An Organizational Hub of Developmentally Regulated Chromatin Loops in the Drosophila Antennapedia Complex

REFERENCES

• Dean A. 2011. In the loop: long range chromatin interactions and gene regulation. Brief Funct Genomics 10:3–10. http://dx.doi.org/10.1093/bfgp/elq033.
   PubMed Web of Science ®Google Scholar
• Murrell A. 2011. Setting up and maintaining differential insulators and boundaries for genomic imprinting. Biochem Cell Biol 89:469–478. http://dx.doi.org/10.1139/o11-043.
   PubMedGoogle Scholar
• Yang J, Corces VG. 2011. Chromatin insulators: a role in nuclear organization and gene expression. Adv Cancer Res 110:43–76. http://dx.doi.org/10.1016/B978-0-12-386469-7.00003-7.
   PubMedGoogle Scholar
• Holwerda SJ, de Laat W. 2013. CTCF: the protein, the binding partners, the binding sites and their chromatin loops. Philos Trans R Soc Lond B Biol Sci 368:20120369. http://dx.doi.org/10.1098/rstb.2012.0369.
   PubMed Web of Science ®Google Scholar
• Maksimenko O, Georgiev P. 2014. Mechanisms and proteins involved in long-distance interactions. Front Genet 5:28.
   PubMedGoogle Scholar
• Celniker SE, Drewell RA. 2007. Chromatin looping mediates boundary element promoter interactions. Bioessays 29:7–10. http://dx.doi.org/10.1002/bies.20520.
   PubMedGoogle Scholar
• Van Bortle K, Corces VG. 2013. The role of chromatin insulators in nuclear architecture and genome function. Curr Opin Genet Dev 23:212–218. http://dx.doi.org/10.1016/j.gde.2012.11.003.
   PubMedGoogle Scholar
• Chetverina D, Aoki T, Erokhin M, Georgiev P, Schedl P. 2014. Making connections: insulators organize eukaryotic chromosomes into independent cis-regulatory networks. Bioessays 36:163–172. http://dx.doi.org/10.1002/bies.201300125.
   PubMed Web of Science ®Google Scholar
• Holwerda S, de Laat W. 2012. Chromatin loops, gene positioning, and gene expression. Front Genet 3:217.
   PubMedGoogle Scholar
• Xu Z, Felsenfeld G. 2012. Order from chaos in the nucleus. Mol Cell 48:327–328. http://dx.doi.org/10.1016/j.molcel.2012.10.021.
   PubMedGoogle Scholar
• Felsenfeld G, Dekker J. 2012. Genome architecture and expression. Curr Opin Genet Dev 22:59–61. http://dx.doi.org/10.1016/j.gde.2012.03.003.
   PubMedGoogle Scholar
• Sun JQ, Hatanaka A, Oki M. 2011. Boundaries of transcriptionally silent chromatin in Saccharomyces cerevisiae. Genes Genet Syst 86:73–81.
   PubMedGoogle Scholar
• Boutanaev AM, Kalmykova AI, Shevelyov YY, Nurminsky DI. 2002. Large clusters of co-expressed genes in the Drosophila genome. Nature 420:666–669. http://dx.doi.org/10.1038/nature01216.
   PubMedGoogle Scholar
• Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, Eaton ML, Landolin JM, Bristow CA, Ma L, Lin MF, Washietl S, Arshinoff BI, Ay F, Meyer PE, Robine N, Washington NL, Di Stefano L, Berezikov E, Brown CD, Candeias R, Carlson JW, Carr A, Jungreis I, Marbach D, Sealfon R, Tolstorukov MY, Will S, Alekseyenko AA, Artieri C, Booth BW, Brooks AN, Dai Q, Davis CA, Duff MO, Feng X, Gorchakov AA, Gu T, Henikoff JG, Kapranov P, Li R, MacAlpine HK, Malone J, Minoda A, Nordman J, Okamura K, Perry M, Powell SK, Riddle NC, Sakai A, Samsonova A, Sandler JE, Schwartz YB, Sher N, Spokony R, Sturgill D, van Baren M, Wan KH, Yang L, Yu C, Feingold E, Good P, Guyer M, Lowdon R, Ahmad K, Andrews J, Berger B, Brenner SE, Brent MR, Cherbas L, Elgin SC, Gingeras TR, Grossman R, Hoskins RA, Kaufman TC, Kent W, Kuroda MI, Orr-Weaver T, Perrimon N, Pirrotta V, Posakony JW, Ren B, Russell S, Cherbas P, Graveley BR, Lewis S, Micklem G, Oliver B, Park PJ, Celniker SE, Henikoff S, Karpen GH, Lai EC, MacAlpine DM, Stein LD, White KP, Kellis M. 2010. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330:1787–1797. http://dx.doi.org/10.1126/science.1198374.
   PubMed Web of Science ®Google Scholar
• Nègre N, Brown CD, Shah PK, Kheradpour P, Morrison CA, Henikoff JG, Feng X, Ahmad K, Russell S, White RA, Stein L, Henikoff S, Kellis M, White KP. 2010. A comprehensive map of insulator elements for the Drosophila genome. PLoS Genet 6:e1000814. http://dx.doi.org/10.1371/journal.pgen.1000814.
   PubMedGoogle Scholar
• Holohan EE, Kwong C, Adryan B, Bartkuhn M, Herold M, Renkawitz R, Russell S, White R. 2007. CTCF genomic binding sites in Drosophila and the organisation of the bithorax complex. PLoS Genet 3:e112. http://dx.doi.org/10.1371/journal.pgen.0030112.
   PubMedGoogle Scholar
• Adryan B, Woerfel G, Birch-Machin I, Gao S, Quick M, Meadows L, Russell S, White R. 2007. Genomic mapping of Suppressor of Hairy-wing binding sites in Drosophila. Genome Biol 8:R167. http://dx.doi.org/10.1186/gb-2007-8-8-r167.
   PubMedGoogle Scholar
• Galloni M, Gyurkovics H, Schedl P, Karch F. 1993. The bluetail transposon: evidence for independent cis-regulatory domains and domain boundaries in the bithorax complex. EMBO J 12:1087–1097.
   PubMedGoogle Scholar
• Hagstrom K, Muller M, Schedl P. 1996. Fab-7 functions as a chromatin domain boundary to ensure proper segment specification by the Drosophila bithorax complex. Genes Dev 10:3202–3215. http://dx.doi.org/10.1101/gad.10.24.3202.
   PubMedGoogle Scholar
• Zhou J, Levine M. 1999. A novel cis-regulatory element, the PTS, mediates an anti-insulator activity in the Drosophila embryo. Cell 99:567–575. http://dx.doi.org/10.1016/S0092-8674(00)81546-9.
   PubMedGoogle Scholar
• Belozerov VE, Majumder P, Shen P, Cai HN. 2003. A novel boundary element may facilitate independent gene regulation in the Antennapedia complex of Drosophila. EMBO J 22:3113–3121. http://dx.doi.org/10.1093/emboj/cdg297.
   PubMedGoogle Scholar
• Barges S, Mihaly J, Galloni M, Hagstrom K, Muller M, Shanower G, Schedl P, Gyurkovics H, Karch F. 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
• Cléard F, Moshkin Y, Karch F, Maeda RK. 2006. Probing long-distance regulatory interactions in the Drosophila melanogaster bithorax complex using Dam identification. Nat Genet 38:931–935. http://dx.doi.org/10.1038/ng1833.
   PubMedGoogle Scholar
• Gyurkovics H, Gausz J, Kummer J, Karch F. 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
• Zhou J, Ashe H, Burks C, Levine M. 1999. Characterization of the transvection mediating region of the abdominal-B locus in Drosophila. Development 126:3057–3065.
   PubMedGoogle Scholar
• Gindhart JG, Jr, Kaufman TC. 1995. Identification of Polycomb and trithorax group responsive elements in the regulatory region of the Drosophila homeotic gene Sex combs reduced. Genetics 139:797–814.
   PubMedGoogle Scholar
• Gindhart JG, Jr, King AN, Kaufman TC. 1995. Characterization of the cis-regulatory region of the Drosophila homeotic gene Sex combs reduced. Genetics 139:781–795.
   PubMedGoogle Scholar
• Gorman MJ, Kaufman TC. 1995. Genetic analysis of embryonic cis-acting regulatory elements of the Drosophila homeotic gene sex combs reduced. Genetics 140:557–572.
   PubMedGoogle Scholar
• Southworth JW, Kennison JA. 2002. Transvection and Silencing of the Scr homeotic gene of Drosophila melanogaster. Genetics 161:733–746.
   PubMedGoogle Scholar
• Cai HN, Zhang Z, Adams JR, Shen P. 2001. Genomic context modulates insulator activity through promoter competition. Development 128:4339–4347.
   PubMed Web of Science ®Google Scholar
• Cai HN, Shen P. 2001. Effects of cis arrangement of chromatin insulators on enhancer-blocking activity. Science 291:493–495. http://dx.doi.org/10.1126/science.291.5503.493.
   PubMedGoogle Scholar
• Muravyova E, Golovnin A, Gracheva E, Parshikov A, Belenkaya T, Pirrotta V, Georgiev P. 2001. Loss of insulator activity by paired Su(Hw) chromatin insulators. Science 291:495–498. http://dx.doi.org/10.1126/science.291.5503.495.
   PubMedGoogle Scholar
• Kyrchanova O, Toshchakov S, Parshikov A, Georgiev P. 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. http://dx.doi.org/10.1128/MCB.02203-06.
   PubMedGoogle Scholar
• Cai HN. 2006. Function and mechanism of chromatin boundaries, p 343–363. In Ma J (ed), Gene expression and regulation. Higher Education Press, Beijing, China.
   Google Scholar
• Dekker J, Rippe K, Dekker M, Kleckner N. 2002. Capturing chromosome conformation. Science 295:1306–1311. http://dx.doi.org/10.1126/science.1067799.
   PubMed Web of Science ®Google Scholar
• Blanton J, Gaszner M, Schedl P. 2003. Protein:protein interactions and the pairing of boundary elements in vivo. Genes Dev 17:664–675. http://dx.doi.org/10.1101/gad.1052003.
   PubMed Web of Science ®Google Scholar
• Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W. 2002. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 10:1453–1465. http://dx.doi.org/10.1016/S1097-2765(02)00781-5.
   PubMed Web of Science ®Google Scholar
• Cai HN, Levine M. 1997. The gypsy insulator can function as a promoter-specific silencer in the Drosophila embryo. EMBO J 16:1732–1741. http://dx.doi.org/10.1093/emboj/16.7.1732.
   PubMed Web of Science ®Google Scholar
• Majumder P, Cai HN. 2003. The functional analysis of insulator interactions in the Drosophila embryo. Proc Natl Acad Sci U S A 100:5223–5228. http://dx.doi.org/10.1073/pnas.0830190100.
   PubMedGoogle Scholar
• Mito Y, Henikoff JG, Henikoff S. 2005. Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37:1090–1097. http://dx.doi.org/10.1038/ng1637.
   PubMed Web of Science ®Google Scholar
• Belton JM, McCord RP, Gibcus JH, Naumova N, Zhan Y, Dekker J. 2012. Hi-C: a comprehensive technique to capture the conformation of genomes. Methods 58:268–276. http://dx.doi.org/10.1016/j.ymeth.2012.05.001.
   PubMed Web of Science ®Google Scholar
• Dostie J, Richmond TA, Arnaout RA, Selzer RR, Lee WL, Honan TA, Rubio ED, Krumm A, Lamb J, Nusbaum C, Green RD, Dekker J. 2006. Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res 16:1299–1309. http://dx.doi.org/10.1101/gr.5571506.
   PubMed Web of Science ®Google Scholar
• Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, van Steensel B, de Laat W. 2006. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat Genet 38:1348–1354. http://dx.doi.org/10.1038/ng1896.
   PubMed Web of Science ®Google Scholar
• Calhoun VC, Levine M. 2003. Long-range enhancer-promoter interactions in the Scr-Antp interval of the Drosophila Antennapedia complex. Proc Natl Acad Sci U S A 100:9878–9883. http://dx.doi.org/10.1073/pnas.1233791100.
   PubMedGoogle Scholar
• Bushey AM, Ramos E, Corces VG. 2009. Three subclasses of a Drosophila insulator show distinct and cell type-specific genomic distributions. Genes Dev 23:1338–1350. http://dx.doi.org/10.1101/gad.1798209.
   PubMed Web of Science ®Google Scholar
• Smith ST, Wickramasinghe P, Olson A, Loukinov D, Lin L, Deng J, Xiong Y, Rux J, Sachidanandam R, Sun H, Lobanenkov V, Zhou J. 2009. Genome wide ChIP-chip analyses reveal important roles for CTCF in Drosophila genome organization. Dev Biol 328:518–528. http://dx.doi.org/10.1016/j.ydbio.2008.12.039.
   PubMedGoogle Scholar
• Bartkuhn M, Straub T, Herold M, Herrmann M, Rathke C, Saumweber H, Gilfillan GD, Becker PB, Renkawitz R. 2009. Active promoters and insulators are marked by the centrosomal protein 190. EMBO J 28:877–888. http://dx.doi.org/10.1038/emboj.2009.34.
   PubMedGoogle Scholar
• Ameres SL, Drueppel L, Pfleiderer K, Schmidt A, Hillen W, Berens C. 2005. Inducible DNA-loop formation blocks transcriptional activation by an SV40 enhancer. EMBO J 24:358–367. http://dx.doi.org/10.1038/sj.emboj.7600531.
   PubMedGoogle Scholar
• Bondarenko VA, Jiang YI, Studitsky VM. 2003. Rationally designed insulator-like elements can block enhancer action in vitro. EMBO J 22:4728–4737. http://dx.doi.org/10.1093/emboj/cdg468.
   PubMedGoogle Scholar
• Dearolf CR, Topol J, Parker CS. 1989. Transcriptional control of Drosophila fushi tarazu zebra stripe expression. Genes Dev 3:384–398. http://dx.doi.org/10.1101/gad.3.3.384.
   PubMedGoogle Scholar
• Gasser SM, Laemmli UK. 1986. Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes of D. melanogaster. Cell 46:521–530. http://dx.doi.org/10.1016/0092-8674(86)90877-9.
   PubMedGoogle Scholar
• Mirkovitch J, Mirault ME, Laemmli UK. 1984. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell 39:223–232. http://dx.doi.org/10.1016/0092-8674(84)90208-3.
   PubMed Web of Science ®Google Scholar
• Hon GC, Hawkins RD, Ren B. 2009. Predictive chromatin signatures in the mammalian genome. Hum Mol Genet 18:R195–R201. http://dx.doi.org/10.1093/hmg/ddp409.
   PubMedGoogle Scholar
• Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39:311–318. http://dx.doi.org/10.1038/ng1966.
   PubMed Web of Science ®Google Scholar
• Bonn S, Zinzen RP, Girardot C, Gustafson EH, Perez-Gonzalez A, Delhomme N, Ghavi-Helm Y, Wilczynski B, Riddell A, Furlong EE. 2012. Tissue-specific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development. Nat Genet 44:148–156. http://dx.doi.org/10.1038/ng.1064.
   PubMed Web of Science ®Google Scholar
• Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470:279–283. http://dx.doi.org/10.1038/nature09692.
   PubMed Web of Science ®Google Scholar
• Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, Artieri CG, van Baren MJ, Boley N, Booth BW, Brown JB, Cherbas L, Davis CA, Dobin A, Li R, Lin W, Malone JH, Mattiuzzo NR, Miller D, Sturgill D, Tuch BB, Zaleski C, Zhang D, Blanchette M, Dudoit S, Eads B, Green RE, Hammonds A, Jiang L, Kapranov P, Langton L, Perrimon N, Sandler JE, Wan KH, Willingham A, Zhang Y, Zou Y, Andrews J, Bickel PJ, Brenner SE, Brent MR, Cherbas P, Gingeras TR, Hoskins RA, Kaufman TC, Oliver B, Celniker SE. 2011. The developmental transcriptome of Drosophila melanogaster. Nature 471:473–479. http://dx.doi.org/10.1038/nature09715.
   PubMed Web of Science ®Google Scholar
• Tautz D, Pfeifle C. 1989. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81–85. http://dx.doi.org/10.1007/BF00291041.
   PubMed Web of Science ®Google Scholar
• Li M, Belozerov VE, Cai HN. 2010. Modulation of chromatin boundary activities by nucleosome-remodeling activities in Drosophila melanogaster. Mol Cell Biol 30:1067–1076. http://dx.doi.org/10.1128/MCB.00183-09.
   PubMedGoogle Scholar
• Mahaffey JW, Kaufman TC. 1987. Distribution of the Sex combs reduced gene products in Drosophila melanogaster. Genetics 117:51–60.
   PubMedGoogle Scholar
• Pattatucci AM, Kaufman TC. 1991. The homeotic gene Sex combs reduced of Drosophila melanogaster is differentially regulated in the embryonic and imaginal stages of development. Genetics 129:443–461.
   PubMedGoogle Scholar
• Pattatucci AM, Otteson DC, Kaufman TC. 1991. A functional and structural analysis of the Sex combs reduced locus of Drosophila melanogaster. Genetics 129:423–441.
   PubMedGoogle Scholar
• Melnikova L, Juge F, Gruzdeva N, Mazur A, Cavalli G, Georgiev P. 2004. Interaction between the GAGA factor and Mod(mdg4) proteins promotes insulator bypass in Drosophila. Proc Natl Acad Sci U S A 101:14806–14811. http://dx.doi.org/10.1073/pnas.0403959101.
   PubMedGoogle Scholar
• Golovnin A, Mazur A, Kopantseva M, Kurshakova M, Gulak PV, Gilmore B, Whitfield WG, Geyer P, Pirrotta V, Georgiev P. 2007. Integrity of the Mod(mdg4)-67.2 BTB domain is critical to insulator function in Drosophila melanogaster. Mol Cell Biol 27:963–974. http://dx.doi.org/10.1128/MCB.00795-06.
   PubMedGoogle Scholar
• Morris JR, Chen JL, Geyer PK, Wu CT. 1998. Two modes of transvection: enhancer action in trans and bypass of a chromatin insulator in cis. Proc Natl Acad Sci U S A 95:10740–10745. http://dx.doi.org/10.1073/pnas.95.18.10740.
   PubMedGoogle Scholar
• Chen JL, Huisinga KL, Viering MM, Ou SA, Wu CT, Geyer PK. 2002. Enhancer action in trans is permitted throughout the Drosophila genome. Proc Natl Acad Sci U S A 99:3723–3728. http://dx.doi.org/10.1073/pnas.062447999.
   PubMed Web of Science ®Google Scholar
• Kuhn EJ, Viering MM, Rhodes KM, Geyer PK. 2003. A test of insulator interactions in Drosophila. EMBO J 22:2463–2471. http://dx.doi.org/10.1093/emboj/cdg241.
   PubMed Web of Science ®Google Scholar
• Karch F, Galloni M, Sipos L, Gausz J, Gyurkovics H, Schedl P. 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. http://dx.doi.org/10.1093/nar/22.15.3138.
   PubMedGoogle Scholar
• Hiromi Y, Kuroiwa A, Gehring WJ. 1985. Control elements of the Drosophila segmentation gene fushi tarazu. Cell 43:603–613. http://dx.doi.org/10.1016/0092-8674(85)90232-6.
   PubMed Web of Science ®Google Scholar
• Hiromi Y, Gehring WJ. 1987. Regulation and function of the Drosophila segmentation gene fushi tarazu. Cell 50:963–974. http://dx.doi.org/10.1016/0092-8674(87)90523-X.
   PubMedGoogle Scholar
• Maier D, Preiss A, Powell JR. 1990. Regulation of the segmentation gene fushi tarazu has been functionally conserved in Drosophila. EMBO J 9:3957–3966.
   PubMedGoogle Scholar
• Pick L, Schier A, Affolter M, Schmidt-Glenewinkel T, Gehring WJ. 1990. Analysis of the ftz upstream element: germ layer-specific enhancers are independently autoregulated. Genes Dev 4:1224–1239. http://dx.doi.org/10.1101/gad.4.7.1224.
   PubMedGoogle Scholar
• Maier D, Sperlich D, Powell JR. 1993. Conservation and change of the developmentally crucial fushi tarazu gene in Drosophila. J Mol Evol 36:315–326.
   PubMedGoogle Scholar
• Parnell TJ, Viering MM, Skjesol A, Helou C, Kuhn EJ, Geyer PK. 2003. An endogenous suppressor of hairy-wing insulator separates regulatory domains in Drosophila. Proc Natl Acad Sci U S A 100:13436–13441. http://dx.doi.org/10.1073/pnas.2333111100.
   PubMedGoogle Scholar
• Kyrchanova O, Toshchakov S, Podstreshnaya Y, Parshikov A, Georgiev P. 2008. Functional interaction between the Fab-7 and Fab-8 boundaries and the upstream promoter region in the Drosophila Abd-B gene. Mol Cell Biol 28:4188–4195. http://dx.doi.org/10.1128/MCB.00229-08.
   PubMedGoogle Scholar
• Kyrchanova O, Ivlieva T, Toshchakov S, Parshikov A, Maksimenko O, Georgiev P. 2011. Selective interactions of boundaries with upstream region of Abd-B promoter in Drosophila bithorax complex and role of dCTCF in this process. Nucleic Acids Res 39:3042–3052. http://dx.doi.org/10.1093/nar/gkq1248.
   PubMedGoogle Scholar
• Gohl D, Aoki T, Blanton J, Shanower G, Kappes G, Schedl P. 2011. Mechanism of chromosomal boundary action: roadblock, sink, or loop? Genetics 187:731–748. http://dx.doi.org/10.1534/genetics.110.123752.
   PubMed Web of Science ®Google Scholar