An insulator embedded in the chicken α-globin locus regulates chromatin domain configuration and differential gene expression

Nucleic Acids Research

Volumn 39, Issue 1, 2011, Pages 89-103

  Furlan Magaril, Mayra ^a   Rebollar, Eria ^a   Guerrero, Georgina ^a   Fernández, Almudena ^b,c   Moltó, Eduardo ^b,c   González Buendía, Edgar ^a   Cantero, Marta ^b,c   Montoliu, Lluís ^b,c   Recillas Targa, Félix ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b Centro Nacional de Biotecnologý a   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GLOBIN; MONOPHENOL MONOOXYGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POLY(ADENOSINE DIPHOSPHATE RIBOSE); TRANSCRIPTION FACTOR CTCF;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CHICKEN; CHROMATIN; CONTROLLED STUDY; ERYTHROBLAST; ERYTHROID CELL; GENE ACTIVATION; GENE DOSAGE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENETIC ORGANIZATION; GENETIC TRANSFECTION; HETEROZYGOSITY; IN VIVO STUDY; INSULATOR ELEMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; TRANSGENE;

MUS MUSCULUS;

EID: 78651288727     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq740     Document Type: Article

References (47)

1. West, A.G. and Fraser, P. (2005) Remote control of gene transcription. Hum. Mol. Genet., 14, R101-R111.
2. Wallace, J.A. and Felsenfeld, G. (2007) We gather together: insulators and genome organization. Curr. Opin. Genet. Develop., 17, 400-407.
3. Phillips, J.E. and Corces, V.G. (2009) CTCF: master weaver of the genome. Cell, 137, 1194-1211.
4. Dorsett, D. (2007) Roles of the sister chromatin cohesion apparatus in gene expression, development and human syndromes. Chromosoma, 116, 1-13.
5. Hou, C., Dale, R. and Dean, A. (2010) Cell type specificity of chromatin organization mediated by CTCF and cohesin. Proc. Natl Acad. Sci. USA, 107, 3651-3656.
6. Bushey, A.M., Ramos, E. and Corces, V.G. (2009) Three subclasses of a Drosophila insulator show distinct and cell-type-specific genomic distributions. Genes Dev., 23, 1338-1350.
7. Murrell, A., Heeson, S. and Reik, W. (2004) Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat. Genet., 36, 889-893.
8. Kurukuti, S., Tiwari, V.K., Tavoosidana, G., Pugacheva, E., Murrell, A., Zhao, Z., Lobanenkov, V., Reik, W. and Ohlsson, R. (2006) 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, 103, 10684-10689.
9. Ribeiro de Almeida, C., Heath, H., Krpic, S., Dingjan, G.M., Van Hamburg, J.P., Bergen, I., Van de Nobelen, S., Grosveld, F., Galjart, N. and Hendriks, R.W. (2009) Critical role of the transcription regulator CCCTC-binding factor in the control of the Th2 cytokine expression. J. Immunol., 182, 999-1010.
10. Splinter, E., Heath, H., Kooren, J., Palstra, R.-J., Klous, P., Grosveld, F., Galjart, N. and de Laat, W. (2006) CTCF mediates long-range chromatin looping and local histone modification in the b-globin locus. Genes Dev., 20, 2349-2354.
11. Majumder, P., Gomez, J.A., Chadwick, B.P. and Boss, J.M. (2008) The insulator factor CTCF controls MHC class II gene expression and is required for the formation of long-distance chromatin interactions. J. Exp. Med., 205, 785-798.
12. Ling, J.Q., Li, T., Hu, J.F., Vu, T.H., Chen, H.L., Qui, X.W., Cherry, A.M. and Hoffman, A.R. (2006) CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1. Science, 312, 269-272.
13. Lutz, M., Burke, L.J., LeFevre, P., Myers, F.A., Thorne, A.W., Crane-Robinson, C., Bonifer, C., Filippova, G.N., Lobanenkov, V. and Renkawitz, R. (2003) Thyroid-hormone regulated enhancer blocking: cooperation of CTCF and thyroid hormone receptor. EMBO J., 22, 1579-1587.
14. Yu, W., Ginjala, V., Pant, V., Chernukhin, I., Whitehead, J., Docquier, F., Farrar, D., Tavoosidena, G., Mukhopadhyay, R., Kanduri, C. et al. (2004) Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat. Genet., 36, 1105-1110.
15. Valadez-Graham, V., Razin, S.V. and Recillas-Targa, F. (2004) CTCF-dependent enhancer blockers at the upstream region of the chicken a-globin gene domain. Nucleic Acids Res., 32, 1354-1362.
16. Vyas, P., Vickers, M.A., Picketts, D.J. and Higgs, D.R. (1995) Conservation of position and sequence of a novel, widely expressed gene containing the major human a-globin regulatory element. Genomics, 29, 679-689.
17. Flint, J., Tufarelli, C., Peden, J., Clark, K., Daniels, R.J., Hardison, R., Miller, W., Philipsen, S., Tan-Un, K.C., McMorrow, T. et al. (2001) Comparative genome analysis delimits a chromosomal domain and identified key regulatory elements in the a globin cluster. Hum. Mol. Genet., 10, 371-382.
18. Recillas-Targa, F., Pikaart, M.J., Burgess-Beusse, B., Bell, A.C., Litt, M.D., West, A.G., Gaszner, M. and Felsenfeld, G. (2002) Position-effect protection and enhancer blocking by the chicken b-globin insulator are separable activities. Proc. Natl Acad. Sci. USA, 99, 6883-6888.
19. Beug, H., von Kirchbach, A., Doderlin, G., Conscience, J.F. and Graf, T. (1979) Chicken haematopoietic cells transformed by seven strains of defective avian leukaemia viruses display three distinct phenotypes of differentiation. Cell, 18, 375-390.
20. Dieken, E.S., Epner, E.M., Fiering, S., Fournier, R.E. and Groudine, M. (1996) Efficient modification of human chromosomal alleles using recombination-proficient chicken/ human microcell hybrids. Nat. Genet., 12, 174-182.
21. Rincón-Arano, H., Guerrero, G., Valdes-Quezada, C. and Recillas-Targa, F. (2009) Chicken a-globin switching depends on autonomous silencing of the embryonic p globin gene by epigenetics mechanisms. J. Cell. Biochem., 108, 675-687.
22. Iarovaia, O., Razin, S.V., Linarez-Cruz, G., Sjakste, N. and Scherrer, K. (2001) In chicken leukemia cells globin genes are fully transcribed but their RNAs are retained in the perinucleolar area. Exp. Cell. Res., 270, 159-165.
23. Pikaart, M.J., Recillas-Targa, F. and Felsenfeld, G. (1998) Loss of transcriptional activity of a transgene is accompanied by DNA methylation and histone deacetylation and is prevented by insulators. Genes Dev., 12, 2852-2862.
24. Beermann, F., Ruppert, S., Hummler, E. and Schütz, G. (1991) Tyrosinase as a marker for transgenic mice. Nucleic Acids Res., 19, 958.
25. Giraldo, P., Mart́nez, A., Regales, L., Lavado, A., Garća-D́az, A., Alonso, A., Busturia, A. and Montoliu, L. (2003) Functional dissection of the mouse tyrosinase locus control region identifies a new putative boundary activity. Nucleic Acids Res., 31, 6290-6305.
26. Ganss, R., Montoliu, L., Monaghan, A.P. and Schütz, G. (1994) A cell-specific enhancer far upstream of the mouse tyrosinase gene confers high level and copy number-related expression in transgenic mice. EMBO J., 13, 3083-3093.
27. Giménez, E., Lavado, A., Giraldo, P. and Montoliu, L. (2003) Tyrosinase gene expression is not detected in mouse brain outside the retinal pigment epithelium cells. Eur. J. Neurosci., 18, 2673-2676.
28. Lavado, A., Olivares, C., Garća-Borrón, J.C. and Montoliu, L. (2005) Molecular basis of the extreme dilution mottled mouse mutation: a combination of coding and noncoding genomic alterations. J. Biol. Chem., 280, 4817-4824.
29. Rincón-Arano, H., Furlan-Magaril, M. and Recillas-Targa, F. (2007) Protection against telomeric position effects by the chicken cHS4 b-globin insulator. Proc. Natl Acad. Sci. USA, 104, 14044-14049.
30. Litt, M.D., Simpson, M., Recillas-Targa, F., Prioleau, M.N. and Felsenfeld, G. (2001) Transitions in histone acetylation reveal boundaries of three separately regulated neighbouring loci. EMBO J., 20, 2224-2235.
31. Lefevre, P., Witham, J., Lacroix, C.E., Cockerill, P.N. and Bonifer, C. (2008) The LPS-induced transcriptional upregulation of the chicken lysozyme locus involves CTCF eviction and noncoding RNA transcription. Mol. Cell, 32, 129-139.
32. Ishihara, K., Oshimura, M. and Nakao, M. (2006) CTCF-dependent chromatin insulator is linked to epigenetic remodeling. Mol. Cell, 23, 733-742.
33. Potts, W., Tucker, D., Wood, H. and Martin, C. (2000) Chicken b-globin 5'HS4 insulators function to reduce variability in transgenic founder mice. Biochem. Biophys. Res. Commun, 273, 1015-1018.
34. Torrano, V., Navascues, J., Docquier, F., Zhanf, R., Burke, L.J., Chernukhin, I., Farrar, D., León, J., Berciano, M.T., Renkawitz, R. et al. (2006) Targeting of CTCF to the nucleolus inhibits nucleolar transcription through a poly(ADP-ribosyl)ationdependent mechanism. J. Cell. Sci., 119, 1746-1759.
35. Witcher, M. and Emerson, B. (2009) Epigenetic silencing of the p16(INK4a) tumor suppressor is associated with loss of CTCF binding and a chromatin boundary. Mol. Cell, 34, 271-284.
36. Farrar, D., Rain, S., Chernukhin, I., Jagodic, M., Ito, Y., Yammine, S., Ohlsson, R., Murrel, A. and Klenova, E. (2010) 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., 30, 1199-1216.
37. Soto-Reyes, E. and Recillas-Targa, F. (2010) Epigenetic regulation of the human p53 gene promoter by the CTCF transcription factor in transformed cell lines. Oncogene, 15, 2217-2227.
38. Gavrilov, A.A. and Razin, S.V. (2008) Spatial configuration of the chicken a-globin gene domain: immature and active chromatin hubs. Nucleic Acids Res., 36, 4629-4640.
39. West, A.G., Huang, S., Gaszner, M., Litt, M.D. and Felsenfeld, G. (2004) Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Mol. Cell, 16, 453-463.
40. Higgs, D.R., Vernimmen, D., Hughes, J. and Gibbons, R. (2007) Using genomics to study how chromatin influences gene expression. Annu. Rev. Genomics Hum. Genet., 8, 299-325.
41. Zhao, H. and Dean, A. (2004) An insulator blocks spreading of histone acetylation and interferes with RNA polymerase II transfer between an enhancer and gene. Nucleic Acids Res., 32, 4903-4914.
42. Gomes, N.P. and Espinosa, J.M. (2010) Gene-specific repression of the p53 target gene PUMA via intragenic CTCF-Cohesin binding. Genes Dev., 24, 1022-1034.
43. Borunova, V., Iarovaia, O.V., Vassetzky, Y.S. and Razin, S.V. (2005) The upstream area of the chicken a-globin gene domain is transcribed in both directions in the same cells. FEBS Lett., 579, 4746-4750.
44. Kleine, H. and Lüscher, B. (2009) Learning how to read ADP-ribosylation. Cell, 139, 17-19.
45. Drissen, R., Palstra, R.J., Gillemans, N., Splinter, E., Grosveld, F., Philipsen, S. and de Laat, W. (2004) The active spatial organization of the b-globin locus requires the transcription factor EKLF. Genes Dev., 18, 2485-2490.
46. Vakoc, C.R., Letting, D.L., Gheldof, N., Sawado, T., Bender, M.A., Groudine, M., Weiss, M.J., Dekker, J. and Blobel, G.A. (2005) Proximity among distant regulatory elements at the b-globin locus requires GATA-1 and FOG-1. Mol. Cell, 17, 453-462.
47. Klochkov, D., Rincón-Arano, H., Ioudinkova, E.S., Valadez-Graham, V., Gavrilov, A., Recillas-Targa, F. and Razin, S.V. (2006) A CTCF-dependent silencer located in the differentially methylated area may regulate expression of a housekeeping gene overlapping a tissue-specific gene domain. Mol. Cell. Biol., 26, 1589-1597.