CTCF controls expression and chromatin architecture of the human major histocompatibility complex class II locus

Molecular and Cellular Biology

Volumn 30, Issue 17, 2010, Pages 4211-4223

  Majumder, Parimal ^a   Boss, Jeremy M ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLASS II TRANSACTIVATOR PROTEIN; COHESIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; CCCTC-BINDING FACTOR; CELL CYCLE PROTEIN; COHESINS; GAMMA INTERFERON; MHC CLASS II TRANSACTIVATOR PROTEIN; NONHISTONE PROTEIN; NUCLEAR PROTEIN; REPRESSOR PROTEIN;

ANTIGEN PRESENTATION; ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; BINDING SITE; CHEMISTRY; CHROMATIN; GENE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; TUMOR CELL LINE;

BASE SEQUENCE; BINDING SITES; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; GENE EXPRESSION REGULATION; GENES, MHC CLASS II; HUMANS; INTERFERON-GAMMA; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; TRANS-ACTIVATORS;

EID: 77956645612     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00327-10     Document Type: Article

References (68)

1. Accolla, R. S. 1983. Human B cell variants immunoselected against a single Ia antigen subset have lost expression of several Ia antigen subsets. J. Exp. Med. 157:1053-1058.
2. Auffray, C., J. Kuo, R. DeMars, and J. L. Strominger. 1983. A minimum of four human class II alpha-chain genes are encoded in the HLA region of chromosome 6. Nature 304:174-177.
3. Auffray, C., J. W. Lillie, A. J. Korman, J. M. Boss, N. Frechin, F. Guillemot, J. Cooper, R. C. Mulligan, and J. L. Strominger. 1987. Structure and expression of HLA-DQ alpha and -DX alpha genes: interallelic alternate splicing of the HLA-DQ alpha gene and functional splicing of the HLA-DQ alpha gene using a retroviral vector. Immunogenetics 26:63-73.
4. Barski, A., S. Cuddapah, K. Cui, T. Y. Roh, D. E. Schones, Z. Wang, G. Wei, I. Chepelev, and K. Zhao. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129:823-837. (Pubitemid 46802390)
5. Bartkuhn, M., and R. Renkawitz. 2008. Long range chromatin interactions involved in gene regulation. Biochim. Biophys. Acta 1783:2161-2166.
6. Beresford, G. W., and J. M. Boss. 2001. CIITA coordinates multiple histone acetylation modifications at the HLA-DRA promoter. Nat. Immunol. 2:652-657.
7. Blackledge, N. P., C. J. Ott, A. E. Gillen, and A. Harris. 2009. An insulator element 3′ to the CFTR gene binds CTCF and reveals an active chromatin hub in primary cells. Nucleic Acids Res. 37:1086-1094.
8. Boss, J. M. 1997. Regulation of transcription of MHC class II genes. Curr. Opin. Immunol. 9:107-113.
9. Boss, J. M., and P. E. Jensen. 2003. Transcriptional regulation of the MHC class II antigen presentation pathway. Curr. Opin. Immunol. 15:105-111.
10. Bushey, A. M., E. R. Dorman, and V. G. Corces. 2008. Chromatin insulators: regulatory mechanisms and epigenetic inheritance. Mol. Cell 32:1-9.
11. Carter, D., L. Chakalova, C. S. Osborne, Y. F. Dai, and P. Fraser. 2002. Long-range chromatin regulatory interactions in vivo. Nat. Genet. 32:623-626.
12. Collins, T., A. J. Korman, C. T. Wake, J. M. Boss, D. J. Kappes, W. Fiers, K. A. Ault, M. A. Gimbrone, Jr., J. L. Strominger, and J. S. Pober. 1984. Immune interferon activates multiple class II major histocompatibility complex genes and the associated invariant chain gene in human endothelial cells and dermal fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 81:4917-4921.
13. Crooks, G. E., G. Hon, J. M. Chandonia, and S. E. Brenner. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188-1190.
14. Dekker, J. 2006. The three 'C's of chromosome conformation capture: controls, controls, controls. Nat. Methods 3:17-21. (Pubitemid 43135343)
15. Dekker, J., K. Rippe, M. Dekker, and N. Kleckner. 2002. Capturing chromosome conformation. Science 295:1306-1311.
16. Der, S. D., A. Zhou, B. R. Williams, and R. H. Silverman. 1998. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. U. S. A. 95:15623-15628.
17. Epstein, M. A., B. G. Achong, Y. M. Barr, B. Zajac, G. Henle, and W. Henle. 1966. Morphological and virological investigations on cultured Burkitt tumor lymphoblasts (strain Raji). J. Natl. Cancer Inst. 37:547-559.
18. Farrell, C. M., A. G. West, and G. Felsenfeld. 2002. Conserved CTCF insulator elements flank the mouse and human beta-globin loci. Mol. Cell. Biol. 22:3820-3831.
19. Filippova, G. N., S. Fagerlie, E. M. Klenova, C. Myers, Y. Dehner, G. Goodwin, P. E. Neiman, S. J. Collins, and V. V. Lobanenkov. 1996. 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. 16:2802-2813.
20. Germain, R. N., N. S. Braunstein, M. A. Brown, L. H. Glimcher, R. I. Lechler, J. McCluskey, D. H. Margulies, J. Miller, M. A. Norcross, W. E. Paul, et al. 1986. Structure and function of murine class II major histocompatibility complex genes. Mt. Sinai J. Med. 53:194-201.
21. Germain, R. N., and D. H. Margulies. 1993. The biochemistry and cell biology of antigen processing and presentation. Annu. Rev. Immunol. 11:403-450.
22. Gomez, J. A., P. Majumder, U. M. Nagarajan, and J. M. Boss. 2005. X box-like sequences in the MHC class II region maintain regulatory function. J. Immunol. 175:1030-1040.
23. Hasegawa, S. L., and J. M. Boss. 1991. Two B cell factors bind the HLADRA X box region and recognize different subsets of HLA class II promoters. Nucleic Acids Res. 19:6269-6276.
24. Jothi, R., S. Cuddapah, A. Barski, K. Cui, and K. Zhao. 2008. Genome-wide identification of in vivo protein-DNA binding sites from ChIP-Seq data. Nucleic Acids Res. 36:5221-5231.
25. Kelly, A., S. H. Powis, L. A. Kerr, I. Mockridge, T. Elliott, J. Bastin, B. Uchanska-Ziegler, A. Ziegler, J. Trowsdale, and A. Townsend. 1992. Assembly and function of the two ABC transporter proteins encoded in the human major histocompatibility complex. Nature 355:641-644.
26. Kim, S. I., S. J. Bultman, C. M. Kiefer, A. Dean, and E. H. Bresnick. 2009. BRG1 requirement for long-range interaction of a locus control region with a downstream promoter. Proc. Natl. Acad. Sci. U. S. A. 106:2259-2264.
27. Kim, T. H., Z. K. Abdullaev, A. D. Smith, K. A. Ching, D. I. Loukinov, R. D. Green, M. Q. Zhang, V. V. Lobanenkov, and B. Ren. 2007. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128:1231-1245.
28. Klenova, E. M., R. H. Nicolas, H. F. Paterson, A. F. Carne, C. M. Heath, G. H. Goodwin, P. E. Neiman, and V. V. Lobanenkov. 1993. CTCF, a conserved nuclear factor required for optimal transcriptional activity of the chicken c-myc gene, is an 11-Zn-finger protein differentially expressed in multiple forms. Mol. Cell. Biol. 13:7612-7624.
29. Korman, A. J., J. M. Boss, T. Spies, R. Sorrentino, K. Okada, and J. L. Strominger. 1985. Genetic complexity and expression of human class II histocompatibility antigens. Immunol. Rev. 85:45-86.
30. Labrador, M., and V. G. Corces. 2002. Setting the boundaries of chromatin domains and nuclear organization. Cell 111:151-154.
31. Lefevre, P., J. Witham, C. E. Lacroix, P. N. Cockerill, and C. Bonifer. 2008. The LPS-induced transcriptional upregulation of the chicken lysozyme locus involves CTCF eviction and noncoding RNA transcription. Mol. Cell 32:129-139.
32. LeibundGut-Landmann, S., J. M. Waldburger, M. Krawczyk, L. A. Otten, T. Suter, A. Fontana, H. Acha-Orbea, and W. Reith. 2004. Mini-review: Specificity and expression of CIITA, the master regulator of MHC class II genes. Eur. J. Immunol. 34:1513-1525.
33. Ling, J. Q., T. Li, J. F. Hu, T. H. Vu, H. L. Chen, X. W. Qiu, A. M. Cherry, and A. R. Hoffman. 2006. CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1. Science 312:269-272.
34. Magdinier, F., T. M. Yusufzai, and G. Felsenfeld. 2004. Both CTCF-dependent and -independent insulators are found between the mouse T cell receptor alpha and Dad1 genes. J. Biol. Chem. 279:25381-25389.
35. Majumder, P., J. A. Gomez, and J. M. Boss. 2006. The human major histocompatibility complex class II HLA-DRB1 and HLA-DQA1 genes are separated by a CTCF-binding enhancer-blocking element. J. Biol. Chem. 281:18435-18443.
36. Majumder, P., J. A. Gomez, B. P. Chadwick, and J. M. Boss. 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.
37. Marston, A. L., and A. Amon. 2004. Meiosis: cell-cycle controls shuffle and deal. Nat. Rev. Mol. Cell Biol. 5:983-997.
38. McCusker, D., T. Jones, D. Sheer, and J. Trowsdale. 1997. Genetic relationships of the genes encoding the human proteasome beta subunits and the proteasome PA28 complex. Genomics 45:362-367. (Pubitemid 27467628)
39. Miele, A., and J. Dekker. 2008. Long-range chromosomal interactions and gene regulation. Mol. Biosyst. 4:1046-1057.
40. Mishiro, T., K. Ishihara, S. Hino, S. Tsutsumi, H. Aburatani, K. Shirahige, Y. Kinoshita, and M. Nakao. 2009. Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster. EMBO J. 28:1234-1245.
41. Moreno, C. S., E. M. Rogers, J. A. Brown, and J. M. Boss. 1997. Regulatory factor X, a bare lymphocyte syndrome transcription factor, is a multimeric phosphoprotein complex. J. Immunol. 158:5841-5848.
42. Nagarajan, U. M., J. Lochamy, X. Chen, G. W. Beresford, R. Nilsen, P. E. Jensen, and J. M. Boss. 2002. Class II transactivator is required for maximal expression of HLA-DOB in B cells. J. Immunol. 168:1780-1786.
43. Ni, Z., M. Abou El Hassan, Z. Xu, T. Yu, and R. Bremner. 2008. The chromatin-remodeling enzyme BRG1 coordinates CIITA induction through many interdependent distal enhancers. Nat. Immunol. 9:785-793.
44. Oestreich, K. J., R. M. Cobb, S. Pierce, J. Chen, P. Ferrier, and E. M. Oltz. 2006. Regulation of TCR beta gene assembly by a promoter/enhancer holocomplex. Immunity 24:381-391.
45. Okada, K., H. L. Prentice, J. M. Boss, D. J. Levy, D. Kappes, T. Spies, R. Raghupathy, R. A. Mengler, C. Auffray, and J. L. Strominger. 1985. SB subregion of the human major histocompatibility complex: gene organization, allelic polymorphism and expression in transformed cells. EMBO J. 4:739-748.
46. Palstra, R. J., B. Tolhuis, E. Splinter, R. Nijmeijer, F. Grosveld, and W. de Laat. 2003. The beta-globin nuclear compartment in development and erythroid differentiation. Nat. Genet. 35:190-194.
47. Pant, V., S. Kurukuti, E. Pugacheva, S. Shamsuddin, P. Mariano, R. Renkawitz, E. Klenova, V. Lobanenkov, and R. Ohlsson. 2004. 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. 24:3497-3504.
48. Parelho, V., S. Hadjur, M. Spivakov, M. Leleu, S. Sauer, H. C. Gregson, A. Jarmuz, C. Canzonetta, Z. Webster, T. Nesterova, B. S. Cobb, K. Yokomori, N. Dillon, L. Aragon, A. G. Fisher, and M. Merkenschlager. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132:422-433.
49. Peters, J. M., A. Tedeschi, and J. Schmitz. 2008. The cohesin complex and its roles in chromosome biology. Genes Dev. 22:3089-3114.
50. Petronczki, M., M. F. Siomos, and K. Nasmyth. 2003. Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423-440. (Pubitemid 36263077)
51. Reith, W., and B. Mach. 2001. The bare lymphocyte syndrome and the regulation of MHC expression. Annu. Rev. Immunol. 19:331-373.
52. Rubio, E. D., D. J. Reiss, P. L. Welcsh, C. M. Disteche, G. N. Filippova, N. S. Baliga, R. Aebersold, J. A. Ranish, and A. Krumm. 2008. CTCF physically links cohesin to chromatin. Proc. Natl. Acad. Sci. U. S. A. 105:8309-8314.
53. Shapiro, D. J., P. A. Sharp, W. W. Wahli, and M. J. Keller. 1988. A high-efficiency HeLa cell nuclear transcription extract. DNA 7:47-55.
54. Simonis, M., J. Kooren, and W. de Laat. 2007. An evaluation of 3C-based methods to capture DNA interactions. Nat. Methods 4:895-901. (Pubitemid 350042374)
55. Sloan, V. S., P. Cameron, G. Porter, M. Gammon, M. Amaya, E. Mellins, and D. M. Zaller. 1995. Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature 375:802-806.
56. Stedman, W., H. Kang, S. Lin, J. L. Kissil, M. S. Bartolomei, and P. M. Lieberman. 2008. Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators. EMBO J. 27:654-666.
57. Steimle, V., L. A. Otten, M. Zufferey, and B. Mach. 1993. Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome). Cell 75:135-146. (Pubitemid 23306027)
58. Steimle, V., C. A. Siegrist, A. Mottet, B. Lisowska-Grospierre, and B. Mach. 1994. Regulation of MHC class II expression by interferon-gamma mediated by the transactivator gene CIITA. Science 265:106-109. (Pubitemid 24253184)
59. Ting, J. P., and J. Trowsdale. 2002. Genetic control of MHC class II expression. Cell 109(Suppl.):S21-S33. (Pubitemid 34457849)
60. Tolhuis, B., R. J. Palstra, E. Splinter, F. Grosveld, and W. de Laat. 2002. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol. Cell 10:1453-1465. (Pubitemid 36050885)
61. Vakoc, C. R., D. L. Letting, N. Gheldof, T. Sawado, M. A. Bender, M. Groudine, M. J. Weiss, J. Dekker, and G. A. Blobel. 2005. Proximity among distant regulatory elements at the beta-globin locus requires GATA-1 and FOG-1. Mol. Cell 17:453-462.
62. Wallace, J. A., and G. Felsenfeld. 2007. We gather together: insulators and genome organization. Curr. Opin. Genet. Dev. 17:400-407.
63. Watanabe, Y. 2004. Modifying sister chromatid cohesion for meiosis. J. Cell Sci. 117:4017-4023. (Pubitemid 39328290)
64. Weber, D. A., B. D. Evavold, and P. E. Jensen. 1996. Enhanced dissociation of HLA-DR-bound peptides in the presence of HLA-DM. Science 274:618-620.
65. Wendt, K. S., K. Yoshida, T. Itoh, M. Bando, B. Koch, E. Schirghuber, S. Tsutsumi, G. Nagae, K. Ishihara, T. Mishiro, K. Yahata, F. Imamoto, H. Aburatani, M. Nakao, N. Imamoto, K. Maeshima, K. Shirahige, and J. M. Peters. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796-801.
66. West, A. G., S. Huang, M. Gaszner, M. D. Litt, and G. Felsenfeld. 2004. Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Mol. Cell 16:453-463.
67. York, I. A., and K. L. Rock. 1996. Antigen processing and presentation by the class I major histocompatibility complex. Annu. Rev. Immunol. 14:369-396.
68. Yusufzai, T. M., H. Tagami, Y. Nakatani, and G. Felsenfeld. 2004. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol. Cell 13:291-298.