Functional Interaction between the Fab-7 and Fab-8 Boundaries and the Upstream Promoter Region in the Drosophila Abd-B Gene

REFERENCES

• Akbari, O. S., A. Bousum, E. Bae, and R. A. Drewell. 2006. Unraveling cis-regulatory mechanisms at the Abdominal-A and Abdominal-B genes in the Drosophila bithorax complex. Dev. Biol. 293:294–304.
   PubMedGoogle Scholar
• Akbari, O. S., E. Bae, H. Johnsen, A. Villaluz, D. Wong, and R. A. Drewell. 2008. A novel promoter-tethering element regulates enhancer-driven gene expression at the bithorax complex in the Drosophila embryo. Development 135:123–131.
   PubMedGoogle Scholar
• Bantignies, F., C. Grimaud, S. Lavrov, M. Gabut, and G. Cavalli. 2003. Inheritance of Polycomb-dependent chromosomal interactions in Drosophila. Genes Dev. 17:2406–2420.
   PubMed Web of Science ®Google Scholar
• Barges, S., J. Mihaly, M. Galloni, K. Hagstrom, M. Muller, G. Shanower, P. Schedl, H. Gyurkovics, and F. Karch. 2000. The Fab-8 boundary defines the distal limit of the bithorax complex iab-7 domain and insulates iab-7 from initiation elements and a PRE in the adjacent iab-8 domain. Development 127:779–790.
   PubMedGoogle Scholar
• Boulet, A. M., A. Lloyd, and S. Sakonju. 1991. Molecular definition of the morphogenetic and regulatory functions and the cis-regulatory elements of the Drosophila Abd-B homeotic gene. Development 111:393–405.
   PubMedGoogle Scholar
• Brasset, E., and C. Vaury. 2005. Insulators and fundamental components of the eukaryotic genomes. Heredity 94:571–576.
   PubMedGoogle Scholar
• Busturia, A., and M. Bienz. 1993. Silencers in abdominal-B, a homeotic Drosophila gene. EMBO J. 12:1415–1425.
   PubMedGoogle Scholar
• Busturia, A., C. D. Wightman, and S. Sakonju. 1997. A silencer is required for maintenance of transcriptional repression throughout Drosophila development. Development 124:4343–4350.
   PubMedGoogle Scholar
• Celniker, S. E., S. Sharma, D. J. Keelan, and E. B. Lewis. 1990. The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. EMBO J. 9:4227–4286.
   Google Scholar
• Chambeyron, S., and W. A. Bickmore. 2004. Does looping and clustering in the nucleus regulate gene expression? Curr. Opin. Cell Biol. 16:256–262.
   PubMed Web of Science ®Google Scholar
• Chen, Q., L. Lin, S. Smith, Q. Lin, and J. Zhou. 2005. Multiple promoter targeting sequences exist in Abdominal-B to regulate long-range gene activation. Dev. Biol. 286:629–636.
   PubMedGoogle Scholar
• Cleard, F., Y. Moshkin, F. Karch, and R. K. Maeda. 2006. Probing long-distance regulatory interactions in the Drosophila melanogaster bithorax complex using Dam identification. Nat. Genet. 38:931–935.
   PubMedGoogle Scholar
• Comet, I., E. Savitskaya, B. Schuettengruber, N. Negre, S. Lavrov, A. Parshikov, F. Juge, E. Gracheva, P. Georgiev, and G. Cavalli. 2006. PRE-mediated bypass of two Su(Hw) insulators targets PcG proteins to a downstream promoter. Dev. Cell 11:117–124.
   PubMedGoogle Scholar
• de Laat, W., and F. Grosveld. 2003. Spatial organization of gene expression: the active chromatin hub. Chromosome Res. 11:447–459.
   PubMedGoogle Scholar
• Dillon, N., and P. Sabbattini. 2000. Functional gene expression domains: defining functional unit of eukaryotic gene regulation. BioEssays 22:657–665.
   PubMedGoogle Scholar
• Dorsett, D. 1999. Distant liaisons: long range enhancer-promoter interactions in Drosophila. Curr. Opin. Genet. 9:505–514.
   PubMedGoogle Scholar
• Duncan, I. 1987. The bithorax complex. Annu. Rev. Genet. 21:285–319.
   PubMedGoogle Scholar
• Fraser, P., and W. Bickmore. 2007. Nuclear organization of the genome and the potential for gene regulation. Nature 447:413–417.
   PubMed Web of Science ®Google Scholar
• Galloni, M., H. Gyurkovics, P. Schedl, and F. Karch. 1993. The bluetail transposon: evidence for independent cis-regulatory domains and domain boundaries in the bithorax complex. EMBO J. 12:1087–1097.
   PubMedGoogle Scholar
• Geyer, P. K., and V. G. Corces. 1987. Separate regulatory elements are responsible for the complex pattern of tissue-specific and developmental transcription of the yellow locus in Drosophila melanogaster. Genes Dev. 1:996–1004.
   PubMedGoogle Scholar
• Golic, K. G., and S. Lindquist. 1989. The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59:499–509.
   PubMed Web of Science ®Google Scholar
• Gruzdeva, N., O. Kyrchanova, A. Parshikov, A. Kullyev, and P. Georgiev. 2005. The Mcp element from the bithorax complex contains an insulator that is capable of pairwise interactions and can facilitate enhancer-promoter communication. Mol. Cell. Biol. 25:3682–3689.
   PubMedGoogle Scholar
• Gyurkovics, H., J. Gausz, J. Kummer, and F. Karch. 1990. A new homeotic mutation in the Drosophila bithorax complex removes a boundary separating two domains of regulation. EMBO J. 9:2579–2585.
   PubMedGoogle Scholar
• Hagstrom, K., M. Muller, and P. Schedl. 1996. Fab-7 functions as a chromatin domain boundary to ensure proper segment specification by the Drosophila bithorax complex. Genes Dev. 10:3202–3215.
   PubMedGoogle Scholar
• Hagstrom, K., M. Muller, and P. Schedl. 1997. A Polycomb and GAGA dependent silencer adjoin the Fab-7 boundary in the Drosophila bithorax complex. Genetics 146:1365–1380.
   PubMedGoogle Scholar
• Hogga, I., J. Mihaly, S. Barges, and F. Karch. 2001. Replacement of Fab-7 by the gypsy or scs insulator disrupts long-distance regulatory interactions in the Abd-B gene of the bithorax complex. Mol. Cell 8:1145–1151.
   PubMedGoogle Scholar
• Holohan, E. E., C. Kwong, B. Adryan, M. Bartkuhn, M. Herold, R. Renkawitz, S. Russel, and R. White. 2007. CTCF genomic binding sites in Drosophila and the organization of the bithorax complex. PLOS Genet. 3:e112.
   PubMedGoogle Scholar
• Karch, F., B. Weiffenbach, M. Peifer, W. Bender, I. Duncan, S. Celniker, M. Crosby, and E. B. Lewis. 1985. The abdominal region of the bithorax complex. Cell 43:81–96.
   PubMedGoogle Scholar
• Karch, F., M. Galloni, L. Sipos, J. Gausz, H. Gyurkovics, and P. Schedl. 1994. Mcp and Fab-7: molecular analysis of putative boundaries of cis-regulatory domains in the bithorax complex of Drosophila melanogaster. Nucleic Acids Res. 22:3138–3146.
   PubMedGoogle Scholar
• Karess, R. E., and G. M. Rubin. 1984. Analysis of P transposable element functions in Drosophila. Cell 38:135–146.
   PubMedGoogle Scholar
• Kravchenko, E., E. Savitskaya, O. Kravchuk, A. Parshikov, P. Georgiev, and M. Savitsky. 2005. Pairing between gypsy insulators facilitates the enhancer action in trans throughout the Drosophila genome. Mol. Cell. Biol. 25:9283–9291.
   PubMedGoogle Scholar
• Kuhn, E. J., and P. K. Geyer. 2003. Genomic insulators: connecting properties to mechanism. Curr. Opin. Cell Biol. 15:259–265.
   PubMedGoogle Scholar
• Kyrchanova, O., S. Toshchakov, A. Parshikov, and P. Georgiev. 2007. Study of the functional interaction between Mcp insulators from the Drosophila bithorax complex: effects of insulator pairing on enhancer-promoter communication. Mol. Cell. Biol. 27:3035–3043.
   PubMedGoogle Scholar
• Lanzuolo, C., V. Roure, J. Dekker, F. Bantignies, and V. Orlando. 2007. Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Nat. Cell Biol. 9:1167–1174.
   PubMed Web of Science ®Google Scholar
• Levine, M. R., and R. Tjian. 2003. Transcription regulation and animal diversity. Nature 424:147–151.
   PubMed Web of Science ®Google Scholar
• Lewis, E. B. 1978. A gene complex controlling segmentation in Drosophila. Nature 276:565–570.
   PubMed Web of Science ®Google Scholar
• Lin, Q., D. Wu, and J. Zhou. 2003. The promoter targeting sequence facilitates and restricts a distant enhancer to a single promoter in the Drosophila embryo. Development 130:519–526.
   PubMedGoogle Scholar
• Lin, Q., Q. Chen, L. Lin, and J. Zhou. 2004. The promoter targeting sequence mediates epigenetically heritable transcription memory. Genes Dev. 18:2639–2651.
   PubMedGoogle Scholar
• Lin, Q., Q. Chen, L. Lin, S. Smith, and J. Zhou. 2007. Promoter targeting sequence mediates enhancer interference in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 104:3237–3242.
   PubMedGoogle Scholar
• Ling, J. Q., T. Li, J. F. Hu, T. H. Vu, H. L. Chen, X. W. Qiu, A. M. Cherry, and A. R. Hoffman. 2006. CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1. Science 312:269–272.
   PubMed Web of Science ®Google Scholar
• Maeda, R. K., and F. Karch. 2006. The ABC of the BX-C: the bithorax complex explained. Development 133:1413–1422.
   PubMedGoogle Scholar
• Maeda, R. K., and F. Karch. 2007. Making connections: boundaries and insulators in Drosophila. Curr. Opin. Genet. Dev. 17:394–399.
   PubMedGoogle Scholar
• Maksimenko, O. G., D. A. Chetverina, and P. G. Georgiev. 2006. Insulators of higher eukaryotes: properties, mechanisms of action, and role in transcription regulation. Genetika 42:1029–1044.
   PubMedGoogle Scholar
• Martin, C. H., C. A. Mayeda, C. A. Davis, C. L. Ericsson, J. D. Knafels, D. R. Mathog, S. E. Celniker, E. B. Lewis, and M. J. Palazzolo. 1995. Complete sequence of the bithorax complex of Drosophila. Proc. Natl. Acad. Sci. USA 92:8398–8402.
   PubMedGoogle Scholar
• McCall, K., M. B. O'Connor, and W. Bender. 1994. Enhancer traps in the Drosophila bithorax complex mark parasegmental domains. Genetics 138:387–399.
   PubMedGoogle Scholar
• Mihaly, J., I. Hogga, J. Gausz, H. Gyurkovics, and F. Karch. 1997. In situ dissection of the Fab-7 region of the bithorax complex into a chromatin domain boundary and a Polycomb-response element. Development 124:1809–1820.
   PubMedGoogle Scholar
• Mihaly, J., I. Hogga, S. Barges, M. Galloni, R. K. Mishra, K. Hagstrom, M. Muller, P. Schedl, L. Sipos, J. Gausz, H. Gyurkovics, and F. Karch. 1998. Chromatin domain boundaries in the bithorax complex. Cell Mol. Life Sci. 54:60–70.
   PubMed Web of Science ®Google Scholar
• Mihaly, J., S. Barges, L. Sipos, R. Maeda, F. Cleard, I. Hogga, W. Bender, H. Gyurkovics, and F. Karch. 2006. Dissecting the regulatory landscape of the Abd-B gene of the bithorax complex. Development 133:2983–2993.
   PubMedGoogle Scholar
• Mohan, M., M. Bartkuhn, M. Herold, A. Philippen, N. Heinl, I. Bardenhagen, J. Leers, R. A. H. White, R. Renkawitz-Pohl, Harald Saumweber, and R. Renkawitz. 2007. The Drosophila insulator proteins CTCF and CP190 link enhancer blocking to body patterning. EMBO J. 26:4203–4214.
   PubMedGoogle Scholar
• Moon, H., G. Filippova, D. Loukinov, E. Pugacheva, Q. Chen, S. T. Smith, A. Munhall, B. Grewe, M. Bartkuhn, R. Arnold, L. J. Burke, R. Renkawitz-Pohl, R. Ohlsson, J. Zhou, R. Renkawitz, and V. Lobanenkov. 2005. CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator. EMBO Rep. 6:165–170.
   PubMedGoogle Scholar
• Muller, M., K. Hagstrom, H. Gyurkovics, V. Pirrotta, and P. Schedl. 1999. The Mcp element from the Drosophila melanogaster bithorax complex mediates long-distance regulatory interactions. Genetics 153:1333–1356.
   PubMedGoogle Scholar
• Petrascheck, M., D. Escher, T. Mahmoudi, C. P. Verrijer, W. Schaffner, and A. Barberis. 2005. DNA looping induced by a transcriptional enhancer in vivo. Nucleic Acids Res. 33:3743–3750.
   PubMedGoogle Scholar
• Ptashne, M. 1986. Gene regulation by proteins acting nearby and at distance. Nature 322:697–701.
   PubMed Web of Science ®Google Scholar
• Rodin, S., O. Kyrchanova, E. Pomerantseva, A. Parshikov, and P. Georgiev. 2007. New properties of Drosophila Fab-7 insulator. Genetics 177:113–121.
   PubMedGoogle Scholar
• Sanchez-Herrero, E., I. Vernos, R. Marco, and G. Morato. 1985. Genetic organization of Drosophila bithorax complex. Nature 313:108–113.
   PubMedGoogle Scholar
• Sanchez-Herrero, E. 1991. Control of the expression of the bithorax complex abdominal-A and Abdominal-B by cis-regulatory regions in Drosophila embryos. Development 111:437–448.
   PubMedGoogle Scholar
• Savitskaya, E., L. Melnikova, M. Kostuchenko, E. Kravchenko, E. Pomerantseva, T. Boikova, D. Chetverina, A. Parshikov, P. Zobacheva, E. Gracheva, A. Galkin, and P. Georgiev. 2006. Study of long-distance functional interactions between Su(Hw) insulators that can regulate enhancer-promoter communication in Drosophila melanogaster. Mol. Cell. Biol. 26:754–761.
   PubMedGoogle Scholar
• Schwartz, Y. B., T. G. Kahn, D. A. Nix, X. Y. Li, R. Bourgon, M. Biggin, and V. Pirrotta. 2006. Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat. Genet. 38:700–705.
   PubMed Web of Science ®Google Scholar
• Schweinsberg, S., and P. Schedl. 2004. Developmental modulation of Fab-7 boundary function. Development 131:4743–4749.
   PubMedGoogle Scholar
• Schweinsberg, S., K. Hagstrom, D. Gohl, P. Schedl, R. P. Kumar, R. Mishra, and F. Karch. 2004. The enhancer-blocking activity of the Fab-7 boundary from the Drosophila bithorax complex requires GAGA-factor-binding sites. Genetics 168:1371–1384.
   PubMedGoogle Scholar
• Siegal, M. L., and D. L. Hartl. 2000. Application of Cre/loxP in Drosophila. Site-specific recombination and transgene co-placement. Methods Mol. Biol. 136:487–495.
   PubMedGoogle Scholar
• Sipos, L., J. Mihaly, F. Karch, P. Schedl, J. Gausz, and H. Gyurkovics. 1998. Transvection in the Drosophila Abd-B domain: extensive upstream sequences are involved in anchoring distant cis-regulatory regions to the promoter. Genetics 149:1031–1050.
   PubMedGoogle Scholar
• Sipos, L., and H. Gyurkovics. 2005. Long-distance interactions between enhancers and promoters. The case of the Abd-B domain of the Drosophila bithorax complex. FEBS J. 272:3253–3259.
   Google Scholar
• Valenzuela, L., and R. T. Kamakaka. 2006. Chromatin insulators. Annu. Rev. Genet. 40:107–138.
   PubMedGoogle Scholar
• Vazquez, J., M. Muller, V. Pirrotta, and J. W. Sedat. 2006. The Mcp element mediates stable long-range chromosome-chromosome interactions in Drosophila. Mol. Biol. Cell 17:2158–2165.
   PubMed Web of Science ®Google Scholar
• Wallace, J. A., and G. Felsenfeld. 2007. We gather together: insulators and genome organization. Curr. Opin. Genet. Dev. 17:400–407.
   PubMed Web of Science ®Google Scholar
• West, A. G., and P. Fraser. 2005. Remote control of gene transcription. Hum. Mol. Genet. 14:R101–R111.
   PubMed Web of Science ®Google Scholar
• Zhao, H., and A. Dean. 2005. Organizing the genome: enhancers and insulators. Biochem. Cell Biol. 83:516–524.
   PubMedGoogle Scholar
• Zhou, J., and M. Levine. 1999. A novel cis-regulatory element, the PTS, mediates an anti-insulator activity in the Drosophila embryo. Cell 99:567–575.
   PubMedGoogle Scholar
• Zhou, J., S. Barolo, P. Szymanski, and M. Levine. 1996. The Fab-7 element of the bithorax complex attenuates enhancer-promoter interactions in the Drosophila embryo. Genes Dev. 10:3195–3201.
   PubMedGoogle Scholar
• Zhou, J., H. Ashe, C. Burks, and M. Levine. 1999. Characterization of the transvection mediating region of the Abdominal-B locus in Drosophila. Development 126:3057–3065.
   PubMedGoogle Scholar