The Binding Site of a Steroid Hormone Receptor-Like Protein within the Drosophila Adh Adult Enhancer Is Required for High Levels of Tissue-Specific Alcohol Dehydrogenase Expression

REFERENCES

• Ashbumer, M. 1989. Drosophila, a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Atkinson, P. W., L. E. Mills, W. T. Starmer, and D. T. Sullivan. 1988. Structure and evolution of the Adh genes of Drosophila mojavensis. Genetics 120:713–723.
   PubMedGoogle Scholar
• Ayer, S., and C. Benyajati. 1990. Conserved enhancer and silencer elements responsible for differential Adh transcription in Drosophila cell lines. Mol. Cell. Biol. 10:3512–3523.
   PubMedGoogle Scholar
• Beato, M. 1989. Gene regulation by steroid hormones. Cell 56:335–344.
   PubMed Web of Science ®Google Scholar
• Benyajati, C. Unpublished observations.
   Google Scholar
• Benyajati, C., S. Ayer, J. McKeon, A. Ewel, and J. Huang. 1987. Role of cis-acting elements and chromatin structure in Drosophila alcohol dehydrogenase gene expression. Nucleic Acids Res. 15:7903–7920.
   PubMedGoogle Scholar
• Benyajati, C., A. Place, N. Wang, E. Pentz, and W. Sofer. 1982. Deletions at intervening sequence splice sites in the alcohol dehydrogenase gene of Drosophila. Nucleic Acids Res. 10:7261–7272.
   PubMedGoogle Scholar
• Benyajati, C., N. Spoerel, H. Haymerle, and M. Ashburner. 1983. The messenger RNA for alcohol dehydrogenase in Drosophila melanogaster differs in its 5′ end in different developmental stages. Cell 33:125–133.
   PubMed Web of Science ®Google Scholar
• Brennan, M. D., and W. J. Dickinson. 1988. Complex developmental regulation of the Drosophila affinidisjuncta alcohol dehydrogenase gene in Drosophila melanogaster. Dev. Biol. 125:64–74.
   PubMedGoogle Scholar
• Cartwright, I. L. 1987. Developmental switch in chromatin structure associated with alternate promoter usage in Drosophila melanogaster. EMBO J. 6:3097–3101.
   PubMedGoogle Scholar
• Cherbas, L., K. Lee, and P. Cherbas. 1991. Identification of ecdysone response elements by analysis of the Drosophila Eip28/29 gene. Genes Dev. 5:120–131.
   PubMed Web of Science ®Google Scholar
• Corbin, V., and T. Maniatis. 1989. Role of transcriptional interference in the Drosophila melanogaster Adh promoter switch. Nature (London) 337:279–282.
   PubMed Web of Science ®Google Scholar
• Corbin, V., and T. Maniatis. 1989. The role of specific enhancerpromoter interactions in the Drosophila Adh promoter switch. Genes Dev. 3:2191–2200.
   PubMedGoogle Scholar
• Corbin, V., and T. Maniatis. 1990. Identification of cis-regulatory elements required for larval expression of the Drosophila melanogaster alcohol dehydrogenase gene. Genetics 124:637–646.
   PubMedGoogle Scholar
• Dobens, L., K. Rudolph, and E. M. Berger. 1991. Ecdysterone regulatory elements function as both transcriptional activators and repressors. Mol. Cell. Biol. 11:1846–1853.
   PubMedGoogle Scholar
• Driever, W., and C. Nusslein-Volhard. 1989. The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature (London) 337:138–143.
   PubMed Web of Science ®Google Scholar
• England, B., U. Heberlein, and R. Tjian. 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.
   PubMedGoogle Scholar
• Evans, R. E. 1988. The steroid and thyroid hormone receptor superfamily. Science 240:889–895.
   PubMed Web of Science ®Google Scholar
• Ewel, A., J. R. Jackson, and C. Benyajati. 1990. Alternative DNA-protein interactions in variable-length intemucleosomal regions associated with Drosophila Adh distal promoter expression. Nucleic Acids Res. 18:1771–1786.
   PubMedGoogle Scholar
• Fischer, J., and T. Maniatis. 1985. Structure and transcription of the Drosophila mulleri alcohol dehydrogenase genes. Nucleic Acids Res. 13:6899–6917.
   PubMedGoogle Scholar
• Fischer, J., and T. Maniatis. 1988. Drosophila Adh: a promoter element expands the tissue specificity of an enhancer. Cell 53:451–461.
   PubMedGoogle Scholar
• Fischer, J. A., and T. Maniatis. 1986. Regulatory elements involved in Drosophila Adh gene expression are conserved in divergent species and separate elements mediate expression in different tissues. EMBO J. 5:1275–1289.
   PubMedGoogle Scholar
• Fraenkel, G., and J. Su. 1984. Hormonal control of eclosion of flies from the puparium. Proc. Natl. Acad. Sci. USA 81:1457–1459.
   PubMedGoogle Scholar
• Garabedian, M. J., B. M. Shepherd, and P. C. Wensink. 1986. A tissue-specific transcription enhancer from the Drosophila yolk protein 1 gene. Cell 45:859–867.
   PubMed Web of Science ®Google Scholar
• Glass, C. K., O. V. Devary, and M. G. Rosenfeld. 1990. Multiple cell type-specific proteins differentially regulate target sequence recognition by the a retinoic acid receptor. Cell 63:729–738.
   PubMed Web of Science ®Google Scholar
• Glass, C. K., S. M. Lipkin, O. V. Devary, and M. G. Rosenfeld. 1989. Positive and negative regulation of gene transcription by a retinoic acid-thyroid hormone receptor heterodimer. Cell 59:697–708.
   PubMed Web of Science ®Google Scholar
• Heberlein, U., B. England, and R. Tjian. 1985. Characterization of Drosophila transcription factors that activate the tandem promoters of the alcohol dehydrogenase gene. Cell 41:965–977.
   PubMedGoogle Scholar
• Heberlein, U., and R. Tjian. 1988. Temporal patterns of alcohol dehydrogenase gene transcription reproduced by Drosophila stage-specific embryonic extracts. Nature (London) 331:410–415.
   PubMedGoogle Scholar
• Henikoff, S. 1983. Cloning exons for mapping transcription: characterization of the Drosophila melanogaster alcohol dehydrogenase gene. Nucleic Acids Res. 11:4735–4752.
   PubMedGoogle Scholar
• Henrich, V. C., T. J. Sliter, D. B. Lubahn, A. MacIntyre, and L. A. Gilbert. 1990. A steroid/thyroid hormone receptor superfamily member in Drosophila melanogaster that shares extensive sequence similarity with a mammalian homologue. Nucleic Acids Res. 18:4143–4148.
   PubMedGoogle Scholar
• Holloway, J. M., C. K. Glass, S. Alder, C. Nelson, and M. G. Rosenfeld. 1990. The C-terminal interaction domain of the T3 receptor confers the ability of the DNA site to dictate positive or negative transcriptional activity. Proc. Natl. Acad. Sci. USA 87:8160–8164.
   PubMedGoogle Scholar
• Jackson, J., and C. Benyajati. Submitted for publication.
   Google Scholar
• Kadonaga, J., and R. Tjian. 1986. Affinity purification of sequence-specific DNA-binding proteins. Proc. Natl. Acad. Sci. USA 83:5889–5893.
   PubMed Web of Science ®Google Scholar
• Karess, R., and G. Rubin. 1984. Analysis of P transposable element functions in Drosophila. Cell 38:135–146.
   PubMed Web of Science ®Google Scholar
• Koelle, M. R., W. S. Talbot, W. A. Segraves, M. T. Bendert, P. Cherbas, and D. S. Hogness. 1991. The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell 67:59–77.
   PubMed Web of Science ®Google Scholar
• Kumar, V., and P. Chambon. 1988. The estrogen receptor binds tightly to its responsive element as a ligand-induced homodimer. Cell 55:145–156.
   PubMed Web of Science ®Google Scholar
• Lavorgna, G., H. Ueda, J. Clos, and C. Wu. 1991. FTZ-F1, a steroid hormone-like protein implicated in the activation of fushi tarazu. Science 252:848–851.
   PubMed Web of Science ®Google Scholar
• Lavorgna, G., and C. Wu. Personal communication.
   Google Scholar
• Lockett, T., and M. Ashburner. 1989. Temporal and spatial utilization of the alcohol dehydrogenase gene promoters during the development of Drosophila melanogaster. Dev. Biol. 134:430–437.
   PubMedGoogle Scholar
• Lou, Y., J. Amin, and R. Voellmy. 1991. Ecdysterone receptor is a sequence-specific transcription factor involved in the developmental regulation of heat shock genes. Mol. Cell. Biol. 11:3660–3675.
   PubMedGoogle Scholar
• Maschat, F., M.-L. Dubertret, and J.-A. Lepesant. 1991. Transformation mapping of the regulatory elements of the ecdysone- inducible Pl gene of Drosophila melanogaster. Mol. Cell. Biol. 11:2913–2917.
   PubMedGoogle Scholar
• Mlodzik, M., Y. Hiromi, U. Weber, C. S. Goodman, and G. M. Rubin. 1990. The Drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell 60:211–224.
   PubMedGoogle Scholar
• Moses, K., U. Heberlein, and M. Ashburner. 1990. The Adh gene promoters of Drosophila melanogaster and Drosophila orena are functionally conserved and share features of sequence structure and nuclease-protected sites. Mol. Cell. Biol. 10:539–548.
   PubMedGoogle Scholar
• Murtha, M., and D. Cavenar. 1989. Ecdysteroid regulation of glucose dehydrogenase and alcohol dehydrogenase gene expression in Drosophila melanogaster. Dev. Biol. 135:66–73.
   PubMed Web of Science ®Google Scholar
• Nauber, U., M. J. Pankratz, A. Kienlin, E. Siefert, U. Klemm, and H. Jackle. 1988. Abdominal segmentation of the Drosophila embryo requires a hormone receptor-like protein encoded by the gap gene knirps. Nature (London) 336:489–492.
   PubMedGoogle Scholar
• Nelson, J. P., and C. Benyajati. Unpublished observations.
   Google Scholar
• O'Connell, P., and M. Rosbash. 1984. Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res. 12:5495–5513.
   PubMed Web of Science ®Google Scholar
• Oro, A. E., M. McKeown, and R. E. Evans. 1990. Relationship between the product of the Drosophila ultraspiracle locus and the vertebrate retinoid X receptor. Nature (London) 347:298–301.
   PubMed Web of Science ®Google Scholar
• Oro, A. E., E. S. Ong, J. S. Margolis, J. W. Posakony, M. McKeown, and R. M. Evans. 1988. The Drosophila gene knirps- related is a member of the steroid-receptor gene superfamily. Nature (London) 336:493–496.
   PubMedGoogle Scholar
• Perkins, K. K., G. M. Dailey, and R. Tjian. 1988. Novel Jun- and Fos-related proteins in Drosophila are functionally homologous to enhancer factor AP-1. EMBO J. 7:4265–4273.
   PubMedGoogle Scholar
• Perkins, K. K., G. M. Dailey, and R. Tjian. 1988. In vitro analysis of the Antennapedia P2 promoter: identification of a new Drosophila transcription factor. Genes Dev. 2:1615–1626.
   PubMedGoogle Scholar
• Pignoni, F., R. M. Baldarelli, E. Steingrimsson, R. J. Diaz, A. Patapoutian, J. R. Merriam, and J. A. Lengyel. 1990. The Drosophila gene tailless is expressed at the embryonic termini and is a member of the steroid receptor superfamily. Cell 62:151–163.
   PubMedGoogle Scholar
• Posakony, J. W., J. A. Fischer, and T. Maniatis. 1985. Identification of DNA sequences required for the regulation of Drosophila alcohol dehydrogenase gene expression. Cold Spring Harbor Symp. Quant. Biol. 50:515–520.
   PubMedGoogle Scholar
• Robertson, H., C. Preston, R. Phillips, D. JohnSon-Schlitz, W. Benz, and W. Engles. 1988. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118:461–470.
   PubMed Web of Science ®Google Scholar
• Rothe, M., U. Nauber, and H. Jackie. 1989. Three hormone receptor-like Drosophila genes encode an identical DNA-binding finger. EMBO J. 8:3087–3094.
   PubMedGoogle Scholar
• Rowan, R. G., and W. J. Dickinson. 1988. Nucleotide sequence of the genomic region encoding alcohol dehydrogenase in Drosophila affinidisjuncta. J. Mol. Evol. 28:43–54.
   PubMedGoogle Scholar
• Rubin, G., and A. Spradling. 1983. Vectors for P element- mediated gene transfer in Drosophila. Nucleic Acids Res. 11:6341–6351.
   PubMed Web of Science ®Google Scholar
• Savakis, C., M. Ashburner, and J. Willis. 1986. The expression of the gene coding for alcohol dehydrogenase during development of Drosophila melanogaster. Dev. Biol. 114:194–207.
   Google Scholar
• Segraves, W. A., and D. S. Hogness. 1990. The E75 ecdysone- inducible gene responsible for the 75B early puff in Drosophila encodes two new members of the steroid receptor superfamily. Genes Dev. 4:204–219.
   PubMedGoogle Scholar
• Shea, M., D. L. King, M. J. Conboy, B. D. Mariani, and F. C. Kafatos. 1990. Proteins that bind to Drosophila chorion cisregulatory elements: a new C2H2 zinc finger protein and a C2C2 steroid receptor-like component. Genes Dev. 4:1128–1140.
   PubMed Web of Science ®Google Scholar
• Shields, G., and J. Sang. 1977. Technical notes. Drosophila Information Service 52:161.
   Google Scholar
• Simcox, A., M. Sobeih, and A. Shearn. 1985. Establishment and characterization of continuous cell lines derived from temperature sensitive mutants of Drosophila melanogaster. Somatic Cell Mol. Genet. 11:63–70.
   PubMedGoogle Scholar
• Steinhauer, W. R., R. C. Walsh, and L. J. Kalfayan. 1989. Sequence and structure of the Drosophila melanogaster ovarian tumor gene and generation of an antibody specific for the ovarian tumor protein. Mol. Cell. Biol. 9:5726–5732.
   PubMed Web of Science ®Google Scholar
• Sullivan, D. T., P. W. Atkinson, C. A. Bayer, and M. A. Menotti-Raymond. 1990. The evolution of Adh expression in the Repleta group of Drosophila, p. 407–417. In J. S. F. Barker, W. T. Starmer, and R. J. MacIntyre (ed.), Ecological and evolutionary genetics of Drosophila. Plenum Publishing Corp., New York.
   Google Scholar
• Sullivan, D. T., P. W. Atkinson, and W. T. Starmer. 1990. Molecular evolution of the alcohol dehydrogenase genes in the genus Drosophila. Evol. Biol. 24:107–147.
   Google Scholar
• Truman, J. W. 1981. Interaction between ecdysteroid, eclosion hormone and bursicon titers in Manduca sexta. Am. Zool. 21:655–661.
   Google Scholar
• Truman, J. W., F. M. Horodyski, R. S. Hewes, and L. M. Riddiford. 1991. Eclosion hormone: from genes to behavior, p. 95–99. In J. J. Menn, T. J. Kelly, and E. P. Masler (ed.), Insect neuropeptides: chemistry, biology, and action. American Chemical Society, Washington, D.C.
   Google Scholar
• Tsai, S. Y., J. Carlstedt-Duke, N. L. Weigel, K. Dahlman, J.-A. Gustafsson, M.-J. Tsai, and B. W. O'Malley. 1988. Molecular interactions of a steroid hormone receptor with its enhancer element: evidence for receptor dimer formation. Cell 55:361–369.
   PubMed Web of Science ®Google Scholar
• Ueda, H., S. Sonoda, J. L. Brown, M. P. Scott, and C. Wu. 1990. A sequence-specific DNA-binding protein that activates fushi tarazu segmentation gene expression. Genes Dev. 4:624–635.
   PubMedGoogle Scholar
• Vinson, C. S., K. L. LaMarco, P. F. Johnson, W. H. Landschulz, and S. L. McKnight. 1988. In situ detection of sequence-specific DNA binding activity specified by a recombinant bacteriophage. Genes Dev. 2:801–806.
   PubMedGoogle Scholar
• Wahli, W., and E. Martinez. 1991. Superfamily of steroid nuclear receptors: positive and negative regulators of gene expression. FASEB J. 5:2243–2249.
   PubMed Web of Science ®Google Scholar
• Wang, L. H., S. Y. Tsai, R. G. Cook, W. G. Beattie, M.-J. Tsai, and B. W. O'Malley. 1989. COUP transcription factor is a member of the steroid receptor superfamily. Nature (London) 340:163–166.
   PubMed Web of Science ®Google Scholar
• Wilson, T. E., T. J. Fahmer, M. Johnston, and J. Milbrandt. 1991. Identification of the DNA binding site for NGFI-B by genetic selection in yeast. Science 252:1296–1300.
   PubMed Web of Science ®Google Scholar