Abstract
We established the size distribution of extrachromosomal covalently closed circular DNA molecules from embryos of various Drosophila melanogaster strains and from Kc0% tissue culture cells. In embryos, more than 80% of the circular DNA molecules are smaller than 2.5 kb and all the distributions show a peak of molecules of between 200 and 400 bp. The Kc0% cell distribution differs mainly from that of embryos in that 48% of the molecules have a size between 4 and 8 kb. Correlating with this, circular molecules homologous to copia, 412 and 297 were detected only in Kc0% cells. The three tandemly repeated families containing the 5S genes, the histone genes and the 240 bp repeat of the ribosomal DNA intergenic spacer, which had previously been identified in circular DNAs from embryos, were also found in cultured cells. A fourth tandemly repeated family corresponding to the 1.688 g/cm3 satellite DNA was detected, both in embryos and Kc0% cells. It consists of circular multimeric molecules containing multiple copies of the 359 bp repeated unit. No circular DNA molecules homologous to the actin genes, the type I ribosomal DNA insertion, or the F and I transposable elements were found in embryos or Kc0% cells. Thus it appears that the extrachromosomal circular DNA molecules from embryos and from tissue culture cells differ mainly in the presence of circular copies of the copia-like transposable elements.
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References
Bregliano JC, Kidwell MG (1983) Hybrid dysgenesis determinants. In: Shapiro JA (ed) Mobile genetic elements. Academic Press, New York, pp 363–410
Bucheton A, Paro R, Sang HM, Pelisson A, Finnegan DJ (1984) The molecular basis of I-R hybrid dysgenesis in Drosophila melanogaster: Identification, cloning and properties of the I factor. Cell 38:153–163
Carlson M, Brutlag D (1977) Cloning and characterization of a complex satellite DNA from Drosophila melanogaster. Cell 11:371–381
Couderc JL, Sobrier ML, Giraud G, Becker JL, Dastugue B (1983) Actin gene expression is modulated by ecdysterone in a Drosophila cell line. J Mol Biol 164:419–430
Davis RW, Simon M, Davidson N (1971) Electron microscope heteroduplex methods for mapping regions of base sequence homology in nucleic acids. Methods Enzymol 21:413–428
Devenish RJ, Newlon CS (1982) Isolation and characterization of yeast ring chromosome III by a method applicable to other circular DNAs. Gene 18:277–288
Di-Nocera PP, Digan NE, Dawid IB (1983) A family of oligoadenylate-terminated transposable sequences in Drosophila melanogaster. J Mol Biol 168:715–727
Dunsmuir P, Brorein WJ, Simon MA, Rubin GM (1980) Insertion of the Drosophila transposable element copia generates a 5 base pair duplication. Cell 21:575–579
Echalier G (1976) In vitro established lines of Drosophila cells and applications in physiological genetics. In: Kurstack E, Maramorosch K (eds) Invertebrate tissue culture. Academic Press, New York, pp 131–150
Finnegan DJ, Fawcet DH (1986) Transposable elements in Drosophila melanogaster. In: McLean N (ed) Oxford surveys on eukaryotic genes, vol 3. Oxford University Press, pp 1–62
Flavell AJ, Ish-Horowicz D (1981) Extrachromosomal circular copies of the eukaryotic transposable element copia in cultured Drosophila cells. Nature 292:591–595
Flavell AJ, Ish-Horowicz D (1983) The origin of extrachromosomal circular copia elements. Cell 34:415–419
Flores SC, Sunnerhagen P, Kay Moore T, Gaubatz J (1988) Characterization of repetitive sequence families in mouse heart small polydisperse circular DNAs: age related studies. Nucleic Acids Res 16:3889–3906
Hollis M, Hindley J (1986) Human Sau3A repeated DNA is enriched in small polydisperse circular DNA from normal lymphocytes. Gene 46:153–160
Ilyin YV, Schuppe NG, Lyubomirskaya NV, Gorelova TV, Arkhipova IR (1984) Circular copies of mobile dispersed genetic elements in Drosophila melanogaster cells. Nucleic Acids Res 12 19:7517–7531
Jones RS, Potter SS (1985) Characterization of cloned human alphoid satellite with an unusual monomeric construction: evidence for enrichment in HeLa small polydisperse circular DNA. Nucleic Acids Res 13:1027–1042
Junakovic N, Ballario P (1984) Circular extrachromosomal copialike transposable elements in Drosophila tissue culture cells. Plasmid 11:109–115
Junakovic N, DiFranco C, Best-Belpomme M, Echalier G (1988) On the transposition of copia-like nomadic elements in Drosophila cultured cells. Chromosoma 97:212–218
Kidd SJ, Glover DM (1980) A DNA segment from D. melanogaster which contains five tandemly repeating units homologous to the major rDNA insertion. Cell 19:103–119
Kiyama R, Okumura K, Matsui H, Brun GAP, Kanda M, Oishi M (1987) Nature of recombination involved in excision and rearrangement of human repetitive DNA. J Mol Biol 198:589–598
Kraszewska EK, Bjerknes CA, Lamm SS, Van't Hof J (1985) Extrachromosomal DNA of pea-root (Pisum sativum) has repeated sequences and ribosomal genes. Plant Mol Biol 5:353–361
Kugimiya W, Ikenaga H, Saigo K (1983) Close relationship between the long terminal repeats of avian leukosis-sarcoma virus and copia-like movable genetic elements of Drosophila. Proc Natl Acad Sci USA 80:3193–3197
Kunisada T, Yamagishi H (1987) Sequence organization of repetitive sequences enriched in small polydisperse circular DNAs from HeLa cells. J Mol Biol 198:557–565
Lohe AR, Brutlag DL (1986) Multiplicity of satellite DNA sequences in Drosophila melanogaster. Proc Natl Acad Sci USA 83:696–700
Long EO, Dawid IB (1979) Expression of ribosomal DNA insertions in Drosophila melanogaster. Cell 18:1185–1196
Micard D, Sobrier ML, Couderc JL, Dastugue B (1985) Purification of RNA-free plasmid DNA using alkaline extraction followed by Ultrogel A2 column chromatography. Anal Biochem 148:121–126
Micard D, Couderc JL, Sobrier ML, Giraud G, Dastugue B (1988) Molecular study of the retrovirus-like transposable element 412, a 20-OH ecdysone responsive repetitive sequence in Drosophila cultured cells. Nucleic Acids Res 16:455–470
Misra R, Shih A, Rush M, Wong E, Schmid CW (1987) Cloned extrachromosomal circular DNA copies of the human transposable element THE-1 are related predominantly to a single type of family member. J Mol Biol 196:233–243
Mossie KG, Young MW, Varmus HE (1985) Extrachromosomal DNA forms of copia-like transposable elements, F elements and middle repetitive DNA sequences in Drosophila melanogaster. J Mol Biol 182:31–43
Peronnet F, Becker JL, Becker J, D'Auriol L, Galibert F, Best-Belpomme M (1986) 1731, a new transposon with hormone modulated expression. Nucleic Acids Res 14:9017–9033
Pont G, Degroote F, Picard G (1987) Some extrachromosomal circular DNAs from Drosophila embryos are homologous to tandemly repeated genes. J Mol Biol 195:447–451
Pont G, Degroote F, Picard G (1988) Illegitimate recombination in the histone multigenic family generates circular DNAs in Drosophila embryos. Nucleic Acids Res 16:8817–8833
Potter SS, Brorein WJ, Dunsmuir P, Rubin GM (1979) Transposition of elements of the 412, copia and 297 dispersed repeated gene families in Drosophila. Cell 17:415–427
Rush MG, Misra R (1985) Extrachromosomal DNA in eucaryotes. Plasmid 14:177–191
Schindler CW, Rush MG (1985) Discrete size classes of monkey extrachromosomal circular DNA containing the L1 family of long interspersed nucleotide sequences are produced by a general non-sequence specific mechanism. Nucleic Acids Res 13:8247–8258
Shepherd BM, Finnegan DJ (1984) 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 180:21–40
Stanfield SW, Helinski DR (1976) Small circular DNA in Drosophila melanogaster. Cell 9:333–345
Stanfield SW, Helinski DR (1986) Multiple mechanisms generate extrachromosomal circular DNA in Chinese hamster ovary cells. Nucleic Acids Res 14 8:3527–3538
Stanfield SW, Lengyel JA (1979) Small circular DNA of Drosophila melanogaster: chromosomal homology and kinetic complexity. Proc Natl Acad Sci USA 76:6142–6146
Sundaresan V, Freeling M (1987) An extrachromosomal form of the Mu transposons of maize. Proc Natl Acad Sci USA 84:4924–4928
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Degroote, F., Pont, G., Micard, D. et al. Extrachromosomal circular DNAs in Drosophila melanogaster: Comparison between embryos and Kc0% cells. Chromosoma 98, 201–206 (1989). https://doi.org/10.1007/BF00329684
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DOI: https://doi.org/10.1007/BF00329684