A Binding Site for Multiple Transcriptional Activators in the fushi tarazu Proximal Enhancer Is Essential for Gene Expression In Vivo

REFERENCES

• Akam, M. 1987. The molecular basis for metameric pattern in the Drosophila embryo. Development 101: 1–22.
   PubMedGoogle Scholar
• Ausubel, F. M., R. Brent, R. E. Kingston, D. P. Moore, J. G. Seidman, J. A. Smith, and K. Struhl 1992. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
   Google Scholar
• Ayer, S., N. Walker, M. Mosammaparast, J. P. Nelson, B. Z. Shilo, and C. Benyajati 1993. Activation and repression of Drosophila alcohol dehydrogenase distal transcription by two steroid hormone receptor superfamily members binding to a common response element. Nucleic Acids Res. 21: 1619–1627.
   PubMedGoogle Scholar
• Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254.
   PubMed Web of Science ®Google Scholar
• Briggs, M. R., J. T. Kadonaga, S. P. Bell, and R. Tjian 1986. Purification and biochemical characterization of the promoter-specific transcription factor Sp1. Science 234: 47–52.
   PubMed Web of Science ®Google Scholar
• Brown, J. L., S. Sonoda, H. Oeda, M. P. Scott, and C. Wu 1991. Repression of the Drosophila fushi tarazu (ftz) segmentation gene. EMBO J. 10: 665–674.
   PubMedGoogle Scholar
• Brown, J. L., and C. Wu 1993. Repression of Drosophila pair-rule segmentation genes by ectopic expression of tramtrack. Development 117: 45–58.
   PubMedGoogle Scholar
• Clark, K. A., and D. M. McKearin 1996. The Drosophila stonewall gene encodes a putative transcription factor essential for germ cell development. Development 122: 937–950.
   PubMedGoogle Scholar
• Cohn, N. S. 1992. P. sativum GA mRNA (clone F) similar to ribosomal protein L9. GenBank accession no. X65155.
   Google Scholar
• Colicelli, J., C. Birchmeier, T. Michaeli, K. O’Neill, M. Riggs, and M. Wigler 1989. Isolation and characterization of a mammalian gene encoding a high-affinity cAMP phosphodiesterase. Proc. Natl. Acad. Sci. USA 86: 3599–3603.
   PubMedGoogle Scholar
• Desplan, C., J. Theis, and P. H. O’Farrell 1985. The Drosophila developmental gene, engrailed, encodes sequence-specific DNA binding activity. Nature 318: 630–635.
   PubMedGoogle Scholar
• England, B. P., A. Admon, and R. Tjian 1992. Cloning of Drosophila transcription factor Adf-1 reveals homology to Myb oncoprotein. Proc. Natl. Acad. Sci. USA 89: 683–687.
   PubMedGoogle Scholar
• England, B. P., 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
• Florence, B., R. Handrow, and A. Laughon 1991. DNA-binding specificity of the fushi tarazu homeodomain. Mol. Cell. Biol. 11: 3613–3623.
   PubMedGoogle Scholar
• Frasch, M., R. Warrior, J. Tugwood, and M. Levine 1988. Molecular analysis of even-skipped mutants in Drosophila development. Genes Dev. 2: 1824–1838.
   PubMed Web of Science ®Google Scholar
• Goto, T., P. Murdonald, and T. Maniatis 1989. Early and late periodic patterns of even-skipped expression are controlled by distinct regulatory elements that respond to different spatial cues. Cell 57: 413–422.
   PubMedGoogle Scholar
• Gross, C. T., and W. McGinnis 1996. DEAF-1, a novel protein that binds an essential region in a Deformed response element. EMBO J. 15: 1961–1970.
   PubMed Web of Science ®Google Scholar
• Guichet, A., J. W. R. Copeland, M. Erdelyi, D. Hlousek, P. Zavorszky, J. Ho, S. Brown, A. Percival-Smith, H. M. Krause, and A. Ephrussi 1997. The nuclear receptor homologue Ftz-F1 and the homeodomain protein Ftz are mutually dependent cofactors. Nature 385: 548–552.
   PubMedGoogle Scholar
• Gutjahr, T., E. Frei, and M. Noll 1993. Complex regulation of early paired expression: initial activation by gap genes and pattern modulation by pair-rule genes. Development 117: 609–623.
   PubMedGoogle Scholar
• Hafen, E., A. Kuroiwa, and W. J. Gehring 1984. Spatial distribution of transcripts from the segmentation gene fushi tarazu during Drosophila embryonic development. Cell 37: 833–841.
   PubMedGoogle Scholar
• Han, W. 1994. Ph.D. thesis. Mt. Sinai School of Medicine, New York, N.Y.
   Google Scholar
• Han, W., Y. Yu, N. Altan, and L. Pick 1993. Multiple proteins interact with the fushi tarazu proximal enhancer. Mol. Cell. Biol. 13: 5549–5559.
   PubMedGoogle Scholar
• Harding, K., T. Hoey, W. Warrior, and M. Levine 1989. Auto-regulatory and gap response elements of the even-skipped promoter of Drosophila. EMBO J. 8: 1205–1212.
   PubMedGoogle Scholar
• Harrison, S. D., and A. Travers 1988. Identification of the binding sites for potential regulation proteins in the upstream enhancer element of Drosophila fushi tarazu gene. Nucleic Acids Res. 16: 11403–11416.
   PubMedGoogle Scholar
• Harrison, S. D., and A. Travers 1990. The tramtrack gene in Drosophila encodes a zinc finger protein that interacts with the ftz transcriptional regulatory region and shows a novel embryonic expression pattern. EMBO J. 9: 207–216.
   PubMedGoogle 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
• Hiromi, Y., and W. J. Gehring 1987. Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell 50: 963–974.
   PubMedGoogle Scholar
• Hiromi, Y., A. Kuroiwa, and W. J. Gehring 1985. Control elements of the Drosophila segmentation gene fushi tarazu. Cell 43: 603–613.
   PubMed Web of Science ®Google Scholar
• Hori, N., K. Murakawa, R. Matoba, A. Fukushima, K. Okubo, and K. Matsubara 1993. A new human ribosomal protein sequence, homologue of rat L9. Nucleic Acids Res. 21: 4395.
   PubMedGoogle Scholar
• Innis, M. A., and D. H. Gelfand 1990. Optimization of PCRs in PCR protocols: a guide to methods and applications. Academic Press, Inc., San Diego, Calif.
   Google Scholar
• Innis, M. B., D. H. Myambo, D. H. Gelfand, and M. A. Drow 1988. DNA sequencing with thermus aquaticus DNA polymerase and direct sequencing of polymerase chain reaction-amplified DNA. Proc. Natl. Acad. Sci. USA 85: 9436–9440.
   PubMed Web of Science ®Google Scholar
• Jiang, J., T. Hoey, and L. Levine 1991. Autoregulation of a segmentation gene in Drosophila: combinatorial interaction of the even-skipped homeo box protein with a distal enhancer element. Genes Dev. 5: 265–277.
   PubMedGoogle Scholar
• Jones, D. G., U. Reusser, and G. H. Braus 1991. Cloning and characterization of a yeast homolog of the mammalian ribosomal protein L9. Nucleic Acids Res. 19: 5785.
   PubMedGoogle Scholar
• Jost, W., Y. Yu, L. Pick, A. Preiss, and D. Maier 1995. Structure and regulation of the fushi tarazu gene from Drosophila hydei. Roux’s Arch. Dev. Biol. 205: 160–170.
   Google Scholar
• Kadonaga, J. T., 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
• Kishore, G. M., and D. M. Shah 1988. Amino acid biosynthesis inhibitors as herbicides. Annu. Rev. Biochem 57: 627–663.
   PubMed Web of Science ®Google Scholar
• Kuroiwa, A., E. Hafen, and W. J. Gehring 1984. Cloning and transcriptional analysis of the segmentation gene fushi tarazu of Drosophila. Cell 37: 825–831.
   PubMedGoogle Scholar
• Laney, J. D., and M. D. Biggin 1996. Redundant control of Ultrabithorax by zeste involves functional levels of zeste protein binding at the Ultrabithorax promoter. Development 122: 2303–2311.
   PubMedGoogle Scholar
• Laughon, A., and M. P. Scott 1984. Sequence of a Drosophila segmentation gene: protein structure homology with DNA-binding proteins. Nature 310: 25–31.
   PubMedGoogle Scholar
• Lavorgna, G., H. Leda, J. Clos, and C. Wu 1991. FTZ-F1, a steroid hormone receptor-like protein implicated in the activation of fushi tarazu. Science 252: 848–851.
   PubMed Web of Science ®Google Scholar
• Maier, D., A. Press, and J. R. Powell 1990. Regulation of the segmentation gene fushi tarazu has been functionally conserved in Drosophila. EMBO J. 9: 3957–3966.
   PubMedGoogle Scholar
• McCombie, W. R., J. M. Kelley, J. C. Venter, and C. A. Fields 1993. Caenorhabditis elegans cDNA clone CEESK81 similar to ribosomal protein L9. GenBank accession no. T00931.
   Google Scholar
• McGinnis, W., and R. Krumlauf 1992. Homeobox genes and axial patterning. Cell 68: 283–302.
   PubMed Web of Science ®Google Scholar
• Nelson, H., and A. Laughon 1993. Drosophila glial architecture and development: analysis using a collection of new cell-specific markers. Roux’s Arch. Dev. Biol. 202: 341–354.
   Google Scholar
• Nusslein-Volhard, C., and E. Wieschaus 1980. Mutations affecting segment number and polarity in Drosophila. Nature 287: 795–801.
   PubMed Web of Science ®Google Scholar
• Ohno, C., H. Ueda, and M. Petkovich 1994. The Drosophila nuclear receptors FTZ-F1a and FTZ-F1b compete as monomers for binding to a site in the fushi tarazu gene. Mol. Cell. Biol. 14: 3166–3175.
   PubMedGoogle Scholar
• Percival-Smith, A., M. Muller, M. Affolter, and W. J. Gehring 1990. The interaction with DNA of wild-type and mutant fushi tarazu homeodomains. EMBO J. 9: 1209–1223.
   PubMedGoogle Scholar
• Pick, L., A. F. Schier, M. Affolter, T. Schmidt-Glenewinkel, and W. J. Gehring 1990. Analysis of the ftz upstream element: germ layer-specific enhancers are independently autoregulated. Genes Dev. 4: 1224–1239.
   PubMedGoogle Scholar
• Read, D., T. Nishigaki, and J. T. Manley 1990. The Drosophila even-skipped promoter is transcribed in a stage-specific manner in vitro and contains multiple, overlapping factor-binding sites. Mol. Cell. Biol. 10: 4334–4344.
   PubMedGoogle Scholar
• Read, D. B. 1992. Ph.D. thesis. Columbia University, New York, N.Y.
   Google Scholar
• Rubin, G. M., and A. C. Spradling 1982. Genetic transformation of Drosophila with transposable element vectors. Science 218: 348–353.
   PubMed Web of Science ®Google Scholar
• Sanger, F., S. Nicklen, and A. R. Coulson 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463–5467.
   PubMed Web of Science ®Google Scholar
• Schier, A. F., and W. J. Gehring 1992. Direct homeodomain-DNA interaction in the autoregulation of the fushi tarazu gene. Nature 356: 804–807.
   PubMed Web of Science ®Google Scholar
• Schier, A. F., and W. J. Gehring 1993. Analysis of a fushi tarazu autoregulatory element: multiple sequence elements contribute to enhancer activity. EMBO J. 12: 1111–1119.
   PubMedGoogle Scholar
• Soeller, W. C., S. J. Pook, and T. Kornberg 1988. In vitro transcription of the Drosophila engrailed gene. Genes Dev. 2: 68–81.
   PubMedGoogle Scholar
• Staudt, L. M., and M. J. Lenardo 1991. Immunoglobulin gene transcription. Annu. Rev. Immunol. 9: 373–398.
   PubMed Web of Science ®Google Scholar
• Steffan, N. H., H. D. Hunt, and L. R. Pease 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51–59.
   PubMedGoogle Scholar
• Struhl, G. 1985. Near-reciprocal phenotypes caused by inactivation or indiscriminate expression of the Drosophila segmentation gene ftz. Nature 318: 677–680.
   PubMedGoogle Scholar
• Su, K., M. Yussa, and L. Pick. Unpublished data.
   Google Scholar
• Suzuki, K., J. Olvera, and I. G. Wool 1990. The primary structure of rat ribosomal protein L9. Gene 93: 297–300.
   PubMedGoogle Scholar
• Thummel, C. S. 1995. From embryogenesis to metamorphosis: the regulation and function of Drosophila nuclear receptor superfamily members. Cell 83: 871–877.
   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
• Vasisht, V., and S. Small. Personal communication.
   Google Scholar
• Wakimoto, B. T., F. R. Turner, and T. C. Kaufman 1984. Defects in embryogenesis in mutants associated with the Antennapedia gene complex of Drosophila melanogaster. Dev. Biol. 102: 147–172.
   PubMedGoogle Scholar
• Wamplar, S. L., C. M. Tyree, and J. T. Kadonaga 1990. Fraction of the general RNA polymerase II transcription factors from Drosophila embryos. J. Biol. Chem. 265: 21223–21231.
   PubMedGoogle Scholar
• Yu, Y., W. Li, K. Su, W. Han, M. Yussa, N. Perrimon, and L. Pick 1997. The nuclear hormone receptor FTZ-F1 is a cofactor for the Drosophila homeodomain protein Ftz. Nature 385: 552–555.
   PubMedGoogle Scholar
• Yu, Y., and L. Pick 1995. Non-periodic cues generate seven ftz stripes in the Drosophila embryo. Mech. Dev. 50: 163–175.
   PubMedGoogle Scholar
• Yu, Y., and L. Pick. Unpublished data.
   Google Scholar
• Yussa, M. 1997. Ph.D. thesis. Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
   Google Scholar
• Zeng, C., J. Pinsonneault, G. Gellon, N. McGinnis, and W. McGinnis 1994. Deformed protein binding sites and cofactor binding sites are required for the function of a small segment-specific regulatory element in Drosophila embryos. EMBO J. 13: 2362–2377.
   PubMedGoogle Scholar
• Zenke, M., T. Grundstrom, H. Matthes, M. Wintzerith, C. Schatz, A. Wildeman, and P. Chambon 1986. Multiple sequence motifs are involved in SV40 enhancer function. EMBO J. 5: 387–397.
   PubMed Web of Science ®Google Scholar