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Conserved (CT) n·(GA) n Repeats in the Non-coding Regions at the Gpdh Locus are Binding Sites for the GAGA Factor in Drosophila melanogaster and its Sibling Species

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Abstract

The (CT) n·(GA) n rich sequences in the upstream and 5′ intron enhancer regions of the sn-glycerol-3-phosphate dehydrogenase (Gpdh) gene in Drosophila melanogaster, its sibling and distantly related species are conserved in their position and in the number of repeats. Using in vitro DNA-footprint analyses we show that the GAGA factor binds to these multiple closely spaced and overlapping conserved (CT) n·(GA) n repeats in D. melanogaster and D. erecta.

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References

  • Bardwell, V.J. & R. Treisman, 1994. The POZ domain-a conserved protein-protein interaction motif. Genes Dev. 8: 1664–1677.

    Google Scholar 

  • Bartoszewski, S. & J.B. Gibson, 1998. Regulation of the expression of the sn-glycerol-3-phosphate dehydrogenase gene in Drosophila melanogaster. Biochem. Genet. 36: 329–350.

    Google Scholar 

  • Bell, A.C., A.G. West & G. Felsenfeld, 2001. Gene regulation insulators and boundaries: versatile regulatory elements in the eukaryotic genome. Science 291: 447–450.

    Google Scholar 

  • Benyajati, C., A. Ewel, J. McKeon, M. Chovav & E. Juan, 1992. Characterization and purification of Adh distal promoter factor 2, Adf-2, a cell-specific and promoter-specific repressor in Drosophila. Nucl. Acids Res. 20: 4481–4489.

    Google Scholar 

  • Benyajati, C., L. Mueller, N. Xu, M. Pappano, J. Gao, M. Mosammaparast, D. Conklin, H. Granok, C. Craig & S. Elgin, 1997. Multiple isoforms of GAGA factor, a critical component of chromatin structure. Nucl. Acids Res. 25: 3345–3353.

    Google Scholar 

  • Bergman, C.M. & M. Kreitman, 2001. Analysis of conserved non-coding DNA in Drosophila reveals similar constraints in intergenic and intronic sequences. Genome Res. 11: 1335–1345.

    Google Scholar 

  • Bewley, G.C., J.L. Cook, S. Kusakabe, T. Mukai, D. Rigby & G. Chambers, 1989. Sequence, structure and evolution of the gene coding for sn-glycerol-3-phosphate dehydrogenase in Drosophila melanogaster. Nucl. Acids Res. 17: 8553–8567.

    Google Scholar 

  • Bhat, K.M., G. Farkas, F. Karch, H. Gyurkovics, J. Gausz & P. Schedl, 1996. The GAGA factor is required in the early Drosophila embryo not only for transcriptional regulation but also for nuclear division. Development 122: 1113–1124.

    Google Scholar 

  • Black, D.M., M.S. Jackson, M.G. Kidwell & G.A. Dover, 1989. KP elements repress P-induced hybrid dysgenesis in Drosophila melanogaster. EMBO J. 6: 4125–4135.

    Google Scholar 

  • Caccone, A., E.N. Moriyama, J.M. Gleason, L. Nigro & J.R. Powell, 1996. A molecular phylogeny for the Drosophila melanogaster subgroup and the problem of polymorphism data. Mol. Biol. Evol. 13: 1224–1232.

    Google Scholar 

  • Chia, W., C. Savakis, R. Karp, H. Pelham & M. Ashburner, 1985. Mutation of the Adh gene of Drosophila melanogaster containing an internal tandem duplication. J. Mol. Biol. 186: 679–688.

    Google Scholar 

  • Cook, J., G. Bewley & J. Shaffer, 1988. Drosophila sn-glycerol-3-phosphate dehydrogenase isozymes are generated by alternate pathways of RNA processing resulting in different carboxyl-terminal amino acid sequence. J. Biol. Chem. 263: 10858–10864.

    Google Scholar 

  • Farkas, G., J. Gausz, M. Galloni, G. Reuter, H. Gyurkovics & F. Karch, 1994. The trithorax-like gene encodes the Drosophila GAGA factor. Nature 371: 806–808.

    Google Scholar 

  • Gibson, J.B., A.V. Wilks, A. Cao & A.L. Freeth, 1986. Dominance for sn-glycerol-3-phosphate dehydrogenase activity in Drosophila melanogaster: evidence for differential allelic expression mediated via a trans-acting effect. Heredity 56: 227–235.

    Google Scholar 

  • Gibson, J.B., A. Cao, J. Symonds & D. Reed, 1991. Low activity sn-glycerol-3-phosphate dehydrogenase variants in natural populations of Drosophila melanogaster. Heredity 66: 75–82.

    Google Scholar 

  • Gibson, J.B., D.S. Reed, S. Bartoszewski & A.V. Wilks, 1999. Structural changes in the promoter region mediate transvection at the sn-glycerol-3-phosphate dehydrogenase gene of Drosophila melanogaster. Biochem. Genet. 37: 301–315.

    Google Scholar 

  • Gilmour, D.S., G.H. Thomas & S.C. Elgin, 1989. Drosophila nuclear proteins bind to regions of alternating C and T residues in gene promoters. Science 245: 1487–1490.

    Google Scholar 

  • Glaser, R.L., G.H. Thomas, E. Siegfried, S. Elgin & J.T. Lis, 1990. Optimal heat-induced expression of the Drosophila hsp26 gene requires a promoter sequence containing (CT)n·(GA)n repeats. J. Mol. Biol. 211: 751–761.

    Google Scholar 

  • Hauck, B., W.J. Gehring & U. Walldorf, 1999. Functional analysis of an eye specific enhancer of the eyeless gene in Drosophila. Proc. Natl. Acad. Sci. USA 96: 564–569.

    Google Scholar 

  • Jareborg, N., E. Birney & R. Durbin, 1999. Comparative analysis of noncoding regions of 77 orthologous mouse and human gene pairs. Genome Res. 9: 815–824.

    Google Scholar 

  • Jiang, C., J.B. Gibson & H. Chen, 1989. Genetic differentiation in populations of Drosophila melanogaster from the People's Republic of China: comparison with patterns on other continents. Heredity 62: 193–198.

    Google Scholar 

  • Kapoun, A.M. & T.C. Kaufman, 1995. Regulatory regions of the homeotic gene proboscipedia are sensitive to chromosomal pairing. Genetics 140: 643–658.

    Google Scholar 

  • Kramer, A., 1996. The structure and function of proteins involved in mammalian pre-mRNA splicing. Ann. Rev. Biochem. 65: 367–409.

    Google Scholar 

  • Lachaise, D.L., M.-L. Cariou, J.R. David, F. Lemeunier & M. Ashburner, 1988. Historical biogeography of the D. melanogaster species subgroup. J. Evol. Biol. 22: 159–226.

    Google Scholar 

  • Lemeunier, F. & M. Ashburner, 1984. Relationships in the melanogaster species subgroup of the genus Drosophila (Sophophora). IV. The chromosomes of two new species. Chromosoma 89: 343–351.

    Google Scholar 

  • Li, W.H., C.C. Luo & C.I. Wu (eds), 1985. Evolution of DNA Sequences. Plenum Press, New York.

    Google Scholar 

  • Lu, Q., L. Wallrath, B. Allan, R. Glaser, J. Lis & S. Elgin, 1992. Promoter sequence containing (CT)n·(GA)n repeats is critical for the formation of the DNaseI hypersensitive sites in the Drosophila hsp26 gene. J. Mol. Biol. 225: 985–998.

    Google Scholar 

  • Lu, Q., L. Wallrath, H. Granok & S. Elgin, 1993. (CT)n·(GA)n repeats and heat shock elements have distinct roles in chromatin and transcriptional activation of the Drosophila hsp26 gene. J. Mol. Cell. Biol. 13: 2802–2814.

    Google Scholar 

  • Mattick, J.S., 1994. Introns: evolution and function. Curr. Opin. Genet. Dev. 4: 823–831.

    Google Scholar 

  • Mattick, J.S., 2001. Non-coding RNAs: the architects of eukaryotic complexity. EMBO Rep. 2: 986–991.

    Google Scholar 

  • Mattick, J.S. & M.J. Gagen, 2001. The evolution of controlled multitasked gene networks: the role of introns and other noncoding RNAs in the development of complex organisms. Mol. Biol. Evol. 18: 1611–1630.

    Google Scholar 

  • Morgenstern, B., 1999. DIALIGN 2: improvement of the segmentto-segment approach to multiple sequence alignment. Bioinformatics 15: 211–218.

    Google Scholar 

  • Newfeld, S.J., R.W. Padgett, S.D. Findley, B.G. Richter, M. Sanicola, M. Decuevas & W.M. Gelbart, 1997. Molecular evolution at the decapentaplegic locus in Drosophila. Genetics 145: 297–309.

    Google Scholar 

  • Omichinski, J.G., P.V. Pedone, G. Felsenfeld, A.M. Gronenborn & G.M. Clore, 1997. The solution structure of a specific GAGA factor-DNA complex reveals a modular binding mode. Nat. Struct. Biol. 4: 122–132.

    Google Scholar 

  • O'Neil, M.T. & J.M. Belote, 1992. Interspecific comparison of the transformer gene of Drosophila reveals an unusually high degree of evolutionary divergence. Genetics 131: 113–128.

    Google Scholar 

  • Papenbrock, T., R.L. Peterson, R.S. Lee, T. Hsu, A. Kuroiwa & A. Awgulewitsch, 1998. Murine hoxc-9 gene contains a structurally and functionally conserved enhancer. Dev. Dyn. 212: 540–547.

    Google Scholar 

  • Quandt, K., K. Frech, H. Karas, E. Wingender & T. Werner, 1995. Matind and matinspector-new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucl. Acids Res. 23: 4878–4884.

    Google Scholar 

  • Reed, D.S., 1989. Molecular analysis of a low activity sn-glycerol-3-phosphate dehydrogenase allele in Drosophila melanogaster. PhD, The Australian National University, Canberra.

    Google Scholar 

  • Reed, D.S. & J.B. Gibson, 1994. Molecular heterogeneity of naturally occurring sn-glycerol-3-phosphate dehydrogenase lowactivity variants in Drosophila melanogaster. Biochem. Genet. 32: 161–179.

    Google Scholar 

  • Soeller, W.C., C.E. Oh & T.B. Kornberg, 1993. Isolation of cDNAs encoding the Drosophila-GAGA transcription factor. Mol. Cell. Biol. 13: 7961–7970.

    Google Scholar 

  • Stallings, R.L., 1995. Conservation and evolution of (CT)(n)/(GA)(n) microsatellite sequences at orthologous positions in diverse mammalian genomes. Genomics 25: 107–113.

    Google Scholar 

  • Symonds, J.E., 1990. Biochemical and molecular studies of snglycerol-3-phosphate dehydrogenase low activity variants in Drosophila melanogaster, PhD, The Australian National University, Canberra.

    Google Scholar 

  • Symonds, J.E. & J.B. Gibson, 1992. Restriction site variation, gene duplication, and the activity of sn-Glycerol-3-phosphate dehydrogenase in Drosophila melanogaster. Biochem. Genet. 30: 169–188.

    Google Scholar 

  • Symonds, J.E., J.B. Gibson, A.V. Wilks & T.M. Wilanowski, 1995. Molecular analysis of a Drosophila melanogaster sn-glycerol-3-phosphate dehydrogenase allozyme variant that has cold labile activity. Insect Biochem. Mol. Biol. 25: 789–798.

    Google Scholar 

  • Thompson, J.D., D.G. Higgins & T.J. Gibson, 1994. ClustalW-improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673–4680.

    Google Scholar 

  • Tominaga, H. & S. Narise, 1995. Sequence evolution of the Gpdh gene in the Drosophila virilis species group. Genetica 96: 293–302.

    Google Scholar 

  • Tominaga, H., T. Shiba & S. Narise, 1992. Structure of Drosophila virilis glycerol-3-phosphate dehydrogenase gene and comparison with the Drosophila melanogaster gene. J. Biochim. Biophys. Acta 1131: 233–238.

    Google Scholar 

  • Tsukiyama, T. & C. Wu, 1996. Purification of GAGA factor and its role in nucleosome disruption. Meth. Enzymol. 274: 291–299.

    Google Scholar 

  • Tsukiyama, T., P. Becker & C. Wu, 1994. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature 367: 525–532.

    Google Scholar 

  • von Kalm, L., J. Weaver, J. Demarco, R. Macintyre & D.T. Sullivan, 1989. Structural characterization of the sn-glycerol-3-phosphate dehydrogenase-encoding gene of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 86: 5020–5024.

    Google Scholar 

  • Wells, R.S., 1995. Sequence and evolution of the Drosophila pseudoobscura glycerol-3-phosphate dehydrogenase locus. J. Mol. Evol. 41: 886–893.

    Google Scholar 

  • Wilanowski, T.M., J.B. Gibson & J.E. Symonds, 1995. Retrotransposon insertion induces an isozyme of sn-glycerol-3-phosphate dehydrogenase in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 92: 12065–12069.

    Google Scholar 

  • Wilkins, R.C. & J.T. Lis, 1998. GAGA factor binding to DNA via a single trinucleotide sequence element. Nucl. Acids Res. 26: 2672–2678.

    Google Scholar 

  • Wilkins, R.C. & J.T. Lis, 1999. DNA distortion and multimerization: novel functions of the glutamine-rich domain of GAGA factor. J. Mol. Biol. 285: 515–525.

    Google Scholar 

  • Wingender, E., X. Chen, R. Hehl, H. Karas, I. Liebich, V. Matys, T. Meinhardt, M. Pruss, I. Reuter & F. Schacherer, 2000. TRANSFAC: an integrated system for gene expression regulation. Nucl. Acids Res. 28: 316–319.

    Google Scholar 

  • Xu, G. & A.G. Goodridge, 1998. A CT repeat in the promoter of the chicken malic enzyme gene is essential for function at an alternative transcription start site. Arch. Biochem. Biophys. 358: 83–91.

    Google Scholar 

  • Zollman, S., D. Godt, G. Prive, J. Couderc & F. Laski, 1994. The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc. Natl. Acad. Sci. USA 91: 10717–10721.

    Google Scholar 

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Tchoubrieva, E., Gibson, J. Conserved (CT) n·(GA) n Repeats in the Non-coding Regions at the Gpdh Locus are Binding Sites for the GAGA Factor in Drosophila melanogaster and its Sibling Species. Genetica 121, 55–63 (2004). https://doi.org/10.1023/B:GENE.0000019922.36436.3c

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