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Spatially regulated expression of retrovirus-like transposons during Drosophila melanogaster embryogenesis

Published online by Cambridge University Press:  14 April 2009

Dali Ding  and
Howard D. Lipshitz
Dali Ding
Affiliation:
Division of Biology 156-29, California Institute of Technology, Pasadena, California 91125, U.S.A. Phone: 818-395-6446, Fax: 818-564-8709, E-mail: LipshitzH@Starbasel.caltech.edu
Howard D. Lipshitz*
Affiliation:
Division of Biology 156-29, California Institute of Technology, Pasadena, California 91125, U.S.A. Phone: 818-395-6446, Fax: 818-564-8709, E-mail: LipshitzH@Starbasel.caltech.edu
*
2 Author for correspondence.
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Over twenty distinct families of long terminal direct repeat (LTR)-containing retrotransposons have been identified in Drosophila melanogaster. While there have been extensive analyses of retrotransposon transcription in cultured cells, there have been few studies of the spatial expression of retrotransposons during normal development. Here we report a detailed analysis of the spatial expression patterns of fifteen families of retrotransposons during Drosophila melanogaster embryogenesis (17.6, 297, 412, 1731, 3S18, blood, copia, gypsy, HMS Beagle, Kermit/flea, mdg1, mdg3, opus, roo/B104 and springer). In each case, analyses were carried out in from two to four wild-type strains. Since the chromosomal insertion sites of any particular family of retrotransposons vary widely among wild-type strains, a spatial expression pattern that is conserved among strains is likely to have been generated through interaction of host transcription factors with cis-regulatory elements resident in the retrotransposons themselves. All fifteen families of retrotransposons showed conserved patterns of spatially and temporally regulated expression during embryogenesis. These results suggest that all families of retrotransposons carry cis-acting elements that control their spatial and temporal expression patterns. Thus, transposition of a retrotransposon into or near a particular host gene-possibly followed by an excision event leaving behind the retrotransposon's cis-regulatory sequences-might impose novel developmental control on such a host gene. Such a mechanism would serve to confer evolutionarily significant alterations in the spatio-temporal control of gene expression.

Information

Type
Research Article
Information
Genetics Research , Volume 64 , Issue 3 , December 1994 , pp. 167 - 181
Copyright
Copyright © Cambridge University Press 1994

References

Adler, A., Scheller, A., Hoffman, Y. & Robins, D. M. (1991). Multiple components of a complex androgen-dependent enhancer. Molecular Endocrinology 5, 1587–1596.CrossRefGoogle ScholarPubMed
Arkhipova, I. R. & Ilyin, Y. V. (1992). Control of transcription of Drosophila retrotransposons. Bio Essays 14, 161–168.Google ScholarPubMed
Bell, J. R., Bogardus, A. M., Schmidt, T. & Pellegrini, M. (1985). A new copia-like transposable element found in a Drosophila rDNA gene unit. Nucleic Acids Research 13, 3861–3871.CrossRefGoogle Scholar
Bender, W., Spierer, P. & Hogness, D. S. (1983). Chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex in Drosophila melanogaster. Journal of Molecular Biology 168, 17–33.CrossRefGoogle ScholarPubMed
Bingham, P. M. & Chapman, C. H. (1986). Evidence that white-blood is a novel type of temperature-sensitive mutation resulting from temperature-dependent effects of a transposon insertion on formation of white transcripts. EMBO Journal 5, 3343–3351.CrossRefGoogle ScholarPubMed
Brookman, J. J., Toosy, A. T., Shashidhara, L. S. & White, R. A. (1992). The 412 retrotransposon and the development of gonadal mesoderm in Drosophila. Development 116, 1185–1192.CrossRefGoogle ScholarPubMed
Cavarec, L. & Heidmann, T. (1993). The Drosophila copia retrotransposon contains binding sites for transcriptional regulation by homeoproteins. Nucleic Acids Research 21, 5041–5049.CrossRefGoogle ScholarPubMed
Ding, D., Parkhurst, S. M. & Lipshitz, H. D. (1993). Different genetic requirements for anterior RNA localization revealed by the distribution of Adducin-like transcripts during Drosophila oogenesis. Proceedings of the National Academy of Sciences USA 90, 2512–2516.CrossRefGoogle ScholarPubMed
Errede, B. (1993). MCM1 binds to a transcriptional control element in Tyl. Molecular and Cellular Biology 13, 57–62.Google Scholar
Fincham, J. R. S. & Sastry, G. R. K. (1974). Controlling elements in maize. Annual Review of Genetics 8, 15–50.CrossRefGoogle ScholarPubMed
Finnegan, D. J. & Fawcett, D. H. (1986). Transposable elements in Drosophila melanogaster. Oxford Surveys on Eukaryotic Genes 3, 1–62.Google ScholarPubMed
Fjose, A., McGinnis, W. J. & Gehring, W. J. (1985). Isolation of a homeobox-containing gene from the engrailed region of Drosophila and the spatial distribution of its transcripts. Nature 313, 284–289.CrossRefGoogle Scholar
Flavell, A. J., Ruby, S. W., Toole, J. J., Roberts, B. E. & Rubin, G. M. (1980). Translation and developmental regulation of RNA encoded by the eukaryotic transposable element copia. Proceedings of the National Academy of Sciences USA 77, 7107–7111.CrossRefGoogle ScholarPubMed
Heidmann, O. & Heidmann, T. (1991). Retrotransposition of a mouse IAP sequence tagged with an indicator gene. Cell 64, 159–170.CrossRefGoogle ScholarPubMed
Huijser, P., Kirchhoff, C., Lankenau, D.-H. & Hennig, W. (1988). Retrotransposon-like sequences are expressed in Y-chromosomal lampbrush loops of Drosophila hydei. Journal of Molecular Biology 203, 689–697.CrossRefGoogle ScholarPubMed
Ilyin, Y. V., Chmeliauskaite, V. G., Ananiev, E. V. & Georgiev, G. P. (1980). Isolation and characterization of a new family of mobile dispersed genetic elements, mdg3, in Drosophila melanogaster. Chromosoma 81, 27–53.CrossRefGoogle ScholarPubMed
Ilyin, Y. V., Chmeliauskaite, V. G., Ananiev, E. V., Lyubomirskaya, N. V., Kulguskin, V. V., Bayev, A. A. & Georgiev, G. P. (1980). Mobile dispersed genetic element mdg1 of Drosophila melanogaster: structural organization. Nucleic Acids Research 8, 5333–5346.CrossRefGoogle ScholarPubMed
Ilyin, Y. V., Tchurikov, N. A., Ananiev, E. V., Ryskov, A. P., Yenikopolov, G. N., Limborska, S. A., Maleeva, N. E., Gvozdev, V. A. & Georgiev, G. P. (1978). Studies on the DNA fragments of mammals and Drosophila containing structural genes and adjacent sequences. Cold Spring Harbor Symposia on Quantitative Biology 42, 959–969.CrossRefGoogle ScholarPubMed
Karlik, C. C. & Fyrberg, E. A. (1985). An insertion within a variably spliced Drosophila tropomyosin gene blocks accumulation of only one encoded isoform. Cell 41, 57–66.CrossRefGoogle ScholarPubMed
Keshet, E., Schiff, R. & Itin, A. (1991). Mouse retrotransposons: A cellular reservoir of long terminal repeat (LTR) elements with diverse transcriptional specificities. Advances in Cancer Research 56, 215–251.CrossRefGoogle ScholarPubMed
Kidd, S. & Young, M. W. (1986). Transposon-dependent mutant phenotypes at the Notch locus of Drosophila. Nature 323, 89–91.CrossRefGoogle ScholarPubMed
King, M. C. & Wilson, A. C. (1975). Evolution at two levels in human and chimpanzees. Science 188, 107–116.CrossRefGoogle ScholarPubMed
Kornberg, T., Siden, I., O'Farrell, P. & Simon, M. (1985). The engrailed locus of Drosophila: in situ localization of transcripts reveals compartment-specific expression. Cell 40, 45–53.CrossRefGoogle ScholarPubMed
Lankenau, S., Corces, V. & Lankenau, D.-H. (1994). The Drosophila micropia retrotransposon encodes a testis specific antisense RNA complementary to reverse transcriptase. Molecular and Cellular Biology 14, 1764–1775.Google ScholarPubMed
Lavorgna, G., Malva, C, Manzi, A., Gigliotti, S. & Graziani, F. (1989). The abnormal oocyte phenotype is correlated with the presence of blood transposon in Drosophila melanogaster. Genetics 123, 485–494.CrossRefGoogle ScholarPubMed
Lewis, E. B. (1951). Pseudoallelism and gene evolution. Cold Spring Harbor Symposia on Quantitative Biology 16, 159–174.CrossRefGoogle ScholarPubMed
Li, X. & Noll, M. (1994). Evolution of distinct developmental functions of three Drosophila genes by acquisition of different cis-regulatory regions. Nature 367, 83–87.CrossRefGoogle ScholarPubMed
Löhning, C, Rosenbaum, C. & Ciriacy, M. (1993). Isolation of the TYE2 gene reveals its identity to SWI3 encoding a general transcription factor in Saccharomyces cereuisiae. Current Genetics 24, 193–199.CrossRefGoogle Scholar
Marlor, R. L., Parkhurst, S. M. & Corces, V. G. (1986). The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Molecular and Cellular Biology 6, 1129–1134.Google ScholarPubMed
Matsumine, H., Herbst, M. A., Ou, S.-H. I., Wilson, J. D. & McPhaul, M. J. (1991). Aromatase mRNA in the extragonadal tissue of chickens with the henny-feathering trait is derived from a distinctive promoter structure that contains a segment of a retroviral long terminal repeat. Journal of Biological Chemistry 266, 19900–19907.CrossRefGoogle ScholarPubMed
McClintock, B. (1951). Chromosome organization and genie expression. Cold Spring Harbor Symposia on Quantitative Biology 16, 13–47.CrossRefGoogle Scholar
Meyerowitz, E. M. & Hogness, D. S. (1982). Molecular organization of a Drosophila puff site that responds to ecdysone. Cell 28, 165–176.CrossRefGoogle ScholarPubMed
Micard, D., Couderc, J. L., Sobrier, M. L., 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 Research 16, 455–470.CrossRefGoogle ScholarPubMed
Mossie, K. G., Young, M. W. & Varmus, H. E. (1985). Extrachromosomal DNA forms of copia-like transposable elements, F elements and middle repetitive DNA sequences in Drosophila melanogaster. Variation in cultured cells and embryos. Journal of Molecular Biology 182, 31–43.CrossRefGoogle ScholarPubMed
Mount, S. M. & Rubin, G. M. (1985). Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins. Molecular and Cellular Biology 5, 1630–1638.Google ScholarPubMed
Mozer, B. A. & Benzer, S. (1994). Ingrowth by photoreceptor axons induces transcription of a retrotransposon in the developing Drosophila brain. Development 120, 1049–1058CrossRefGoogle ScholarPubMed
Parkhurst, S. M. & Corces, S. M. (1985). forked, gypsys, and suppressors in Drosophila. Cell 41, 429–437.CrossRefGoogle ScholarPubMed
Parkhurst, S. M. & Corces, V. G. (1987). Developmental expression of Drosophila melanogaster retrovirus-like transposable elements. EMBO Journal 6, 419–424.CrossRefGoogle ScholarPubMed
Peronnet, F., Becker, J. L., Becker, J., d'auriol, L., Galibert, F. & Best-Belpomme, M. (1986). 1731, a new retrotransposon with hormone modulated expression. Nucleic Acids Research 14, 9017–9033.CrossRefGoogle ScholarPubMed
Pouteau, S., Huttner, E., Grandbastien, M. A. & Caboche, M. (1991). Specific expression of the tobacco Tntl retrotransposon in protoplasts. EMBO Journal 10, 1911–1918.CrossRefGoogle Scholar
Radicella, J. P., Brown, D., Tolar, L. A. & Chandler, V. L. (1992). Allelic diversity of the maize B regulatory gene: different leader and promoter sequences of two B alleles determine distinct tissue specificities of anthocyanin production. Genes and Development 6, 2152–2164.CrossRefGoogle ScholarPubMed
Robins, D. M. & Samuelson, L. C. (1992). Retrotransposons and the evolution of mammalian gene expression. Genetica 86, 191–201.CrossRefGoogle ScholarPubMed
Scherer, G., Telford, J., Baldari, C. & Pirrotta, V. (1981). Isolation of cloned genes differentially expressed at early and late stages of Drosophila embryonic development. Developmental Biology 86, 438–447.CrossRefGoogle ScholarPubMed
Scherer, G., Tschudi, C., Perera, J., Delius, H. & Pirrotta, V. (1982). B104, a new dispersed repeated gene family in Drosophila melanogaster and its analogies with retroviruses. J Mol. Biol. 157, 435–451.CrossRefGoogle ScholarPubMed
Schwartz, H. E., Lockett, T. J. & Young, M. W. (1982). Analysis of transcripts from two families of nomadic DNA. Journal of Molecular Biology 157, 49–68.CrossRefGoogle ScholarPubMed
Snyder, M. P., Kimbrell, D., Hunkapiller, M., Hill, R., Fristrom, J. & Davidson, N. (1982). A transposable element that splits the promoter region inactivates a Drosophila cuticle protein gene. Proceedings of the National Academy of Sciences USA 79, 7430–7434.CrossRefGoogle ScholarPubMed
Stravenhagen, J. B. & Robins, D. M. (1988). An ancient provirus has imposed androgen regulation on the adjacent mouse sex-limited protein gene. Cell 55, 247–254.CrossRefGoogle Scholar
Strobel, E., Dunsmuir, P. & Rubin, G. M. (1979). Polymorphisms in the chromosomal locations of elements of the 412, copia and 297 dispersed repeated families in Drosophila. Cell 17, 429–439.CrossRefGoogle ScholarPubMed
Tanda, S. & Corces, V. G. (1991). Retrotransposon-induced overexpression of a homeobox gene causes defects in eye morphogenesis in Drosophila. EMBO Journal 10, 407–417.CrossRefGoogle ScholarPubMed
Tautz, D. & Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81–85.CrossRefGoogle ScholarPubMed
Ting, C.-N., Rosenberg, M. P., Snow, C. M., Samuelson, L. C. & Meisler, M. H. (1992). Endogenous retroviral sequences are required for tissue-specific expression of a human salivary amylase gene. Genes and Development 6, 1457–1465.CrossRefGoogle ScholarPubMed
Will, B. M., Bayev, A. A. & Finnegan, D. J. (1981). Nucleotide sequence of terminal repeats of 412 transposable elements of Drosophila melanogaster. Journal of Molecular Biology 153, 897–915.CrossRefGoogle ScholarPubMed
Young, M. W. & Schwartz, H. E. (1981). Nomadic gene families in Drosophila. Cold Spring Harbor Symposia on Quantitative Biology 45, 629–640.CrossRefGoogle ScholarPubMed
Yu, G. & Fassler, J. S. (1993). SPT13 (GAL11) of Saccharomyces cerevisiae negatively regulates activity of the MCM1 transcription factor in Ty1 elements. Molecular and Cellular Biology 13, 63–71.Google ScholarPubMed
Yuki, S., Inouye, S., Ishimaru, S. & Saigo, K. (1986). Nucleotide sequence characterization of a Drosophila retrotransposon, 412. European Journal of Biochemistry 158, 403–410.CrossRefGoogle ScholarPubMed