CTCF binding site classes exhibit distinct evolutionary, genomic, epigenomic and transcriptomic features

Genome Biology

Volumn 10, Issue 11, 2009, Pages

  Essien, Kobby ^a   Vigneau, Sebastien ^a   Apreleva, Sofia ^a   Singh, Larry N ^a   Bartolomei, Marisa S ^a   Hannenhalli, Sridhar ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE; TRANSCRIPTION FACTOR CTCF; ZINC FINGER PROTEIN; CCCTC-BINDING FACTOR; REPRESSOR PROTEIN;

ARTICLE; BINDING SITE; CD4+ T LYMPHOCYTE; DNA BINDING MOTIF; EPIGENETICS; GENE EXPRESSION; GENOMICS; HUMAN; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN FUNCTION; TRANSCRIPTOMICS; BIOLOGICAL MODEL; CHEMISTRY; CYTOLOGY; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; LEUKEMIA CELL LINE; METABOLISM; MULTIGENE FAMILY; PROTEIN MOTIF;

AMINO ACID MOTIFS; BINDING SITES; CD4-POSITIVE T-LYMPHOCYTES; DNA; EPIGENESIS, GENETIC; EVOLUTION, MOLECULAR; GENOMICS; HISTONES; HUMANS; JURKAT CELLS; MODELS, GENETIC; MULTIGENE FAMILY; REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC;

EID: 76249107162     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2009-10-11-r131     Document Type: Article

References (54)

1. Ohlsson R, Renkawitz R, Lobanenkov V. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet 2001, 17:520-527. 10.1016/S0168-9525(01)02366-6, 11525835.
2. Fedoriw AM, Stein P, Svoboda P, Schultz RM, Bartolomei MS. Transgenic RNAi reveals essential function for CTCF in H19 gene imprinting. Science 2004, 303:238-240. 10.1126/science.1090934, 14716017.
3. Wan LB, Pan H, Hannenhalli S, Cheng Y, Ma J, Fedoriw A, Lobanenkov V, Latham KE, Schultz RM, Bartolomei MS. Maternal depletion of CTCF reveals multiple functions during oocyte and preimplantation embryo development. Development 2008, 135:2729-2738. 10.1242/dev.024539, 2596970, 18614575.
4. Heath H, Ribeiro de Almeida C, Sleutels F, Dingjan G, Nobelen S, Jonkers I, Ling KW, Gribnau J, Renkawitz R, Grosveld F, Hendriks RW, Galjart N. CTCF regulates cell cycle progression of alphabeta T cells in the thymus. EMBO J 2008, 27:2839-2850. 10.1038/emboj.2008.214, 2580790, 18923423.
5. 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, 5:1743-1753.
6. 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, 16:2802-2813. 231272, 8649389.
7. Gombert WM, Farris SD, Rubio ED, Morey-Rosler KM, Schubach WH, Krumm A. The c-myc insulator element and matrix attachment regions define the c-myc chromosomal domain. Mol Cell Biol 2003, 23:9338-9348. 10.1128/MCB.23.24.9338-9348.2003, 309672, 14645543.
8. Gombert WM, 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:e6109. 10.1371/journal.pone.0006109, 2699473, 19568426.
9. Vostrov AA, Quitschke WW. The zinc finger protein CTCF binds to the APBbeta domain of the amyloid beta-protein precursor promoter. Evidence for a role in transcriptional activation. J Biol Chem 1997, 272:33353-33359. 10.1074/jbc.272.52.33353, 9407128.
10. Engel N, Thorvaldsen JL, Bartolomei MS. CTCF binding sites promote transcription initiation and prevent DNA methylation on the maternal allele at the imprinted H19/Igf2 locus. Hum Mol Genet 2006, 15:2945-2954. 10.1093/hmg/ddl237, 16928784.
11. Vigneau S, Augui S, Navarro P, Avner P, Clerc P. An essential role for the DXPas34 tandem repeat and Tsix transcription in the counting process of X chromosome inactivation. Proc Natl Acad Sci USA 2006, 103:7390-7395. 10.1073/pnas.0602381103, 1464350, 16648248.
12. Donohoe ME, Zhang LF, Xu N, Shi Y, Lee JT. Identification of a Ctcf cofactor, Yy1, for the X chromosome binary switch. Mol Cell 2007, 25:43-56. 10.1016/j.molcel.2006.11.017, 17218270.
13. 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, 205:785-798. 10.1084/jem.20071843, 2292219, 18347100.
14. Phillips JE, Corces VG. CTCF: master weaver of the genome. Cell 2009, 137:1194-1211. 10.1016/j.cell.2009.06.001, 19563753.
15. Meijsing SH, Pufall MA, So AY, Bates DL, Chen L, Yamamoto KR. DNA binding site sequence directs glucocorticoid receptor structure and activity. Science 2009, 324:407-410. 10.1126/science.1164265, 2777810, 19372434.
16. Bruce AW, Lopez-Contreras AJ, Flicek P, Down TA, Dhami P, Dillon SC, Koch CM, Langford CF, Dunham I, Andrews RM, Vetrie D. Functional diversity for REST (NRSF) is defined by in vivo binding affinity hierarchies at the DNA sequence level. Genome Res 2009, 19:994-1005. 10.1101/gr.089086.108, 2694481, 19401398.
17. Tuteja G, Jensen ST, White P, Kaestner KH. Cis-regulatory modules in the mammalian liver: composition depends on strength of Foxa2 consensus site. Nucleic Acids Res 2008, 36:4149-4157. 10.1093/nar/gkn366, 2475634, 18556755.
18. Tanay A. Extensive low-affinity transcriptional interactions in the yeast genome. Genome Res 2006, 16:962-972. 10.1101/gr.5113606, 1524868, 16809671.
19. Hannenhalli S, Wang LS. Enhanced position weight matrices using mixture models. Bioinformatics 2005, 21(Suppl 1):i204-i212. 10.1093/bioinformatics/bti1001, 15961459.
20. Bao L, Zhou M, Cui Y. CTCFBSDB: a CTCF-binding site database for characterization of vertebrate genomic insulators. Nucleic Acids Res 2008, 36:D83-87. 10.1093/nar/gkm875, 2238977, 17981843.
21. 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, 129:823-837. 10.1016/j.cell.2007.05.009, 17512414.
22. 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, 128:1231-1245. 10.1016/j.cell.2006.12.048, 2572726, 17382889.
23. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, Loh YH, Yeo HC, Yeo ZX, Narang V, Govindarajan KR, Leong B, Shahab A, Ruan Y, Bourque G, Sung WK, Clarke ND, Wei CL, Ng HH. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008, 133:1106-1117. 10.1016/j.cell.2008.04.043, 18555785.
24. Fu Y, Sinha M, Peterson CL, Weng Z. The insulator binding protein CTCF positions 20 nucleosomes around its binding sites across the human genome. PLoS Genet 2008, 4:e1000138. 10.1371/journal.pgen.1000138, 2453330, 18654629.
25. Cuddapah S, Jothi R, Schones DE, Roh TY, 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. 10.1101/gr.082800.108, 2612964, 19056695.
26. Zlatanova J, Caiafa P. CTCF and its protein partners: divide and rule?. J Cell Sci 2009, 122:1275-1284. 10.1242/jcs.039990, 19386894.
27. Jothi R, Cuddapah S, Barski A, Cui K, Zhao K. Genome-wide identification of in vivo protein-DNA binding sites from ChIP-Seq data. Nucleic Acids Res 2008, 36:5221-5231. 10.1093/nar/gkn488, 2532738, 18684996.
28. Ren B. CTCF Project at Ren Lab. , http://bioinformatics-renlab.ucsd.edu/rentrac/wiki/CTCF_Project
29. Levy S, Hannenhalli S. Identification of transcription factor binding sites in the human genome sequence. Mamm Genome 2002, 13:510-514. 10.1007/s00335-002-2175-6, 12370781.
30. Stormo GD. DNA binding sites: representation and discovery. Bioinformatics 2000, 16:16-23. 10.1093/bioinformatics/16.1.16, 10812473.
31. Furey TS, Haussler D. Integration of the cytogenetic map with the draft human genome sequence. Hum Mol Genet 2003, 12:1037-1044. 10.1093/hmg/ddg113, 12700172.
32. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, Zhao K. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 2008, 40:897-903. 10.1038/ng.154, 2769248, 18552846.
33. Tanimoto K, Liu Q, Bungert J, Engel JD. Effects of altered gene order or orientation of the locus control region on human beta-globin gene expression in mice. Nature 1999, 398:344-348. 10.1038/18698, 10192336.
34. Du M, Beatty LG, Zhou W, Lew J, Schoenherr C, Weksberg R, Sadowski PD. Insulator and silencer sequences in the imprinted region of human chromosome 11p15.5. Hum Mol Genet 2003, 12:1927-1939. 10.1093/hmg/ddg194, 12874112.
35. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 2004, 101:6062-6067. 10.1073/pnas.0400782101, 395923, 15075390.
36. Su AI, Cooke MP, Ching KA, Hakak Y, Walker JR, Wiltshire T, Orth AP, Vega RG, Sapinoso LM, Moqrich A, Patapoutian A, Hampton GM, Schultz PG, Hogenesch JB. Large-scale analysis of the human and mouse transcriptomes. Proc Natl Acad Sci USA 2002, 99:4465-4470. 10.1073/pnas.012025199, 123671, 11904358.
37. 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, 104:7145-7150. 10.1073/pnas.0701811104, 1852749,1852749, 17442748.
38. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, Barre-Dirrie A, Reuter I, Chekmenev D, Krull M, Hornischer K, Voss N, Stegmaier P, Lewicki-Potapov B, Saxel H, Kel AE, Wingender E. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 2006, 34:D108-110. 10.1093/nar/gkj143, 1347505, 16381825.
39. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 2003, 4:P3. 10.1186/gb-2003-4-5-p3, 12734009.
40. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J, Miller W, Kent WJ, Nekrutenko A. Galaxy: a platform for interactive large-scale genome analysis. Genome Res 2005, 15:1451-1455. 10.1101/gr.4086505, 1240089, 16169926.
41. Tanay A, Gat-Viks I, Shamir R. A global view of the selection forces in the evolution of yeast cis-regulation. Genome Res 2004, 14:829-834. 10.1101/gr.2064404, 479109, 15123582.
42. Chernukhin I, Shamsuddin S, Kang SY, Bergstrom R, Kwon YW, Yu W, Whitehead J, Mukhopadhyay R, Docquier F, Farrar D, Morrison I, Vigneron M, Wu SY, Chiang CM, Loukinov D, Lobanenkov V, Ohlsson R, Klenova E. CTCF interacts with and recruits the largest subunit of RNA polymerase II to CTCF target sites genome-wide. Mol Cell Biol 2007, 27:1631-1648. 10.1128/MCB.01993-06, 1820452, 17210645.
43. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 2008, 453:948-951. 10.1038/nature06947, 18463634.
44. 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. Nucleic Acids Res 2000, 28:3370-3378. 10.1093/nar/28.17.3370, 110710, 10954607.
45. 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, 282:33336-33345. 10.1074/jbc.M706213200, 17827499.
46. Gause M, Schaaf CA, Dorsett D. Cohesin and CTCF: cooperating to control chromosome conformation?. Bioessays 2008, 30:715-718. 10.1002/bies.20787, 18623068.
47. Payer B, Lee JT. X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet 2008, 42:733-772. 10.1146/annurev.genet.42.110807.091711, 18729722.
48. Rapkins RW, Hore T, Smithwick M, Ager E, Pask AJ, Renfree MB, Kohn M, Hameister H, Nicholls RD, Deakin JE, Graves JA. Recent assembly of an imprinted domain from non-imprinted components. PLoS Genet 2006, 2:e182. 10.1371/journal.pgen.0020182, 1626109, 17069464.
49. Edwards CA, Mungall AJ, Matthews L, Ryder E, Gray DJ, Pask AJ, Shaw G, Graves JA, Rogers J, Dunham I, Renfree MB, Ferguson-Smith AC. The evolution of the DLK1-DIO3 imprinted domain in mammals. PLoS Biol 2008, 6:e135. 10.1371/journal.pbio.0060135, 2408620,2408620, 18532878.
50. Smits G, Mungall AJ, Griffiths-Jones S, Smith P, Beury D, Matthews L, Rogers J, Pask AJ, Shaw G, VandeBerg JL, McCarrey JR, Renfree MB, Reik W, Dunham I. Conservation of the H19 noncoding RNA and H19-IGF2 imprinting mechanism in therians. Nat Genet 2008, 40:971-976. 10.1038/ng.168, 18587395.
51. Hore TA, Rapkins RW, Graves JA. Construction and evolution of imprinted loci in mammals. Trends Genet 2007, 23:440-448. 10.1016/j.tig.2007.07.003, 17683825.
52. Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, van Steensel B, de Laat W. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat Genet 2006, 38:1348-1354. 10.1038/ng1896, 17033623.
53. Hannenhalli S, Putt ME, Gilmore JM, Wang J, Parmacek MS, Epstein JA, Morrisey EE, Margulies KB, Cappola TP. Transcriptional genomics associates FOX transcription factors with human heart failure. Circulation 2006, 114:1269-1276. 10.1161/CIRCULATIONAHA.106.632430, 16952980.
54. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci USA 2003, 100:9440-9445. 10.1073/pnas.1530509100, 170937, 12883005.