Chromatin Insulators: A Role in Nuclear Organization and Gene Expression

Advances in Cancer Research

Volumn 110, Issue , 2011, Pages 43-76

  Yang, Jingping ^a   Corces, Victor G ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

Chromatin; Gene expression; Insulator; Interchromosomal; Promoter; Transcription

Indexed keywords

DNA BINDING PROTEIN; HEAT SHOCK PROTEIN 70; ZINC FINGER PROTEIN;

BOOK; CELL DIFFERENTIATION; CELL NUCLEUS; CELL STRUCTURE; CHROMATIN; CHROMOSOME; DNA METHYLATION; DNA PROTEIN COMPLEX; DNA SEQUENCE; DROSOPHILA; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOME; HUMAN; INSULATOR ELEMENT; INTRON; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; RNA INTERFERENCE; TRANSCRIPTION REGULATION;

EID: 79959448657     PISSN: 0065230X     EISSN: 0065230X     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386469-7.00003-7     Document Type: Chapter

References (126)

1. Barski A., Cuddapah S., et al. High-resolution profiling of histone methylations in the human genome. Cell 2007, 129(4):823-837.
2. Bartkuhn M, Straub T., et al. Active promoters and insulators are marked by the centrosomal protein 190. EMBO J. 2009, 28(7):877-888.
3. Bell A.C., Felsenfeld G. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 2000, 405(6785):482-485.
4. Belozerov V.E., Majumder P., et al. A novel boundary element may facilitate independent gene regulation in the Antennapedia complex of Drosophila. EMBO J. 2003, 22(12):3113-3121.
5. Blanton J, Gaszner M., et al. Protein:protein interactions and the pairing of boundary elements in vivo. Genes Dev. 2003, 17(5):664-675.
6. Buchner K., Roth P., et al. Genetic and molecular complexity of the position effect variegation modifier mod(mdg4) in Drosophila. Genetics 2000, 155(1):141-157.
7. Bushey A.M, Dorman E.R., et al. Chromatin insulators: Regulatory mechanisms and epigenetic inheritance. Mol. Cell 2008, 32(1):1-9.
8. Bushey A.M., Ramos E., et al. Three subclasses of a Drosophila insulator show distinct and cell type-specific genomic distributions. Genes Dev. 2009, 23(11):1338-1350.
9. Byrd K., Corces V.G. Visualization of chromatin domains created by the gypsy insulator of Drosophila. J. Cell Biol. 2003, 162(4):565-574.
10. Capelson M., Corces V.G. The ubiquitin ligase dTopors directs the nuclear organization of a chromatin insulator. Mol. Cell 2005, 20(1):105-116.
11. Capelson M., Corces V.G. SUMO conjugation attenuates the activity of the gypsy chromatin insulator. EMBO J. 2006, 25(9):1906-1914.
12. Chen X., Xu H., et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008, 133(6):1106-1117.
13. Chernukhin I.V., Shamsuddin S., et al. Physical and functional interaction between two pluripotent proteins, the Y-box DNA/RNA-binding factor, YB-1, and the multivalent zinc finger factor, CTCF. J. Biol. Chem. 2000, 275(38):29915-29921.
14. Chernukhin I., Shamsuddin S., et al. CTCF interacts with and recruits the largest subunit of RNA polymerase II to CTCF target sites genome-wide. Mol. Cell. Biol. 2007, 27(5):1631-1648.
15. Cho D.H., Thienes C.P., et al. Antisense transcription and heterochromatin at the DM1 CTG repeats are constrained by CTCF. Mol. Cell 2005, 20(3):483-489.
16. Choi J.-H., Min N.Y., et al. TSA-induced DNMT1 down-regulation represses hTERT expression via recruiting CTCF into demethylated core promoter region of hTERT in HCT116. Biochem. Biophys. Res. Commun. 2010, 391(1):449-454.
17. Cleary J.D., Tome S., et al. Tissue- and age-specific DNA replication patterns at the CTG/CAG-expanded human myotonic dystrophy type 1 locus. Nat. Struct. Mol. Biol. 2010, 17(99):1079-1087.
18. Cuddapah S, Jothi R., et al. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res. 2009, 19(1):24-32.
19. Darci T.B., Debora N.M.-D., et al. DNA binding sites for putative methylation boundaries in the unmethylated region of the BRCA1 promoter. Int. J. Cancer 2004, 111(5):669-678.
20. D'Arcy V., Pore N., et al. BORIS, a paralogue of the transcription factor, CTCF, is aberrantly expressed in breast tumours. Br. J. Cancer 2008, 98(3):571-579.
21. Defossez P.-A., Kelly K.F., et al. The human enhancer blocker CTC-binding factor interacts with the transcription factor Kaiso. J. Biol. Chem. 2005, 280(52):43017-43023.
22. Degner-Leisso S.C., Feeney A.J. Epigenetic and 3-dimensional regulation of V(D)J rearrangement of immunoglobulin genes. Semin. Immunol. 2010, 22(6):346-352.
23. Degner S.C., Wong T.P., et al. Cutting edge: Developmental stage-specific recruitment of cohesin to CTCF sites throughout immunoglobulin loci during B lymphocyte development. J. Immunol. 2009, 182(1):44-48.
24. De La Rosa-Velázquez I.A., Rincón-Arano H., et al. Epigenetic regulation of the human retinoblastoma tumor suppressor gene promoter by CTCF. Cancer Res. 2007, 67(6):2577-2585.
25. Dhillon N., Raab J., et al. DNA polymerase epsilon, acetylases and remodellers cooperate to form a specialized chromatin structure at a tRNA insulator. EMBO J. 2009, 28(17):2583-2600.
26. Donohoe M.E., Silva S.S., et al. The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting. Nature 2009, 460(7251):128-132.
27. Donohoe M.E., Zhang L.-F., et al. Identification of a Ctcf cofactor, Yy1, for the X chromosome binary switch. Mol. Cell 2007, 25(1):43-56.
28. El-Kady A., Klenova E. Regulation of the transcription factor, CTCF, by phosphorylation with protein kinase CK2. FEBS Lett. 2005, 579(6):1424-1434.
29. Emberly E., Blattes R., et al. BEAF regulates cell-cycle genes through the controlled deposition of H3K9 methylation marks into its conserved dual-core binding sites. PLoS Biol. 2008, 6(12):2896-2910.
30. Farrar D., Rai S., et al. Mutational analysis of the poly(ADP-ribosyl)ation sites of the transcription factor CTCF provides an insight into the mechanism of its regulation by poly(ADP-ribosyl)ation. Mol. Cell. Biol. 2010, 30(5):1199-1216.
31. Farrell C.M., Grinberg A., et al. A large upstream region is not necessary for gene expression or hypersensitive site formation at the mouse β-globin locus. Proc. Natl. Acad. Sci. U.S.A. 2000, 97(26):14554-14559.
32. Ferraiuolo M.A., Rousseau M., et al. The three-dimensional architecture of Hox cluster silencing. Nucleic Acids Res. 2010, 38(21):7472-7484.
33. Filippova G.N. Genetics and epigenetics of the multifunctional protein CTCF. Current Topics in Developmental Biology 2007, Vol. 80:337-360. Academic Press, New York.
34. Filippova G.N., Fagerlie S., et al. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol. Cell. Biol. 1996, 16(6):2802-2813.
35. Filippova G.N., Qi C.-F., et al. Tumor-associated zinc finger mutations in the CTCF transcription factor selectively alter its DNA-binding specificity. Cancer Res. 2002, 62(1):48-52.
36. Filippova G.N., Thienes C.P., et al. CTCF-binding sites flank CTG/CAG repeats and form a methylation-sensitive insulator at the DM1 locus. Nat. Genet. 2001, 28(4):335-343.
37. Fitzpatrick G.V., Pugacheva E.M., et al. Allele-specific binding of CTCF to the multipartite imprinting control region KvDMR1. Mol. Cell. Biol. 2007, 27(7):2636-2647.
38. Gaszner M., Felsenfeld G. Insulators: Exploiting transcriptional and epigenetic mechanisms. Nat. Rev. Genet. 2006, 7(9):703-713.
39. Gaszner M., Vazquez J., et al. The Zw5 protein, a component of the scs chromatin domain boundary, is able to block enhancer-promoter interaction. Genes Dev. 1999, 13(16):2098-2107.
40. Gause M., Morcillo P., et al. Insulation of enhancer-promoter communication by a gypsy transposon insert in the Drosophila cut gene: Cooperation between suppressor of hairy-wing and modifier of mdg4 proteins. Mol. Cell. Biol. 2001, 21(14):4807-4817.
41. Gerasimova T.I., Byrd K., et al. A chromatin insulator determines the nuclear localization of DNA. Mol. Cell 2000, 6(5):1025-1035.
42. Gerasimova T.I., Gdula D.A., et al. A Drosophila protein that imparts directionality on a chromatin insulator is an enhancer of position-effect variegation. Cell 1995, 82(4):587-597.
43. Gerasimova T.I., Lei E.P., et al. Coordinated control of dCTCF and gypsy chromatin insulators in Drosophila. Mol. Cell 2007, 28(5):761-772.
44. Geyer P.K., Corces V.G. DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev. 1992, 6(10):1865-1873.
45. Ghosh D., Gerasimova T.I., et al. Interactions between the Su(Hw) and Mod(mdg4) proteins required for gypsy insulator function. EMBO J. 2001, 20(10):2518-2527.
46. Gilbert M.K., Tan Y.Y., et al. The Drosophila boundary element-associated factors BEAF-32A and BEAF-32B affect chromatin structure. Genetics 2006, 173(3):1365-1375.
47. Gombert W.M., et al. The c-myc insulator element and matrix attachment regions define the c-myc chromosomal domain. Mol. Cell. Biol. 2003, 23:9338-9348.
48. Gombert W.M., Krumm A. Targeted deletion of multiple CTCF-binding elements in the human C-MYC gene reveals a requirement for CTCF in C-MYC expression. PLoS ONE 2009, 4(7):e6109.
49. Guastafierro T., Cecchinelli B., et al. CCCTC-binding factor activates PARP-1 affecting DNA methylation machinery. J. Biol. Chem. 2008, 283(32):21873-21880.
50. Guelen L., Pagie L., et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 2008, 453(7197):948-951.
51. Gyurkovics H., Gausz J., et al. A new homeotic mutation in the Drosophila bithorax complex removes a boundary separating two domains of regulation. EMBO J. 1990, 9(8):2579-2585.
52. Hadjur S., Williams L.M., et al. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 2009, 460(7253):410-413.
53. Hark A.T., Schoenherr C.J., et al. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 2000, 405(6785):486-489.
54. Harrison D.A, Gdula D.A., et al. A leucine zipper domain of the suppressor of Hairy-wing protein mediates its repressive effect on enhancer function. Genes Dev. 1993, 7(10):1966-1978.
55. Hart C.M., Cuvier O., et al. Evidence for an antagonistic relationship between the boundary element-associated factor BEAF and the transcription factor DREF. Chromosoma 1999, 108(6):375-383.
56. Heath H., Ribeiro de Almeida C., et al. CTCF regulates cell cycle progression of alphabeta T cells in the thymus. EMBO J. 2008, 27(21):2839-2850.
57. Hikichi T., Kohda T., et al. Imprinting regulation of the murine Meg1/Grb10 and human GRB10 genes; roles of brain-specific promoters and mouse-specific CTCF-binding sites. Nucleic Acids Res. 2003, 31(5):1398-1406.
58. Holohan E.E., Kwong C., et al. CTCF genomic binding sites in Drosophila and the organisation of the bithorax complex. PLoS Genet. 2007, 3(7):e112.
59. Hong J.A., Kang Y., et al. Reciprocal binding of CTCF and BORIS to the NY-ESO-1 promoter coincides with derepression of this cancer-testis gene in lung cancer cells. Cancer Res. 2005, 65(17):7763-7774.
60. Hoover K.K., Chien A.J., et al. Effects of transposable elements on the expression of the forked gene of Drosophila melanogaster. Genetics 1993, 135(2):507-526.
61. Hou C., Dale R., et al. Cell type specificity of chromatin organization mediated by CTCF and cohesin. Proc. Natl. Acad. Sci. U.S.A. 2010, 107(8):3651-3656.
62. Huang S., Li X., et al. USF1 recruits histone modification complexes and is critical for maintenance of a chromatin barrier. Mol. Cell. Biol. 2007, 27(22):7991-8002.
63. Ishihara K., Oshimura M., et al. CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol. Cell 2006, 23(5):733-742.
64. Jelinic P., Shaw P. Loss of imprinting and cancer. J. Pathol. 2007, 211(3):261-268.
65. Jelinic P., Stehle J.-C., et al. The testis-specific factor CTCFL cooperates with the protein methyltransferase PRMT7 in H19 imprinting control region methylation. PLoS Biol. 2006, 4(11):e355.
66. Jiang N., Emberly E., et al. Genome-wide mapping of BEAF binding sites in Drosophila links BEAF to transcription. Mol. Cell. Biol. 2009, 29(13):3556-3568.
67. Johnatty S.E., Beesley J., et al. Evaluation of candidate stromal epithelial cross-talk genes identifies association between risk of serous ovarian cancer and TERT, a cancer susceptibility " Hot-Spot" PLoS Genet. 2010, 6(7):e1001016.
68. Jothi R., Cuddapah S., et al. Genome-wide identification of in vivo protein-DNA binding sites from ChIP-Seq data. Nucleic Acids Res. 2008, 36(16):5221-5231.
69. Kang Y., Hong J.A., et al. Dynamic transcriptional regulatory complexes including BORIS, CTCF and Sp1 modulate NY-ESO-1 expression in lung cancer cells. Oncogene 2007, 26(30):4394-4403.
70. Karch F., O M., Galloni, et al. 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(15):3138-3146.
71. Kellum R., Schedl P. A group of scs elements function as domain boundaries in an enhancer-blocking assay. Mol. Cell. Biol. 1992, 12(5):2424-2431.
72. Kim T.H., Abdullaev Z.K., et al. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 2007, 128(6):1231-1245.
73. Kim J., Kollhoff A., et al. Methylation-sensitive binding of transcription factor YY1 to an insulator sequence within the paternally expressed imprinted gene, Peg3. Hum. Mol. Genet. 2003, 12(3):233-245.
74. Klenova E.M., Chernukhin I.V., et al. Functional phosphorylation sites in the C-terminal region of the multivalent multifunctional transcriptional factor CTCF. Mol. Cell. Biol. 2001, 21(6):2221-2234.
75. Klenova E.M., Morse H.C., et al. The novel BORIS+CTCF gene family is uniquely involved in the epigenetics of normal biology and cancer. Semin. Cancer Biol. 2002, 12(5):399-414.
76. Kurukuti S., Tiwari V.K., et al. CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc. Natl. Acad. Sci. U.S.A. 2006, 103(28):10684-10689.
77. Labrador M., Corces V.G. Extensive exon reshuffling over evolutionary time coupled to trans-splicing in Drosophila. Genome Res. 2003, 13(10):2220-2228.
78. Labrador M., Mongelard F., et al. Protein encoding by both DNA strands. Nature 2001, 409:1000.
79. Lei E.P., Corces V.G. RNA interference machinery influences the nuclear organization of a chromatin insulator. Nat. Genet. 2006, 38(8):936-941.
80. Libby R.T., Hagerman K.A., et al. CTCF cis-regulates trinucleotide repeat instability in an epigenetic manner: A novel basis for mutational hot spot determination. PLoS Genet. 2008, 4(11):e1000257.
81. Ling J.Q., Li T., et al. CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1. Science 2006, 312(5771):269-272.
82. Loukinov D.I., Pugacheva E., et al. BORIS, a novel male germ-line-specific protein associated with epigenetic reprogramming events, shares the same 11-zinc-finger domain with CTCF, the insulator protein involved in reading imprinting marks in the soma. Proc. Natl. Acad. Sci. U.S.A. 2002, 99(10):6806-6811.
83. Lutz M., Burke L.J., et al. Transcriptional repression by the insulator protein CTCF involves histone deacetylases. Nucleic Acids Res. 2000, 28(8):1707-1713.
84. Majumder P., Gomez J.A., et al. The insulator factor CTCF controls MHC class II gene expression and is required for the formation of long-distance chromatin interactions. J. Exp. Med. 2008, 205(4):785-798.
85. Melnikova L., Juge F., et al. Interaction between the GAGA factor and Mod(mdg4) proteins promotes insulator bypass in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 2004, 101(41):14806-14811.
86. Mishiro T., Ishihara K., et al. Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster. EMBO J. 2009, 28(9):1234-1245.
87. Mohan M., Bartkuhn M., et al. The Drosophila insulator proteins CTCF and CP190 link enhancer blocking to body patterning. EMBO J. 2007, 26(19):4203-4214.
88. Murrell A., Heeson S., et al. Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat. Genet. 2004, 36(8):889-893.
89. Nativio R., Wendt K.S., et al. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLoS Genet. 2009, 5(11):e1000739.
90. Nguyen P., Cui H., et al. CTCFL/BORIS Is a methylation-independent DNA-binding protein that preferentially binds to the paternal H19 differentially methylated region. Cancer Res. 2008, 68(14):5546-5551.
91. Ohlsson R., Renkawitz R., et al. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet. 2001, 17(9):520-527.
92. Ottaviani A., Rival-Gervier S., et al. The D4Z4 macrosatellite repeat acts as a CTCF and A-type Lamins-dependent insulator in facio-scapulo-humeral dystrophy. PLoS Genet. 2009, 5(2):e1000394.
93. Ottaviani A., Schluth-Bolard C., et al. Identification of a perinuclear positioning element in human subtelomeres that requires A-type Lamins and CTCF. EMBO J. 2009, 28(16):2428-2436.
94. Pai C.Y., Lei E.P., et al. The centrosomal protein CP190 is a component of the gypsy chromatin insulator. Mol. Cell 2004, 16(5):737-748.
95. Pant V., Mariano P., et al. The nucleotides responsible for the direct physical contact between the chromatin insulator protein CTCF and the H19 imprinting control region manifest parent of origin-specific long-distance insulation and methylation-free domains. Genes Dev. 2003, 17(5):586-590.
96. Parelho V., Hadjur S., et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 2008, 132(3):422-433.
97. Pathak R.U., Rangaraj N., et al. Boundary element-associated factor 32B connects chromatin domains to the nuclear matrix. Mol. Cell. Biol. 2007, 27(13):4796-4806.
98. Phillips J.E., Corces V.G. CTCF: Master weaver of the genome. Cell 2009, 137(7):1194-1211.
99. Qi C.F., Martensson A., et al. CTCF functions as a critical regulator of cell-cycle arrest and death after ligation of the B cell receptor on immature B cells. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(2):633-638.
100. Renaud S., Loukinov D., et al. CTCF binds the proximal exonic region of hTERT and inhibits its transcription. Nucleic Acids Res. 2005, 33(21):6850-6860.
101. Renaud S., Loukinov D., et al. BORIS/CTCFL-mediated transcriptional regulation of the hTERT telomerase gene in testicular and ovarian tumor cells. Nucleic Acids Res. 2010, 39(3):862-873.
102. Renaud S., Pugacheva E.M., et al. Expression of the CTCF-paralogous cancer-testis gene, brother of the regulator of imprinted sites (BORIS), is regulated by three alternative promoters modulated by CpG methylation and by CTCF and p53 transcription factors. Nucleic Acids Res. 2007, 35(21):7372-7388.
103. Rodriguez C., Borgel J., et al. CTCF is a DNA methylation-sensitive positive regulator of the INK/ARF locus. Biochem. Biophys. Res. Commun. 2010, 392(2):129-134.
104. Roy S., Gilbert M.K., et al. Characterization of BEAF mutations isolated by homologous recombination in Drosophila. Genetics 2007, 176(2):801-813.
105. Roy S., Tan Y.Y., et al. 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. Genom. 2007, 277(3):273-286.
106. Rubio E.D., Reiss D.J., et al. CTCF physically links cohesin to chromatin. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(24):8309-8314.
107. Sandhu K.S., Shi C., et al. Nonallelic transvection of multiple imprinted loci is organized by the H19 imprinting control region during germline development. Genes Dev. 2009, 23(22):2598-2603.
108. Schweinsberg S., Hagstrom K., et al. The enhancer-blocking activity of the Fab-7 boundary from the Drosophila bithorax complex requires GAGA-factor-binding sites. Genetics 2004, 168(3):1371-1384.
109. Sekimata M., Pérez-Melgosa M., et al. CCCTC-binding factor and the transcription factor T-bet orchestrate T helper 1 cell-specific structure and function at the interferon-[gamma] locus. Immunity 2009, 31(4):551-564.
110. Splinter E., Heath H., et al. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev. 2006, 20(17):2349-2354.
111. Stedman W., Kang H., et al. Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators. EMBO J. 2008, 27(4):654-666.
112. Tam A.S., Devereux T.R., et al. Perturbations of the Ink4a/Arf gene locus in aflatoxin B1-induced mouse lung tumors. Carcinogenesis 2003, 24(1):121-132.
113. Tolhuis B., Palstra R.-J., et al. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol. Cell 2002, 10(6):1453-1465.
114. Torrano V., Chernukhin I., et al. CTCF regulates growth and erythroid differentiation of human myeloid leukemia cells. J. Biol. Chem. 2005, 280(30):28152-28161.
115. Wallace J.A., Felsenfeld G. We gather together: Insulators and genome organization. Curr. Opin. Genet. Dev. 2007, 17(5):400-407.
116. Wendt K.S, Yoshida K., et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 2008, 451(7180):796-801.
117. Weth O., Weth C., et al. Modular insulators: Genome wide search for composite CTCF/thyroid hormone receptor binding sites. PLoS ONE 2010, 5(4):e10119.
118. Witcher M., Emerson B.M. Epigenetic silencing of the p16INK4a tumor suppressor is associated with loss of CTCF binding and a chromatin boundary. Mol. Cell 2009, 34(3):271-284.
119. Xu N., Donohoe M.E., et al. Evidence that homologous X-chromosome pairing requires transcription and Ctcf protein. Nat. Genet. 2007, 39(11):1390-1396.
120. Xu J., Huo D., et al. CpG island methylation affects accessibility of the proximal BRCA1 promoter to transcription factors. Breast Cancer Res. Treat. 2010, 120(3):593-601.
121. Yao H., Brick K., et al. Mediation of CTCF transcriptional insulation by DEAD-box RNA-binding protein p68 and steroid receptor RNA activator SRA. Genes Dev. 2010, 24(22):2543-2555.
122. Yoon B., Herman H., et al. Rasgrf1 imprinting is regulated by a CTCF-dependent methylation-sensitive enhancer blocker. Mol. Cell. Biol. 2005, 25(24):11184-11190.
123. Yu W., Ginjala V., et al. Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat. Genet. 2004, 36(10):1105-1110.
124. Yusufzai T.M., Tagami H., et al. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol. Cell 2004, 13(2):291-298.
125. Zhao K., Hart C.M., et al. Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell 1995, 81(6):879-889.
126. Zhao Z., Tavoosidana G., et al. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat. Genet. 2006, 38(11):1341-1347.