CTCF-binding sites within the H19 ICR differentially regulate local chromatin structures and cis-acting functions

Epigenetics

Volumn 7, Issue 4, 2012, Pages 361-369

  Guibert, Sylvain ^a,c   Zhao, Zhihu ^a,d   Sjölinder, Mikael ^a,b   Göndör, Anita ^a,b   Fernandez, Alejandro ^b   Pant, Vinod ^a,e   Ohlsson, Rolf ^a,b  

^a UPPSALA UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d BEIJING INSTITUTE OF BIOTECHNOLOGY   (China)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Chromatin; CTCF; H19; Imprinting; Insulator; Replication timing

Indexed keywords

CIS ACTING ELEMENT; TRANSCRIPTION FACTOR CTCF;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CHROMATIN STRUCTURE; CHROMOSOME; CONTROLLED STUDY; DNA METHYLATION; DNA REPLICATION; GENE EXPRESSION; GENE LOCUS; INSULATOR ELEMENT; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84860572987     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.19487     Document Type: Article

References (41)

1. Tremblay KD, Saam JR, Ingram RS, Tilghman SM, Bartolomei MS. A paternal-specific methylation imprint marks the alleles of the mouse H19 gene. Nat Genet 1995; 9:407-13; PMID:7795647; http://dx.doi.org/10.1038/ng0495-407.
2. Tremblay KD, Duran KL, Bartolomei MS. A 5' 2-kilobase-pair region of the imprinted mouse H19 gene exhibits exclusive paternal methylation throughout development. Mol Cell Biol 1997; 17:4322-9; PMID:9234689.
3. Srivastava M, Frolova E, Rottinghaus B, Boe SP, Grinberg A, Lee E, et al. Imprint control elementmediated secondary methylation imprints at the Igf2/H19 locus. J Biol Chem 2003; 278:5977-83; PMID:12270940; http://dx.doi.org/10.1074/jbc.M208437200.
4. Svensson K, Mattsson R, James TC, Wentzel P, Pilartz M, MacLaughlin J, et al. The paternal allele of the H19 gene is progressively silenced during early mouse development: the acetylation status of histones may be involved in the generation of variegated expression patterns. Development 1998; 125:61-9; PMID:9389664.
5. Srivastava M, Hsieh S, Grinberg A, Williams-Simons L, Huang SP, Pfeifer K. H19 and Igf2 monoallelic expression is regulated in two distinct ways by a shared cis acting regulatory region upstream of H19. Genes Dev 2000; 14:1186-95; PMID:10817754.
6. Leighton PA, Saam JR, Ingram RS, Stewart CL, Tilghman SM. An enhancer deletion affects both H19 and Igf2 expression. Genes Dev 1995; 9:2079-89; PMID:7544754; http://dx.doi.org/10.1101/gad.9.17.2079.
7. Bell AC, Felsenfeld G. Methylation of a CTCFdependent boundary controls imprinted expression of the Igf2 gene. Nature 2000; 405:482-5; PMID:10839546; http://dx.doi.org/10.1038/35013100.
8. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM. CTCF mediates methylationsensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 2000; 405:486-9; PMID:10839547; http://dx.doi.org/10.1038/35013106.
9. Kanduri C, Pant V, Loukinov D, Pugacheva E, Qi CF, Wolffe A, et al. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr Biol 2000; 10:853-6; PMID:10899010; http://dx.doi.org/10.1016/S0960-9822(00)00597-2.
10. Hou C, Corces VG. Insulators and imprinting from flies to mammals. BMC Biol 2010; 8:104; PMID:20687908; http://dx.doi.org/10.1186/1741-7007-8-104.
11. Webber AL, Ingram RS, Levorse JM, Tilghman SM. Location of enhancers is essential for the imprinting of H19 and Igf2 genes. Nature 1998; 391:711-5; PMID:9490417; http://dx.doi.org/10.1038/35781.
12. Ohlsson R, Lobanenkov V, Klenova E. Does CTCF mediate between nuclear organization and gene expression? Bioessays 2010; 32:37-50; PMID:20020479; http://dx.doi.org/10.1002/bies.200900118.
13. Schoenherr CJ, Levorse JM, Tilghman SM. CTCF maintains differential methylation at the Igf2/H19 locus. Nat Genet 2003; 33:66-9; PMID:12461525; http://dx.doi.org/10.1038/ng1057.
14. Pant V, Mariano P, Kanduri C, Mattsson A, Lobanenkov V, Heuchel R, 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; 17:586-90; PMID:12629040; http://dx.doi.org/10.1101/gad.254903.
15. 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; 36:889-93; PMID:15273689; http://dx.doi.org/10.1038/ng1402.
16. Kurukuti S, Tiwari VK, Tavoosidana G, Pugacheva E, Murrell A, Zhao Z, 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 USA 2006; 103:10684-9; PMID:16815976; http://dx.doi.org/10.1073/pnas.0600326103.
17. Nativio R, Wendt KS, Ito Y, Huddleston JE, Uribe-Lewis S, Woodfine K, et al. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLoS Genet 2009; 5:1000739; PMID:19956766; http://dx.doi.org/10.1371/journal.pgen.1000739.
18. Constância M, Dean W, Lopes S, Moore T, Kelsey G, Reik W. Deletion of a silencer element in Igf2 results in loss of imprinting independent of H19. Nat Genet 2000; 26:203-6; PMID:11017078; http://dx.doi.org/10.1038/79930.
19. Göndör A, Ohlsson R. Chromatin insulators and cohesins. EMBO Rep 2008; 9:327-9; PMID:18379583; http://dx.doi.org/10.1038/embor.2008.46.
20. Mukhopadhyay R, Yu W, Whitehead J, Xu J, Lezcano M, Pack S, et al. The binding sites for the chromatin insulator protein CTCF map to DNA methylation-free domains genome-wide. Genome Res 2004; 14:1594-602; PMID:15256511; http://dx.doi.org/10.1101/gr.2408304.
21. Pugacheva EM, Tiwari VK, Abdullaev Z, Vostrov AA, Flanagan PT, Quitschke WW, et al. Familial cases of point mutations in the XIST promoter reveal a correlation between CTCF binding and pre-emptive choices of X chromosome inactivation. Hum Mol Genet 2005; 14:953-65; PMID:15731119; http://dx.doi.org/10.1093/hmg/ddi089.
22. Chernukhin I, Shamsuddin S, Kang SY, Bergström R, Kwon YW, Yu W, et al. CTCF interacts with and recruits the largest subunit of RNA polymerase II to CTCF target sites genome-wide. Mol Cell Biol 2007; 27:1631-48; PMID:17210645; http://dx.doi.org/10.1128/MCB.01993-06.
23. 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; PMID:19056695; http://dx.doi.org/10.1101/gr.082800.108.
24. Bergström R, Whitehead J, Kurukuti S, Ohlsson R. CTCF regulates asynchronous replication of the imprinted H19/Igf2 domain. Cell Cycle 2007; 6:450-4; PMID:17329968; http://dx.doi.org/10.4161/cc.6.4.3854.
25. Ohlsson R, Renkawitz R, Lobanenkov V. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet 2001; 17:520-7; PMID:11525835; http://dx.doi.org/10.1016/S0168-9525(01)02366-6.
26. Pant V, Kurukuti S, Pugacheva E, Shamsuddin S, Mariano P, Renkawitz R, et al. 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; 24:3497-504; PMID:15060168; http://dx.doi.org/10.1128/MCB.24.8.3497-504.2004.
27. Zhao Z, Tavoosidana G, Sjölinder M, Göndör A, Mariano P, Wang S, et al. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat Genet 2006; 38:1341-7; PMID:17033624; http://dx.doi.org/10.1038/ng1891.
28. Sandhu KS, Shi C, Sjölinder M, Zhao Z, Göndör A, Liu L, et al. Nonallelic transvection of multiple imprinted loci is organized by the H19 imprinting control region during germline development. Genes Dev 2009; 23:2598-603; PMID:19933149; http://dx.doi.org/10.1101/gad.552109.
29. Phillips JE, Corces VG. CTCF: master weaver of the genome. Cell 2009; 137:1194-211; PMID:19563753; http://dx.doi.org/10.1016/j.cell.2009.06.001.
30. Handoko L, Xu H, Li G, Ngan CY, Chew E, Schnapp M, et al. CTCF-mediated functional chromatin interactome in pluripotent cells. Nat Genet 2011; 43:630-8; PMID:21685913; http://dx.doi.org/10.1038/ng.857.
31. Dean W, Bowden L, Aitchison A, Klose J, Moore T, Meneses JJ, et al. Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: association with aberrant phenotypes. Development 1998; 125:2273-82; PMID:9584126.
32. Simon I, Tenzen T, Reubinoff BE, Hillman D, McCarrey JR, Cedar H. Asynchronous replication of imprinted genes is established in the gametes and maintained during development. Nature 1999; 401:929-32; PMID:10553911; http://dx.doi.org/10.1038/44866.
33. Göndör A, Ohlsson R. Replication timing and epigenetic reprogramming of gene expression: a twoway relationship? Nat Rev Genet 2009; 10:269-76; PMID:19274048; http://dx.doi.org/10.1038/nrg2555.
34. Cerrato F, Dean W, Davies K, Kagotani K, Mitsuya K, Okumura K, et al. Paternal imprints can be established on the maternal Igf2-H19 locus without altering replication timing of DNA. Hum Mol Genet 2003; 12:3123-32; PMID:14532328; http://dx.doi.org/10.1093/hmg/ddg338.
35. Kang H, Wiedmer A, Yuan Y, Robertson E, Lieberman PM. Coordination of KSHV latent and lytic gene control by CTCF-cohesin mediated chromosome conformation. PLoS Pathog 2011; 7:1002140; PMID:21876668; http://dx.doi.org/10.1371/journal.ppat.1002140.
36. Poole RL, Leith DJ, Docherty LE, Shmela ME, Gicquel C, Splitt M, et al. Beckwith-Wiedemann syndrome caused by maternally inherited mutation of an OCT-binding motif in the IGF2/H19-imprinting control region, ICR1. Eur J Hum Genet 2011; 20:240-3; PMID:21863054.
37. Demars J, Shmela ME, Rossignol S, Okabe J, Netchine I, Azzi S, et al. Analysis of the IGF2/H19 imprinting control region uncovers new genetic defects, including mutations of OCT-binding sequences, in patients with 11p15 fetal growth disorders. Hum Mol Genet 2010; 19:803-14; PMID:20007505; http://dx.doi.org/10.1093/hmg/ddp549.
38. Weth O, Renkawitz R. CTCF function is modulated by neighboring DNA binding factors. Biochem Cell Biol 2011; 89:459-68; PMID:21895576; http://dx.doi.org/10.1139/o11-033.
39. Burke LJ, Zhang R, Bartkuhn M, Tiwari VK, Tavoosidana G, Kurukuti S, et al. CTCF binding and higher order chromatin structure of the H19 locus are maintained in mitotic chromatin. EMBO J 2005; 24:3291-300; PMID:16107875; http://dx.doi.org/10.1038/sj.emboj.7600793.
40. Bacher CP, Guggiari M, Brors B, Augui S, Clerc P, Avner P, et al. Transient colocalization of X-inactivation centres accompanies the initiation of X inactivation. Nat Cell Biol 2006; 8:293-9; PMID:16434960; http://dx.doi.org/10.1038/ncb1365.
41. Göndör A, Rougier C, Ohlsson R. High-resolution circular chromosome conformation capture assay. Nat Protoc 2008; 3:303-13; PMID:18274532; http://dx.doi.org/10.1038/nprot.2007.540.