CTCF demarcates chicken embryonic α-globin gene autonomous silencing and contributes to adult stage-specific gene expression

Epigenetics

Volumn 8, Issue 8, 2013, Pages 827-838

  Valdes Quezada, Christian ^a   Arriaga Canon, Cristian ^a   Fonseca Guzmán, Yael ^a   Guerrero, Georgina ^a   Recillas Targa, Félix ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

5 hydroxymethylcytosine; Chromosome conformation capture; CTCF; DNA methylation; Enhancer promoter interaction; Epigenetic silencing

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; 5 HYDROXYMETHYLCYTOSINE; HEMOGLOBIN ALPHA CHAIN; HISTONE ACETYLTRANSFERASE; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR SP1; TRICHOSTATIN A;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CHICKEN; CHROMOSOME STRUCTURE; CONTROLLED STUDY; CPG ISLAND; DEVELOPMENT; DNA METHYLATION; EMBRYO; ERYTHROID CELL; FLOW CYTOMETRY; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; IMMUNOPRECIPITATION; NONHUMAN; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION;

AVES;

5-HYDROXYMETHYLCYTOSINE; CHROMOSOME CONFORMATION CAPTURE; CTCF; DNA METHYLATION; ENHANCER-PROMOTER INTERACTION; EPIGENETIC SILENCING;

ALPHA-GLOBINS; ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CHICK EMBRYO; CHROMATIN; CPG ISLANDS; DNA METHYLATION; EMBRYONIC DEVELOPMENT; EPIGENESIS, GENETIC; ERYTHROID CELLS; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC LOCI; HISTONES; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS;

EID: 84880972346     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.25472     Document Type: Article

References (46)

1. Ghirlando R, Giles K, Gowher H, Xiao T, Xu Z, Yao H, et al. Chromatin domains, insulators, and the regulation of gene expression. Biochim Biophys Acta 2012; 1819:644-51; PMID:22326678; http://dx.doi. org/10.1016/j.bbagrm.2012.01.016
2. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012; 485:376-80; PMID:22495300; http://dx.doi. org/10.1038/nature11082
3. Rincón-Arano H, Guerrero G, Valdes-Quezada C, Recillas-Targa F. Chicken α-globin switching depends on autonomous silencing of the embryonic π globin gene by epigenetics mechanisms. J Cell Biochem 2009; 108:675-87; PMID:19693775; http://dx.doi. org/10.1002/jcb.22304
4. Stamatoyannopoulos G. Control of globin gene expression during development and erythroid differentiation. Exp Hematol 2005; 33:259-71; PMID:15730849; http://dx.doi.org/10.1016/j.exphem.2004.11.007
5. West AG, Fraser P. Remote control of gene transcription. Hum Mol Genet 2005; 14(Spec No 1):R101-11; PMID:15809261; http://dx.doi.org/10.1093/hmg/ ddi104
6. Ragoczy T, Bender MA, Telling A, Byron R, Groudine M. The locus control region is required for association of the murine β-globin locus with engaged transcription factories during erythroid maturation. Genes Dev 2006; 20:1447-57; PMID:16705039; http://dx.doi. org/10.1101/gad.1419506
7. Furlan-Magaril M, Rebollar E, Guerrero G, Fernández A, Moltó E, González-Buendía E, et al. An insulator embedded in the chicken α-globin locus regulates chromatin domain configuration and differential gene expression. Nucleic Acids Res 2011; 39:89-103; PMID:20813760; http://dx.doi.org/10.1093/nar/ gkq740
8. Vyas P, Vickers MA, Picketts DJ, Higgs DR. Conservation of position and sequence of a novel, widely expressed gene containing the major human α-globin regulatory element. Genomics 1995; 29:679-89; PMID:8575760; http://dx.doi.org/10.1006/ geno.1995.9951
9. Flint J, Tufarelli C, Peden J, Clark K, Daniels RJ, Hardison R, et al. Comparative genome analysis delimits a chromosomal domain and identifies key regulatory elements in the α globin cluster. Hum Mol Genet 2001; 10:371-82; PMID:11157800; http://dx.doi. org/10.1093/hmg/10.4.371
10. Escamilla-Del-Arenal M, Recillas-Targa F. GATA-1 modulates the chromatin structure and activity of the chicken α-globin 3' enhancer. Mol Cell Biol 2008; 28:575-86; PMID:17984219; http://dx.doi. org/10.1128/MCB.00943-07
11. Harju-Baker S, Costa FC, Fedosyuk H, Neades R, Peterson KR. Silencing of Agamma-globin gene expression during adult definitive erythropoiesis mediated by GATA-1-FOG-1-Mi2 complex binding at the-566 GATA site. Mol Cell Biol 2008; 28:3101-13; PMID:18347053; http://dx.doi.org/10.1128/ MCB.01858-07
12. Knezetic JA, Felsenfeld G. Mechanism of developmental regulation of α π, the chicken embryonic α-globin gene. Mol Cell Biol 1993; 13:4632-9; PMID:8336706
13. Zhang Y, Shu J, Si J, Shen L, Estecio MR, Issa JP. Repetitive elements and enforced transcriptional repression co-operate to enhance DNA methylation spreading into a promoter CpG-island. Nucleic Acids Res 2012; 40:7257-68; PMID:22600741; http:// dx.doi.org/10.1093/nar/gks429
14. Recillas-Targa F, de la Rosa-Velázquez IA, Soto-Reyes E. Insulation of tumor suppressor genes by the nuclear factor CTCF. Biochem Cell Biol 2011; 89:479-88; PMID:21846316; http://dx.doi.org/10.1139/o11-031
15. Lienert F, Wirbelauer C, Som I, Dean A, Mohn F, Schübeler D. Identification of genetic elements that autonomously determine DNA methylation states. Nat Genet 2011; 43:1091-7; PMID:21964573; http:// dx.doi.org/10.1038/ng.946
16. Beug H, von Kirchbach A, Döderlein G, Conscience JF, Graf T. Chicken hematopoietic cells transformed by seven strains of defective avian leukemia viruses display three distinct phenotypes of differentiation. Cell 1979; 18:375-90; PMID:227607; http://dx.doi. org/10.1016/0092-8674(79)90057-6
17. Gavrilov AA, Razin SV. Spatial configuration of the chicken α-globin gene domain: immature and active chromatin hubs. Nucleic Acids Res 2008; 36:4629-40; PMID:18621783; http://dx.doi.org/10.1093/nar/ gkn429
18. Wu H, Zhang Y. Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev 2011; 25:2436-52; PMID:22156206; http://dx.doi. org/10.1101/gad.179184.111
19. Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA, et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011; 473:398-402; PMID:21460836; http://dx.doi.org/10.1038/nature10008
20. Martin D, Pantoja C, Fernández Miñán A, Valdes-Quezada C, Moltó E, Matesanz F, et al. Genome-wide CTCF distribution in vertebrates defines equivalent sites that aid the identification of disease-associated genes. Nat Struct Mol Biol 2011; 18:708-14; PMID:21602820; http://dx.doi.org/10.1038/ nsmb.2059
21. Ioudinkova ES, Ulianov SV, Bunina D, Iarovaia OV, Gavrilov AA, Razin SV. The inactivation of the π gene in chicken erythroblasts of adult lineage is not mediated by packaging of the embryonic part of the α-globin gene domain into a repressive heterochromatin-like structure. Epigenetics 2011; 6:1481-8; PMID:22139578; http://dx.doi.org/10.4161/epi.6.12.18215
22. Klochkov D, Rincón-Arano H, Ioudinkova ES, Valadez-Graham V, Gavrilov A, Recillas-Targa F, et al. A CTCFdependent silencer located in the differentially methylated area may regulate expression of a housekeeping gene overlapping a tissue-specific gene domain. Mol Cell Biol 2006; 26:1589-97; PMID:16478981; http:// dx.doi.org/10.1128/MCB.26.5.1589-1597.2006
23. Kim A, Dean A. A human globin enhancer causes both discrete and widespread alterations in chromatin structure. Mol Cell Biol 2003; 23:8099-109; PMID:14585970; http://dx.doi.org/10.1128/ MCB.23.22.8099-8109.2003
24. Zhao H, Dean A. An insulator blocks spreading of histone acetylation and interferes with RNA polymerase II transfer between an enhancer and gene. Nucleic Acids Res 2004; 32:4903-19; PMID:15371553; http:// dx.doi.org/10.1093/nar/gkh832
25. Mutskov V, Felsenfeld G. Silencing of transgene transcription precedes methylation of promoter DNA and histone H3 lysine 9. EMBO J 2004; 23:138-49; PMID:14685282; http://dx.doi.org/10.1038/ sj.emboj.7600013
26. Holwerda S, de Laat W. Chromatin loops, gene positioning, and gene expression. Front Genet 2012; 3:217; PMID:23087710; http://dx.doi.org/10.3389/ fgene.2012.00217
27. Hagège H, Klous P, Braem C, Splinter E, Dekker J, Cathala G, et al. Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Protoc 2007; 2:1722-33; PMID:17641637; http://dx.doi. org/10.1038/nprot.2007.243
28. Dekker J, Rippe K, Dekker M, Kleckner N. Capturing chromosome conformation. Science 2002; 295:1306-11; PMID:11847345; http://dx.doi.org/10.1126/science. 1067799
29. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P, Grosveld F, et al. CTCF mediates long-range chromatin looping and local histone modification in the β-globin locus. Genes Dev 2006; 20:2349-54; PMID:16951251; http://dx.doi.org/10.1101/gad.399506
30. Soto-Reyes E, González-Barrios R, Cisneros-Soberanis F, Herrera-Goepfert R, Pérez V, Cantú D, et al. Disruption of CTCF at the miR-125b1 locus in gynecological cancers. BMC Cancer 2012; 12:40; PMID:22277129; http://dx.doi.org/10.1186/1471-2407-12-40
31. Witcher M, Emerson BM. Epigenetic silencing of the p16(INK4a) tumor suppressor is associated with loss of CTCF binding and a chromatin boundary. Mol Cell 2009; 34:271-84; PMID:19450526; http://dx.doi. org/10.1016/j.molcel.2009.04.001
32. Brandeis M, Frank D, Keshet I, Siegfried Z, Mendelsohn M, Nemes A, et al. Sp1 elements protect a CpG island from de novo methylation. Nature 1994; 371:435-8; PMID:8090226; http://dx.doi.org/10.1038/371435a0
33. Dickson J, Gowher H, Strogantsev R, Gaszner M, Hair A, Felsenfeld G, et al. VEZF1 elements mediate protection from DNA methylation. PLoS Genet 2010; 6:e1000804; PMID:20062523; http://dx.doi. org/10.1371/journal.pgen.1000804
34. Recillas-Targa F, Pikaart MJ, Burgess-Beusse B, Bell AC, Litt MD, West AG, et al. Position-effect protection and enhancer blocking by the chicken β-globin insulator are separable activities. Proc Natl Acad Sci U S A 2002; 99:6883-8; PMID:12011446; http://dx.doi. org/10.1073/pnas.102179399
35. Weber M, Hellmann I, Stadler MB, Ramos L, Pääbo S, Rebhan M, et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 2007; 39:457-66; PMID:17334365; http://dx.doi.org/10.1038/ng1990
36. Sun Z, Terragni J, Borgaro JG, Liu Y, Yu L, Guan S, et al. High-resolution enzymatic mapping of genomic 5-hydroxymethylcytosine in mouse embryonic stem cells. Cell Rep 2013; 3:567-76; PMID:23352666; http://dx.doi.org/10.1016/j.celrep.2013.01.001
37. Guastafierro T, Cecchinelli B, Zampieri M, Reale A, Riggio G, Sthandier O, et al. CCCTC-binding factor activates PARP-1 affecting DNA methylation machinery. J Biol Chem 2008; 283:21873-80; PMID:18539602; http://dx.doi.org/10.1074/jbc. M801170200
38. Zampieri M, Guastafierro T, Calabrese R, Ciccarone F, Bacalini MG, Reale A, et al. ADP-ribose polymers localized on Ctcf-Parp1-Dnmt1 complex prevent methylation of Ctcf target sites. Biochem J 2012; 441:645-52; PMID:21985173; http://dx.doi. org/10.1042/BJ20111417
39. Palstra RJ, Tolhuis B, Splinter E, Nijmeijer R, Grosveld F, de Laat W. The β-globin nuclear compartment in development and erythroid differentiation. Nat Genet 2003; 35:190-4; PMID:14517543; http://dx.doi. org/10.1038/ng1244
40. Razin SV, Farrell CM, Recillas-Targa F. Genomic domains and regulatory elements operating at the domain level. Int Rev Cytol 2003; 226:63-125; PMID:12921236; http://dx.doi.org/10.1016/S0074-7696(03)01002-7
41. Liu Z, Scannell DR, Eisen MB, Tjian R. Control of embryonic stem cell lineage commitment by core promoter factor, TAF3. Cell 2011; 146:720-31; PMID:21884934; http://dx.doi.org/10.1016/j. cell.2011.08.005
42. Le May N, Fradin D, Iltis I, Bougnères P, Egly JM. XPG and XPF endonucleases trigger chromatin looping and DNA demethylation for accurate expression of activated genes. Mol Cell 2012; 47:622-32; PMID:22771116; http://dx.doi.org/10.1016/j.molcel. 2012.05.050
43. Mohn F, Weber M, Schübeler D, Roloff TC. Methylated DNA immunoprecipitation (MeDIP). Methods Mol Biol 2009; 507:55-64; PMID:18987806; http:// dx.doi.org/10.1007/978-1-59745-522-0_5
44. Williams K, Christensen J, Pedersen MT, Johansen JV, Cloos PA, Rappsilber J, et al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 2011; 473:343-8; PMID:21490601; http://dx.doi.org/10.1038/nature10066
45. Valadez-Graham V, Razin SV, Recillas-Targa F. CTCFdependent enhancer blockers at the upstream region of the chicken α-globin gene domain. Nucleic Acids Res 2004; 32:1354-62; PMID:14981153; http://dx.doi. org/10.1093/nar/gkh301
46. Litt MD, Simpson M, Recillas-Targa F, Prioleau MN, Felsenfeld G. Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J 2001; 20:2224-35; PMID:11331588; http://dx.doi.org/10.1093/emboj/20.9.2224