Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1985 Jul;5(7):1630–1638. doi: 10.1128/mcb.5.7.1630

Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins.

S M Mount, G M Rubin
PMCID: PMC367281  PMID: 2410772

Abstract

We have determined the complete nucleotide sequence of the copia element present at the white-apricot allele of the white locus in Drosophila melanogaster. This transposable element is 5,146 nucleotides long and contains a single long open reading frame of 4,227 nucleotides. Analysis of the coding potential of the large open reading frame, which appears to encode a polyprotein, revealed weak homology to a number of retroviral proteins, including a protease, nucleic acid-binding protein, and reverse transcriptase. Better homology existed between another part of the copia open reading frame and a region of the retroviral pol gene recently shown to be distinct from reverse transcriptase and required for the integration of circular DNA forms of the retroviral genome to form proviruses. Comparison of the copia sequence with those of the Saccharomyces cerevisiae transposable element Ty, several vertebrate retroviruses, and the D. melanogaster copia-like element 17.6 showed that Ty was most similar to copia, sharing amino acid sequence homology and organizational features not found in the other genetic elements.

Full text

PDF
1630

Selected References

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

  1. Bayev A. A., Jr, Lyubomirskaya N. V., Dzhumagaliev E. B., Ananiev E. V., Amiantova I. G., Ilyin Y. V. Structural organization of transposable element mdg4 from Drosophila melanogaster and a nucleotide sequence of its long terminal repeats. Nucleic Acids Res. 1984 Apr 25;12(8):3707–3723. doi: 10.1093/nar/12.8.3707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bender W., Akam M., Karch F., Beachy P. A., Peifer M., Spierer P., Lewis E. B., Hogness D. S. Molecular Genetics of the Bithorax Complex in Drosophila melanogaster. Science. 1983 Jul 1;221(4605):23–29. doi: 10.1126/science.221.4605.23. [DOI] [PubMed] [Google Scholar]
  3. Bingham P. M., Judd B. H. A copy of the copia transposable element is very tightly linked to the Wa allele at the white locus of D. melanogaster. Cell. 1981 Sep;25(3):705–711. doi: 10.1016/0092-8674(81)90177-x. [DOI] [PubMed] [Google Scholar]
  4. Bingham P. M., Levis R., Rubin G. M. Cloning of DNA sequences from the white locus of D. melanogaster by a novel and general method. Cell. 1981 Sep;25(3):693–704. doi: 10.1016/0092-8674(81)90176-8. [DOI] [PubMed] [Google Scholar]
  5. Boeke J. D., Garfinkel D. J., Styles C. A., Fink G. R. Ty elements transpose through an RNA intermediate. Cell. 1985 Mar;40(3):491–500. doi: 10.1016/0092-8674(85)90197-7. [DOI] [PubMed] [Google Scholar]
  6. Carlson M., Brutlag D. One of the copia genes is adjacent to satellite DNA in Drosophila melanogaster. Cell. 1978 Nov;15(3):733–742. doi: 10.1016/0092-8674(78)90259-3. [DOI] [PubMed] [Google Scholar]
  7. Chiu I. M., Callahan R., Tronick S. R., Schlom J., Aaronson S. A. Major pol gene progenitors in the evolution of oncoviruses. Science. 1984 Jan 27;223(4634):364–370. doi: 10.1126/science.6197754. [DOI] [PubMed] [Google Scholar]
  8. Copeland N. G., Hutchison K. W., Jenkins N. A. Excision of the DBA ecotropic provirus in dilute coat-color revertants of mice occurs by homologous recombination involving the viral LTRs. Cell. 1983 Jun;33(2):379–387. doi: 10.1016/0092-8674(83)90419-1. [DOI] [PubMed] [Google Scholar]
  9. Copeland T. D., Oroszlan S., Kalyanaraman V. S., Sarngadharan M. G., Gallo R. C. Complete amino acid sequence of human T-cell leukemia virus structural protein p15. FEBS Lett. 1983 Oct 17;162(2):390–395. doi: 10.1016/0014-5793(83)80793-5. [DOI] [PubMed] [Google Scholar]
  10. Dente L., Cesareni G., Cortese R. pEMBL: a new family of single stranded plasmids. Nucleic Acids Res. 1983 Mar 25;11(6):1645–1655. doi: 10.1093/nar/11.6.1645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Devare S. G., Reddy E. P., Law J. D., Robbins K. C., Aaronson S. A. Nucleotide sequence of the simian sarcoma virus genome: demonstration that its acquired cellular sequences encode the transforming gene product p28sis. Proc Natl Acad Sci U S A. 1983 Feb;80(3):731–735. doi: 10.1073/pnas.80.3.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Donehower L. A., Varmus H. E. A mutant murine leukemia virus with a single missense codon in pol is defective in a function affecting integration. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6461–6465. doi: 10.1073/pnas.81.20.6461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Duyk G., Leis J., Longiaru M., Skalka A. M. Selective cleavage in the avian retroviral long terminal repeat sequence by the endonuclease associated with the alpha beta form of avian reverse transcriptase. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6745–6749. doi: 10.1073/pnas.80.22.6745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Elder R. T., Loh E. Y., Davis R. W. RNA from the yeast transposable element Ty1 has both ends in the direct repeats, a structure similar to retrovirus RNA. Proc Natl Acad Sci U S A. 1983 May;80(9):2432–2436. doi: 10.1073/pnas.80.9.2432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Falkenthal S., Graham M. L., Korn E. L., Lengyel J. A. Transcription, processing, and turnover of RNA from the Drosophila mobile genetic element copia. Dev Biol. 1982 Aug;92(2):294–305. doi: 10.1016/0012-1606(82)90176-2. [DOI] [PubMed] [Google Scholar]
  16. Falkenthal S., Lengyel J. A. Structure, translation, and metabolism of the cytoplasmic copia ribonucleic acid of Drosophila melanogaster. Biochemistry. 1980 Dec 9;19(25):5842–5850. doi: 10.1021/bi00566a028. [DOI] [PubMed] [Google Scholar]
  17. Flavell A. J., Ish-Horowicz D. Extrachromosomal circular copies of the eukaryotic transposable element copia in cultured Drosophila cells. Nature. 1981 Aug 13;292(5824):591–595. doi: 10.1038/292591a0. [DOI] [PubMed] [Google Scholar]
  18. Flavell A. J., Ish-Horowicz D. The origin of extrachromosomal circular copia elements. Cell. 1983 Sep;34(2):415–419. doi: 10.1016/0092-8674(83)90375-6. [DOI] [PubMed] [Google Scholar]
  19. Flavell A. J., Levis R., Simon M. A., Rubin G. M. The 5' termini of RNAs encoded by the transposable element copia. Nucleic Acids Res. 1981 Dec 11;9(23):6279–6291. doi: 10.1093/nar/9.23.6279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Flavell A. J. Role of reverse transcription in the generation of extrachromosomal copia mobile genetic elements. Nature. 1984 Aug 9;310(5977):514–516. doi: 10.1038/310514a0. [DOI] [PubMed] [Google Scholar]
  21. Flavell A. J., Ruby S. W., Toole J. J., Roberts B. E., Rubin G. M. Translation and developmental regulation of RNA encoded by the eukaryotic transposable element copia. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7107–7111. doi: 10.1073/pnas.77.12.7107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fouts D. L., Manning J. E., Fox G. M., Schmid C. W. A complex repeated DNA sequence within the Drosophila transposable element copia. Nucleic Acids Res. 1981 Dec 21;9(24):7053–7064. doi: 10.1093/nar/9.24.7053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Freund R., Meselson M. Long terminal repeat nucleotide sequence and specific insertion of the gypsy transposon. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4462–4464. doi: 10.1073/pnas.81.14.4462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gehring W. J., Paro R. Isolation of a hybrid plasmid with homologous sequences to a transposing element of Drosophila melanogaster. Cell. 1980 Apr;19(4):897–904. doi: 10.1016/0092-8674(80)90081-1. [DOI] [PubMed] [Google Scholar]
  25. Gibson W., Verma I. M. Studies on the reverse transcriptase of RNA tumor viruses. Structural relatedness of two subunits of avian RNA tumor viruses. Proc Natl Acad Sci U S A. 1974 Dec;71(12):4991–4994. doi: 10.1073/pnas.71.12.4991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Goldberg M. L., Paro R., Gehring W. J. Molecular cloning of the white locus region of Drosophila melanogaster using a large transposable element. EMBO J. 1982;1(1):93–98. doi: 10.1002/j.1460-2075.1982.tb01130.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Goldberg M. L., Sheen J. Y., Gehring W. J., Green M. M. Unequal crossing-over associated with asymmetrical synapsis between nomadic elements in the Drosophila melanogaster genome. Proc Natl Acad Sci U S A. 1983 Aug;80(16):5017–5021. doi: 10.1073/pnas.80.16.5017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Grandgenett D. P., Vora A. C., Schiff R. D. A 32,000-dalton nucleic acid-binding protein from avian retravirus cores possesses DNA endonuclease activity. Virology. 1978 Aug;89(1):119–132. doi: 10.1016/0042-6822(78)90046-6. [DOI] [PubMed] [Google Scholar]
  29. Grantham R., Gautier C., Gouy M., Jacobzone M., Mercier R. Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res. 1981 Jan 10;9(1):r43–r74. doi: 10.1093/nar/9.1.213-b. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Herr W., Corbin V., Gilbert W. Nucleotide sequence of the 3' half of AKV. Nucleic Acids Res. 1982 Nov 11;10(21):6931–6944. doi: 10.1093/nar/10.21.6931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hutchison K. W., Copeland N. G., Jenkins N. A. Dilute-coat-color locus of mice: nucleotide sequence analysis of the d+2J and d+Ha revertant alleles. Mol Cell Biol. 1984 Dec;4(12):2899–2904. doi: 10.1128/mcb.4.12.2899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ilyin Y. V., Schuppe N. G., Lyubomirskaya N. V., Gorelova T. V., Arkhipova I. R. Circular copies of mobile dispersed genetic elements in cultured Drosophila melanogaster cells. Nucleic Acids Res. 1984 Oct 11;12(19):7517–7531. doi: 10.1093/nar/12.19.7517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. James M. N. An X-ray crystallographic approach to enzyme structure and function. Can J Biochem. 1980 Apr;58(4):252–271. [PubMed] [Google Scholar]
  34. Kamer G., Argos P. Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses. Nucleic Acids Res. 1984 Sep 25;12(18):7269–7282. doi: 10.1093/nar/12.18.7269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kozak M. How do eukaryotic ribosomes recognize the unique AUG initiator codon in messenger RNA? Biochem Soc Symp. 1982;47:113–128. [PubMed] [Google Scholar]
  36. Kugimiya W., Ikenaga H., Saigo K. Close relationship between the long terminal repeats of avian leukosis-sarcoma virus and copia-like movable genetic elements of Drosophila. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3193–3197. doi: 10.1073/pnas.80.11.3193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  38. Levis R., Bingham P. M., Rubin G. M. Physical map of the white locus of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1982 Jan;79(2):564–568. doi: 10.1073/pnas.79.2.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Levis R., Dunsmuir P., Rubin G. M. Terminal repeats of the Drosophila transposable element copia: nucleotide sequence and genomic organization. Cell. 1980 Sep;21(2):581–588. doi: 10.1016/0092-8674(80)90496-1. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Lipman D. J., Pearson W. R. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. doi: 10.1126/science.2983426. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. Misra T. K., Grandgenett D. P., Parsons J. T. Avian retrovirus pp32 DNA-binding protein. I. Recognition of specific sequences on retrovirus DNA terminal repeats. J Virol. 1982 Oct;44(1):330–343. doi: 10.1128/jvi.44.1.330-343.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Modolell J., Bender W., Meselson M. Drosophila melanogaster mutations suppressible by the suppressor of Hairy-wing are insertions of a 7.3-kilobase mobile element. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1678–1682. doi: 10.1073/pnas.80.6.1678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Needleman S. B., Wunsch C. D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 1970 Mar;48(3):443–453. doi: 10.1016/0022-2836(70)90057-4. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. O'Hare K., Murphy C., Levis R., Rubin G. M. DNA sequence of the white locus of Drosophila melanogaster. J Mol Biol. 1984 Dec 15;180(3):437–455. doi: 10.1016/0022-2836(84)90021-4. [DOI] [PubMed] [Google Scholar]
  49. Panganiban A. T., Temin H. M. Circles with two tandem LTRs are precursors to integrated retrovirus DNA. Cell. 1984 Mar;36(3):673–679. doi: 10.1016/0092-8674(84)90347-7. [DOI] [PubMed] [Google Scholar]
  50. Panganiban A. T., Temin H. M. The retrovirus pol gene encodes a product required for DNA integration: identification of a retrovirus int locus. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7885–7889. doi: 10.1073/pnas.81.24.7885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Pirrotta V., Bröckl C. Transcription of the Drosophila white locus and some of its mutants. EMBO J. 1984 Mar;3(3):563–568. doi: 10.1002/j.1460-2075.1984.tb01847.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Potter S. S., Brorein W. J., Jr, Dunsmuir P., Rubin G. M. Transposition of elements of the 412, copia and 297 dispersed repeated gene families in Drosophila. Cell. 1979 Jun;17(2):415–427. doi: 10.1016/0092-8674(79)90168-5. [DOI] [PubMed] [Google Scholar]
  53. Redmond S. M., Dickson C. Sequence and expression of the mouse mammary tumour virus env gene. EMBO J. 1983;2(1):125–131. doi: 10.1002/j.1460-2075.1983.tb01393.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Rho H. M., Grandgenett D. P., Green M. Sequence relatedness between the subunits of avian myeloblastosis virus reverse transcriptase. J Biol Chem. 1975 Jul 10;250(13):5278–5280. [PubMed] [Google Scholar]
  55. Rubin G. M., Kidwell M. G., Bingham P. M. The molecular basis of P-M hybrid dysgenesis: the nature of induced mutations. Cell. 1982 Jul;29(3):987–994. doi: 10.1016/0092-8674(82)90462-7. [DOI] [PubMed] [Google Scholar]
  56. 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]
  57. 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]
  58. Scherer G., Tschudi C., Perera J., Delius H., Pirrotta V. B104, a new dispersed repeated gene family in Drosophila melanogaster and its analogies with retroviruses. J Mol Biol. 1982 May 25;157(3):435–451. doi: 10.1016/0022-2836(82)90470-3. [DOI] [PubMed] [Google Scholar]
  59. 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]
  60. Schwartz H. E., Lockett T. J., Young M. W. Analysis of transcripts from two families of nomadic DNA. J Mol Biol. 1982 May 5;157(1):49–68. doi: 10.1016/0022-2836(82)90512-5. [DOI] [PubMed] [Google Scholar]
  61. Schwartzberg P., Colicelli J., Goff S. P. Construction and analysis of deletion mutations in the pol gene of Moloney murine leukemia virus: a new viral function required for productive infection. Cell. 1984 Jul;37(3):1043–1052. doi: 10.1016/0092-8674(84)90439-2. [DOI] [PubMed] [Google Scholar]
  62. 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]
  63. Shepherd B. M., Finnegan D. J. Structure of circular copies of the 412 transposable element present in Drosophila melanogaster tissue culture cells, and isolation of a free 412 long terminal repeat. J Mol Biol. 1984 Nov 25;180(1):21–40. doi: 10.1016/0022-2836(84)90428-5. [DOI] [PubMed] [Google Scholar]
  64. 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]
  65. 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]
  66. Shoemaker C., Hoffman J., Goff S. P., Baltimore D. Intramolecular integration within Moloney murine leukemia virus DNA. J Virol. 1981 Oct;40(1):164–172. doi: 10.1128/jvi.40.1.164-172.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Snyder M. P., Kimbrell D., Hunkapiller M., Hill R., Fristrom J., Davidson N. A transposable element that splits the promoter region inactivates a Drosophila cuticle protein gene. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7430–7434. doi: 10.1073/pnas.79.23.7430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Staden R., McLachlan A. D. Codon preference and its use in identifying protein coding regions in long DNA sequences. Nucleic Acids Res. 1982 Jan 11;10(1):141–156. doi: 10.1093/nar/10.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Sweet H. O. Dilute suppressor, a new suppressor gene in the house mouse. J Hered. 1983 Jul-Aug;74(4):305–306. doi: 10.1093/oxfordjournals.jhered.a109794. [DOI] [PubMed] [Google Scholar]
  70. Temin H. M. Origin of retroviruses from cellular moveable genetic elements. Cell. 1980 Oct;21(3):599–600. doi: 10.1016/0092-8674(80)90420-1. [DOI] [PubMed] [Google Scholar]
  71. Toh H., Hayashida H., Miyata T. Sequence homology between retroviral reverse transcriptase and putative polymerases of hepatitis B virus and cauliflower mosaic virus. 1983 Oct 27-Nov 2Nature. 305(5937):827–829. doi: 10.1038/305827a0. [DOI] [PubMed] [Google Scholar]
  72. Varmus H. E., Quintrell N., Ortiz S. Retroviruses as mutagens: insertion and excision of a nontransforming provirus alter expression of a resident transforming provirus. Cell. 1981 Jul;25(1):23–36. doi: 10.1016/0092-8674(81)90228-2. [DOI] [PubMed] [Google Scholar]
  73. Weiher H., König M., Gruss P. Multiple point mutations affecting the simian virus 40 enhancer. Science. 1983 Feb 11;219(4585):626–631. doi: 10.1126/science.6297005. [DOI] [PubMed] [Google Scholar]
  74. Winston F., Chaleff D. T., Valent B., Fink G. R. Mutations affecting Ty-mediated expression of the HIS4 gene of Saccharomyces cerevisiae. Genetics. 1984 Jun;107(2):179–197. doi: 10.1093/genetics/107.2.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Young M. W., Schwartz H. E. Nomadic gene families in Drosophila. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 2):629–640. doi: 10.1101/sqb.1981.045.01.081. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES