Folia Biologica
Journal of Cellular and Molecular Biology, Charles University 

Crossref logo

Fol. Biol. 2014, 60, 13-20

https://doi.org/10.14712/fb2014060S10013

Structural Basis of Polycomb Bodies

Jana Šmigová1, P. Juda1, J. Krejčí2, I. Raška1

1Institute of Cellular Biology and Pathology, First Faculty of Medicine, Charles University in Prague, Czech Republic
2Institute of Biophysics, Academy of Sciences of the Czech Republic, v. v. i., Brno, Czech Republic

Received June 27, 2014
Accepted July 21, 2014

References

1. Ahmed, K., Li, R., Bazett-Jones, D. P. (2009) Electron spectroscopic imaging of the nuclear landscape. Methods Mol. Biol. 464, 415-423. <https://doi.org/10.1007/978-1-60327-461-6_23>
2. Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jorgensen, H. F., John, R. M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M., Fisher, A. G. (2006) Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8, 532-538. <https://doi.org/10.1038/ncb1403>
3. Bantignies, F., Cavalli, G. (2011) Polycomb group proteins: repression in 3D. Trends Genet. 27, 454-464. <https://doi.org/10.1016/j.tig.2011.06.008>
4. Bantignies, F., Roure, V., Comet, I., Leblanc, B., Schuet­ tengruber, B., Bonnet, J., Tixier, V., Mas, A., Cavalli, G. (2011) Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila. Cell 144, 214-226. <https://doi.org/10.1016/j.cell.2010.12.026>
5. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., Jaenisch, R., Wagschal, A., Feil, R., Schreiber, S. L., Lander, E. S. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326. <https://doi.org/10.1016/j.cell.2006.02.041>
6. Bian, Q., Belmont, A. S. (2012) Revisiting higher-order and large-scale chromatin organization. Curr. Opin. Cell Biol. 24, 359-366. <https://doi.org/10.1016/j.ceb.2012.03.003>
7. Bracken, A. P., Dietrich, N., Pasini, D., Hansen, K. H., Helin, K. (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 20, 1123-1136. <https://doi.org/10.1101/gad.381706>
8. Buchenau, P., Hodgson, J., Strutt, H., Arndt-Jovin, D. J. (1998) The distribution of polycomb-group proteins during cell division and development in Drosophila embryos: impact on models for silencing. J. Cell Biol. 141, 469-481. <https://doi.org/10.1083/jcb.141.2.469>
9. Cao, R., Wang, L., Wang, H., Xia, L., Erdjument-Bromage, H., Tempst, P., Jones, R. S., Zhang, Y. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298, 1039-1043. <https://doi.org/10.1126/science.1076997>
10. Cao, R., Tsukada, Y., Zhang, Y. (2005) Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol. Cell. 20, 845-854. <https://doi.org/10.1016/j.molcel.2005.12.002>
11. Cavalli, G. (2007) Chromosome kissing. Curr. Opin. Genet. Dev. 17, 443-450. <https://doi.org/10.1016/j.gde.2007.08.013>
12. Chandra, T., Kirschner, K., Thuret, J. Y., Pope, B. D., Ryba, T., Newman, S., Ahmed, K., Samarajiwa, S. A., Salama, R., Carroll, T., Stark, R., Janky, R., Narita, M., Xue, L., Chicas, A., Nunez, S., Janknecht, R., Hayashi-Takanaka, Y., Wilson, M. D., Marshall, A., Odom, D. T., Babu, M. M., Bazett-Jones, D. P., Tavare, S., Edwards, P. A., Lowe, S. W., Kimura, H., Gilbert, D. M., Narita, M. (2012) Independence of repressive histone marks and chromatin compaction during senescent heterochromatic layer formation. Mol. Cell 47, 203-214. <https://doi.org/10.1016/j.molcel.2012.06.010>
13. Cheutin, T., Cavalli, G. (2012) Progressive polycomb assembly on H3K27me3 compartments generates polycomb bodies with developmentally regulated motion. PLoS Genet. 8, e1002465. <https://doi.org/10.1371/journal.pgen.1002465>
14. Comet, I., Schuettengruber, B., Sexton, T., Cavalli, G. (2011) A chromatin insulator driving three-dimensional Polycomb response element (PRE) contacts and Polycomb association with the chromatin fiber. Proc. Natl. Acad. Sci. USA 108, 2294-2299. <https://doi.org/10.1073/pnas.1002059108>
15. Czermin, B., Melfi, R., Mccabe, D., Seitz, V., Imhof, A., Pirrotta, V. (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111, 185-196. <https://doi.org/10.1016/S0092-8674(02)00975-3>
16. Dundr, M., Misteli, T. (2010) Biogenesis of nuclear bodies. Cold Spring Harb. Perspect. Biol. 2, a000711. <https://doi.org/10.1101/cshperspect.a000711>
17. Dundr, M. (2011) Seed and grow: a two-step model for nuclear body biogenesis. J. Cell Biol. 193, 605-606. <https://doi.org/10.1083/jcb.201104087>
18. Eltsov, M., Maclellan, K. M., Maeshima, K., Frangakis, A. S., Dubochet, J. (2008) Analysis of cryo-electron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ. Proc. Natl. Acad. Sci. USA 105, 19732-19737. <https://doi.org/10.1073/pnas.0810057105>
19. Enderle, D., Beisel, C., Stadler, M. B., Gerstung, M., Athri, P., Paro, R. (2011) Polycomb preferentially targets stalled promoters of coding and noncoding transcripts. Genome Res. 21, 216-226. <https://doi.org/10.1101/gr.114348.110>
20. Fauvarque, M. O., Dura, J. M. (1993) Polyhomeotic regulatory sequences induce developmental regulator-dependent variegation and targeted P-element insertions in Drosophila. Genes Dev. 7, 1508-1520. <https://doi.org/10.1101/gad.7.8.1508>
21. Ficz, G., Heintzmann, R., Arndt-Jovin, D. J. (2005) Polycomb group protein complexes exchange rapidly in living Drosophila. Development 132, 3963-3976. <https://doi.org/10.1242/dev.01950>
22. Filion, G. J., Van Steensel, B. (2010) Reassessing the abundance of H3K9me2 chromatin domains in embryonic stem cells. Nat. Genet. 42, 4, author reply 5-6. <https://doi.org/10.1038/ng0110-4>
23. Fischle, W., Wang, Y., Jacobs, S. A., Kim, Y., Allis, C. D., Khorasanizadeh, S. (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 17, 1870-1881. <https://doi.org/10.1101/gad.1110503>
24. Fonseca, J. P., Steffen, P. A., Muller, S., Lu, J., Sawicka, A., Seiser, C., Ringrose, L. (2012) In vivo Polycomb kinetics and mitotic chromatin binding distinguish stem cells from differentiated cells. Genes Dev. 26, 857-871. <https://doi.org/10.1101/gad.184648.111>
25. Francis, N. J., Kingston, R. E., Woodcock, C. L. (2004) Chromatin compaction by a polycomb group protein complex. Science 306, 1574-1577. <https://doi.org/10.1126/science.1100576>
26. Fussner, E., Ching, R. W., Bazett-Jones, D. P. (2011) Living without 30nm chromatin fibers. Trends Biochem. Sci. 36, 1-6. <https://doi.org/10.1016/j.tibs.2010.09.002>
27. Gao, Z., Zhang, J., Bonasio, R., Strino, F., Sawai, A., Parisi, F., Kluger, Y., Reinberg, D. (2012) PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol. Cell 45, 344-356. <https://doi.org/10.1016/j.molcel.2012.01.002>
28. Grau, D. J., Chapman, B. A., Garlick, J. D., Borowsky, M., Francis, N. J., Kingston, R. E. (2011) Compaction of chromatin by diverse Polycomb group proteins requires localized regions of high charge. Genes Dev. 25, 2210-2221. <https://doi.org/10.1101/gad.17288211>
29. Gunster, M. J., Satijn, D. P., Hamer, K. M., Den Blaauwen, J. L., De Bruijn, D., Alkema, M. J., Van Lohuizen, M., Van Driel, R., Otte, A. P. (1997) Identification and characterization of interactions between the vertebrate polycomb-group protein BMI1 and human homologs of polyhomeotic. Mol. Cell. Biol. 17, 2326-2335. <https://doi.org/10.1128/MCB.17.4.2326>
30. Hernandez-Munoz, I., Taghavi, P., Kuijl, C., Neefjes, J., Van Lohuizen, M. (2005) Association of BMI1 with polycomb bodies is dynamic and requires PRC2/EZH2 and the maintenance DNA methyltransferase DNMT1. Mol. Cell. Biol. 25, 11047-11058. <https://doi.org/10.1128/MCB.25.24.11047-11058.2005>
31. Hodgson, J. W., Brock, H. W. (2011) Are polycomb group bodies gene silencing factories? Cell 144, 170-171. <https://doi.org/10.1016/j.cell.2011.01.006>
32. Kagey, M. H., Melhuish, T. A., Wotton, D. (2003) The polycomb protein Pc2 is a SUMO E3. Cell, 113, 127-137. <https://doi.org/10.1016/S0092-8674(03)00159-4>
33. Kuzmichev, A., Nishioka, K., Erdjument-Bromage, H., Tempst, P., Reinberg, D. (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 16, 2893-2905. <https://doi.org/10.1101/gad.1035902>
34. Lee, M. G., Wynder, C., Bochar, D. A., Hakimi, M. A., Cooch, N., Shiekhattar, R. (2006) Functional interplay between histone demethylase and deacetylase enzymes. Mol. Cell. Biol. 26, 6395-6402. <https://doi.org/10.1128/MCB.00723-06>
35. Lei, E. P., Corces, V. G. (2006) RNA interference machinery influences the nuclear organization of a chromatin insulator. Nat. Genet. 38, 936-941. <https://doi.org/10.1038/ng1850>
36. Levine, S. S., King, I. F., Kingston, R. E. (2004) Division of labor in polycomb group repression. Trends Biochem. Sci. 29, 478-485. <https://doi.org/10.1016/j.tibs.2004.07.007>
37. Li, H. B., Muller, M., Bahechar, I. A., Kyrchanova, O., Ohno, K., Georgiev, P., Pirrotta, V. (2011) Insulators, not Polycomb response elements, are required for long-range interactions between Polycomb targets in Drosophila melanogaster. Mol. Cell. Biol. 31, 616-625. <https://doi.org/10.1128/MCB.00849-10>
38. Li, H. B., Ohno, K., Gui, H., Pirrotta, V. (2013) Insulators target active genes to transcription factories and polycomb-repressed genes to polycomb bodies. PLoS Genet. 9, e1003436. <https://doi.org/10.1371/journal.pgen.1003436>
39. Lund, A. H., Van Lohuizen, M. (2004) Polycomb complexes and silencing mechanisms. Curr. Opin. Cell Biol. 16, 239-246. <https://doi.org/10.1016/j.ceb.2004.03.010>
40. MacPherson, M. J., Beatty, L. G., Zhou, W., Du, M., Sadowski, P. D. (2009) The CTCF insulator protein is posttranslationally modified by SUMO. Mol. Cell. Biol. 29, 714-725. <https://doi.org/10.1128/MCB.00825-08>
41. Maertens, G. N., El Messaoudi-Aubert, S., Racek, T., Stock, J. K., Nicholls, J., Rodriguez-Niedenfuhr, M., Gil, J., Peters, G. (2009) Several distinct polycomb complexes regulate and co-localize on the INK4a tumor suppressor locus. PLoS One 4, e6380. <https://doi.org/10.1371/journal.pone.0006380>
42. Martinez, A. M., Cavalli, G. (2006) The role of polycomb group proteins in cell cycle regulation during development. Cell Cycle 5, 1189-1197. <https://doi.org/10.4161/cc.5.11.2781>
43. Martin-Perez, D., Piris, M. A., Sanchez-Beato, M. (2010) Polycomb proteins in hematologic malignancies. Blood 116, 5465-5475. <https://doi.org/10.1182/blood-2010-05-267096>
44. McElroy, K. A., Kang, H., Kuroda, M. I. (2014) Are we there yet? Initial targeting of the Male-Specific Lethal and Polycomb group chromatin complexes in Drosophila. Open Biol. 4, 140006. <https://doi.org/10.1098/rsob.140006>
45. Min, J., Zhang, Y., Xu, R. M. (2003) Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev. 17, 1823-1828. <https://doi.org/10.1101/gad.269603>
46. Muller, J., Hart, C. M., Francis, N. J., Vargas, M. L., Sengupta, A., Wild, B., Miller, E. L., O’Connor, M. B., Kingston, R. E., Simon, J. A. (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111, 197-208. <https://doi.org/10.1016/S0092-8674(02)00976-5>
47. Nozawa, R. S., Nagao, K., Igami, K. T., Shibata, S., Shirai, N., Nozaki, N., Sado, T., Kimura, H., Obuse, C. (2013) Human inactive X chromosome is compacted through a PRC2independent SMCHD1-HBiX1 pathway. Nat. Struct. Mol. Biol. 20, 566-573. <https://doi.org/10.1038/nsmb.2532>
48. Pemberton, H., Anderton, E., Patel, H., Brookes, S., Chandler, H., Palermo, R., Stock, J., Rodriguez-Niedenfuhr, M., Racek, T., De Breed, L., Stewart, A., Matthews, N., Peters, G. (2014) Genome-wide co-localization of Polycomb orthologs and their effects on gene expression in human fibroblasts. Genome Biol. 15, R23. <https://doi.org/10.1186/gb-2014-15-2-r23>
49. Pirrotta, V., Li, H. B. (2012) A view of nuclear Polycomb ­ bodies. Curr. Opin. Genet. Dev. 22, 101-109. <https://doi.org/10.1016/j.gde.2011.11.004>
50. Plath, K., Talbot, D., Hamer, K. M., Otte, A. P., Yang, T. P., Jaenisch, R., Panning, B. (2004) Developmentally regulated alterations in Polycomb repressive complex 1 proteins on the inactive X chromosome. J. Cell Biol. 167, 1025-1035. <https://doi.org/10.1083/jcb.200409026>
51. Ren, X., Vincenz, C., Kerppola, T. K. (2008) Changes in the distributions and dynamics of polycomb repressive complexes during embryonic stem cell differentiation. Mol. Cell. Biol. 28, 2884-2895. <https://doi.org/10.1128/MCB.00949-07>
52. Ringrose, L., Paro, R. (2004) Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu. Rev. Genet. 38, 413-443. <https://doi.org/10.1146/annurev.genet.38.072902.091907>
53. Sanchez, C., Sanchez, I., Demmers, J. A., Rodriguez, P., Strouboulis, J., Vidal, M. (2007) Proteomics analysis of Ring1B/Rnf2 interactors identifies a novel complex with the Fbxl10/Jhdm1B histone demethylase and the Bcl6 interacting corepressor. Mol. Cell. Proteomics 6, 820-834. <https://doi.org/10.1074/mcp.M600275-MCP200>
54. Satijn, D. P., Gunster, M. J., Van Der Vlag, J., Hamer, K. M., Schul, W., Alkema, M. J., Saurin, A. J., Freemont, P. S., Van Driel, R., Otte, A. P. (1997) RING1 is associated with the polycomb group protein complex and acts as a transcriptional repressor. Mol. Cell. Biol. 17, 4105-4113. <https://doi.org/10.1128/MCB.17.7.4105>
55. Saurin, A. J., Shiels, C., Williamson, J., Satijn, D. P., Otte, A. P., Sheer, D., Freemont, P. S. (1998) The human polycomb group complex associates with pericentromeric heterochromatin to form a novel nuclear domain. J. Cell Biol. 142, 887-898. <https://doi.org/10.1083/jcb.142.4.887>
56. Scheffer, M. P., Eltsov, M., Frangakis, A. S. (2011) Evidence for short-range helical order in the 30-nm chromatin fibers of erythrocyte nuclei. Proc. Natl. Acad. Sci. USA 108, 16992-16997. <https://doi.org/10.1073/pnas.1108268108>
57. Schoorlemmer, J., Marcos-Gutierrez, C., Were, F., Martinez, R., Garcia, E., Satijn, D. P., Otte, A. P., Vidal, M. (1997) Ring1A is a transcriptional repressor that interacts with the Polycomb-M33 protein and is expressed at rhombomere boundaries in the mouse hindbrain. EMBO J. 16, 5930-5942. <https://doi.org/10.1093/emboj/16.19.5930>
58. Schuettengruber, B., Ganapathi, M., Leblanc, B., Portoso, M., Jaschek, R., Tolhuis, B., Van Lohuizen, M., Tanay, A., Cavalli, G. (2009) Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLoS Biol. 7, e13. <https://doi.org/10.1371/journal.pbio.1000013>
59. Schwartz, Y. B., Kahn, T. G., Stenberg, P., Ohno, K., Bourgon, R., Pirrotta, V. (2010) Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet. 6, e1000805. <https://doi.org/10.1371/journal.pgen.1000805>
60. Shao, Z., Raible, F., Mollaaghababa, R., Guyon, J. R., Wu, C. T., Bender, W., Kingston, R. E. (1999) Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98, 37-46. <https://doi.org/10.1016/S0092-8674(00)80604-2>
61. Simon, J., Chiang, A., Bender, W., Shimell, M. J., O’Connor, M. (1993) Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products. Dev. Biol. 158, 131-144. <https://doi.org/10.1006/dbio.1993.1174>
62. Smigova, J., Juda, P., Cmarko, D., Raska, I. (2011) Fine structure of the “PcG body” in human U-2 OS cells established by correlative light-electron microscopy. Nucleus 2, 219-228. <https://doi.org/10.4161/nucl.2.3.15737>
63. Smigova, J., Juda, P., Bartova, E., Raska, I. (2013) Dynamics of Polycomb chromatin domains under conditions of increased molecular crowding. Biol. Cell 105, 519-534. <https://doi.org/10.1111/boc.201300022>
64. Song, F., Chen, P., Sun, D., Wang, M., Dong, L., Liang, D., Xu, R. M., Zhu, P., Li, G. (2014) Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units. Science 344, 376-380. <https://doi.org/10.1126/science.1251413>
65. Sparmann, A., Van Lohuizen, M. (2006) Polycomb silencers control cell fate, development and cancer. Nat. Rev. 6, 846-856. <https://doi.org/10.1038/nrc1991>
66. Sustackova, G., Kozubek, S., Stixova, L., Legartova, S., Matula, P., Orlova, D., Bartova, E. (2012) Acetylation-dependent nuclear arrangement and recruitment of BMI1 protein to UV-damaged chromatin. J. Cell. Physiol. 227, 1838-1850. <https://doi.org/10.1002/jcp.22912>
67. Tavares, L., Dimitrova, E., Oxley, D., Webster, J., Poot, R., Demmers, J., Bezstarosti, K., Taylor, S., Ura, H., Koide, H., Wutz, A., Vidal, M., Elderkin, S., Brockdorff, N. (2012) RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell 148, 664-678. <https://doi.org/10.1016/j.cell.2011.12.029>
68. Tolhuis, B., Blom, M., Kerkhoven, R. M., Pagie, L., Teunissen, H., Nieuwland, M., Simonis, M., De Laat, W., Van Lohuizen, M., Van Steensel, B. (2011) Interactions among Polycomb domains are guided by chromosome architecture. PLoS Genet. 7, e1001343. <https://doi.org/10.1371/journal.pgen.1001343>
69. Van Der Vlag, J., Den Blaauwen, J. L., Sewalt, R. G., Van Driel, R., Otte, A. P. (2000) Transcriptional repression mediated by polycomb group proteins and other chromatinassociated repressors is selectively blocked by insulators. J. Biol. Chem. 275, 697-704. <https://doi.org/10.1074/jbc.275.1.697>
70. Van Holde, K., Zlatanova, J. (1995) Chromatin higher order structure: chasing a mirage? J. Biol. Chem. 270, 8373-8376. <https://doi.org/10.1074/jbc.270.15.8373>
71. Van Steensel, B. (2011) Chromatin: constructing the big picture. EMBO J. 30, 1885-1895. <https://doi.org/10.1038/emboj.2011.135>
72. Vandamme, J., Volkel, P., Rosnoblet, C., Le Faou, P., Angrand, P. O. (2011) Interaction proteomics analysis of polycomb proteins defines distinct PRC1 complexes in mammalian cells. Mol. Cell. Proteomics 10, M110002642. <https://doi.org/10.1074/mcp.M110.002642>
73. Vandenbunder, B., Fourre, N., Leray, A., Mueller, F., Volkel, P., Angrand, P. O., Heliot, L. (2014) PRC1 components exhibit different binding kinetics in Polycomb bodies. Biol. Cell 106, 111-125. <https://doi.org/10.1111/boc.201300077>
74. Voncken, J. W., Schweizer, D., Aagaard, L., Sattler, L., Jantsch, M. F., Van Lohuizen, M. (1999) Chromatin-association of the Polycomb group protein BMI1 is cell cycleregulated and correlates with its phosphorylation status. J. Cell Sci. 112(Pt 24), 4627-4639. <https://doi.org/10.1242/jcs.112.24.4627>
75. Wang, H., Wang, L., Erdjument-Bromage, H., Vidal, M., Tempst, P., Jones, R. S., Zhang, Y. (2004) Role of histone H2A ubiquitination in Polycomb silencing. Nature 431, 873-878. <https://doi.org/10.1038/nature02985>
76. West, A. G., Gaszner, M., Felsenfeld, G. (2002) Insulators: many functions, many mechanisms. Genes Dev. 16, 271-288. <https://doi.org/10.1101/gad.954702>
77. Yang, N., Wang, J., Li, J., Wang, Q. H., Wang, Y., Cheng, M. S. (2011) A three-dimensional pharmacophore model for IMPDH inhibitors. Chem. Biol. Drug Des. 78, 175-182. <https://doi.org/10.1111/j.1747-0285.2011.01128.x>
78. Zhang, T., Sun, Y., Tian, E., Deng, H., Zhang, Y., Luo, X., Cai, Q., Wang, H., Chai, J., Zhang, H. (2006) RNA-binding proteins SOP-2 and SOR-1 form a novel PcG-like complex in C. elegans. Development 133, 1023-1033. <https://doi.org/10.1242/dev.02275>
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Submissions

Archive