Chromatin insulator elements: Establishing barriers to set heterochromatin boundaries

Epigenomics

Volumn 4, Issue 1, 2012, Pages 67-80

  Barkess, Gráinne ^a   West, Adam G ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

barrier; boundary; chromatin; CTCF; domain; insulator; USF1; VEZF1

Indexed keywords

POLYCOMB GROUP PROTEIN; PROTEIN; PROTEIN VEZF1; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; UPSTREAM STIMULATORY FACTOR 1;

CHROMATIN; CHROMATIN STRUCTURE; EPIGENETICS; GENE REPRESSION; HETEROCHROMATIN; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; REVIEW;

ANIMALS; CHROMATIN; EPIGENOMICS; HETEROCHROMATIN; HISTONES; HUMANS; INSULATOR ELEMENTS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; UPSTREAM STIMULATORY FACTORS;

EID: 84857321616     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.11.112     Document Type: Review

References (112)

1. Adolph KW. Organization of chromosomes in mitotic HeLa cells. Exp. Cell Res. 125(1), 95-103 (1980). (Pubitemid 10140120)
2. Belmont AS, Braunfeld MB, Sedat JW, Agard DA. Large-scale chromatin structural domains within mitotic and interphase chromosomes in vivo and in vitro. Chromosoma 98(2), 129-143 (1989). (Pubitemid 19205972)
3. Benyajati C, Worcel A. Isolation, characterization, and structure of the folded interphase genome of Drosophila melanogaster. Cell 9(3), 393-407 (1976). (Pubitemid 8003666)
4. Marsden MP, Laemmli UK. Metaphase chromosome structure. evidence for a radial loop model. Cell 17(4), 849-858 (1979). (Pubitemid 9252294)
5. Rattner JB, Lin CC. Radial loops and helical coils coexist in metaphase chromosomes. Cell 42(1), 291-296 (1985). (Pubitemid 16237579)
6. Stalder J, Larsen A, Engel JD, Dolan M, Groudine M, Weintraub H. Tissue-specific DNA cleavages in the globin chromatin domain introduced by DNAase I. Cell 20(2), 451-460 (1980). (Pubitemid 10117761)
7. Hawkins RD, Hon GC, Ren B. Next-generation genomics. an integrative approach. Nat. Rev. Genet. 11(7), 476-486 (2010).
8. Beisel C, Paro R. Silencing chromatin. comparing modes and mechanisms. Nat. Rev. Genet. 12(2), 123-135 (2011).
9. Pauler FM, Sloane MA, Huang R et al. H3K27me3 forms BLOCs over silent genes and intergenic regions and specifies a histone banding pattern on a mouse autosomal chromosome. Genome Res. 19(2), 221-233 (2009).
10. Thurman RE, Day N, Noble WS, Stamatoyannopoulos JA. Identification of higher-order functional domains in the human ENCODE regions. Genome Res. 17(6), 917-927 (2007). (Pubitemid 46919726)
11. Filion Gj, van Bemmel JG, Braunschweig U et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143(2), 212-224 (2010).
12. Kharchenko PV, Alekseyenko AA, Schwartz YB et al. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471(7339), 480-485 (2011).
13. Riddle NC, Minoda A, Kharchenko PV et al. Plasticity in patterns of histone modifications and chromosomal proteins in Drosophila heterochromatin. Genome Res. 21(2), 147-163 (2011).
14. Bernatavichute YV, Zhang X, Cokus S, Pellegrini M, Jacobsen SE. Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS ONE 3(9), e3156 (2008).
15. Turck F, Roudier F, Farrona S et al. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet. 3(6), e86 (2007).
16. Zhang X, Clarenz O, Cokus S et al. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 5(5), e129 (2007).
17. Gerstein MB, Lu ZJ, van Nostrand EL et al. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330(6012), 1775-1787 (2010).
18. Liu T, Rechtsteiner A, Egelhofer TA et al. Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res. 21(2), 227-236 (2011).
19. Hawkins RD, Hon GC, Lee LK et al. Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 6(5), 479-491 (2010).
20. Mikkelsen TS, Ku M, Jaffe DB et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448(7153), 553-560 (2007). (Pubitemid 47206934)
21. Wen B, Wu H, Shinkai Y, Irizarry RA, Feinberg AP. Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat. Genet. 41(2), 246-250 (2009).
22. Guelen L, Pagie L, Brasset E et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453(7197), 948-951 (2008). (Pubitemid 351832561)
23. Filion GJ, van Steensel B. Reassessing the abundance of H3K9me2 chromatin domains in embryonic stem cells. Nat. Genet. 42(1), 4; author reply 5-6 (2010).
24. Dodge JE, Kang YK, Beppu H, Lei H, Li E. Histone H3-K9 methyltransferase ESET is essential for early development. Mol. Cell. Biol. 24(6), 2478-2486 (2004). (Pubitemid 38326002)
25. Faust C, Lawson KA, Schork NJ, Thiel B, Magnuson T. The Polycomb-group gene eed is required for normal morphogenetic movements during gastrulation in the mouse embryo. Development 125(22), 4495-4506 (1998). (Pubitemid 28564293)
26. O?Carroll D, Erhardt S, Pagani M, Barton SC, Surani MA, Jenuwein T. The Polycomb-group gene Ezh2 is required for early mouse development. Mol. Cell. Biol. 21(13), 4330-4336 (2001). (Pubitemid 32565314)
27. Pasini D, Bracken AP, Hansen JB, Capillo M, Helin K. The Polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell. Biol. 27(10), 3769-3779 (2007). (Pubitemid 46726184)
28. Peters AH, O?Carroll D, Scherthan H et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107(3), 323-337 (2001). (Pubitemid 33049976)
29. Tachibana M, Sugimoto K, Nozaki M et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16(14), 1779-1791 (2002). (Pubitemid 34803894)
30. Negre N, Brown Cd, Shah PK et al. A comprehensive map of insulator elements for the Drosophila genome. PLoS Genet. 6(1), e1000814 (2010).
31. Negre N, Brown CD, Ma L et al. A cis-regulatory map of the Drosophila genome. Nature 471(7339), 527-531 (2011).
32. Gurudatta BV, Corces VG. Chromatin insulators: lessons from the fly. Brief Funct. Genomic Proteomic 8(4), 276-282 (2009).
33. Moshkovich N, Nisha P, Boyle PJ, Thompson BA, Dale RK, Lei EP. RNAi-independent role for Argonaute2 in CTCF/CP190 chromatin insulator function. Genes Dev. 25(16), 1686-1701 (2011).
34. Bell AC, West AG, Felsenfeld G. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98(3), 387-396 (1999). (Pubitemid 29380573)
35. West AG, Gaszner M, Felsenfeld G. Insulators: many functions, many mechanisms. Genes Dev. 16(3), 271-288 (2002).
36. Scott Kc, Taubman AD, Geyer PK. Enhancer blocking by the Drosophila gypsy insulator depends upon insulator anatomy and enhancer strength. Genetics 153(2), 787-798 (1999). (Pubitemid 29482335)
37. Kellum R, Schedl P. A position-effect assay for boundaries of higher order chromosomal domains. Cell 64(5), 941-950 (1991). (Pubitemid 121001181)
38. Roseman RR, Pirrotta V, Geyer Pk. The su(Hw) protein insulates expression of the Drosophila melanogaster white gene from chromosomal position-effects. EMBO J. 12(2), 435-442 (1993). (Pubitemid 23073689)
39. Mutskov V, Felsenfeld G. Silencing of transgene transcription precedes methylation of promoter DNA and histone H3 lysine 9. EMBO J. 23(1), 138-149 (2004). (Pubitemid 38165754)
40. Mutskov VJ, Farrell CM, Wade PA, Wolffe AP, Felsenfeld G. The barrier function of an insulator couples high histone acetylation levels with specific protection of promoter DNA from methylation. Genes Dev. 16(12), 1540-1554 (2002). (Pubitemid 34686335)
41. Pikaart MJ, Recillas-Targa F, Felsenfeld G. Loss of transcriptional activity of a transgene is accompanied by DNA methylation and histone deacetylation and is prevented by insulators. Genes Dev. 12(18), 2852-2862 (1998). (Pubitemid 28440144)
42. Recillas-Targa F, Pikaart MJ, Burgess-Beusse B et al. Position-effect protection and enhancer blocking by the chicken beta-globin insulator are separable activities. Proc. Natl Acad. Sci. USA 99(10), 6883-6888 (2002). (Pubitemid 34526227)
43. Aker M, Tubb J, Groth AC et al. Extended core sequences from the cHS4 insulator are necessary for protecting retroviral vectors from silencing position effects. Hum. Gene Ther. 18(4), 333-343 (2007). (Pubitemid 46709345)
44. Van Der Vlag J, Den Blaauwen JL, Sewalt RG, Van Driel R, Otte AP. Transcriptional repression mediated by Polycomb group proteins and other chromatin-associated repressors is selectively blocked by insulators. J. Biol. Chem. 275(1), 697-704 (2000). (Pubitemid 30039036)
45. Moreno R, Martinez I, Petriz J, Gonzalez JR, Gratacos E, Aran JM. Boundary sequences stabilize transgene expression from subtle position effects in retroviral vectors. Blood Cells Mol. Dis. 43(2), 214-220 (2009).
46. Yannaki E, Tubb J, Aker M, Stamatoyannopoulos G, Emery Dw. Topological constraints governing the use of the chicken HS4 chromatin insulator in oncoretrovirus vectors. Mol. Ther. 5(5 Pt 1), 589-598 (2002). (Pubitemid 34546089)
47. Hanawa H, Yamamoto M, Zhao H, Shimada T, Persons DA. Optimized lentiviral vector design improves titer and transgene expression of vectors containing the chicken beta-globin locus HS4 insulator element. Mol. Ther. 17(4), 667-674 (2009).
48. Reddy KL, Zullo JM, Bertolino E, Singh H. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452(7184), 243-247 (2008). (Pubitemid 351380248)
49. Kim YJ, Cecchini KR, Kim TH. Conserved, developmentally regulated mechanism couples chromosomal looping and heterochromatin barrier activity at the homeobox gene A locus. Proc. Natl Acad. Sci. USA 108(18), 7391-7396 (2011).
50. 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. 20(9), 2224-2235 (2001). (Pubitemid 32410592)
51. Prioleau MN, Nony P, Simpson M, Felsenfeld G. An insulator element and condensed chromatin region separate the chicken beta-globin locus from an independently regulated erythroid-specific folate receptor gene. EMBO J. 18(14), 4035-4048 (1999). (Pubitemid 29335856)
52. Hebbes TR, Clayton AL, Thorne AW, Crane-Robinson C. Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken beta-globin chromosomal domain. EMBO J. 13(8), 1823-1830 (1994). (Pubitemid 24124515)
53. Bruce K, Myers FA, Mantouvalou E et al. The replacement histone H2A.Z in a hyperacetylated form is a feature of active genes in the chicken. Nucleic Acids Res. 33(17), 5633-5639 (2005). (Pubitemid 41548829)
54. Ma MK, Heath C, Hair A, West AG. Histone crosstalk directed by H2B ubiquitination is required for chromatin boundary integrity. PLoS Genet. 7(7), e1002175 (2011).
55. Myers FA, Chong W, Evans DR, Thorne AW, Crane-Robinson C. Acetylation of histone H2B mirrors that of H4 and H3 at the chicken beta-globin locus but not at housekeeping genes. J. Biol. Chem. 278(38), 36315-36322 (2003). (Pubitemid 37139957)
56. Felsenfeld G, Burgess-Beusse B, Farrell C et al. Chromatin boundaries and chromatin domains. Cold Spring Harb. Symp. Quant. Biol. 69, 245-250 (2004). (Pubitemid 41056560)
57. Litt MD, Simpson M, Gaszner M, Allis CD, Felsenfeld G. Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus. Science 293(5539), 2453-2455 (2001). (Pubitemid 32917326)
58. Ghirlando R, Litt MD, Prioleau MN, Recillas-Targa F, Felsenfeld G. Physical properties of a genomic condensed chromatin fragment. J. Mol. Biol. 336(3), 597-605 (2004). (Pubitemid 38183016)
59. Chung JH, Whiteley M, Felsenfeld G. A 5? element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell 74(3), 505-514 (1993). (Pubitemid 23244616)
60. Yao S, Osborne CS, Bharadwaj RR et al. Retrovirus silencer blocking by the cHS4 insulator is CTCF independent. Nucleic Acids Res. 31(18), 5317-5323 (2003). (Pubitemid 37441899)
61. Dickson J, Gowher H, Strogantsev R et al. VEZF1 elements mediate protection from DNA methylation. PLoS Genet. 6(1), e1000804 (2010).
62. West AG, Huang S, Gaszner M, Litt MD, Felsenfeld G. Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Mol. Cell 16(3), 453-463 (2004). (Pubitemid 39504798)
63. Huang S, Li X, Yusufzai TM, Qiu Y, Felsenfeld G. USF1 recruits histone modification complexes and is critical for maintenance of a chromatin barrier. Mol. Cell. Biol. 27(22), 7991-8002 (2007). (Pubitemid 350086431)
64. Huang S, Litt M, Felsenfeld G. Methylation of histone H4 by arginine methyltransferase PRMT1 is essential in vivo for many subsequent histone modifications. Genes Dev. 19(16), 1885-1893 (2005). (Pubitemid 41186989)
65. Chung JH, Bell AC, Felsenfeld G. Characterization of the chicken beta-globin insulator. Proc. Natl Acad. Sci. USA 94(2), 575-580 (1997).
66. Gowher H, Stuhlmann H, Felsenfeld G. Vezf1 regulates genomic DNA methylation through its effects on expression of DNA methyltransferase Dnmt3b. Genes Dev. 22(15), 2075-2084 (2008).
67. Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10(5), 295-304 (2009).
68. Heath H, Ribeiro de Almeida C, Sleutels F et al. CTCF regulates cell cycle progression of alphabeta T cells in the thymus. EMBO J. 27(21), 2839-2850 (2008).
69. Phillips JE, Corces VG. CTCF: master weaver of the genome. Cell 137(7), 1194-1211 (2009).
70. Chan PK, Wai A, Philipsen S, Tan-Un KC. 5?HS5 of the human beta-globin locus control region is dispensable for the formation of the beta-globin active chromatin hub. PLoS ONE 3(5), e2134 (2008).
71. Zakany J, Duboule D. The role of Hox genes during vertebrate limb development. Curr. Opin. Genet. Dev. 17(4), 359-366 (2007). (Pubitemid 47241269)
72. Goto Y, Kimura H. Inactive X chromosome-specific histone H3 modifications and CpG hypomethylation flank a chromatin boundary between an X-inactivated and an escape gene. Nucleic Acids Res. 37(22), 7416-7428 (2009).
73. Miller J.C., Tan S., Qiao G., et al. A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29 (2) 143-148.
74. Miller JC, Tan S, Qiao G et al. A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29(2), 143-148 (2011). 74 Kim TH, Abdullaev ZK, Smith AD et al. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128(6), 1231-1245 (2007). (Pubitemid 46427876)
75. Xi H, Shulha HP, Lin JM et al. Identification and characterization of cell type-specific and ubiquitous chromatin regulatory structures in the human genome. PLoS Genet. 3(8), e136 (2007).
76. 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 104(17), 7145-7150 (2007). (Pubitemid 47186023)
77. 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. 19(1), 24-32 (2009).
78. Barski A, Cuddapah S, Cui K et al. High-resolution profiling of histone methylations in the human genome. Cell 129(4), 823-837 (2007). (Pubitemid 46802390)
79. 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. 36(16), 5221-5231 (2008).
80. Chen X, Xu H, Yuan P et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133(6), 1106-1117 (2008). (Pubitemid 351787745)
81. Schmidt D, Schwalie PC, Ross-Innes CS et al. A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res. 20(5), 578-588 (2010).
82. Bernstein BE, Stamatoyannopoulos JA, Costello JF et al. The NIH Roadmap Epigenomics Mapping Consortium. Nat. Biotechnol. 28(10), 1045-1048 (2010).
83. Myers RM, Stamatoyannopoulos J, Snyder M et al. A user?s guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 9(4), e1001046 (2011).
84. Martin D, Pantoja C, Fernandez Minan A et al. Genome-wide CTCF distribution in vertebrates defines equivalent sites that aid the identification of disease-associated genes. Nat. Struct. Mol. Biol. 18(6), 708-714 (2011).
85. Bao L, Zhou M, Cui Y. CTCFBSDB: a CTCF-binding site database for characterization of vertebrate genomic insulators. Nucleic Acids Res. 36(Database issue), D83-D87 (2008). (Pubitemid 351149700)
86. Wallace JA, Felsenfeld G. We gather together: insulators and genome organization. Curr. Opin. Genet. Dev. 17(5), 400-407 (2007). (Pubitemid 350016897)
87. Lieberman-Aiden E, van Berkum NL, Williams L et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326(5950), 289-293 (2009).
88. Yao H, Brick K, Evrard Y, Xiao T, Camerini- Otero RD, Felsenfeld G. Mediation of CTCF transcriptional insulation by DEAD-box RNA-binding protein p68 and steroid receptor RNA activator SRA. Genes Dev. 24(22), 2543-2555 (2010).
89. Parelho V, Hadjur S, Spivakov M et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132(3), 422-433 (2008).
90. Wendt KS, Yoshida K, Itoh T et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451(7180), 796-801 (2008). (Pubitemid 351253176)
91. Chien R, Zeng W, Kawauchi S et al. Cohesin mediates chromatin interactions that regulate mammalian beta-globin expression. J. Biol. Chem. 286(20), 17870-17878 (2011).
92. Dorsett D. Cohesin: genomic insights into controlling gene transcription and development. Curr. Opin. Genet. Dev. 21(2), 199-206 (2011).
93. Hadjur S, Williams LM, Ryan NK et al. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 460(7253), 410-413 (2009).
94. Mishiro T, Ishihara K, Hino S et al. Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster. EMBO J. 28(9), 1234-1245 (2009).
95. Nativio R, Wendt KS, Ito Y et al. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLoS Genet. 5(11), e1000739 (2009).
96. 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. 23(24), 9338-9348 (2003). (Pubitemid 37499820)
97. 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 4(7), e6109 (2009).
98. Essafi A, Webb A, Berry RL et al. A wt1- controlled chromatin switching mechanism underpins tissue-specific wnt4 activation and repression. Dev. Cell 21(3), 559-574 (2011).
99. Bartolomei MS. Genomic imprinting: employing and avoiding epigenetic processes. Genes Dev. 23(18), 2124-2133 (2009).
100. Lin S, Ferguson-Smith AC, Schultz RM, Bartolomei MS. Nonallelic transcriptional roles of CTCF and cohesins at imprinted loci. Mol. Cell. Biol. 31(15), 3094-3104 (2011).
101. de Laat W, Grosveld F. Spatial organization of gene expression: the active chromatin hub. Chromosome Res. 11(5), 447-459 (2003). (Pubitemid 37041205)
102. Splinter E, Heath H, Kooren J et al. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev. 20(17), 2349-2354 (2006). (Pubitemid 44320383)
103. Farrell CM, West AG, Felsenfeld G. Conserved CTCF insulator elements flank the mouse and human beta-globin loci. Mol. Cell. Biol. 22(11), 3820-3831 (2002). (Pubitemid 34525223)
104. Bender MA, Byron R, Ragoczy T, Telling A, Bulger M, Groudine M. Flanking HS-62.5 and 3? HS1, and regions upstream of the LCR, are not required for beta-globin transcription. Blood 108(4), 1395-1401 (2006). (Pubitemid 44232043)
105. Filippova GN, Cheng MK, Moore JM et al. Boundaries between chromosomal domains of X inactivation and escape bind CTCF and lack CpG methylation during early development. Dev. Cell 8(1), 31-42 (2005). (Pubitemid 40058003)
106. Bernstein BE, Kamal M, Lindblad-Toh K et al. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120(2), 169-181 (2005). (Pubitemid 40174761)
107. Magdinier F, Yusufzai Tm, Felsenfeld G. Both CTCF-dependent and -independent insulators are found between the mouse T cell receptor alpha and Dad1 genes. J. Biol. Chem. 279(24), 25381-25389 (2004). (Pubitemid 38756795)
108. Gomos-Klein J, Harrow F, Alarcon J, Ortiz Bd. CTCF-independent, but not CTCF-dependent, elements significantly contribute to TCR-alpha locus control region activity. J. Immunol. 179(2), 1088-1095 (2007).
109. Harrow F, Amuta Ju, Hutchinson Sr, Akwaa F, Ortiz Bd. Factors binding a non-classical Cis-element prevent heterochromatin effects on locus control region activity. J. Biol. Chem. 279(17), 17842-17849 (2004). (Pubitemid 38560552)
110. Ortiz BD, Harrow F, Cado D, Santoso B, Winoto A. Function and factor interactions of a locus control region element in the mouse T cell receptor-alpha/Dad1 gene locus. J. Immunol. 167(7), 3836-3845 (2001). (Pubitemid 32916055)
111. Raab JR, Kamakaka RT. Insulators and promoters: closer than we think. Nat. Rev. Genet. 11(6), 439-446 (2010).
112. Gallagher PG, Nilson DG, Steiner LA, Maksimova YD, Lin JY, Bodine DM. An insulator with barrier-element activity promotes alpha-spectrin gene expression in erythroid cells. Blood 113(7), 1547-1554 (2009).