstract

The structural organization of Drosophila F elements closely resembles that of L1 sequences, a major family of repetitive DNA elements dispersed in the genome of all mammals. Members of both families are flanked by target-site duplications of different length, vary in size because of heterogeneity at one end, and invariably terminate at the other end in characteristic adenosine-rich stretches often preceded by polyadenylylation signals. The nucleotide sequence of Fw, an F element found in the white locus of wi+A flies, reveals a large open reading frame upstream of the 3' adenosine-rich terminus encoding a possible reverse transcriptase homologous to those potentially encoded by functional L1 units and Drosophila I factors. A cysteine-rich region within an interrupted frame located at the 5' terminus of Fw suggests that complete F elements might additionally encode a nucleic acid binding protein. The observation that F elements and I factors encode functionally related polypeptides, and the extensive similarity of their hypothetical reverse transcriptases to L1 open reading frames, favors the hypothesis that all these sequences are evolutionarily related and transpose upon the cDNA conversion of RNA intermediates.

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Selected References

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  1. Bonitz S. G., Coruzzi G., Thalenfeld B. E., Tzagoloff A., Macino G. Assembly of the mitochondrial membrane system. Structure and nucleotide sequence of the gene coding for subunit 1 of yeast cytochrme oxidase. J Biol Chem. 1980 Dec 25;255(24):11927–11941. [PubMed] [Google Scholar]
  2. Burton F. H., Loeb D. D., Voliva C. F., Martin S. L., Edgell M. H., Hutchison C. A., 3rd Conservation throughout mammalia and extensive protein-encoding capacity of the highly repeated DNA long interspersed sequence one. J Mol Biol. 1986 Jan 20;187(2):291–304. doi: 10.1016/0022-2836(86)90235-4. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Dawid I. B., Long E. O., DiNocera P. P., Pardue M. L. Ribosomal insertion-like elements in Drosophila melanogaster are interspersed with mobile sequences. Cell. 1981 Aug;25(2):399–408. doi: 10.1016/0092-8674(81)90058-1. [DOI] [PubMed] [Google Scholar]
  5. Di Nocera P. P., Dawid I. B. Interdigitated arrangement of two oligo(A)-terminated DNA sequences in Drosophila. Nucleic Acids Res. 1983 Aug 25;11(16):5475–5482. doi: 10.1093/nar/11.16.5475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Di Nocera P. P., Digan M. E., Dawid I. B. A family of oligo-adenylate-terminated transposable sequences in Drosophila melanogaster. J Mol Biol. 1983 Aug 25;168(4):715–727. doi: 10.1016/s0022-2836(83)80071-0. [DOI] [PubMed] [Google Scholar]
  7. Di Nocera P. P., Graziani F., Lavorgna G. Genomic and structural organization of Drosophila melanogaster G elements. Nucleic Acids Res. 1986 Jan 24;14(2):675–691. doi: 10.1093/nar/14.2.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Emori Y., Shiba T., Kanaya S., Inouye S., Yuki S., Saigo K. The nucleotide sequences of copia and copia-related RNA in Drosophila virus-like particles. 1985 Jun 27-Jul 3Nature. 315(6022):773–776. doi: 10.1038/315773a0. [DOI] [PubMed] [Google Scholar]
  9. Fanning T., Singer M. The LINE-1 DNA sequences in four mammalian orders predict proteins that conserve homologies to retrovirus proteins. Nucleic Acids Res. 1987 Mar 11;15(5):2251–2260. doi: 10.1093/nar/15.5.2251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Finnegan D. J. Transposable elements in eukaryotes. Int Rev Cytol. 1985;93:281–326. doi: 10.1016/s0074-7696(08)61376-5. [DOI] [PubMed] [Google Scholar]
  12. Galibert F., Mandart E., Fitoussi F., Tiollais P., Charnay P. Nucleotide sequence of the hepatitis B virus genome (subtype ayw) cloned in E. coli. Nature. 1979 Oct 25;281(5733):646–650. doi: 10.1038/281646a0. [DOI] [PubMed] [Google Scholar]
  13. Gardner R. C., Howarth A. J., Hahn P., Brown-Luedi M., Shepherd R. J., Messing J. The complete nucleotide sequence of an infectious clone of cauliflower mosaic virus by M13mp7 shotgun sequencing. Nucleic Acids Res. 1981 Jun 25;9(12):2871–2888. doi: 10.1093/nar/9.12.2871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grimaldi G., Skowronski J., Singer M. F. Defining the beginning and end of KpnI family segments. EMBO J. 1984 Aug;3(8):1753–1759. doi: 10.1002/j.1460-2075.1984.tb02042.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hattori M., Kuhara S., Takenaka O., Sakaki Y. L1 family of repetitive DNA sequences in primates may be derived from a sequence encoding a reverse transcriptase-related protein. Nature. 1986 Jun 5;321(6070):625–628. doi: 10.1038/321625a0. [DOI] [PubMed] [Google Scholar]
  16. Inouye S., Yuki S., Saigo K. Complete nucleotide sequence and genome organization of a Drosophila transposable genetic element, 297. Eur J Biochem. 1986 Jan 15;154(2):417–425. doi: 10.1111/j.1432-1033.1986.tb09414.x. [DOI] [PubMed] [Google Scholar]
  17. Karess R. E., Rubin G. M. A small tandem duplication is responsible for the unstable white-ivory mutation in Drosophila. Cell. 1982 Aug;30(1):63–69. doi: 10.1016/0092-8674(82)90012-5. [DOI] [PubMed] [Google Scholar]
  18. Kleckner N. Transposable elements in prokaryotes. Annu Rev Genet. 1981;15:341–404. doi: 10.1146/annurev.ge.15.120181.002013. [DOI] [PubMed] [Google Scholar]
  19. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 1984 Jan 25;12(2):857–872. doi: 10.1093/nar/12.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Levis R., O'Hare K., Rubin G. M. Effects of transposable element insertions on RNA encoded by the white gene of Drosophila. Cell. 1984 Sep;38(2):471–481. doi: 10.1016/0092-8674(84)90502-6. [DOI] [PubMed] [Google Scholar]
  21. Loeb D. D., Padgett R. W., Hardies S. C., Shehee W. R., Comer M. B., Edgell M. H., Hutchison C. A., 3rd The sequence of a large L1Md element reveals a tandemly repeated 5' end and several features found in retrotransposons. Mol Cell Biol. 1986 Jan;6(1):168–182. doi: 10.1128/mcb.6.1.168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mossie K. G., Young M. W., Varmus H. E. Extrachromosomal DNA forms of copia-like transposable elements, F elements and middle repetitive DNA sequences in Drosophila melanogaster. Variation in cultured cells and embryos. J Mol Biol. 1985 Mar 5;182(1):31–43. doi: 10.1016/0022-2836(85)90025-7. [DOI] [PubMed] [Google Scholar]
  23. Pardue M. L., Dawid I. B. Chromosomal locations of two DNA segments that flank ribosomal insertion-like sequences in Drosophila: flanking sequences are mobile elements. Chromosoma. 1981;83(1):29–43. doi: 10.1007/BF00286014. [DOI] [PubMed] [Google Scholar]
  24. Rogers J. H. The origin and evolution of retroposons. Int Rev Cytol. 1985;93:187–279. doi: 10.1016/s0074-7696(08)61375-3. [DOI] [PubMed] [Google Scholar]
  25. Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
  26. Saigo K., Kugimiya W., Matsuo Y., Inouye S., Yoshioka K., Yuki S. Identification of the coding sequence for a reverse transcriptase-like enzyme in a transposable genetic element in Drosophila melanogaster. Nature. 1984 Dec 13;312(5995):659–661. doi: 10.1038/312659a0. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Scott M. P., Weiner A. J., Hazelrigg T. I., Polisky B. A., Pirrotta V., Scalenghe F., Kaufman T. C. The molecular organization of the Antennapedia locus of Drosophila. Cell. 1983 Dec;35(3 Pt 2):763–776. doi: 10.1016/0092-8674(83)90109-5. [DOI] [PubMed] [Google Scholar]
  30. Seiki M., Hattori S., Hirayama Y., Yoshida M. Human adult T-cell leukemia virus: complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3618–3622. doi: 10.1073/pnas.80.12.3618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Shiba T., Saigo K. Retrovirus-like particles containing RNA homologous to the transposable element copia in Drosophila melanogaster. Nature. 1983 Mar 10;302(5904):119–124. doi: 10.1038/302119a0. [DOI] [PubMed] [Google Scholar]
  32. Shinnick T. M., Lerner R. A., Sutcliffe J. G. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981 Oct 15;293(5833):543–548. doi: 10.1038/293543a0. [DOI] [PubMed] [Google Scholar]
  33. Singer M. F. Highly repeated sequences in mammalian genomes. Int Rev Cytol. 1982;76:67–112. doi: 10.1016/s0074-7696(08)61789-1. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Skowronski J., Singer M. F. The abundant LINE-1 family of repeated DNA sequences in mammals: genes and pseudogenes. Cold Spring Harb Symp Quant Biol. 1986;51(Pt 1):457–464. doi: 10.1101/sqb.1986.051.01.055. [DOI] [PubMed] [Google Scholar]
  36. Spradling A. C., Rubin G. M. Drosophila genome organization: conserved and dynamic aspects. Annu Rev Genet. 1981;15:219–264. doi: 10.1146/annurev.ge.15.120181.001251. [DOI] [PubMed] [Google Scholar]
  37. Tchurikov N. A., Naumova A. K., Zelentsova E. S., Georgiev G. P. A cloned unique gene of Drosophila melanogaster contains a repetitive 3' exon whose sequence is present at the 3' ends of many different mRNAs. Cell. 1982 Feb;28(2):365–373. doi: 10.1016/0092-8674(82)90354-3. [DOI] [PubMed] [Google Scholar]
  38. Tchurikov Nickolai A., Ebralidze Alexander K., Georgiev Georgii P. The suffix sequence is involved in processing the 3' ends of different mRNAs in Drosophila melanogaster. EMBO J. 1986 Sep;5(9):2341–2347. doi: 10.1002/j.1460-2075.1986.tb04502.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Toh H., Kikuno R., Hayashida H., Miyata T., Kugimiya W., Inouye S., Yuki S., Saigo K. Close structural resemblance between putative polymerase of a Drosophila transposable genetic element 17.6 and pol gene product of Moloney murine leukaemia virus. EMBO J. 1985 May;4(5):1267–1272. doi: 10.1002/j.1460-2075.1985.tb03771.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wilde C. D. Pseudogenes. CRC Crit Rev Biochem. 1986;19(4):323–352. [PubMed] [Google Scholar]
  41. Yuki S., Inouye S., Ishimaru S., Saigo K. Nucleotide sequence characterization of a Drosophila retrotransposon, 412. Eur J Biochem. 1986 Jul 15;158(2):403–410. doi: 10.1111/j.1432-1033.1986.tb09767.x. [DOI] [PubMed] [Google Scholar]
  42. Yuki S., Ishimaru S., Inouye S., Saigo K. Identification of genes for reverse transcriptase-like enzymes in two Drosophila retrotransposons, 412 and gypsy; a rapid detection method of reverse transcriptase genes using YXDD box probes. Nucleic Acids Res. 1986 Apr 11;14(7):3017–3030. doi: 10.1093/nar/14.7.3017. [DOI] [PMC free article] [PubMed] [Google Scholar]

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