Abstract
A major component of Drosophila telomeres is the retrotransposonHeT-A, which is clearly related to other retrotransposons and retroviruses. This retrotransposon is distinguished by its exclusively telomeric location, and by the fact that, unlike other retrotransposons, it does not encode its own reverse transcriptase.HeT-A coding sequences diverge significantly, even between elements within the same genome. Such rapid divergence has been noted previously in studies ofgag genes from other retroelements. Sequence comparisons indicate that the entireHeT-A coding region codes forgag protein, with regions of similarity to other insect retrotransposongag proteins found throughout the open reading frame (ORF). Similarity is most striking in the zinc knuckle region, a region characteristic ofgag genes of most replication-competent retroelements. We identify a subgroup of insect non-LTR retrotransposons with three zinc knuckles of the form: (1) CX2CX4HX4C, (2) CX2CX3HX4C, (3) CX2CX3HX6C. The first and third knuckles are invariant, but the second shows some differences between members of this subgroup. This subgroup includesHeT-A and a second Drosophila telomeric retrotransposon,TART. Unlike other gag regions,HeT-A requires a −1 frameshift for complete translation. Such frameshifts are common between thegag andpol sequences of retroviruses but have not before been seen within agag sequence. The frameshift allowsHeT-A to encode two polypeptides; this mechanism may substitute for the post-translational cleavage that creates multiplegag polypeptides in retroviruses.D. melanogaster HeT-A coding sequences have a polymorphic region with insertions/deletions of 1–31 codons and many nucleotide changes. None of these changes interrupt the open reading frame, arguing that only elements with translatable ORFs can be incorporated into the chromosomes. PerhapsHeT-A translation products act incis to target the RNA to chromosome ends.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Biessmann H, Champion LE, O'Hare M, Ikenaga K, Kasravi B, Mason JM (1992) Frequent transpositions of Drosophila melanogaster HeT-A transposable elements to receding chromosome ends. EMBO J 11:4495–4469
Biessmann H, Kasravi B, Bui T, Fujiwara G, Champion LE, Mason JM (1994) Comparison of two active Het-A retroposons of Drosophila melanogaster. Chromosoma 103:90–98
Boeke JD, Corces VG (1989) Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol 43:403–424
Corpet F (1988) Multiple sequence alignment with hierarchial clustering. Nucleic Acids Res 16:10881–10890
Covey SN (1986) Amino acid sequence homology in gag region of reverse transcribing elements and the coat protein gene of cauliflower mosaic virus. Nucleic Acids Res 14:623–633
Danilevskaya ON, Lapta GE (1991) Long telomeres in the polytene chromosomes ofDrosophila melanogaster are associated with amplification of subtelomeric repeat sequences. Genet Sel Evol 23:15–24
Danilevskaya ON, Petrov DA, Pavlova MA, Koga A, Kurenova EV, Hartl DL (1992) A repetitive DNA element, associated with telomeric sequences inDrosophila melanogaster, contains open reading frames. Chromsoma 102:32–40
Danilevskaya ON, Slot F, Pavlova M, Pardue ML (1994a) Structure of the Drosophila HeT-A transposon: a retrotransposon-like element forming telomeres. Chromosoma 103:215–224
Danilevskaya ON, Slot F, Traverse KL, Hogan NC, Pardue ML (1994b) The Drosophila telomere transposon HeT-A produces a transcript with tightly bound protein. Proc Natl Acad Sci USA 91:6679–6682
Devereux J, Haberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395
Doolittle RF, Feng D-F, Johnson MS, McClure MA (1989) Origins and evolutionary relationships of retroviruses. Q Rev Biol 64:1–30
Eickbush TH (1994) Origin and evolutionary relationships of retroelements. In: Morse SS (ed) The evolutionary biology of viruses. Raven Press, New York, pp 121–157
Fuetterer J, Hohn T (1987) Involvement of nucleocapsids in reverse transcription: a general phenomenon? Trends Biochem Sci 12:92–95
Furano AV, Robb SM, Robb FT (1988) The structure of the regulatory region of the rat L1 (L1Rn, long interspersed repeated) DNA family of transposable elements. Nucleic Acids Res 16:9215–9231
Hansen LJ, Chalker DL, Orlinsky KJ, Sandemeyer SB (1992) Ty3 GAG3 and POL3 genes encode the components of intracellular particles. J Virol 66:1414–1424
Hogan NC, Traverse KL, Sullivan DE, Pardue ML (1994) The nucleus-limited Hsr-omega-1 transcript is a polyadenylated RNA with a regulated intranuclear turnover. J Cell Biol 125:21–30
Lindsley DL, Zimm GG (1992) The genome ofDrosophila melanogaster. Academic Press, San Diego, CA
Loeb DD, Pagett RW, Hardies SC, Shehee WR, Corner MB, Edgell MH, Hutchison CA III (1986) The sequence of a large L1md element reveals a tandemly repeated 5′ end and several features found in retrotransposons. Mol Cell Biol 6:168–172
Luan DD, Korman MH, Jakubczak JL, Eickbush TH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72:595–605
McClure MA, Johnson MS, Feng D-F, Doolittle RF (1988) Sequence comparisons of retroviral proteins: relative rates of change and general phylogeny. Proc Natl Acad Sci USA 85:2467–2473
Pardue ML (1995) Drosophila telomeres: another way to end it all. In: Greider C, Blackburn E (eds) Telomeres. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 339–370
Pardue ML, Dawid IB (1981) Chromosomal locations of two DNA segments that flank ribosomal insertion-like sequences in Drosophila: flanking sequences are mobile elements. Chromosoma 83:29–43
Pardue ML, Danilevskaya ON, Lowenhaupt K, Slot F, Traverse KL (1996) Drosophila telomeres: new views on chromosome evolution. Trends Genet 12:48–52
Schickman SA, Severynse DM, Edgell MH, Hutchinson CA III (1992) Strand-specific LINE-1 transcription in mouse F-9 cells originates from the youngest phylogenetic subgroup of LINE-1 elements. J Mol Biol 224:550–574
Schneider I (1972) Cell lines derived from late embryonic stages ofDrosophila melanogaster. J Embryol Exp Morph 27:353–365
Schneider I, Blumenthal AB (1978) Drosophila cell and tissue culture. In: Ashburner M, Wright TRF (eds) The genetics and biology of Drosophila, vol 2a. Academic Press, London, pp. 265–315
Schwarz-Sommer Z, Leclerq L, Gobel E, Saedler H (1987) Cin4, an insert altering the structure of the A1 gene in zea mays, exhibits properties of non-viral retrotransposons. EMBO J 6:3873–3880
Sheen F-m, Levis RW (1994) Transposition of the LINE-like retro-transposon TART to Drosophila chromsome termini. Proc Natl Acad Sci USA 91:12510–12514
Summers MF, South TI, Kim B, Hare DR (1990) High-resolution structure of an HIV finger-like domain via a new NMR-based distance geometry approach. Biochemistry 29:329–340
Valgeisdottir K, Traverse KL, Pardue ML (1990) HeT DNA: a family of mosaic repeated sequences specific for heterochromatin in Drosophila melanogaster. Proc Natl Acad Sci USA 87:7998–8002
Varmus H (1988) Retroviruses. Science 240:1427–1435
Varmus H, Brown P (1989) Retroviruses. In: Berg D, Howe MM (eds) Mobile DNA. Am Soc Microbiol, Washington, DC, pp 53–108
Wills JW, Craven RC (1991) Form, function, and use of retroviral Gag proteins. AIDS 5:639–654
Winker P, Maurin V, Roizes G (1987) Unrelated sequences at the 5′ end of mouse LINE-1 repeated elements define two distinct subfamilies. Nucleic Acids Res 15:8593–8606
Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362
Young BS, Pession A, Traverse KL, French C, Pardue ML (1983) Telomere regions in Drosophila share complex DNA sequences with pericentric heterochromatin. Cell 34:85–94
Zakian VA (1989) Structure and function of telomeres. Annu Rev Genet 23:579–604
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Pardue, ML., Danilevskaya, O.N., Lowenhaupt, K. et al. Thegag coding region of theDrosophila telomeric retrotransposon,HeT-A, has an internal frame shift and a length polymorphic region. J Mol Evol 43, 572–583 (1996). https://doi.org/10.1007/BF02202105
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DOI: https://doi.org/10.1007/BF02202105