Epigenetic regulation of genes during development: A conserved theme from flies to mammals

Centre for Cellular and Molecular Biology, Council for Scientific and Industrial Research, Uppal Road, Hyderabad 500007, India

More Information

Corresponding author: E-mail address: mishra@ccmb.res.in (Rakesh K Mishra)

摘要

- /
- /
- /
- /
- /
- /
Abstract: Eukaryotic genome is organized in form of chromatin within the nucleus. This organization is important for compaction of DNA as well as for the proper expression of the genes. During early embryonic development, genomic packaging receives variety of signals to eventually set up cell type specific expression patterns of genes. This process of regulated chromatinization leads to “cell type specific epigenomes”. The expression states attained during differentiation process need to be maintained subsequently throughout the life of the organism. Epigenetic modifications are responsible for chromatin dependent regulatory mechanism and play a key role in maintenance of the expression state—a process referred to as cellular memory. Another key feature in the packaging of the genome is formation of chromatin domains that are thought to be structural as well as functional units of the higher order chromatin organization. Boundary elements that function to define such domains set the limits of regulatory elements and that of epigenetic modifications. This connection of epigenetic modification, chromatin structure and genome organization has emerged from several studies. Hox genes are among the best studied in this context and have led to the significant understanding of the epigenetic regulation during development. Here we discuss the evolutionarily conserved features of epigenetic mechanisms emerged from studies on homeotic gene clusters.
- epigenetic /
- Hox cluster /
- chromatin /
- boundary /
- Polycomb group /
- tirthorax group /
- cellular memory

HTML全文

参考文献(162)

[1]	Akasaka, T., Kanno, M., Balling, R. et al. Development, 122 (1996),pp. 1513-1522
[2]	Americo, J., Whiteley, M., Brown, J.L. et al. Genetics, 160 (2002),pp. 1561-1571
[3]	Barges, S., Mihaly, J., Galloni, M. et al. The Fab-8 boundary defines the distal limit of the bithorax complex iab-7 domain and insulates iab-7 from initiation elements and a PRE in the adjacent iab-8 domain Development, 127 (2000),pp. 779-790
[4]	Barski, A., Cuddapah, S., Cui, K. et al. High-resolution profiling of histone methylations in the human genome Cell, 129 (2007),pp. 823-837
[5]	Beisel, C., Imhof, A., Greene, J. et al. Nature, 419 (2002),pp. 857-862
[6]	Bell, A.C., Felsenfeld, G. Nature, 405 (2000),pp. 482-485
[7]	Bell, A.C., West, A.G., Felsenfeld, G. Insulators and boundaries: Versatile regulatory elements in the eukaryotic genome Science, 291 (2001),pp. 447-450
[8]	Bender, W., Hudson, A. Development, 127 (2000),pp. 3981-3992
[9]	Bernstein, B.E., Mikkelsen, T.S., Xie, X. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells Cell, 125 (2006),pp. 315-326
[10]	Bird, A. DNA methylation patterns and epigenetic memory Genes Dev., 16 (2002),pp. 6-21
[11]	Blanton, J., Gaszner, M., Schedl, P. Genes Dev., 17 (2003),pp. 664-675
[12]	Blastyak, A., Mishra, R.K., Karch, F. et al. Efficient and specific targeting of Polycomb group proteins requires cooperative interaction between Grainyhead and Pleiohomeotic Mol. Cell. Biol., 26 (2006),pp. 1434-1444
[13]	Bloyer, S., Cavalli, G., Brock, H.W. et al. Identification and characterization of polyhomeotic PREs and TREs Dev Biol., 261 (2003),pp. 426-442
[14]	Boyer, L.A., Plath, K., Zeitlinger, J. et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells Nature, 441 (2006),pp. 349-353
[15]	Bracken, A.P., Dietrich, N., Pasini, D. et al. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions Genes Dev., 20 (2006),pp. 1123-1136
[16]	Breiling, A., Turner, B.M., Bianchi, M.E. et al. General transcription factors bind promoters repressed by Polycomb group proteins Nature, 412 (2001),pp. 651-655
[17]	Brock, H.W., Fisher, C.L. Maintenance of gene expression patterns Dev. Dyn., 232 (2005),pp. 633-655
[18]	Buchenau, P., Hodgson, J., Strutt, H. et al. J. Cell Biol., 141 (1998),pp. 469-481
[19]	Cao, R., Zhang, Y. The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3 Curr. Opin. Genet. Dev., 14 (2004),pp. 155-164
[20]	Cao, R., Tsukada, Y., Zhang, Y. Mol. Cell, 20 (2005),pp. 845-854
[21]	Capelson, M., Corces, V.G. Boundary elements and nuclear organization Biol. Cell., 96 (2004),pp. 617-629
[22]	Carroll, S.B. Homeotic genes and the evolution of arthropods and chordates Nature, 376 (1995),pp. 479-485
[23]	Cavalli, G. Chromosome kissing Curr. Opin. Genet. Dev., 17 (2007),pp. 443-450
[24]	Cavalli, G., Paro, R. Cell, 93 (1998),pp. 505-518
[25]	Cavalli, G., Paro, R. Epigenetic inheritance of active chromatin after removal of the main transactivator Science, 286 (1999),pp. 955-958
[26]	Chan, C.S., Rastelli, L., Pirrotta, V. EMBO J., 13 (1994),pp. 2553-2564
[27]	Chanas, G., Lavrov, S., Iral, F. et al. Engrailed and polyhomeotic maintain posterior cell identity through cubitus-interruptus regulation Dev. Biol., 272 (2004),pp. 522-535
[28]	Chen, X., Hiller, M., Sancak, Y. et al. Tissue-specific TAFs counteract Polycomb to turn on terminal differentiation Science, 310 (2005),pp. 869-872
[29]	Christen, B., Bienz, M. Imaginal disc silencers from Ultrabithorax: Evidence for Polycomb response elements Mech. Dev., 48 (1994),pp. 255-266
[30]	Chung, J.H., Whiteley, M., Felsenfeld, G. Cell, 74 (1993),pp. 505-514
[31]	Chung, J.H., Bell, A.C., Felsenfeld, G. Characterization of the chicken beta-globin insulator Proc. Natl. Acad. Sci. USA, 94 (1997),pp. 575-580
[32]	Core, N., Bel, S., Gaunt, S.J. et al. Altered cellular proliferation and mesoderm patterning in Polycomb-M33-deficient mice Development, 124 (1997),pp. 721-729
[33]	Corona, D.F., Armstrong, J.A., Tamkun, J.W. Methods Enzymol., 377 (2004),pp. 70-85
[34]	de Laat, W., Grosveld, F. Inter-chromosomal gene regulation in the mammalian cell nucleus Curr. Opin. Genet. Dev., 17 (2007),pp. 456-464
[35]	de Rosa, R., Grenier, J.K., Andreeva, T. et al. Nature, 399 (1999),pp. 772-776
[36]	Dejardin, J., Cavalli, G. Chromatin inheritance upon Zeste-mediated Brahma recruitment at a minimal cellular memory module EMBO J., 23 (2004),pp. 857-868
[37]	Dejardin, J., Rappailles, A., Cuvier, O. et al. Nature, 434 (2005),pp. 533-538
[38]	Deschamps, J., van den Akker, E., Forlani, S. et al. Int. J. Dev. Biol., 43 (1999),pp. 635-650
[39]	Dorsett, D. Curr. Opin. Genet. Dev., 9 (1999),pp. 505-514
[40]	Duncan, I. The bithorax complex Annu. Rev. Genet., 21 (1987),pp. 285-319
[41]	Engel, N., West, A.G., Felsenfeld, G. et al. Antagonism between DNA hypermethylation and enhancer-blocking activity at the H19 DMD is uncovered by CpG mutations Nat. Genet., 36 (2004),pp. 883-888
[42]	Ferrier, D.E., Holland, P.W. Ciona intestinalis ParaHox genes: Evolution of Hox/ParaHox cluster integrity, developmental mode, and temporal colinearity Mol. Phylogenet. Evol., 24 (2002),pp. 412-417
[43]	Ferrier, D.E., Minguillon, C. Evolution of the Hox/ParaHox gene clusters Int. J. Dev. Biol., 47 (2003),pp. 605-611
[44]	Ficz, G., Heintzmann, R., Arndt-Jovin, D.J. Development, 132 (2005),pp. 3963-3976
[45]	Fiedler, T., Rehmsmeier, M. jPREdictor: A versatile tool for the prediction of cis-regulatory elements Nucleic Acids Res., 34 (2006),pp. 546-550
[46]	Francis, N.J., Kingston, R.E., Woodcock, C.L. Chromatin compaction by a polycomb group protein complex Science, 306 (2004),pp. 1574-1577
[47]	Francis, N.J., Saurin, A.J., Shao, Z. et al. Reconstitution of a functional core polycomb repressive complex Mol. Cell, 8 (2001),pp. 545-556
[48]	Galloni, M., Gyurkovics, H., Schedl, P. et al. The bluetail transposon: Evidence for independent cis-regulatory domains and domain boundaries in the bithorax complex EMBO J., 12 (1993),pp. 1087-1097
[49]	Gaszner, M., Felsenfeld, G. Insulators: Exploiting transcriptional and epigenetic mechanisms Nat. Rev. Genet., 7 (2006),pp. 703-713
[50]	Gaszner, M., Vazquez, J., Schedl, P. The Zw5 protein, a component of the scs chromatin domain boundary, is able to block enhancer-promoter interaction Genes Dev., 13 (1999),pp. 2098-2107
[51]	Gause, M., Morcillo, P., Dorsett, D. Mol. Cell. Biol., 21 (2001),pp. 4807-4817
[52]	Gerasimova, T.I., Corces, V.G. Chromatin insulators and boundaries: Effects on transcription and nuclear organization Annu. Rev. Genet., 35 (2001),pp. 193-208
[53]	Geyer, P.K. The role of insulator elements in defining domains of gene expression Curr. Opin. Genet. Dev., 7 (1997),pp. 242-248
[54]	Geyer, P.K., Corces, V.G. Genes Dev., 6 (1992),pp. 1865-1873
[55]	Glinsky, G.V., Ivanova, Y.A., Glinskii, A.B. Common malignancy-associated regions of transcriptional activation (MARTA) in human prostate, breast, ovarian, and colon cancers are targets for DNA amplification Cancer Lett., 201 (2003),pp. 67-77
[56]	Gould, A. Functions of mammalian Polycomb group and trithorax group related genes Curr. Opin. Genet. Dev., 7 (1997),pp. 488-494
[57]	Hark, A.T., Schoenherr, C.J., Katz, D.J. et al. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus Nature, 405 (2000),pp. 486-489
[58]	Hur, M.W., Laney, J.D., Jeon, S.H. et al. Zeste maintains repression of Ubx transgenes: Support for a new model of Polycomb repression Development, 129 (2002),pp. 1339-1343
[59]	Iqbal, H., Mishra, R.K. Chromatin domain boundaries: Defining the functional domains in genome Proc. Indian Natl. Sci. Acad., 73 (2007),pp. 239-253
[60]	Izpisua-Belmonte, J.C., Tickle, C., Dolle, P. et al. Nature, 350 (1991),pp. 585-589
[61]	Kang, M.K., Kim, R.H., Kim, S.J. et al. Br. J. Cancer., 96 (2007),pp. 126-133
[62]	Karch, F., Galloni, M., Sipos, L. et al. Nucleic Acids Res., 22 (1994),pp. 3138-3146
[63]	Kassis, J.A. Genetics, 136 (1994),pp. 1025-1038
[64]	Kassis, J.A. Adv. Genet., 46 (2002),pp. 421-438
[65]	Kaufman, T.C., Seeger, M.A., Olsen, G. Adv. Genet., 27 (1990),pp. 309-362
[66]	Kellum, R., Schedl, P. A position-effect assay for boundaries of higher order chromosomal domains Cell, 64 (1991),pp. 941-950
[67]	Kellum, R., Schedl, P. A group of scs elements function as domain boundaries in an enhancer-blocking assay Mol. Cell. Biol., 12 (1992),pp. 2424-2431
[68]	Kennison, J.A. Annu. Rev. Genet., 29 (1995),pp. 289-303
[69]	Kennison, J.A. Methods Enzymol., 377 (2004),pp. 61-70
[70]	Klebes, A., Sustar, A., Kechris, K. et al. Development, 132 (2005),pp. 3753-3765
[71]	Klymenko, T., Muller, J. The histone methyltransferases Trithorax and Ash1 prevent transcriptional silencing by Polycomb group proteins EMBO Rep., 5 (2004),pp. 373-377
[72]	Klymenko, T., Papp, B., Fischle, W. et al. A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities Genes Dev., 20 (2006),pp. 1110-1122
[73]	Kondo, T., Duboule, D. Breaking colinearity in the mouse HoxD complex Cell, 97 (1999),pp. 407-417
[74]	Kouzarides, T. Chromatin modifications and their function Cell, 128 (2007),pp. 693-705
[75]	Krumlauf, R., Holland, P.W., McVey, J.H. et al. Development, 99 (1987),pp. 603-617
[76]	Kuhn, E.J., Geyer, P.K. Genomic insulators: Connecting properties to mechanism Curr. Opin. Cell Biol., 15 (2003),pp. 259-265
[77]	Lee, M.G., Villa, R., Trojer, P. et al. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination Science, 318 (2007),pp. 447-450
[78]	Lee, N., Maurange, C., Ringrose, L. et al. Nature, 438 (2005),pp. 234-237
[79]	Lee, T.I., Jenner, R.G., Boyer, L.A. et al. Control of developmental regulators by Polycomb in human embryonic stem cells Cell, 125 (2006),pp. 301-313
[80]	Levine, S.S., King, I.F., Kingston, R.E. Division of labor in polycomb group repression Trends Biochem. Sci., 29 (2004),pp. 478-485
[81]	Lewis, E.B. Nature, 276 (1978),pp. 565-570
[82]	Litt, M.D., Simpson, M., Recillas-Targa, F. et al. Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci Embo J., 20 (2001),pp. 2224-2235
[83]	Litt, M.D., Simpson, M., Gaszner, M. et al. Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus Science, 293 (2001),pp. 2453-2455
[84]	Liu, X.F., Olsson, P., Wolfgang, C.D. et al. PRAC: A novel small nuclear protein that is specifically expressed in human prostate and colon Prostate, 47 (2001),pp. 125-131
[85]	Maeda, R.K., Karch, F. The ABC of the BX-C: The bithorax complex explained Development, 133 (2006),pp. 1413-1422
[86]	Mahmoudi, T., Verrijzer, C.P. Chromatin silencing and activation by Polycomb and trithorax group proteins Oncogene, 20 (2001),pp. 3055-3066
[87]	Marshall, H., Studer, M., Popperl, H. et al. Nature, 370 (1994),pp. 567-571
[88]	Maurange, C., Paro, R. Genes Dev., 16 (2002),pp. 2672-2683
[89]	McCall, K., O'Connor, M.B., Bender, W. Genetics, 138 (1994),pp. 387-399
[90]	Mihaly, J., Mishra, R.K., Karch, F. A conserved sequence motif in Polycomb-response elements Mol. Cell, 1 (1998),pp. 1065-1066
[91]	Mihaly, J., Hogga, I., Barges, S. et al. Chromatin domain boundaries in the Bithorax complex Cell Mol. Life Sci., 54 (1998),pp. 60-70
[92]	Min, J., Zhang, Y., Xu, R.M. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27 Genes Dev., 17 (2003),pp. 1823-1828
[93]	Minguillon, C., Gardenyes, J., Serra, E. et al. No more than 14: The end of the amphioxus Hox cluster Int. J. Biol. Sci., 1 (2005),pp. 19-23
[94]	Mishra, R.K., Karch, F. Boundaries that demarcate structural and functional domains of chromatin J. Biosci., 24 (1999),pp. 377-399
[95]	Mishra, R.K., Yamagishi, T., Vasanthi, D. et al. Genesis, 45 (2007),pp. 570-576
[96]	Mishra, R.K., Mihaly, J., Barges, S. et al. The iab-7 polycomb response element maps to a nucleosome-free region of chromatin and requires both GAGA and pleiohomeotic for silencing activity Mol. Cell. Biol., 21 (2001),pp. 1311-1318
[97]	Miyagishima, H., Isono, K., Fujimura, Y. et al. Dissociation of mammalian Polycomb-group proteins, Ring1B and Rae28/Ph1, from the chromatin correlates with configuration changes of the chromatin in mitotic and meiotic prophase Histochem. Cell Biol., 120 (2003),pp. 111-119
[98]	Moghadam, H.K., Ferguson, M.M., Danzmann, R.G. Evolution of Hox clusters in Salmonidae: A comparative analysis between Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) J. Mol. Evol., 61 (2005),pp. 636-649
[99]	Mohd-Sarip, A., Cleard, F., Mishra, R.K. et al. Synergistic recognition of an epigenetic DNA element by Pleiohomeotic and a Polycomb core complex Genes Dev., 19 (2005),pp. 1755-1760
[100]	Mohd-Sarip, A., van der Knaap, J.A., Wyman, C. et al. Architecture of a polycomb nucleoprotein complex Mol. Cell, 24 (2006),pp. 91-100
[101]	Moon, H., Filippova, G., Loukinov, D. et al. EMBO Rep., 6 (2005),pp. 165-170
[102]	Muller, J., Bienz, M. EMBO J., 10 (1991),pp. 3147-3155
[103]	Muller, J., Hart, C.M., Francis, N.J. et al. Cell, 111 (2002),pp. 197-208
[104]	Munke, M., Cox, D.R., Jackson, I.J. et al. The murine Hox-2 cluster of homeo box containing genes maps distal on chromosome 11 near the tail-short (Ts) locus Cytogenet. Cell Genet., 42 (1986),pp. 236-240
[105]	Negre, N., Hennetin, J., Sun, L.V. et al. PLoS Biol., 4 (2006),p. e170
[106]	Offield, M.F., Jetton, T.L., Labosky, P.A. et al. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum Development, 122 (1996),pp. 983-995
[107]	Oki, M., Kamakaka, R.T. Blockers and barriers to transcription: Competing activities? Curr. Opin. Cell Biol., 14 (2002),pp. 299-304
[108]	Orlando, V., Jane, E.P., Chinwalla, V. et al. EMBO J., 17 (1998),pp. 5141-5150
[109]	Papoulas, O., Beek, S.J., Moseley, S.L. et al. Development, 125 (1998),pp. 3955-3966
[110]	Pasini, D., Bracken, A.P., Helin, K. Polycomb group proteins in cell cycle progression and cancer Cell Cycle, 3 (2004),pp. 396-400
[111]	Pasini, D., Bracken, A.P., Jensen, M.R. et al. Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity EMBO J., 23 (2004),pp. 4061-4071
[112]	Passarge, E. Emil Heitz and the concept of heterochromatin: Longitudinal chromosome differentiation was recognized fifty years ago Am. J. Hum. Genet., 31 (1979),pp. 106-115
[113]	Pathak, R.U., Rangaraj, N., Kallappagoudar, S. et al. Boundary element-associated factor 32B connects chromatin domains to the nuclear matrix Mol. Cell. Biol., 27 (2007),pp. 4796-4806
[114]	Petruk, S., Sedkov, Y., Smith, S. et al. Trithorax and dCBP acting in a complex to maintain expression of a homeotic gene Science, 294 (2001),pp. 1331-1334
[115]	Pikaart, M.J., 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 (1998),pp. 2852-2862
[116]	Pirrotta, V. PcG complexes and chromatin silencing Curr. Opin. Genet. Dev., 7 (1997),pp. 249-258
[117]	Powers, T.P., Amemiya, C.T. Evidence for a Hox14 paralog group in vertebrates Curr. Biol., 14 (2004),pp. R183-R184
[118]	Prioleau, M.N., Nony, P., Simpson, M. et al. 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 (1999),pp. 4035-4048
[119]	Recillas-Targa, F., Pikaart, M.J., 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 (2002),pp. 6883-6888
[120]	Regulski, M., Harding, K., Kostriken, R. et al. Cell, 43 (1985),pp. 71-80
[121]	Ringrose, L., Paro, R. Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins Annu. Rev. Genet., 38 (2004),pp. 413-443
[122]	Ringrose, L., Paro, R. Polycomb/Trithorax response elements and epigenetic memory of cell identity Development, 134 (2007),pp. 223-232
[123]	Ringrose, L., Rehmsmeier, M., Dura, J.M. et al. Dev. Cell, 5 (2003),pp. 759-771
[124]	Roguev, A., Schaft, D., Shevchenko, A. et al. The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4 EMBO J., 20 (2001),pp. 7137-7148
[125]	Ross, J.M., Zarkower, D. Dev. Cell, 4 (2003),pp. 891-901
[126]	Sabarinadh, C., Subramanian, S., Tripathi, A. et al. Extreme conservation of noncoding DNA near HoxD complex of vertebrates BMC Genomics, 5 (2004),p. 75
[127]	Santini, S., Boore, J.L., Meyer, A. Evolutionary conservation of regulatory elements in vertebrate Hox gene clusters Genome Res., 13 (2003),pp. 1111-1122
[128]	Satijn, D.P., Otte, A.P. Polycomb group protein complexes: Do different complexes regulate distinct target genes? Biochim. Biophys. Acta, 1447 (1999),pp. 1-16
[129]	Schneider, R., Grosschedl, R. Dynamics and interplay of nuclear architecture, genome organization, and gene expression Genes Dev., 21 (2007),pp. 3027-3043
[130]	Schneider, R., Bannister, A.J., Myers, F.A. et al. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes Nat. Cell Biol., 6 (2004),pp. 73-77
[131]	Schuettengruber, B., Chourrout, D., Vervoort, M. et al. Genome regulation by polycomb and trithorax proteins Cell, 128 (2007),pp. 735-745
[132]	Schwartz, Y.B., Kahn, T.G., Nix, D.A. et al. Nat. Genet., 38 (2006),pp. 700-705
[133]	Schweinsberg, S., Hagstrom, K., Gohl, D. et al. Genetics, 168 (2004),pp. 1371-1384
[134]	Schweinsberg, S.E., Schedl, P. Developmental modulation of Fab-7 boundary function Development, 131 (2004),pp. 4743-4749
[135]	Seeler, J.S., Dejean, A. Nuclear and unclear functions of SUMO Nat. Rev. Mol. Cell. Biol., 4 (2003),pp. 690-699
[136]	Simeone, A., Acampora, D., Nigro, V. et al. Differential regulation by retinoic acid of the homeobox genes of the four HOX loci in human embryonal carcinoma cells Mech. Dev., 33 (1991),pp. 215-227
[137]	Simon, J., Peifer, M., Bender, W. et al. Regulatory elements of the bithorax complex that control expression along the anterior-posterior axis EMBO J., 9 (1990),pp. 3945-3956
[138]	Simon, J., Bornemann, D., Lunde, K. et al. The extra sex combs product contains WD40 repeats and its time of action implies a role distinct from other Polycomb group products Mech. Dev., 53 (1995),pp. 197-208
[139]	Simon, J., Chiang, A., Bender, W. et al. Dev. Biol., 158 (1993),pp. 131-144
[140]	Smith, S.T., Petruk, S., Sedkov, Y. et al. Modulation of heat shock gene expression by the TAC1 chromatin-modifying complex Nat. Cell Biol., 6 (2004),pp. 162-167
[141]	Song, L.B., Zeng, M.S., Liao, W.T. et al. Bmi-1 is a novel molecular marker of nasopharyngeal carcinoma progression and immortalizes primary human nasopharyngeal epithelial cells Cancer Res., 66 (2006),pp. 6225-6232
[142]	Soutoglou, E., Misteli, T. Mobility and immobility of chromatin in transcription and genome stability Curr. Opin. Genet. Dev., 17 (2007),pp. 435-442
[143]	Spector, D.L. The dynamics of chromosome organization and gene regulation Annu. Rev. Biochem., 72 (2003),pp. 573-608
[144]	Stornaiuolo, A., Acampora, D., Pannese, M. et al. Cell Differ. Dev., 31 (1990),pp. 119-127
[145]	Takihara, Y., Tomotsune, D., Shirai, M. et al. Development, 124 (1997),pp. 3673-3682
[146]	Tolhuis, B., de Wit, E., Muijrers, I. et al. Nat. Genet., 38 (2006),pp. 694-699
[147]	Udvardy, A., Maine, E., Schedl, P. The 87A7 chromomere. Identification of novel chromatin structures flanking the heat shock locus that may define the boundaries of higher order domains J. Mol. Biol., 185 (1985),pp. 341-358
[148]	Valenzuela, L., Kamakaka, R.T. Chromatin insulators Annu. Rev. Genet., 40 (2006),pp. 107-138
[149]	Valk-Lingbeek, M.E., Bruggeman, S.W., van Lohuizen, M. Stem cells and cancer; the polycomb connection Cell, 118 (2004),pp. 409-418
[150]	van der Lugt, N.M., Domen, J., Linders, K. et al. Genes Dev., 8 (1994),pp. 757-769
[151]	van der Vlag, J., Otte, A.P. Transcriptional repression mediated by the human polycomb-group protein EED involves histone deacetylation Nat. Genet., 23 (1999),pp. 474-478
[152]	Vazquez, J., Farkas, G., Gaszner, M. et al. Genetic and molecular analysis of chromatin domains Cold Spring Harb. Symp. Quant. Biol., 58 (1993),pp. 45-54
[153]	Voncken, J.W., Schweizer, D., Aagaard, L. et al. Chromatin-association of the Polycomb group protein BMI1 is cell cycle-regulated and correlates with its phosphorylation status J. Cell Sci., 112 (1999),pp. 4627-4639
[154]	Voncken, J.W., Niessen, H., Neufeld, B. et al. MAPKAP kinase 3pK phosphorylates and regulates chromatin association of the polycomb group protein Bmi1 J. Biol. Chem., 280 (2005),pp. 5178-5187
[155]	Wang, H., Wang, L., Erdjument-Bromage, H. et al. Role of histone H2A ubiquitination in Polycomb silencing Nature, 431 (2004),pp. 873-878
[156]	Wang, L., Brown, J.L., Cao, R. et al. Hierarchical recruitment of polycomb group silencing complexes Mol. Cell, 14 (2004),pp. 637-646
[157]	West, A.G., Gaszner, M., Felsenfeld, G. Insulators: Many functions, many mechanisms Genes Dev., 16 (2002),pp. 271-288
[158]	West, A.G., Huang, S., Gaszner, M. et al. Recruitment of histone modifications by USF proteins at a vertebrate barrier element Mol. Cell, 16 (2004),pp. 453-463
[159]	Yusufzai, T.M., Felsenfeld, G. The 5′-HS4 chicken beta-globin insulator is a CTCF-dependent nuclear matrix-associated element Proc. Natl. Acad. Sci. USA, 101 (2004),pp. 8620-8624
[160]	Zeltser, L., Desplan, C., Heintz, N. Development, 122 (1996),pp. 2475-2484
[161]	Zhao, K., Hart, C.M., Laemmli, U.K. Visualization of chromosomal domains with boundary element-associated factor BEAF-32 Cell, 81 (1995),pp. 879-889
[162]	Zink, B., Paro, R. Nature, 337 (1989),pp. 468-471