Formation of an active tissue-specific chromatin domain initiated by epigenetic marking at the embryonic stem cell stage

Molecular and Cellular Biology

Volumn 25, Issue 5, 2005, Pages 1804-1820

  Szutorisz, Henrietta ^a   Canzonetta, Claudia ^a   Georgiou, Andrew ^a   Chow, Cheok Man ^a   Tora, László ^b   Dillon, Niall ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE II; TRANSCRIPTION FACTOR;

ACETYLATION; ARTICLE; B LYMPHOCYTE; CELL DIFFERENTIATION; CHROMATIN; DEVELOPMENTAL STAGE; DNA MODIFICATION; EMBRYONIC STEM CELL; EPIGENETICS; GENE EXPRESSION; GENE LOCUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; STEM CELL;

ACETYLATION; ANIMALS; B-LYMPHOCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA TOPOISOMERASES, TYPE I; DNA, INTERGENIC; DNA-BINDING PROTEINS; EMBRYO; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMATOPOIETIC STEM CELLS; HISTONES; IMMUNOGLOBULIN LIGHT CHAINS; ISOENZYMES; MEMBRANE GLYCOPROTEINS; METHYLATION; MICE; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

EID: 14044259362     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.5.1804-1820.2005     Document Type: Article

References (86)

1. Akashi, K., D. Traver, T. Miyamoto, and I. L. Weissman. 2000. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404:193-197.
2. Anderson, M. K., G. Hernandez-Hoyos, R. A. Diamond, and E. V. Rothenberg. 1999. Precise developmental regulation of Ets family transcription factors during specification and commitment to the T cell lineage. Development 126:3131-3148.
3. Anguita, E., J. Hughes, C. Heyworth, G. A. Blobel, W. G. Wood, and D. R. Higgs. 2004. Globin gene activation during haemopoiesis is driven by protein complexes nucleated by GATA-1 and GATA-2. EMBO J. 23:2841-2852.
4. Anguita, E., C. A. Johnson, W. G. Wood, B. M. Turner, and D. R. Higgs. 2001. Identification of a conserved erythroid specific domain of histone acetylation across the alpha-globin gene cluster. Proc. Natl. Acad. Sci. USA 98:12114-12119.
5. Besse, S., M. Vigneron, E. Pichard, and F. Puvion-Dutilleul. 1995. Synthesis and maturation of viral transcripts in herpes simplex virus type 1 infected HeLa cells: the role of interchromatin granules. Gene Expr. 4:143-161.
6. Bottardi, S., A. Aumont, F. Grosveld, and E. Milot. 2003. Developmental stage-specific epigenetic control of human beta-globin gene expression is potentiated in hematopoietic progenitor cells prior to their transcriptional activation. Blood 102:3989-3997.
7. Brand, M., K. Yamamoto, A. Staub, and L. Tora. 1999. Identification of TATA-binding protein-free TAFII-containing complex subunits suggests a role in nucleosome acetylation and signal transduction. J. Biol. Chem. 274:18285-18289.
8. Burdon, T., A. Smith, and P. Savatier. 2002. Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol. 12:432-438.
9. Chambers, I., D. Colby, M. Robertson, J. Nichols, S. Lee, S. Tweedie, and A. Smith. 2003. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643-655.
10. DeKoter, R. P., and H. Singh. 2000. Regulation of B lymphocyte and macrophage development by graded expression of PU.1. Science 288:1439-1441.
11. Dieci, G., and A. Sentenac. 2003. Detours and shortcuts to transcription reinitiation. Trends Biochem. Sci. 28:202-209.
12. Dillon, N., and P. Sabbattini. 2000. Functional gene expression domains: defining the functional unit of eukaryotic gene regulation. Bioessays 22:657-665.
13. Drewell, R. A., E. Bae, J. Burr, and E. B. Lewis. 2002. Transcription defines the embryonic domains of cis-regulatory activity at the Drosophila bithorax complex. Proc. Natl. Acad. Sci. USA 99:16853-16858.
14. Dugray, A., J. F. Geay, A. Foudi, M. L. Bonnet, W. Vainchenker, F. Wendling, F. Louache, and A. G. Turhan. 2001. Rapid generation of a tetracycline-inducible BCR-ABL defective retrovirus using a single autoregulatory retroviral cassette. Leukemia 15:1658-1662.
15. Eisenbeis, C. F., H. Singh, and U. Storb. 1993. PU.1 is a component of a multiprotein complex which binds an essential site in the murine immunoglobulin lambda 2-4 enhancer. Mol. Cell. Biol. 13:6452-6461.
16. Fisher, A. G. 2002. Cellular identity and lineage choice. Nat. Rev. Immunol. 2:977-982.
17. Forsberg, E. C., K. M. Downs, H. M. Christensen, H. Im, P. A. Nuzzi, and E. H. Bresnick. 2000. Developmentally dynamic histone acetylation pattern of a tissue-specific chromatin domain. Proc. Natl. Acad. Sci. USA 97:14494-14499.
18. Frank, S. R., T. Parisi, S. Taubert, P. Fernandez, M. Fuchs, H. M. Chan, D. M. Livingston, and B. Amati. 2003. MYC recruits the TIP60 histone acetyltransferase complex to chromatin. EMBO Rep. 4:575-580.
19. Gribnau, J., K. Diderich, S. Pruzina, R. Calzolari, and P. Fraser. 2000. Intergenic transcription and developmental remodeling of chromatin subdomains in the human beta-globin locus. Mol. Cell 5:377-386.
20. Hamalainen, H. K., J. C. Tubman, S. Vikman, T. Kyrola, E. Ylikoski, J. A. Warrington, and R. Lahesmaa. 2001. Identification and validation of endogenous reference genes for expression profiling of T helper cell differentiation by quantitative real-time RT-PCR. Anal. Biochem. 299:63-70.
21. Hatzis, P., and I. Talianidis. 2002. Dynamics of enhancer-promoter communication during differentiation-induced gene activation. Mol. Cell 10:1467-1477.
22. Helmlinger, D., S. Hardy, S. Sasorith, F. Klein, F. Robert, C. Weber, L. Miguet, N. Potier, A. Van-Dorsselaer, J. M. Wurtz, J. L. Mandel, L. Tora, and D. Devys. 2004. Ataxin-7 is a subunit of GCN5 histone acetyltransferase-containing complexes. Hum. Mol. Genet. 13:1257-1265.
23. Hirota, S., T. Nishida, K. Isozaki, M. Taniguchi, K. Nishikawa, A. Ohashi, A. Takabayashi, T. Obayashi, T. Okuno, K. Kinoshita, H. Chen, Y. Shinomura, and Y. Kitamura. 2002. Familial gastrointestinal stromal tumors associated with dysphagia and novel type germline mutation of KIT gene. Gastroenterology 122:1493-1499.
24. Ho, Y., F. Elefant, N. Cooke, and S. Liebhaber. 2002. A defined locus control region determinant links chromatin domain acetylation with long-range gene activation. Mol. Cell 9:291-302.
25. Hromas, R., A. Orazi, R. S. Neiman, R. Maki, C. Van Beveran, J. Moore, and M. Klemsz. 1993. Hematopoietic lineage- and stage-restricted expression of the ETS oncogene family member PU.1. Blood 82:2998-3004.
26. Hu, M., D. Krause, M. Greaves, S. Sharkis, M. Dexter, C. Heyworth, and T. Enver. 1997. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev. 11:774-785.
27. Ishihara, K., W. J. Wood, Jr., M. Damore, G. G. Hermanson, R. Wall, and P. W. Kincade. 1992. B29 gene products complex with immunoglobulins on B lymphocytes. Proc. Natl. Acad. Sci. USA 89:633-637.
28. Jenuwein, T., and C. D. Allis. 2001. Translating the histone code. Science 293:1074-1080.
29. Jimenez, G., S. D. Griffiths, A. M. Ford, M. F. Greaves, and T. Enver. 1992. Activation of the beta-globin locus control region precedes commitment to the erythroid lineage. Proc. Natl. Acad. Sci. USA 89:10618-10622.
30. Johnson, K. D., H. M. Christensen, B. Zhao, and E. H. Bresnick. 2001. Distinct mechanisms control RNA polymerase II recruitment to a tissue-specific locus control region and a downstream promoter. Mol. Cell 8:465-471.
31. Johnson, K. D., J. A. Grass, C. Park, H. Im, K. Choi, and E. H. Bresnick. 2003. Highly restricted localization of RNA polymerase II within a locus control region of a tissue-specific chromatin domain. Mol. Cell. Biol. 23:6484-6493.
32. Katsura, Y. 2002. Redefinition of lymphoid progenitors. Nat. Rev. Immunol. 2:127-132.
33. Kee, B. L., M. W. Quong, and C. Murre. 2000. E2A proteins: essential regulators at multiple stages of B-cell development. Immunol. Rev. 175:138-149.
34. Kiekhaefer, C. M., J. A. Grass, K. D. Johnson, M. E. Boyer, and E. H. Bresnick. 2002. Hematopoietic-specific activators establish an overlapping pattern of histone acetylation and methylation within a mammalian chromatin domain. Proc. Natl. Acad. Sci. USA 99:14309-14314.
35. Kim, A., and A. Dean. 2004. Developmental stage differences in chromatin subdomains of the beta-globin locus. Proc. Natl. Acad. Sci. USA 101:7028-7033.
36. Kimura, A. P., S. A. Liebhaber, and N. E. Cooke. 2004. Epigenetic modifications at the human growth hormone locus predict distinct roles for histone acetylation and methylation in placental gene activation. Mol. Endocrinol. 18:1018-1032.
37. Kimura, H., M. Tada, N. Nakatsuji, and T. Tada. 2004. Histone code modifications on pluripotential nuclei of reprogrammed somatic cells. Mol. Cell. Biol. 24:5710-5720.
38. Kitanaka, A., T. Suzuki, C. Ito, H. Nishigaki, E. Coustan-Smith, T. Tanaka, Y. Kubota, and D. Campana. 1999. CD38-mediated signaling events in murine pro-B cells expressing human CD38 with or without its cytoplasmic domain. J. Immunol. 162:1952-1958.
39. Kontaraki, J., H. H. Chen, A. Riggs, and C. Bonifer. 2000. Chromatin fine structure profiles for a developmentally regulated gene: reorganization of the lysozyme locus before trans-activator binding and gene expression. Genes Dev. 14:2106-2122.
40. Koyama, N., D. Hoelzer, and O. G. Ottmann. 2004. Regulation of human IL-18 gene expression: interaction of PU.1 with GC-box binding protein is involved in human IL-18 expression in myeloid cells. Eur. J. Immunol. 34:817-826.
41. Lee, J. H., S. R. Hart, and D. G. Skalnik. 2004. Histone deacetylase activity is required for embryonic stem cell differentiation. Genesis 38:32-38.
42. Lefevre, P., S. Melnik, N. Wilson, A. D. Riggs, and C. Bonifer. 2003. Developmentally regulated recruitment of transcription factors and chromatin modification activities to chicken lysozyme cis-regulatory elements in vivo. Mol. Cell. Biol. 23:4386-4400.
43. Li, Y. S., K. Hayakawa, and R. R. Hardy. 1993. The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver. J. Exp. Med. 178:951-960.
44. Litt, M. D., M. Simpson, M. Gaszner, C. D. Allis, and G. Felsenfeld. 2001. Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus. Science 293:2453-2455.
45. Litt, M. D., M. Simpson, F. Recillas-Targa, M. N. Prioleau, and G. Felsenfeld. 2001. Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J. 20:2224-2235.
46. Liu, X., J. Tesfai, Y. A. Evrard, S. Y. Dent, and E. Martinez. 2003. c-Myc transformation domain recruits the human STAGA complex and requires TRRAP and GCN5 acetylase activity for transcription activation. J. Biol. Chem. 278:20405-20412.
47. Lundgren, M., C. M. Chow, P. Sabbattini, A. Georgiou, S. Minaee, and N. Dillon. 2000. Transcription factor dosage affects changes in higher order chromatin structure associated with activation of a heterochromatic gene. Cell 103:733-743.
48. Masternak, K., N. Peyraud, M. Krawczyk, E. Barras, and W. Reith. 2003. Chromatin remodeling and extragenic transcription at the MHC class II locus control region. Nat. Immunol. 4:132-137.
49. Melchers, F., H. Karasuyama, D. Haasner, S. Bauer, A. Kudo, N. Sakaguchi, B. Jameson, and A. Rolink. 1993. The surrogate light chain in B-cell development. Immunol Today. 14:60-68.
50. Minaee, S., D. Farmer, A. Georgiou, P. Sabbattini, Z. Webster, C.-M. Chow, and N. Dillon. Mapping and Functional analysis of regulatory sequences in the mouse λ5-VpreB1 domain. Mol. Immunol., in press.
51. Miyamoto, T., H. Iwasaki, B. Reizis, M. Ye, T. Graf, I. L. Weissman, and K. Akashi. 2002. Myeloid or lymphoid promiscuity as a critical step in hematopoietic lineage commitment. Dev. Cell 3:137-147.
52. Muchardt, C., and M. Yaniv. 2001. When the SWI/SNF complex remodels, the cell cycle. Oncogene 20:3067-3075.
53. Muller, F., and L. Tora. 2004. The multicoloured world of promoter recognition complexes. EMBO J. 23:2-8.
54. Musikacharoen, T., A. Oguma, Y. Yoshikai, N. Chiba, A. Masuda, and T. Matsuguchi. 2005. Interleukin-15 induces IL-12 receptor {beta}1 gene expression through PU.1 and IRF 3 by targeting chromatin remodeling. Blood 105:711-720.
55. Nielsen, A. L., C. Sanchez, H. Ichinose, M. Cervino, T. Lerouge, P. Chambon, and R. Losson. 2002. Selective interaction between the chromatin-remodeling factor BRG1 and the heterochromatin-associated protein HP1alpha. EMBO J. 21:5797-5806.
56. Niwa, H., J. Miyazaki, and A. G. Smith. 2000. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24:372-376.
57. O'Neill, L. P., and B. M. Turner. 2003. Immunoprecipitation of native chromatin: NChIP. Methods 31:76-82.
58. Palacios, R., and M. Steinmetz. 1985. IL-3-dependent mouse clones that express B-220 surface antigen, contain Ig genes in germ-line configuration, and generate B lymphocytes in vivo. Cell 41:727-734.
59. Palstra, R. J., B. Tolhuis, E. Splinter, R. Nymeijer, F. Grosveld, and W. de Laat. 2003. The beta-globin nuclear compartment in development and erythroid differentiation. Nat. Genet. 35:190-194.
60. Pesu, M., S. Aittomaki, T. Valineva, and O. Silvennoinen. 2003. PU.1 is required for transcriptional activation of the Stat6 response element in the Igepsilon promoter. Eur. J. Immunol. 33:1727-1735.
61. Plant, K. E., S. J. Routledge, and N. J. Proudfoot. 2001. Intergenic transcription in the human beta-globin gene cluster. Mol. Cell. Biol. 21:6507-6514.
62. Rank, G., M. Prestel, and R. Paro. 2002. Transcription through intergenic chromosomal memory elements of the Drosophila bithorax complex correlates with an epigenetic switch. Mol. Cell. Biol. 22:8026-8034.
63. Rastegar, M., L. Kobrossy, E. N. Kovacs, I. Rambaldi, and M. Featherstone. 2004. Sequential histone modifications at hoxd4 regulatory regions distinguish anterior from posterior embryonic compartments. Mol. Cell. Biol. 24:8090-8103.
64. Rogan, D. F., D. J. Cousins, S. Santangelo, P. A. Ioannou, M. Antoniou, T. H. Lee, and D. Z. Staynov. 2004. Analysis of intergenic transcription in the human IL-4/IL-13 gene cluster. Proc. Natl. Acad. Sci. USA 101:2446-2451.
65. Rossant, J. 2001. Stem cells from the mammalian blastocyst. Stem Cells 19:477-482.
66. Routledge, S. J., and N. J. Proudfoot. 2002. Definition of transcriptional promoters in the human beta globin locus control region. J. Mol. Biol. 323:601-611.
67. Sabbattini, P., A. Georgiou, C. Sinclair, and N. Dillon. 1999. Analysis of mice with single and multiple copies of transgenes reveals a novel arrangement for the λ5-VpreB1 locus control region. Mol. Cell. Biol. 19:671-679.
68. Sakaguchi, N., S. Kashiwamura, M. Kimoto, P. Thalmann, and F. Melchers. 1988. B lymphocyte lineage-restricted expression of mb-1, a gene with CD3-like structural properties. EMBO J. 7:3457-3464.
69. Sakamoto, N., K. Shibuya, Y. Shimizu, K. Yotsumoto, T. Miyabayashi, S. Sakano, T. Tsuji, E. Nakayama, H. Nakauchi, and A. Shibuya. 2001. A novel Fc receptor for IgA and IgM is expressed on both hematopoietic and non-hematopoietic tissues. Eur. J. Immunol. 31:1310-1316.
70. Schneider, R., A. J. Bannister, F. A. Myers, A. W. Thorne, C. Crane-Robinson, and T. Kouzarides. 2004. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat. Cell Biol. 6:73-77.
71. Schubeler, D., C. Francastel, D. M. Cimbora, A. Reik, D. I. Martin, and M. Groudine. 2000. Nuclear localization and histone acetylation: a pathway for chromatin opening and transcriptional activation of the human beta-globin locus. Genes Dev. 14:940-950.
72. Sigvardsson, M., M. O'Riordan, and R. Grosschedl. 1997. EBF and E47 collaborate to induce expression of the endogenous immunoglobulin surrogate light chain genes. Immunity 7:25-36.
73. Soutoglou, E., and I. Talianidis. 2002. Coordination of PIC assembly and chromatin remodeling during differentiation-induced gene activation. Science 295:1901-1904.
74. Spicuglia, S., S. Kumar, J. H. Yeh, E. Vachez, L. Chasson, S. Gorbatch, J. Cautres, and P. Ferrier. 2002. Promoter activation by enhancer-dependent and -independent loading of activator and coactivator complexes. Mol. Cell 10:1479-1487.
75. Suzuki, M., T. Yamada, F. Kihara-Negishi, T. Sakurai, and T. Oikawa. 2003. Direct association between PU.1 and MeCP2 that recruits mSin3A-HDAC complex for PU.1-mediated transcriptional repression. Oncogene 22:8688-8698.
76. Svanvik, N., A. Stahlberg, U. Sehlstedt, R. Sjoback, and M. Kubista. 2000. Detection of PCR products in real time using light-up probes. Anal. Biochem. 287:179-182.
77. Tagoh, H., R. Himes, D. Clarke, P. J. Leenen, A. D. Riggs, D. Hume, and C. Bonifer. 2002. Transcription factor complex formation and chromatin fine structure alterations at the murine c-fms (CSF-1 receptor) locus during maturation of myeloid precursor cells. Genes Dev. 16:1721-1737.
78. Tagoh, H., S. Melnik, P. Lefevre, S. Chong, A. D. Riggs, and C. Bonifer. 2004. Dynamic reorganization of chromatin structure and selective DNA demethylation prior to stable enhancer complex formation during differentiation of primary hematopoietic cells in vitro. Blood 103:2950-2955.
79. Tagoh, H., A. Schebesta, P. Lefevre, N. Wilson, D. Hume, M. Busslinger, and C. Bonifer. 2004. Epigenetic silencing of the c-fms locus during B-lymphopoiesis occurs in discrete steps and is reversible. EMBO J. 23:4275-4285.
80. Tufarelli, C., J. A. Stanley, D. Garrick, J. A. Sharpe, H. Ayyub, W. G. Wood, and D. R. Higgs. 2003. Transcription of antisense RNA leading to gene silencing and methylation as a novel cause of human genetic disease. Nat. Genet. 34:157-165.
81. Turner, B. M. 2002. Cellular memory and the histone code. Cell 111:285-291.
82. van der Stoep, N., E. Quinten, M. M. Rezende, and P. J. van den Elsen. 2004. E47, IRF-4, and PU.1 synergize to induce B-cell-specific activation of the class II transactivator promoter III (CIITA-PIII). Blood 104:2849-2857.
83. Volpe, C. P., A. Lundgren, A. Aints, A. J. Mohamed, P. Jaakkola, B. Christensson, G. Gahrton, M. Jalkanen, C. I. Smith, and M. S. Dilber. 2001. Proximal promoter of the murine syndecan-1 gene is not sufficient for the developmental pattern of syndecan expression in B lineage cells. Am. J. Hematol. 67:20-26.
84. White, J., C. Brou, J. Wu, Y. Lutz, V. Moncollin, and P. Chambon. 1992. The acidic transcriptional activator GAL-VP16 acts on preformed template-committed complexes. EMBO J. 11:2229-2240.
85. Wieczorek, E., M. Brand, X. Jacq, and L. Tora. 1998. Function of TAF(II)-containing complex without TBP in transcription by RNA polymerase II. Nature 393:187-191.
86. Ye, M., H. Iwasaki, C. V. Laiosa, M. Stadtfeld, H. Xie, S. Heck, B. Clausen, K. Akashi, and T. Graf. 2003. Hematopoietic stem cells expressing the myeloid lysozyme gene retain long-term, multilineage repopulation potential. Immunity 19:689-699.