Surviving an identity crisis: A revised view of chromatin insulators in the genomics era

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1839, Issue 3, 2014, Pages 203-214

  Matzat, Leah H ^a   Lei, Elissa P ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Chromatin; Drosophila; Insulator; Nuclear organization

Indexed keywords

BOUNDARY ELEMENT ASSOCIATED FACTOR OF 32 KDA; CENTROSOMAL PROTEIN 190; CIS ACTING ELEMENT; DNA BINDING PROTEIN; MEMBRANE PROTEIN; RNA; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; ZESTE WHITE 5;

CELL TYPE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN INSULATOR; DROSOPHILA; EPIGENETICS; GENE EXPRESSION; GENE REPRESSION; GENETIC ANALYSIS; GENETIC REGULATION; GENOME ANALYSIS; GENOMICS; HOX GENE; HUMAN; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; TISSUE GROWTH; TRANSGENICS; VERTEBRATE;

ANIMALIA; DROSOPHILA MELANOGASTER;

CHROMATIN; DROSOPHILA; INSULATOR; NUCLEAR ORGANIZATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CHROMATIN ASSEMBLY AND DISASSEMBLY; DROSOPHILA MELANOGASTER; GENETIC LOCI; GENOMICS; HUMANS; INSULATOR ELEMENTS;

EID: 84896735322     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2013.10.007     Document Type: Review

References (152)

1. Cavalli G., Misteli T. Functional implications of genome topology. Nat. Struct. Mol. Biol. 2013, 20:290-299.
2. Parelho V., Hadjur S., Spivakov M., Leleu M., Sauer S., Gregson H.C., Jarmuz A., Canzonetta C., Webster Z., Nesterova T., Cobb B.S., Yokomori K., Dillon N., Aragon L., Fisher A.G., Merkenschlager M. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 2008, 132:422-433.
3. Peters J.M., Tedeschi A., Schmitz J. The cohesin complex and its roles in chromosome biology. Genes Dev. 2008, 22:3089-3114.
4. Schwartz Y.B., Linder-Basso D., Kharchenko P.V., Tolstorukov M.Y., Kim M., Li H.B., Gorchakov A.A., Minoda A., Shanower G., Alekseyenko A.A., Riddle N.C., Jung Y.L., Gu T., Plachetka A., Elgin S.C., Kuroda M.I., Park P.J., Savitsky M., Karpen G.H., Pirrotta V. Nature and function of insulator protein binding sites in the Drosophila genome. Genome Res. 2012, 22:2188-2198.
5. Van Bortle K., Ramos E., Takenaka N., Yang J., Wahi J.E., Corces V.G. Drosophila CTCF tandemly aligns with other insulator proteins at the borders of H3K27me3 domains. Genome Res. 2012, 22:2176-2187.
6. Peifer M., Bender W. Sequences of the gypsy transposon of Drosophila necessary for its effects on adjacent genes. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:9650-9654.
7. Spana C., Harrison D.A., Corces V.G. The Drosophila melanogaster Suppressor of Hairy-wing protein binds to specific sequences of the gypsy retrotransposon. Genes Dev. 1988, 2:1414-1423.
8. Ramos E., Ghosh D., Baxter E., Corces V.G. Genomic organization of gypsy chromatin insulators in Drosophila melanogaster. Genetics 2006, 172:2337-2349.
9. Parnell T.J., Viering M.M., Skjesol A., Helou C., Kuhn E.J., Geyer P.K. An endogenous Suppressor of Hairy-wing insulator separates regulatory domains in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:13436-13441.
10. Geyer P.K., Corces V.G. DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev. 1992, 6:1865-1873.
11. Parkhurst S.M., Harrison D.A., Remington M.P., Spana C., Kelley R.L., Coyne R.S., Corces V.G. The Drosophila su(Hw) gene, which controls the phenotypic effect of the gypsy transposable element, encodes a putative DNA-binding protein. Genes Dev. 1988, 2:1205-1215.
12. Smith P.A., Corces V.G. The Suppressor of Hairy-wing binding region is required for gypsy mutagenesis. Mol. Gen. Genet. 1992, 233:65-70.
13. Spana C., Corces V.G. DNA bending is a determinant of binding specificity for a Drosophila zinc finger protein. Genes Dev. 1990, 4:1505-1515.
14. Golovnin A., Biryukova I., Romanova O., Silicheva M., Parshikov A., Savitskaya E., Pirrotta V., Georgiev P. An endogenous Su(Hw) insulator separates the yellow gene from the Achaete-scute gene complex in Drosophila. Development 2003, 130:3249-3258.
15. Kim J., Shen B., Rosen C., Dorsett D. The DNA-binding and enhancer-blocking domains of the Drosophila Suppressor of Hairy-wing protein. Mol. Cell. Biol. 1996, 16:3381-3392.
16. Gabler M., Volkmar M., Weinlich S., Herbst A., Dobberthien P., Sklarss S., Fanti L., Pimpinelli S., Kress H., Reuter G., Dorn R. Trans-splicing of the mod(mdg4) complex locus is conserved between the distantly related species Drosophila melanogaster and D. virilis. Genetics 2005, 169:723-736.
17. Gerasimova T.I., Gdula D.A., Gerasimov D.V., Simonova O., Corces V.G. A Drosophila protein that imparts directionality on a chromatin insulator is an enhancer of position-effect variegation. Cell 1995, 82:587-597.
18. Cai H.N., Levine M. The gypsy insulator can function as a promoter-specific silencer in the Drosophila embryo. EMBO J. 1997, 16:1732-1741.
19. Pai C.Y., Lei E.P., Ghosh D., Corces V.G. The centrosomal protein CP190 is a component of the gypsy chromatin insulator. Mol. Cell 2004, 16:737-748.
20. Gerasimova T.I., Byrd K., Corces V.G. A chromatin insulator determines the nuclear localization of DNA. Mol. Cell 2000, 6:1025-1035.
21. Buchner K., Roth P., Schotta G., Krauss V., Saumweber H., Reuter G., Dorn R. Genetic and molecular complexity of the position effect variegation modifier mod(mdg4) in Drosophila. Genetics 2000, 155:141-157.
22. Cai H.N., Shen P. Effects of cis arrangement of chromatin insulators on enhancer-blocking activity. Science 2001, 291:493-495.
23. Muravyova E., Golovnin A., Gracheva E., Parshikov A., Belenkaya T., Pirrotta V., Georgiev P. Loss of insulator activity by paired Su(Hw) chromatin insulators. Science 2001, 291:495-498.
24. Nabirochkin S., Ossokina M., Heidmann T. A nuclear matrix/scaffold attachment region co-localizes with the gypsy retrotransposon insulator sequence. J. Biol. Chem. 1998, 273:2473-2479.
25. Byrd K., Corces V.G. Visualization of chromatin domains created by the gypsy insulator of Drosophila. J. Cell Biol. 2003, 162:565-574.
26. Capelson M., Corces V.G. The ubiquitin ligase dTopors directs the nuclear organization of a chromatin insulator. Mol. Cell 2005, 20:105-116.
27. Xu Q., Li M., Adams J., Cai H.N. Nuclear location of a chromatin insulator in Drosophila melanogaster. J. Cell Sci. 2004, 117:1025-1032.
28. Ghosh D., Gerasimova T.I., Corces V.G. Interactions between the Su(Hw) and Mod(mdg4) proteins required for gypsy insulator function. EMBO J. 2001, 20:2518-2527.
29. Gerasimova T.I., Corces V.G. Polycomb and trithorax group proteins mediate the function of a chromatin insulator. Cell 1998, 92:511-521.
30. Golovnin A., Volkov I., Georgiev P. SUMO conjugation is required for the assembly of Drosophila Su(Hw) and mod(mdg4) into insulator bodies that facilitate insulator complex formation. J. Cell Sci. 2012, 125:2064-2074.
31. Matzat L.H., Dale R.K., Moshkovich N., Lei E.P. Tissue-specific regulation of chromatin insulator function. PLoS Genet. 2012, 8:e1003069.
32. Moshkovich N., Nisha P., Boyle P.J., Thompson B.A., Dale R.K., Lei E.P. RNAi-independent role for Argonaute2 in CTCF/CP190 chromatin insulator function. Genes Dev. 2011, 25:1686-1701.
33. Capelson M., Corces V.G. SUMO conjugation attenuates the activity of the gypsy chromatin insulator. EMBO J. 2006, 25:1906-1914.
34. Gerasimova T.I., Lei E.P., Bushey A.M., Corces V.G. Coordinated control of dCTCF and gypsy chromatin insulators in Drosophila. Mol. Cell 2007, 28:761-772.
35. Rohrbaugh M., Clore A., Davis J., Johnson S., Jones B., Jones K., Kim J., Kithuka B., Lunsford K., Mitchell J., Mott B., Ramos E., Tchedou M.R., Acosta G., Araujo M., Cushing S., Duffy G., Graves F., Griffin K., Gurudatta B.V., Jackson D., Jaimes D., Jamison K., Jones K., Kelley D., Kilgore M., Laramore D., Le T., Mazhar B., Mazhar M.M., McCrary B., Miller T., Moreland C., Mullins A., Munye E., Okoorie S., Pittman E., Roberts N., Rose D., Rowland A., Shagarabi A., Smith J., Stallworth T., Stroud N., Sung E., Sung K., Takenaka N., Torre E., Veira J., Vu K., Wagstaff W., Wood A.M., Wu K., Yang J., Corces V.G. Identification and characterization of proteins involved in nuclear organization using Drosophila GFP protein trap lines. PLoS One 2013, 8:e53091.
36. Wood A.M., Van Bortle K., Ramos E., Takenaka N., Rohrbaugh M., Jones B.C., Jones K.C., Corces V.G. Regulation of chromatin organization and inducible gene expression by a Drosophila insulator. Mol. Cell 2011, 44:29-38.
37. Ramos E., Torre E.A., Bushey A.M., Gurudatta B.V., Corces V.G. DNA topoisomerase II modulates insulator function in Drosophila. PLoS One 2011, 6:e16562.
38. Lei E.P., Corces V.G. RNA interference machinery influences the nuclear organization of a chromatin insulator. Nat. Genet. 2006, 38:936-941.
39. Golovnin A., Melnikova L., Volkov I., Kostuchenko M., Galkin A.V., Georgiev P. ''Insulator bodies' are aggregates of proteins but not of insulators. EMBO Rep. 2008, 9:440-445.
40. Cuddapah S., Jothi R., Schones D.E., Roh T.Y., Cui K., Zhao K. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res. 2009, 19:24-32.
41. Kim T.H., Abdullaev Z.K., Smith A.D., Ching K.A., Loukinov D.I., Green R.D., Zhang M.Q., Lobanenkov V.V., Ren B. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 2007, 128:1231-1245.
42. Bushey A.M., Ramos E., Corces V.G. Three subclasses of a Drosophila insulator show distinct and cell type-specific genomic distributions. Genes Dev. 2009, 23:1338-1350.
43. Negre N., Brown C.D., Shah P.K., Kheradpour P., Morrison C.A., Henikoff J.G., Feng X., Ahmad K., Russell S., White R.A., Stein L., Henikoff S., Kellis M., White K.P. A comprehensive map of insulator elements for the Drosophila genome. PLoS Genet. 2010, 6:e1000814.
44. Soshnev A.A., He B., Baxley R.M., Jiang N., Hart C.M., Tan K., Geyer P.K. Genome-wide studies of the multi-zinc finger Drosophila Suppressor of Hairy-wing protein in the ovary. Nucleic Acids Res. 2012, 40:5415-5431.
45. van Bemmel J.G., Pagie L., Braunschweig U., Brugman W., Meuleman W., Kerkhoven R.M., van Steensel B. The insulator protein Su(Hw) fine-tunes nuclear lamina interactions of the Drosophila genome. PLoS One 2010, 5:e15013.
46. Pickersgill H., Kalverda B., de Wit E., Talhout W., Fornerod M., van Steensel B. Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat. Genet. 2006, 38:1005-1014.
47. Filion G.J., van Bemmel J.G., Braunschweig U., Talhout W., Kind J., Ward L.D., Brugman W., de Castro I.J., Kerkhoven R.M., Bussemaker H.J., van Steensel B. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 2010, 143:212-224.
48. Roy S., Ernst J., Kharchenko P.V., Kheradpour P., Negre N., Eaton M.L., Landolin J.M., Bristow C.A., Ma L., Lin M.F., Washietl S., Arshinoff B.I., Ay F., Meyer P.E., Robine N., Washington N.L., Di Stefano L., Berezikov E., Brown C.D., Candeias R., Carlson J.W., Carr A., Jungreis I., Marbach D., Sealfon R., Tolstorukov M.Y., Will S., Alekseyenko A.A., Artieri C., Booth B.W., Brooks A.N., Dai Q., Davis C.A., Duff M.O., Feng X., Gorchakov A.A., Gu T., Henikoff J.G., Kapranov P., Li R., MacAlpine H.K., Malone J., Minoda A., Nordman J., Okamura K., Perry M., Powell S.K., Riddle N.C., Sakai A., Samsonova A., Sandler J.E., Schwartz Y.B., Sher N., Spokony R., Sturgill D., van Baren M., Wan K.H., Yang L., Yu C., Feingold E., Good P., Guyer M., Lowdon R., Ahmad K., Andrews J., Berger B., Brenner S.E., Brent M.R., Cherbas L., Elgin S.C., Gingeras T.R., Grossman R., Hoskins R.A., Kaufman T.C., Kent W., Kuroda M.I., Orr-Weaver T., Perrimon N., Pirrotta V., Posakony J.W., Ren B., Russell S., Cherbas P., Graveley B.R., Lewis S., Micklem G., Oliver B., Park P.J., Celniker S.E., Henikoff S., Karpen G.H., Lai E.C., MacAlpine D.M., Stein L.D., White K.P., Kellis M. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 2010, 330:1787-1797.
49. Adryan B., Woerfel G., Birch-Machin I., Gao S., Quick M., Meadows L., Russell S., White R. Genomic mapping of Suppressor of Hairy-wing binding sites in Drosophila. Genome Biol. 2007, 8:R167.
50. Harrison D.A., Mortin M.A., Corces V.G. The RNA polymerase II 15-kilodalton subunit is essential for viability in Drosophila melanogaster. Mol. Cell. Biol. 1992, 12:928-935.
51. Soshnev A.A., Li X., Wehling M.D., Geyer P.K. Context differences reveal insulator and activator functions of a Su(Hw) binding region. PLoS Genet. 2008, 4:e1000159.
52. Harrison D.A., Gdula D.A., Coyne R.S., Corces V.G. A leucine zipper domain of the Suppressor of Hairy-wing protein mediates its repressive effect on enhancer function. Genes Dev. 1993, 7:1966-1978.
53. Klug W.S., Bodenstein D., King R.C. Oogenesis in the Suppressor of Hairy-wing mutant of Drosophila melanogaster. I. Phenotypic characterization and transplantation experiments. J. Exp. Zool. 1968, 167:151-156.
54. Baxley R.M., Soshnev A.A., Koryakov D.E., Zhimulev I.F., Geyer P.K. The role of the Suppressor of Hairy-wing insulator protein in Drosophila oogenesis. Dev. Biol. 2011, 356:398-410.
55. Fritsch C., Ploeger G., Arndt-Jovin D.J. Drosophila under the lens: imaging from chromosomes to whole embryos. Chromosome Res. 2006, 14:451-464.
56. Udvardy A., Maine E., Schedl P. The 87A7 chromomere. Identification of novel chromatin structures flanking the heat shock locus that may define the boundaries of higher order domains. J. Mol. Biol. 1985, 185:341-358.
57. Kellum R., Schedl P. A position-effect assay for boundaries of higher order chromosomal domains. Cell 1991, 64:941-950.
58. Kellum R., Schedl P. A group of scs elements function as domain boundaries in an enhancer-blocking assay. Mol. Cell. Biol. 1992, 12:2424-2431.
59. Gaszner M., Vazquez J., Schedl P. The Zw5 protein, a component of the scs chromatin domain boundary, is able to block enhancer-promoter interaction. Genes Dev. 1999, 13:2098-2107.
60. Zhao K., Hart C.M., Laemmli U.K. Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell 1995, 81:879-889.
61. Gilbert M.K., Tan Y.Y., Hart C.M. The Drosophila boundary element-associated factors BEAF-32A and BEAF-32B affect chromatin structure. Genetics 2006, 173:1365-1375.
62. Roy S., Gilbert M.K., Hart C.M. Characterization of BEAF mutations isolated by homologous recombination in Drosophila. Genetics 2007, 176:801-813.
63. Kuhn E.J., Hart C.M., Geyer P.K. Studies of the role of the Drosophila scs and scs' insulators in defining boundaries of a chromosome puff. Mol. Cell. Biol. 2004, 24:1470-1480.
64. Kyrchanova O., Leman D., Parshikov A., Fedotova A., Studitsky V., Maksimenko O., Georgiev P. New properties of Drosophila scs and scs' insulators. PLoS One 2013, 8:e62690.
65. Aravind L. The BED finger, a novel DNA-binding domain in chromatin-boundary-element-binding proteins and transposases. Trends Biochem. Sci. 2000, 25:421-423.
66. Jiang N., Emberly E., Cuvier O., Hart C.M. Genome-wide mapping of boundary element-associated factor (BEAF) binding sites in Drosophila melanogaster links BEAF to transcription. Mol. Cell. Biol. 2009, 29:3556-3568.
67. Cuvier O., Hart C.M., Laemmli U.K. Identification of a class of chromatin boundary elements. Mol. Cell. Biol. 1998, 18:7478-7486.
68. Sultana H., Verma S., Mishra R.K. A BEAF dependent chromatin domain boundary separates myoglianin and eyeless genes of Drosophila melanogaster. Nucleic Acids Res. 2011, 39:3543-3557.
69. Hart C.M., Cuvier O., Laemmli U.K. Evidence for an antagonistic relationship between the boundary element-associated factor BEAF and the transcription factor DREF. Chromosoma 1999, 108:375-383.
70. Emberly E., Blattes R., Schuettengruber B., Hennion M., Jiang N., Hart C.M., Kas E., Cuvier O. BEAF regulates cell-cycle genes through the controlled deposition of H3K9 methylation marks into its conserved dual-core binding sites. PLoS Biol. 2008, 6:2896-2910.
71. Yang J., Ramos E., Corces V.G. The BEAF-32 insulator coordinates genome organization and function during the evolution of Drosophila species. Genome Res. 2012, 22:2199-2207.
72. Lim S.J., Boyle P.J., Chinen M., Dale R.K., Lei E.P. Genome-wide localization of exosome components to active promoters and chromatin insulators in Drosophila. Nucleic Acids Res. 2013, 41:2963-2980.
73. Blanton J., Gaszner M., Schedl P. Protein:protein interactions and the pairing of boundary elements in vivo. Genes Dev. 2003, 17:664-675.
74. Gurudatta B.V., Ramos E., Corces V.G. The BEAF insulator regulates genes involved in cell polarity and neoplastic growth. Dev. Biol. 2012, 369:124-132.
75. Roy S., Tan Y.Y., Hart C.M. A genetic screen supports a broad role for the Drosophila insulator proteins BEAF-32A and BEAF-32B in maintaining patterns of gene expression. Mol. Genet. Genomics 2007, 277:273-286.
76. Yamaguchi M., Yoshida H., Hirose F., Inoue Y.H., Hayashi Y., Yamagishi M., Nishi Y., Tamai K., Sakaguchi K., Matsukage A. Ectopic expression of BEAF32A in the Drosophila eye imaginal disc inhibits differentiation of photoreceptor cells and induces apoptosis. Chromosoma 2001, 110:313-321.
77. Moon H., Filippova G., Loukinov D., Pugacheva E., Chen Q., Smith S.T., Munhall A., Grewe B., Bartkuhn M., Arnold R., Burke L.J., Renkawitz-Pohl R., Ohlsson R., Zhou J., Renkawitz R., Lobanenkov V. CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator. EMBO Rep. 2005, 6:165-170.
78. Maeda R.K., Karch F. The ABC of the BX-C: the bithorax complex explained. Development 2006, 133:1413-1422.
79. Akbari O.S., Bousum A., Bae E., Drewell R.A. Unraveling cis-regulatory mechanisms at the abdominal-A and abdominal-B genes in the Drosophila bithorax complex. Dev. Biol. 2006, 293:294-304.
80. Holohan E.E., Kwong C., Adryan B., Bartkuhn M., Herold M., Renkawitz R., Russell S., White R. CTCF genomic binding sites in Drosophila and the organisation of the bithorax complex. PLoS Genet. 2007, 3:e112.
81. Smith S.T., Wickramasinghe P., Olson A., Loukinov D., Lin L., Deng J., Xiong Y., Rux J., Sachidanandam R., Sun H., Lobanenkov V., Zhou J. Genome wide ChIP-chip analyses reveal important roles for CTCF in Drosophila genome organization. Dev. Biol. 2009, 328:518-528.
82. Bartkuhn M., Straub T., Herold M., Herrmann M., Rathke C., Saumweber H., Gilfillan G.D., Becker P.B., Renkawitz R. Active promoters and insulators are marked by the centrosomal protein 190. EMBO J. 2009, 28:877-888.
83. Mohan M., Bartkuhn M., Herold M., Philippen A., Heinl N., Bardenhagen I., Leers J., White R.A., Renkawitz-Pohl R., Saumweber H., Renkawitz R. The Drosophila insulator proteins CTCF and CP190 link enhancer blocking to body patterning. EMBO J. 2007, 26:4203-4214.
84. Perez-Lluch S., Cuartero S., Azorin F., Espinas M.L. Characterization of new regulatory elements within the Drosophila bithorax complex. Nucleic Acids Res. 2008, 36:6926-6933.
85. Kyrchanova O., Ivlieva T., Toshchakov S., Parshikov A., Maksimenko O., Georgiev P. 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. 2011, 39:3042-3052.
86. Cleard F., Moshkin Y., Karch F., Maeda R.K. Probing long-distance regulatory interactions in the Drosophila melanogaster bithorax complex using Dam identification. Nat. Genet. 2006, 38:931-935.
87. Lanzuolo C., Roure V., Dekker J., Bantignies F., Orlando V. Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Nat. Cell Biol. 2007, 9:1167-1174.
88. Lin Q., Lin L., Zhou J. Chromatin insulator and the promoter targeting sequence modulate the timing of long-range enhancer-promoter interactions in the Drosophila embryo. Dev. Biol. 2010, 339:329-337.
89. Guo Y., Monahan K., Wu H., Gertz J., Varley K.E., Li W., Myers R.M., Maniatis T., Wu Q. CTCF/cohesin-mediated DNA looping is required for protocadherin alpha promoter choice. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:21081-21086.
90. Monahan K., Rudnick N.D., Kehayova P.D., Pauli F., Newberry K.M., Myers R.M., Maniatis T. Role of CCCTC binding factor (CTCF) and cohesin in the generation of single-cell diversity of protocadherin-alpha gene expression. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:9125-9130.
91. Celniker S.E., Keelan D.J., Lewis E.B. The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the abdominal-B domain. Genes Dev. 1989, 3:1424-1436.
92. Handoko L., Xu H., Li G., Ngan C.Y., Chew E., Schnapp M., Lee C.W., Ye C., Ping J.L., Mulawadi F., Wong E., Sheng J., Zhang Y., Poh T., Chan C.S., Kunarso G., Shahab A., Bourque G., Cacheux-Rataboul V., Sung W.K., Ruan Y., Wei C.L. CTCF-mediated functional chromatin interactome in pluripotent cells. Nat. Genet. 2011, 43:630-638.
93. Fujioka M., Wu X., Jaynes J.B. A chromatin insulator mediates transgene homing and very long-range enhancer-promoter communication. Development 2009, 136:3077-3087.
94. Kassis J.A., Noll E., VanSickle E.P., Odenwald W.F., Perrimon N. Altering the insertional specificity of a Drosophila transposable element. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:1919-1923.
95. Hama C., Ali Z., Kornberg T.B. Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev. 1990, 4:1079-1093.
96. Barges S., Mihaly J., Galloni M., Hagstrom K., Muller M., Shanower G., Schedl P., Gyurkovics H., Karch F. 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 2000, 127:779-790.
97. Karch F., Galloni M., Sipos L., Gausz J., Gyurkovics H., Schedl P. Mcp and Fab-7: molecular analysis of putative boundaries of cis-regulatory domains in the bithorax complex of Drosophila melanogaster. Nucleic Acids Res. 1994, 22:3138-3146.
98. Karch F., Weiffenbach B., Peifer M., Bender W., Duncan I., Celniker S., Crosby M., Lewis E.B. The abdominal region of the bithorax complex. Cell 1985, 43:81-96.
99. Schmitges F.W., Prusty A.B., Faty M., Stutzer A., Lingaraju G.M., Aiwazian J., Sack R., Hess D., Li L., Zhou S., Bunker R.D., Wirth U., Bouwmeester T., Bauer A., Ly-Hartig N., Zhao K., Chan H., Gu J., Gut H., Fischle W., Muller J., Thoma N.H. Histone methylation by PRC2 is inhibited by active chromatin marks. Mol. Cell 2011, 42:330-341.
100. Schuettengruber B., Cavalli G. Polycomb domain formation depends on short and long distance regulatory cues. PLoS One 2013, 8:e56531.
101. Sigrist C.J., Pirrotta V. Chromatin insulator elements block the silencing of a target gene by the Drosophila polycomb response element (PRE) but allow trans interactions between PREs on different chromosomes. Genetics 1997, 147:209-221.
102. Comet I., Savitskaya E., Schuettengruber B., Negre N., Lavrov S., Parshikov A., Juge F., Gracheva E., Georgiev P., Cavalli G. PRE-mediated bypass of two Su(Hw) insulators targets PcG proteins to a downstream promoter. Dev. Cell 2006, 11:117-124.
103. Comet I., Schuettengruber B., Sexton T., Cavalli G. A chromatin insulator driving three-dimensional polycomb response element (PRE) contacts and polycomb association with the chromatin fiber. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:2294-2299.
104. Kassis J.A. Unusual properties of regulatory DNA from the Drosophila engrailed gene: three "pairing-sensitive" sites within a 1.6-kb region. Genetics 1994, 136:1025-1038.
105. Li H.B., Muller M., Bahechar I.A., Kyrchanova O., Ohno K., Georgiev P., Pirrotta V. Insulators, not polycomb response elements, are required for long-range interactions between polycomb targets in Drosophila melanogaster. Mol. Cell. Biol. 2011, 31:616-625.
106. Bantignies F., Grimaud C., Lavrov S., Gabut M., Cavalli G. Inheritance of polycomb-dependent chromosomal interactions in Drosophila. Genes Dev. 2003, 17:2406-2420.
107. Fritsch C., Brown J.L., Kassis J.A., Muller J. The DNA-binding polycomb group protein pleiohomeotic mediates silencing of a Drosophila homeotic gene. Development 1999, 126:3905-3913.
108. Vazquez J., Muller M., Pirrotta V., Sedat J.W. The Mcp element mediates stable long-range chromosome-chromosome interactions in Drosophila. Mol. Biol. Cell 2006, 17:2158-2165.
109. Li H.B., Ohno K., Gui H., Pirrotta V. Insulators target active genes to transcription factories and polycomb-repressed genes to polycomb bodies. PLoS Genet. 2013, 9:e1003436.
110. Oki M., Kamakaka R.T. Barrier function at HMR. Mol. Cell 2005, 19:707-716.
111. Jin C., Felsenfeld G. Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev. 2007, 21:1519-1529.
112. Jin C., Zang C., Wei G., Cui K., Peng W., Zhao K., Felsenfeld G. H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat. Genet. 2009, 41:941-945.
113. Mito Y., Henikoff J.G., Henikoff S. Histone replacement marks the boundaries of cis-regulatory domains. Science 2007, 315:1408-1411.
114. Li M., Belozerov V.E., Cai H.N. Modulation of chromatin boundary activities by nucleosome-remodeling activities in Drosophila melanogaster. Mol. Cell. Biol. 2010, 30:1067-1076.
115. Schweinsberg S., Hagstrom K., Gohl D., Schedl P., Kumar R.P., Mishra R., Karch F. The enhancer-blocking activity of the Fab-7 boundary from the Drosophila bithorax complex requires GAGA-factor-binding sites. Genetics 2004, 168:1371-1384.
116. Gilchrist D.A., Dos Santos G., Fargo D.C., Xie B., Gao Y., Li L., Adelman K. Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation. Cell 2010, 143:540-551.
117. Chopra V.S., Cande J., Hong J.W., Levine M. Stalled Hox promoters as chromosomal boundaries. Genes Dev. 2009, 23:1505-1509.
118. Bondarenko V.A., Jiang Y.I., Studitsky V.M. Rationally designed insulator-like elements can block enhancer action in vitro. EMBO J. 2003, 22:4728-4737.
119. Hou C., Li L., Qin Z.S., Corces V.G. Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol. Cell 2012, 48:471-484.
120. Sexton T., Yaffe E., Kenigsberg E., Bantignies F., Leblanc B., Hoichman M., Parrinello H., Tanay A., Cavalli G. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 2012, 148:458-472.
121. Kharchenko P.V., Alekseyenko A.A., Schwartz Y.B., Minoda A., Riddle N.C., Ernst J., Sabo P.J., Larschan E., Gorchakov A.A., Gu T., Linder-Basso D., Plachetka A., Shanower G., Tolstorukov M.Y., Luquette L.J., Xi R., Jung Y.L., Park R.W., Bishop E.P., Canfield T.K., Sandstrom R., Thurman R.E., MacAlpine D.M., Stamatoyannopoulos J.A., Kellis M., Elgin S.C., Kuroda M.I., Pirrotta V., Karpen G.H., Park P.J. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 2011, 471:480-485.
122. Dixon J.R., Selvaraj S., Yue F., Kim A., Li Y., Shen Y., Hu M., Liu J.S., Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
123. Lieberman-Aiden E., van Berkum N.L., Williams L., Imakaev M., Ragoczy T., Telling A., Amit I., Lajoie B.R., Sabo P.J., Dorschner M.O., Sandstrom R., Bernstein B., Bender M.A., Groudine M., Gnirke A., Stamatoyannopoulos J., Mirny L.A., Lander E.S., Dekker J. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293.
124. Nora E.P., Lajoie B.R., Schulz E.G., Giorgetti L., Okamoto I., Servant N., Piolot T., van Berkum N.L., Meisig J., Sedat J., Gribnau J., Barillot E., Bluthgen N., Dekker J., Heard E. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012, 485:381-385.
125. Phillips-Cremins J.E., Sauria M.E., Sanyal A., Gerasimova T.I., Lajoie B.R., Bell J.S., Ong C.T., Hookway T.A., Guo C., Sun Y., Bland M.J., Wagstaff W., Dalton S., McDevitt T.C., Sen R., Dekker J., Taylor J., Corces V.G. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 2013, 153:1281-1295.
126. Heger P., Marin B., Schierenberg E. Loss of the insulator protein CTCF during nematode evolution. BMC Mol. Biol. 2009, 10:84.
127. Schoborg T.A., Labrador M. The phylogenetic distribution of non-CTCF insulator proteins is limited to insects and reveals that BEAF-32 is Drosophila lineage specific. J. Mol. Evol. 2010, 70:74-84.
128. Xu Z., Wei G., Chepelev I., Zhao K., Felsenfeld G. Mapping of INS promoter interactions reveals its role in long-range regulation of SYT8 transcription. Nat. Struct. Mol. Biol. 2011, 18:372-378.
129. Nativio R., Wendt K.S., Ito Y., Huddleston J.E., Uribe-Lewis S., Woodfine K., Krueger C., Reik W., Peters J.M., Murrell A. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLoS Genet. 2009, 5:e1000739.
130. Bau D., Sanyal A., Lajoie B.R., Capriotti E., Byron M., Lawrence J.B., Dekker J., Marti-Renom M.A. The three-dimensional folding of the alpha-globin gene domain reveals formation of chromatin globules. Nat. Struct. Mol. Biol. 2011, 18:107-114.
131. Yu W., Ginjala V., Pant V., Chernukhin I., Whitehead J., Docquier F., Farrar D., Tavoosidana G., Mukhopadhyay R., Kanduri C., Oshimura M., Feinberg A.P., Lobanenkov V., Klenova E., Ohlsson R. Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat. Genet. 2004, 36:1105-1110.
132. Ong C.T., Van Bortle K., Ramos E., Corces V.G. Poly(ADP-ribosyl)ation regulates insulator function and intrachromosomal interactions in Drosophila. Cell 2013, 155:148-159.
133. Matsui M., Sharma K.C., Cooke C., Wakimoto B.T., Rasool M., Hayworth M., Hylton C.A., Tomkiel J.E. Nuclear structure and chromosome segregation in Drosophila male meiosis depend on the ubiquitin ligase dTopors. Genetics 2011, 189:779-793.
134. Aoki T., Sarkeshik A., Yates J., Schedl P. Elba, a novel developmentally regulated chromatin boundary factor is a hetero-tripartite DNA binding complex. eLife 2012, 1:e00171.
135. Aoki T., Schweinsberg S., Manasson J., Schedl P. A stage-specific factor confers Fab-7 boundary activity during early embryogenesis in Drosophila. Mol. Cell. Biol. 2008, 28:1047-1060.
136. Dai Q., Ren A., Westholm J.O., Serganov A.A., Patel D.J., Lai E.C. The BEN domain is a novel sequence-specific DNA-binding domain conserved in neural transcriptional repressors. Genes Dev. 2013, 27:602-614.
137. Trojer P., Li G., Sims R.J., Vaquero A., Kalakonda N., Boccuni P., Lee D., Erdjument-Bromage H., Tempst P., Nimer S.D., Wang Y.H., Reinberg D. L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 2007, 129:915-928.
138. Grimm C., Matos R., Ly-Hartig N., Steuerwald U., Lindner D., Rybin V., Muller J., Muller C.W. Molecular recognition of histone lysine methylation by the polycomb group repressor dSfmbt. EMBO J. 2009, 28:1965-1977.
139. Richter C., Oktaba K., Steinmann J., Muller J., Knoblich J.A. The tumour suppressor L(3)mbt inhibits neuroepithelial proliferation and acts on insulator elements. Nat. Cell Biol. 2011, 13:1029-1039.
140. Csink A.K., Linsk R., Birchler J.A. The lighten up (Lip) gene of Drosophila melanogaster, a modifier of retroelement expression, position effect variegation and white locus insertion alleles. Genetics 1994, 138:153-163.
141. Park J.W., Parisky K., Celotto A.M., Reenan R.A., Graveley B.R. Identification of alternative splicing regulators by RNA interference in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:15974-15979.
142. Ishizuka A., Siomi M.C., Siomi H. A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 2002, 16:2497-2508.
143. Yao H., Brick K., Evrard Y., Xiao T., Camerini-Otero R.D., Felsenfeld G. Mediation of CTCF transcriptional insulation by DEAD-box RNA-binding protein p68 and steroid receptor RNA activator SRA. Genes Dev. 2010, 24:2543-2555.
144. Sun S., Del Rosario B.C., Szanto A., Ogawa Y., Jeon Y., Lee J.T. Jpx RNA activates Xist by evicting CTCF. Cell 2013, 153:1537-1551.
145. Matzat L.H., Dale R.K., Lei E.P. Messenger RNA is a functional component of a chromatin insulator complex. EMBO Rep. 2013, 14:916-922.
146. Brennecke J., Aravin A.A., Stark A., Dus M., Kellis M., Sachidanandam R., Hannon G.J. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128:1089-1103.
147. Georgiev P.G., Gerasimova T.I. Novel genes influencing the expression of the yellow locus and mdg4 (gypsy) in Drosophila melanogaster. Mol. Gen. Genet. 1989, 220:121-126.
148. Georgieva S., Nabirochkina E., Dilworth F.J., Eickhoff H., Becker P., Tora L., Georgiev P., Soldatov A. The novel transcription factor e(y)2 interacts with TAF(II)40 and potentiates transcription activation on chromatin templates. Mol. Cell. Biol. 2001, 21:5223-5231.
149. Kurshakova M.M., Krasnov A.N., Kopytova D.V., Shidlovskii Y.V., Nikolenko J.V., Nabirochkina E.N., Spehner D., Schultz P., Tora L., Georgieva S.G. SAGA and a novel Drosophila export complex anchor efficient transcription and mRNA export to NPC. EMBO J. 2007, 26:4956-4965.
150. Kurshakova M., Maksimenko O., Golovnin A., Pulina M., Georgieva S., Georgiev P., Krasnov A. Evolutionarily conserved E(y)2/Sus1 protein is essential for the barrier activity of Su(Hw)-dependent insulators in Drosophila. Mol. Cell 2007, 27:332-338.
151. Vorobyeva N.E., Mazina M.U., Golovnin A.K., Kopytova D.V., Gurskiy D.Y., Nabirochkina E.N., Georgieva S.G., Georgiev P.G., Krasnov A.N. Insulator protein Su(Hw) recruits SAGA and Brahma complexes and constitutes part of origin recognition complex-binding sites in the Drosophila genome. Nucleic Acids Res. 2013, 41:5717-5730.
152. Yang J., Sung E., Donlin-Asp P.G., Corces V.G. A subset of Drosophila Myc sites remain associated with mitotic chromosomes colocalized with insulator proteins. Nat. Commun. 2013, 4:1464.