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Cis-regulatory sequences leading to female-specific expression of yolk protein genes 1 and 2 in the fat body of Drosophila melanogaster

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Summary

The three yolk protein genes (yp) of Drosophila melanogaster are transcribed in a sex- and tissue-limited fashion. We have searched for cis-regulatory sequences in regions flanking yp1 and yp2 to identify the elements that confer female-specific expression in the fat body. One such 127 by element has previously been identified in this region. We show here the existence of two additional regions which confer female fat body-specific expression on an Adh reporter gene and on the native yp2 gene, respectively. This suggests some redundancy in the regulation of expression of the yp genes. Computer searches for putative binding sites for the DSX protein, which regulates sex-specific expression of the yp genes, revealed several such sites in our constructs. However, the significance of these is unclear since many such sites also occur in genes which one would not expect to be regulated in a sex-specific manner (e.g. Adh, Actin 5C). We suggest that DSX acts in concert with other proteins to mediate sex- and tissue-specific expression of the yp genes.

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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 Dev 6:466–480

    Google Scholar 

  • Baker BS (1989) Sex in flies: the splice of life. Nature 340:521–524

    Google Scholar 

  • Baker BS, Ridge KA (1980) Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 94:383–423

    Google Scholar 

  • Baker BS, Wolfner MF (1988) A molecular analysis of doublesex, a bifunctional gene that controls both male and female sexual differentiation in Drosophila melanogaster. Genes Dev 2:477–489

    Google Scholar 

  • Barnett T, Pachl C, Gergen JP, Wensink PC (1980) The isolation and characterization of Drosophila yolk protein genes. Cell 21:729–738

    Google Scholar 

  • Barnett T, Wensink PC (1981) Transcription and translation of yolk protein mRNA in fat bodies of Drosophila. In: Brown DD, Fox CF (eds) Developmental biology using purified genes UCLA-ICN Symposium. University of California Press, Berkeley, vol 23, pp 99–106

    Google Scholar 

  • Beck E, Ludwig G, Auerswald EA, Reiss B, Schaller H (1982) Nucleotide sequence and exact localization of the neomycin phosphotransferase gene from transposon Tn5. Gene 19:327–336

    Google Scholar 

  • Biggin MD, Tjian R (1989) Transcription factors and the control of Drosophila development. Trends Genet 5:377–383

    Google Scholar 

  • Bonner JJ, Parks C, Parker-Thornburg J, Martin MA, Pelham HRB (1984) The use of promoter fusions in Drosophila genetics isolation of mutations affecting the heat shock response. Cell 37:979–991

    Google Scholar 

  • Bownes M (1980) The use of yolk protein variations in Drosophila species to analyse the control of vitellogenesis. Differentiation 16:104–116

    Google Scholar 

  • Bownes M, Hames BD (1978) Analysis of the yolk proteins in Drosophila melanogaster. FEBS Lett 96:327–330

    Google Scholar 

  • Bownes M, Nöthiger R (1981) Sex-determining genes and vitellogenin synthesis in Drosophila melanogaster. Mol Gen Genet 182:222–228

    Google Scholar 

  • Bownes M, Scott A, Blair M (1987) The use of an inhibitor of protein synthesis to investigate the roles of ecdysteroids and sex-determination genes on the expression of the genes encoding the Drosophila yolk proteins. Development 101:931–941

    Google Scholar 

  • Bownes M, Scott A, Shirras A (1988) Dietary components modulate yolk protein gene transcription in Drosophila melanogaster. Development 103:119–128

    Google Scholar 

  • Brennan MD, Weiner AJ, Goralski TJ, Mahowald AP (1982) The follicle cells are a major site of vitellogenin synthesis in Drosophila melanogaster. Dev Biol 89:225–236

    Google Scholar 

  • Burtis KC, Baker BS (1989) Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56:997–1010

    Google Scholar 

  • Burtis KC, Coschigano KT, Baker BS, Wensink PC (1991) The Doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO J 10:2577–2582

    Google Scholar 

  • England BP, Heberlein U, Tjian R (1990) Purified Drosophila transcription factor, Adh distal factor-1 (Adf-1), binds to sites in several Drosophila promoters and activates transcription. J Biol Chem 265:5086–5094

    Google Scholar 

  • Falb D, Maniatis T (1992) A conserved regulatory unit implicated in tissue-specific gene expression in Drosophila and man. Genes Dev 6:454–465

    Google Scholar 

  • Friederich E, Baeuerle PA, Garoff H, Hovemann B, Hüttner WB (1988) Expression, tyrosine sulfation and secretion of the yolk protein 2 of Drosophila melanogaster in mouse fibroblasts. J Biol Chem 263:14930–14938

    Google Scholar 

  • Fischer JA, Maniatis T (1988) Drosophila Adh: a promoter element expands the tissue specificity of an enhancer. Cell 53:451–461

    Google Scholar 

  • Garabedian MJ, Hung M-C, Wensink PC (1985) Independent control elements that determine yolk protein gene expression in alternative Drosophila tissues. Proc Natl Acad Sci USA 82:1396–1400

    Google Scholar 

  • Garabedian MJ, Shepherd BM, Wensink PC (1986) A tissue-specific transcription enhancer from the Drosophila yolk protein 1 gene. Cell 45:859–967

    Google Scholar 

  • Garabedian MJ, Shirras AD, Bownes M, Wensink PC (1987) The nucleotide sequence of the gene coding for Drosophila melanogaster yolk protein 3. Gene 55:1–8

    Google Scholar 

  • Hoveman B, Galler R, Walldorf U, Küpper H, Bautz EKF (1981) Vitellogenin in Drosophila melanogaster: sequence of the yolk protein I gene and its flanking regions. Nucleic Acids Res 9:4721–4734

    Google Scholar 

  • Hung M-C, Wensink PC (1981) The sequence of the Drosophila melanogaster gene for yolk protein 1. Nucleic Acids Res 9:6407–6419

    Google Scholar 

  • Hung M-C, Wensink PC (1983) Sequence and structure conservation in yolk proteins and their genes. J Mol Biol 164:481–492

    Google Scholar 

  • Jowett T (1986) Preparation of nucleic acids. In: Roberts DB (ed) Drosophila, a practical approach. IRL Press, Oxford, pp 275–286

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Google Scholar 

  • Lindsley DL, Grell EH (1968) Genetic variations of Drosophila. Carnegie Institution of Washington Publ. No. 627

  • Logan SK, Garabedian MJ, Wensink PC (1989) DNA regions that regulate the ovarian transcriptional specificity of Drosophila yolk protein genes. Genes Dev 3:1453–1461

    Google Scholar 

  • Logan SK, Wensink PC (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 Dev 4:613–623

    Google Scholar 

  • Nielsen O, Egel R (1989) Mapping the double-strand breaks at the mating-type locus in fission yeast by genomic sequencing. EMBO J 8:269–276

    Google Scholar 

  • Nöthiger R, Leuthold M, Andersen N, Gerschwiler P, Grüter A, Keller W, Leist C, Roost M, Schmid H (1987) Genetic and developmental analysis of the sex-determining gene double sex (dsx) of Drosophila melanogaster. Genet Res Camb 50:113–123

    Google Scholar 

  • Perkins KK, Dailey GM, Tjian R (1988) Novel Jun- and Fosrelated proteins in Drosophila are functionally homologous to enhancer factor AP-1. EMBO J 7:4265–4273

    Google Scholar 

  • Postlethwait JH, Lange G, Handler AM (1980) Yolk protein synthesis in ovariectomized and genetically agametic [X87] Drosophila melanogaster. Gen Comp Endocrinology 40:385–390

    Google Scholar 

  • Rio DC, Rubin GM (1985) Transformation of cultured Drosophila melanogaster cells with a dominant selectable marker. Mol Cell Biol 5:1833–1838

    Google Scholar 

  • Rubin GM, Spradling AC (1983) Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res 11:6341–6351

    Google Scholar 

  • Shirras AD, Bownes M (1987) Separate DNA sequences are required for normal female and ecdysone-induced male expression of Drosophila melanogaster yolk protein 1. Mol Gen Genet 210:153–155

    Google Scholar 

  • Slee R, Bownes M (1990) Sex determination in Drosophila melanogaster. Quart Rev Biol 65:175–204

    Google Scholar 

  • Spradling AC, Rubin GM (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218:341–347

    Google Scholar 

  • Stanojevic D, Hoey T, Levine M (1989) Sequence-specific DNA-binding activities of the gap proteins encoded by hunchback and Krüppel in Drosophila. Nature 341:331–335

    Google Scholar 

  • Steinmann-Zwicky M, Amrein H, Nöthiger R (1990) Genetic control of sex determination in Drosophila. Adv Genet 27:189–237

    Google Scholar 

  • Steller H, Pirrotta V (1985) A transposable P vector that confers selectable G418 resistance to Drosophila larvae. EMBO J 4:167–171

    Google Scholar 

  • Tamura T, Kunert C, Postlethwait J (1985) Sex- and cell-specific regulation of yolk polypeptide genes introduced into Drosophila by P-element-mediated gene transfer. Proc Natl Acad Sci USA 82:7000–7004

    Google Scholar 

  • Wildeman AG (1988) Regulation of SV40 early gene expression. Biochem Cell Biol 66:567–577

    Google Scholar 

  • Xiao H, Perisic O, Lis J (1991) Cooperative binding of Drosophila heat shock factor to arrays of a conserved 5 by unit. Cell 64:585–593

    Google Scholar 

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Authors and Affiliations

  1. Developmental Biology Center, Institute of Cell and Molecular Biology, Division of Biological Sciences, University of Edinburgh, EH9 3JR, Edinburgh, Scotland

    Niels Abrahamsen, Alberto Martinez & Mary Bownes

  2. Institute of Genetics, University of Copenhagen, DK-1353, Denmark

    Niels Abrahamsen, Torben Kjær & Leif Søndergaard

Authors
  1. Niels Abrahamsen
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  2. Alberto Martinez
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  3. Torben Kjær
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  4. Leif Søndergaard
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  5. Mary Bownes
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Communicated by K. Illmensee

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Abrahamsen, N., Martinez, A., Kjær, T. et al. Cis-regulatory sequences leading to female-specific expression of yolk protein genes 1 and 2 in the fat body of Drosophila melanogaster . Molec. Gen. Genet. 237, 41–48 (1993). https://doi.org/10.1007/BF00282782

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  • DOI: https://doi.org/10.1007/BF00282782

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