The CTCF insulator protein forms an unusual DNA structure

BMC Molecular Biology

Volumn 11, Issue , 2010, Pages

  MacPherson, Melissa J ^a   Sadowski, Paul D ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLOBIN; MYC PROTEIN; TRANSCRIPTION FACTOR CTCF; ZINC FINGER PROTEIN; CCCTC-BINDING FACTOR; DNA; REPRESSOR PROTEIN;

ARTICLE; BINDING SITE; BIOCHEMISTRY; DNA BINDING; DNA SEQUENCE; DNA STRUCTURE; ELECTROPHORESIS; HUMAN; IN VITRO STUDY; NONHUMAN; ANIMAL; CHEMISTRY; CHICKEN; CONFORMATION; METABOLISM; MOUSE; NUCLEOTIDE SEQUENCE; PROTEIN BINDING;

MAMMALIA;

ANIMALS; BASE SEQUENCE; BINDING SITES; CHICKENS; DNA; MICE; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; REPRESSOR PROTEINS; ZINC FINGERS;

EID: 78650270810     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-11-101     Document Type: Article

References (41)

1. Lobanenkov VV, Nicolas RH, Adler VV, Paterson H, Klenova EM, Polotskaja AV, Goodwin GH. A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5'-flanking sequence of the chicken c-myc gene. Oncogene 1990, 5(12):1743-1753.
2. Baniahmad A, Steiner C, Kohne AC, Renkawitz R. Modular structure of a chicken lysozyme silencer: involvement of an unusual thyroid hormone receptor binding site. Cell 1990, 61(3):505-514. 10.1016/0092-8674(90)90532-J, 2159385.
3. Ohlsson R, Renkawitz R, Lobanenkov V. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet 2001, 17(9):520-527. 10.1016/S0168-9525(01)02366-6, 11525835.
4. Filippova GN, Fagerlie S, Klenova EM, Myers C, Dehner Y, Goodwin G, Neiman PE, Collins SJ, Lobanenkov VV. 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. 231272, 8649389.
5. Burcin M, Arnold R, Lutz M, Kaiser B, Runge D, Lottspeich F, Filippova GN, Lobanenkov VV, Renkawitz R. Negative protein 1, which is required for function of the chicken lysozyme gene silencer in conjunction with hormone receptors, is identical to the multivalent zinc finger repressor CTCF. Mol Cell Biol 1997, 17(3):1281-1288. 231853, 9032255.
6. Awad TA, Bigler J, Ulmer JE, Hu YJ, Moore JM, Lutz M, Neiman PE, Collins SJ, Renkawitz R, Lobanenkov VV, et al. Negative transcriptional regulation mediated by thyroid hormone response element 144 requires binding of the multivalent factor CTCF to a novel target DNA sequence. J Biol Chem 1999, 274(38):27092-27098. 10.1074/jbc.274.38.27092, 10480923.
7. Kanduri C, Pant V, Loukinov D, Pugacheva E, Qi CF, Wolffe A, Ohlsson R, Lobanenkov VV. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr Biol 2000, 10(14):853-856. 10.1016/S0960-9822(00)00597-2, 10899010.
8. Quitschke WW, Taheny MJ, Fochtmann LJ, Vostrov AA. Differential effect of zinc finger deletions on the binding of CTCF to the promoter of the amyloid precursor protein gene [In Process Citation]. Nucleic Acids Res 2000, 28(17):3370-3378. 10.1093/nar/28.17.3370, 110710, 10954607.
9. Renda M, Baglivo I, Burgess-Beusse B, Esposito S, Fattorusso R, Felsenfeld G, Pedone PV. Critical DNA binding interactions of the insulator protein CTCF: A small number of zinc fingers mediate strong binding, and a single finger-DNA interaction controls binding at imprinted loci. J Biol Chem 2007, 282(46):33336-33345. 10.1074/jbc.M706213200, 17827499.
10. Holohan EE, 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(7):e112. 10.1371/journal.pgen.0030112, 1904468, 17616980.
11. Kim TH, Abdullaev ZK, Smith AD, Ching KA, Loukinov DI, Green RD, Zhang MQ, Lobanenkov VV, Ren B. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 2007, 128(6):1231-1245. 10.1016/j.cell.2006.12.048, 2572726, 17382889.
12. Klenova EM, Chernukhin IV, El-Kady A, Lee RE, Pugacheva EM, Loukinov DI, Goodwin GH, Delgado D, Filippova GN, Leon J, 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. 10.1128/MCB.21.6.2221-2234.2001, 86856, 11238955.
13. El-Kady A, Klenova E. Regulation of the transcription factor, CTCF, by phosphorylation with protein kinase CK2. FEBS Lett 2005, 579(6):1424-1434. 10.1016/j.febslet.2005.01.044, 15733852.
14. Yu W, Ginjala V, Pant V, Chernukhin I, Whitehead J, Docquier F, Farrar D, Tavoosidana G, Mukhopadhyay R, Kanduri C, et al. Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat Genet 2004, 36(10):1105-1110. 10.1038/ng1426, 15361875.
15. MacPherson MJ, Beatty LG, Zhou W, Du M, Sadowski PD. The CTCF insulator protein is posttranslationally modified by SUMO. Mol Cell Biol 2009, 29(3):714-725. 10.1128/MCB.00825-08, 2630690, 19029252.
16. Filippova GN. Genetics and epigenetics of the multifunctional protein CTCF. Curr Top Dev Biol 2008, 80:337-360. full_text, 17950379.
17. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P, Grosveld F, Galjart N, de Laat W. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev 2006, 20(17):2349-2354. 10.1101/gad.399506, 1560409, 16951251.
18. Hou C, Zhao H, Tanimoto K, Dean A. CTCF-dependent enhancer-blocking by alternative chromatin loop formation. Proc Natl Acad Sci USA 2008, 105(51):20398-20403. 10.1073/pnas.0808506106, 2629272, 19074263.
19. Kurukuti S, Tiwari VK, Tavoosidana G, Pugacheva E, Murrell A, Zhao Z, Lobanenkov V, Reik W, Ohlsson R. 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 USA 2006, 103(28):10684-10689. 10.1073/pnas.0600326103, 1484419, 16815976.
20. Murrell A, Heeson S, Reik W. Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat Genet 2004, 36(8):889-893. 10.1038/ng1402, 15273689.
21. Yoon YS, Jeong S, Rong Q, Chung JH, Pfeifer K. Analysis of the H19ICR Insulator. Mol Cell Biol 2007, 27(9):3499-3510. 10.1128/MCB.02170-06, 1899958, 17339341.
22. Li T, Hu JF, Qiu X, Ling J, Chen H, Wang S, Hou A, Vu TH, Hoffman AR. CTCF regulates allelic expression of Igf2 by orchestrating a promoter-polycomb repressive complex 2 intrachromosomal loop. Mol Cell Biol 2008, 28(20):6473-6482. 10.1128/MCB.00204-08, 2577414, 18662993.
23. Engel N, Raval AK, Thorvaldsen JL, Bartolomei SM. Three-dimensional conformation at the H19/Igf2 locus supports a model of enhancer tracking. Hum Mol Genet 2008, 17(19):3021-3029. 10.1093/hmg/ddn200, 2536502, 18617529.
24. Majumder P, Gomez JA, Chadwick BP, Boss JM. 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. 10.1084/jem.20071843, 2292219, 18347100.
25. Blackledge NP, Ott CJ, Gillen AE, Harris A. An insulator element 3' to the CFTR gene binds CTCF and reveals an active chromatin hub in primary cells. Nucleic Acids Res 2009, 37(4):1086-1094. 10.1093/nar/gkn1056, 2651798, 19129223.
26. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. High-resolution profiling of histone methylations in the human genome. Cell 2007, 129(4):823-837. 10.1016/j.cell.2007.05.009, 17512414.
27. Mukhopadhyay R, Yu W, Whitehead J, Xu J, Lezcano M, Pack S, Kanduri C, Kanduri M, Ginjala V, Vostrov A, et al. The Binding Sites for the Chromatin Insulator Protein CTCF Map to DNA Methylation-Free Domains Genome-Wide. Genome Res 2004, 14(8):1594-1602. 10.1101/gr.2408304, 509268, 15256511.
28. Xi H, Shulha HP, Lin JM, Vales TR, Fu Y, Bodine DM, McKay RD, Chenoweth JG, Tesar PJ, Furey TS, et al. Identification and Characterization of Cell Type-Specific and Ubiquitous Chromatin Regulatory Structures in the Human Genome. PLoS Genet 2007, 3(8):e136. 10.1371/journal.pgen.0030136, 1950163, 17708682.
29. Xie X, Mikkelsen TS, Gnirke A, Lindblad-Toh K, Kellis M, Lander ES. Systematic discovery of regulatory motifs in conserved regions of the human genome, including thousands of CTCF insulator sites. Proc Natl Acad Sci USA 2007, 104(17):7145-7150. 10.1073/pnas.0701811104, 1852749, 17442748.
30. Phillips JE, Corces VG. CTCF: master weaver of the genome. Cell 2009, 137(7):1194-1211. 10.1016/j.cell.2009.06.001, 19563753.
31. Yusufzai TM, Tagami H, Nakatani Y, Felsenfeld G. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol Cell 2004, 13(2):291-298. 10.1016/S1097-2765(04)00029-2, 14759373.
32. Arnold R, Burcin M, Kaiser B, Muller M, Renkawitz R. DNA bending by the silencer protein NeP1 is modulated by TR and RXR. Nucleic Acids Res 1996, 24(14):2640-2647. 10.1093/nar/24.14.2640, 146006, 8758989.
33. Kim J, Zwieb C, Wu C, Adhya S. Bending of DNA by gene-regulatory proteins: construction and use of a DNA bending vector. Gene 1989, 85(1):15-23. 10.1016/0378-1119(89)90459-9, 2533576.
34. Zinkel SS, Crothers DM. DNA bend direction by phase sensitive detection. Nature 1987, 328(6126):178-181. 10.1038/328178a0, 3600796.
35. Register JC, Griffith J. The direction of RecA protein assembly onto single strand DNA is the same as the direction of strand assimilation during strand exchange. J Biol Chem 1985, 260(22):12308-12312.
36. Pant V, Kurukuti S, Pugacheva E, Shamsuddin S, Mariano P, Renkawitz R, Klenova E, Lobanenkov V, Ohlsson R. Mutation of a single CTCF target site within the H19 imprinting control region leads to loss of Igf2 imprinting and complex patterns of de novo methylation upon maternal inheritance. Mol Cell Biol 2004, 24(8):3497-3504. 10.1128/MCB.24.8.3497-3504.2004, 381662, 15060168.
37. Kramer H, Niemoller M, Amouyal M, Revet B, von Wilcken-Bergmann B, Muller-Hill B. lac repressor forms loops with linear DNA carrying two suitably spaced lac operators. Embo J 1987, 6(5):1481-1491. 553955, 3301328.
38. Schleif R. DNA looping. Annu Rev Biochem 1992, 61:199-223. 10.1146/annurev.bi.61.070192.001215, 1497310.
39. Radman-Livaja M, Biswas T, Ellenberger T, Landy A, Aihara H. DNA arms do the legwork to ensure the directionality of lambda site-specific recombination. Curr Opin Struct Biol 2006, 16(1):42-50. 10.1016/j.sbi.2005.12.003, 1892226, 16368232.
40. Kyrchanova O, Chetverina D, Maksimenko O, Kullyev A, Georgiev P. Orientation-dependent interaction between Drosophila insulators is a property of this class of regulatory elements. Nucleic Acids Res 2008, 36(22):7019-7028. 10.1093/nar/gkn781, 2602758, 18987002.
41. Stothard P. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 2000, 28(6):1102-1104.