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Two independent cis-acting elements regulate the sex- and tissue-specific expression of yp3 in Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Elaine Ronaldson
Affiliation:
Institute of Cell and Molecular Biology, University of Edinburgh, Mayfield Road, Edinburgh EH9 3JR, Tel: 031 650 5368, fax: 031 668 3870, E-mail: [email protected]
Mary Bownes*
Affiliation:
Institute of Cell and Molecular Biology, University of Edinburgh, Mayfield Road, Edinburgh EH9 3JR, Tel: 031 650 5368, fax: 031 668 3870, E-mail: [email protected]
*
* Corresponding author.
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Summary

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In Drosophila, the three yolk protein (yp) genes are transcribed in a sex-, tissue- and developmentally specific manner, providing an ideal system in which to investigate the factors involved in their regulation. The yolk proteins are synthesized in the fat body of adult females, and in the ovarian follicle cells surrounding the developing oocyte during stages 8–10 of oogenesis. We report here an analysis of the yolk protein 3 (yp3) gene and its flanking sequences by means of P-element mediated germ-line transformation and demonstrate that a 747 bp promoter region is sufficient to direct sex-specific expression in the female fat body and both the temporal- and cell-type-specificity of expression during oogenesis. Two elements that independently govern yp3 transcription in these tissues have been separated and no other sequences in the upstream, downstream or coding regions have been identified that are autonomously involved in yp3 expression.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1995

References

Abel, T., Bhatt, R. & Maniatis, T. (1992). A Drosophila CREB/ATF transcriptional activator binds to both fat body- and liver-specific regulatory elements. Genes and Development 6, 466480.CrossRefGoogle ScholarPubMed
Abrahamsen, N., Martinez, A., Kjaer, T., Sondergaard, L., & Bownes, M. (1993). Cis-regulatory sequences leading to female-specific expression of yolk protein genes 1 and 2 in the fat body of Drosophila melanogaster. Molecular and General Genetics 237, 4148.CrossRefGoogle ScholarPubMed
Baniahmad, A., Muller, M., Steiner, C., & Renkawitz, R. (1987). Activity of two different silencer elements of the chicken lysozyme gene can be compensated by enhancer elements. EM BO Journal 6, 22972303.Google ScholarPubMed
Barnett, T., Pachl, C., Gergen, J. P., & Wensink, P. C. (1980). The isolation and characterization of Drosophila yolk protein genes. Cell 21, 729738.CrossRefGoogle ScholarPubMed
Belote, J. M., Handler, A. M., Wolfner, M. F., Livak, K. J., & Baker, B. S. (1985). Sex-specific regulation of yolk protein gene expression in Drosophila. Cell 40, 339348.CrossRefGoogle ScholarPubMed
Bownes, M., & Hames, B. D. (1978). Analysis of the yolk proteins in Drosophila melanogaster. FEBS Letters 96, 327330.CrossRefGoogle ScholarPubMed
Bownes, M., & Nöthiger, R. (1981). Sex determining genes and vitellogenin synthesis in Drosophila melanogaster. Molecular and General Genetics 182, 222228.CrossRefGoogle ScholarPubMed
Bownes, M., Scott, A., & Shirras, A. (1988). Dietary components modulate yolk protein gene transcription in Drosophila melanogaster. Development 103, 119128.CrossRefGoogle ScholarPubMed
Bownes, M., Steinmann-Zwicky, M., & Nöthiger, R. (1990). Differential control of yolk protein gene expression fat bodies and gonads by the sex-determining gene tra-2 of Drosophila. EMBO Journal 9, 39753980.CrossRefGoogle ScholarPubMed
Bownes, M., Ronaldson, E., Mauchline, D., & Martinez, A. (1993). Regulation of vitellogenesis in Drosophila. International Journal of Insect Morphology and Embryology 22, 349367.CrossRefGoogle Scholar
Brennan, M. D., Weiner, A. J., Goralski, T. J., & Mahowald, A. P. (1982). The follicle cells are a major site of vitellogenin synthesis in Drosophila melanogaster. Developmental Biology 89, 225236.CrossRefGoogle Scholar
Burtis, K. C., Coschigano, K. T., Baker, B. S., & Wensink, P. C. (1991). The doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO Journal 10, 25772582.CrossRefGoogle ScholarPubMed
Christianson, A. M. K., King, D. L., Hatzivassiliou, E., Casas, J. E., Hallenbeck, P. L., Nikodem, V. M., Mitsialis, A., & Kafatos, F. C. (1992). DNA binding and heteromerization of the Drosophila transcription factor chorion factorl/ultraspiracle. Proceedings of the National Academy of Sciences, USA 89, 11 503–11 507.CrossRefGoogle Scholar
Coschigano, K. T., & Wensink, P. C. (1993). Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes and Development 7, 4254.CrossRefGoogle ScholarPubMed
Devereux, J., Haeberli, P., & Smithies, O. (1984). A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Research 12, 387395.CrossRefGoogle ScholarPubMed
Dudler, T., & Travers, A. A. (1984). Upstream elements necessary for optimal function of the hsp70 promoter in transformed flies. Cell 38, 391398.CrossRefGoogle Scholar
Falb, D., & Maniatis, T. (1992). A conserved regulatory unit implicated in tissue-specific gene expression in Drosophila and man. Genes and Development 6, 454465.CrossRefGoogle ScholarPubMed
Garabedian, M. J., Shepherd, B. M., & Wensink, P. C. (1986). A tissue-specific transcription enhancer from the Drosophila yolk protein 1 gene. Cell 45, 859867.CrossRefGoogle ScholarPubMed
Garabedian, M. J., Shirras, A. D., Bownes, M., & Wensink, P. C. (1987). The nucleotide sequence of the gene coding for Drosophila melanogaster yolk protein 3. Gene 55, 18.CrossRefGoogle ScholarPubMed
M.-C., Hung, & Wensink, P. C. (1983). Sequence and structure conservation in yolk proteins and their genes. Journal of Molecular Biology 164, 481492.Google Scholar
Ingolia, T. D., Craig, E. A., & McCarthy, B. J. (1980). Sequence of three copies of the gene for the major Drosophila heat shock induced protein and their flanking regions. Cell 21, 669679.CrossRefGoogle ScholarPubMed
Isaac, P. G., & Bownes, M. (1982). Ovarian and fat-body vitellogenin synthesis in Drosophila melanogaster. European Journal of Biochemistry 123, 527534.CrossRefGoogle ScholarPubMed
Jacoby, D. B., & Wensink, P. C. (1994). Yolk protein factor 1 is a Drosophila homologue of Ku, the DNA-binding subunit of a DNA-dependent protein kinase from humans. Journal of Biological Chemistry 269, 1148411491.CrossRefGoogle Scholar
King, R. C. (1970). Ovarian Development in Drosophila melanogaster. New York: Academic Press.Google Scholar
Liddell, S., & Bownes, M. (1991). Investigation of cis-acting sequences regulating expression of the gene encoding yolk protein 3 in Drosophila melanogaster. Molecular and General Genetics 230, 219224.CrossRefGoogle ScholarPubMed
Logan, S. K., Garabedian, M. J., & Wensink, P. C. (1989). DNA regions that regulate the ovarian transcriptional specificity of Drosophila yolk protein genes. Genes and Development 3, 14531461.CrossRefGoogle ScholarPubMed
Logan, S. K., & Wensink, P. C. (1990). Ovarian follicle cell enhancers from the Drosophila yolk protein genes: different segments of one enhancer have different cell-type specificities that interact to give normal expression. Genes and Development 4, 613623.CrossRefGoogle ScholarPubMed
Lüning, K. G. (1981). Genetics of inbred Drosophila melanogaster. Hereditas 95, 181188.CrossRefGoogle Scholar
Meyer, K. B., & Neuberger, M. S. (1989). The immunoglobulin kappa-locus contains a second, stronger, B-cell-specific enhancer which is located downstream of the constant region. EMBO Journal 8, 19591964.CrossRefGoogle ScholarPubMed
Mitsis, P. G., & Wensink, P. C. (1989a). Identification of yolk protein factor 1, a sequence of specific DNA binding protein from Drosophila melanogaster. Journal of Biological Chemistry 264, 51885194.CrossRefGoogle ScholarPubMed
Mitsis, P. G., & Wensink, P. C. (1989b). Purification and properties of YPF1, a sequence specific DNA-binding protein from Drosophila melanogaster. Journal of Biological Chemistry 264, 51955202.CrossRefGoogle ScholarPubMed
Postlethwait, J. H., Bownes, M., & T., Jowett (1980). Sexual phenotype and vitellogenin synthesis in Drosophila melanogaster. Developmental Biology 79, 379387.CrossRefGoogle ScholarPubMed
Rubin, G. M., & Spradling, A. C. (1982). Genetic transformation of Drosophila with transposable element vectors. Science 218, 348353.CrossRefGoogle ScholarPubMed
Serfling, E., Jasin, M., & Schaffner, W. (1985). Enhancers and eukaryotic gene transcription. Trends in Genetics 1, 224230.CrossRefGoogle Scholar
Shirras, A., & Bownes, M. (1987). Separate DNA sequences are required for normal female and ecdysone-induced male expression of Drosophila melanogaster yolk protein 1. Molecular and General Genetics 210, 153155.CrossRefGoogle ScholarPubMed
Slee, R., & M., Bownes (1990). Sex determination in Drosophila melanogaster. Quarterly Review of Biology 65, 175204.CrossRefGoogle ScholarPubMed
Spradling, A. C., & Rubin, G. M. (1982d). Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218, 341347.CrossRefGoogle ScholarPubMed
Steinmann-Zwicky, M., Amrein, H., & Nöthiger, R. (1990). Genetic control of sex determination in Drosophila. Advances in Genetics 27, 189237.CrossRefGoogle ScholarPubMed
Thummel, C. S., Boulet, A. M., & Lipshitz, H. D. (1988). Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene 74, 445456.CrossRefGoogle ScholarPubMed