Regulation of Genome Architecture and Function by Polycomb Proteins

Trends in Cell Biology

Volumn 26, Issue 7, 2016, Pages 511-525

  Entrevan, Marianne ^a   Schuettengruber, Bernd ^a   Cavalli, Giacomo ^a  

^a UNIV MONTPELLIER   (France)

Author keywords

Chromatin organization; Chromosome architecture; Epigenetics; Gene regulation; Polycomb group

Indexed keywords

BMI1 PROTEIN; POLYCOMB PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN; UNCLASSIFIED DRUG; POLYCOMB GROUP PROTEIN;

BINDING SITE; CELL DIFFERENTIATION; CHROMATIN; DROSOPHILA; ECTOPIC EXPRESSION; ENHANCER REGION; GENE ACTIVATION; GENE REPRESSION; GENE SILENCING; GLOBAL CHANGE; NONHUMAN; OLIGOMERIZATION; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN METHYLATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; UBIQUITINATION; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; GENETIC EPIGENESIS; GENOME; HUMAN; METABOLISM;

ANIMALS; CHROMATIN; EPIGENESIS, GENETIC; GENOME; HUMANS; MODELS, BIOLOGICAL; POLYCOMB-GROUP PROTEINS;

EID: 84967121127     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2016.04.009     Document Type: Review

References (133)

1. Ptashne M. On the use of the word 'epigenetic'. Curr. Biol. 2007, 17:R233-R236.
2. Sexton T., Cavalli G. The role of chromosome domains in shaping the functional genome. Cell 2015, 160:1049-1059.
3. Di Croce L., Helin K. Transcriptional regulation by Polycomb group proteins. Nat. Struct. Mol. Biol. 2013, 20:1147-1155.
4. Lewis E.B. A gene complex controlling segmentation in Drosophila. Nature 1978, 276:565-570.
5. Duncan I.M. Polycomblike: a gene that appears to be required for the normal expression of the bithorax and antennapedia gene complexes of Drosophila melanogaster. Genetics 1982, 102:49-70.
6. Schuettengruber B., Cavalli G. Recruitment of Polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 2009, 136:3531-3542.
7. Aranda S., et al. Regulation of gene transcription by Polycomb proteins. Sci. Adv. 2015, 1:e1500737.
8. de Napoles M., et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell 2004, 7:663-676.
9. Wang H., et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature 2004, 431:873-878.
10. Fischle W., et al. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 2003, 17:1870-1881.
11. Min J., et al. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev. 2003, 17:1823-1828.
12. Tavares L., et al. RYBP-PRC1 complexes mediate H2A ubiquitylation at Polycomb target sites independently of PRC2 and H3K27me3. Cell 2012, 148:664-678.
13. Basu A., et al. YY1 DNA binding and interaction with YAF2 is essential for Polycomb recruitment. Nucleic Acids Res. 2014, 42:2208-2223.
14. Lo S.M., et al. Polycomb group protein Suppressor 2 of zeste is a functional homolog of Posterior Sex Combs. Mol. Cell Biol. 2009, 29:515-525.
15. Francis N.J., et al. Reconstitution of a functional core Polycomb repressive complex. Mol. Cell 2001, 8:545-556.
16. Lagarou A., et al. dKDM2 couples histone H2A ubiquitylation to histone H3 demethylation during Polycomb group silencing. Genes Dev. 2008, 22:2799-2810.
17. Gearhart M.D., et al. Polycomb group and SCF ubiquitin ligases are found in a novel BCOR complex that is recruited to BCL6 targets. Mol. Cell Biol. 2006, 26:6880-6889.
18. Sanchez C., et al. Proteomics analysis of Ring1B/Rnf2 interactors identifies a novel complex with the Fbxl10/Jhdm1B histone demethylase and the Bcl6 interacting corepressor. Mol. Cell Proteomics 2007, 6:820-834.
19. Pasini D., et al. Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J. 2004, 23:4061-4071.
20. Muller J., et al. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 2002, 111:197-208.
21. Cao R., Zhang Y. The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr. Opin. Genet. Dev. 2004, 14:155-164.
22. Margueron R., et al. Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol. Cell 2008, 32:503-518.
23. Shen X., et al. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol. Cell 2008, 32:491-502.
24. Hansen K.H., et al. A model for transmission of the H3K27me3 epigenetic mark. Nat. Cell Biol. 2008, 10:1291-1300.
25. Margueron R., et al. Role of the Polycomb protein EED in the propagation of repressive histone marks. Nature 2009, 461:762-767.
26. Ciferri C., et al. Molecular architecture of human Polycomb repressive complex 2. Elife 2012, 1:e00005.
27. Satrimafitrah P., et al. RbAp48 is essential for viability of vertebrate cells and plays a role in chromosome stability. Chromosome Res. 2015.
28. Anderson A.E., et al. The enhancer of trithorax and Polycomb gene Caf1/p55 is essential for cell survival and patterning in Drosophila development. Development 2011, 138:1957-1966.
29. Nekrasov M., et al. Nucleosome binding and histone methyltransferase activity of Drosophila PRC2. EMBO Rep. 2005, 6:348-353.
30. Nekrasov M., et al. Pcl-PRC2 is needed to generate high levels of H3-K27 trimethylation at Polycomb target genes. EMBO J. 2007, 26:4078-4088.
31. Sarma K., et al. Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo. Mol. Cell Biol. 2008, 28:2718-2731.
32. Cao R., Zhang Y. SUZ12 is required for both the histone methyltransferase activity and the silencing function of the EED-EZH2 complex. Mol. Cell 2004, 15:57-67.
33. Kim H., et al. AEBP2 as a potential targeting protein for Polycomb repression complex PRC2. Nucleic Acids Res. 2009, 37:2940-2950.
34. Peng J.C., et al. Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 2009, 139:1290-1302.
35. Zhang Z., et al. PRC2 complexes with JARID2, MTF2, and esPRC2p48 in ES cells to modulate ES cell pluripotency and somatic cell reprogramming. Stem Cells 2011, 29:229-240.
36. da Rocha S.T., et al. Jarid2 Is implicated in the initial xist-induced targeting of PRC2 to the inactive X chromosome. Mol. Cell 2014, 53:301-316.
37. Landeira D., et al. Jarid2 is a PRC2 component in embryonic stem cells required for multi-lineage differentiation and recruitment of PRC1 and RNA polymerase II to developmental regulators. Nat. Cell Biol. 2010, 12:618-624.
38. Pasini D., et al. JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 2010, 464:306-310.
39. Son J., et al. Nucleosome-binding activities within JARID2 and EZH1 regulate the function of PRC2 on chromatin. Genes Dev. 2013, 27:2663-2677.
40. Klymenko T., et al. A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev. 2006, 20:1110-1122.
41. Lecona E., et al. Polycomb protein SCML2 regulates the cell cycle by binding and modulating CDK/CYCLIN/p21 complexes. PLoS Biol. 2013, 11:e1001737.
42. Ray P., et al. Combgap contributes to recruitment of Polycomb group proteins in Drosophila. Proc. Natl. Acad Sci. U.S.A. 2016, 113:3826-3831.
43. Kassis J.A., Brown J.L. Polycomb group response elements in Drosophila and vertebrates. Adv. Genet. 2013, 81:83-118.
44. Wang L., et al. Hierarchical recruitment of Polycomb group silencing complexes. Mol. Cell 2004, 14:637-646.
45. Pasini D., et al. The Polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell Biol. 2007, 27:3769-3779.
46. Grimm C., et al. Molecular recognition of histone lysine methylation by the Polycomb group repressor dSfmbt. EMBO J. 2009, 28:1965-1977.
47. Kim C.A., et al. Structural organization of a sex-comb-on-midleg/polyhomeotic copolymer. J. Biol. Chem. 2005, 280:27769-27775.
48. Peterson A.J., et al. A domain shared by the Polycomb group proteins Scm and ph mediates heterotypic and homotypic interactions. Mol. Cell Biol. 1997, 17:6683-6692.
49. Peterson A.J., et al. Requirement for sex comb on midleg protein interactions in Drosophila Polycomb group repression. Genetics 2004, 167:1225-1239.
50. Blackledge N.P., et al. Variant PRC1 complex-dependent H2A ubiquitylation drives PRC2 recruitment and Polycomb domain formation. Cell 2014, 157:1445-1459.
51. Cooper S., et al. Targeting Polycomb to pericentric heterochromatin in embryonic stem cells reveals a role for H2AK119u1 in PRC2 recruitment. Cell Rep. 2014, 7:1456-1470.
52. Kalb R., et al. Histone H2A monoubiquitination promotes histone H3 methylation in Polycomb repression. Nat. Struct. Mol. Biol. 2014, 21:569-571.
53. Kahn T.G., et al. Combinatorial interactions are required for the efficient recruitment of pho repressive complex (PhoRC) to Polycomb response elements. PLoS Genet. 2014, 10:e1004495.
54. Schuettengruber B., et al. Cooperativity, specificity, and evolutionary stability of Polycomb targeting in Drosophila. Cell Rep. 2014, 9:219-233.
55. Mendenhall E.M., et al. GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet. 2010, 6:e1001244.
56. Riising E.M., et al. Gene silencing triggers Polycomb repressive complex 2 recruitment to CpG islands genome wide. Mol. Cell 2014, 55:347-360.
57. Farcas A.M., et al. KDM2B links the Polycomb repressive complex 1 (PRC1) to recognition of CpG islands. Elife 2012, 1:e00205.
58. Wu X., et al. Fbxl10/Kdm2b recruits Polycomb repressive complex 1 to CpG islands and regulates H2A ubiquitylation. Mol. Cell 2013, 49:1134-1146.
59. Klose R.J., et al. Chromatin sampling - an emerging perspective on targeting Polycomb repressor proteins. PLoS Genet. 2013, 9:e1003717.
60. van Heeringen S.J., et al. Principles of nucleation of H3K27 methylation during embryonic development. Genome Res. 2014, 24:401-410.
61. Kim H., et al. AEBP2 as a transcriptional activator and its role in cell migration. Genomics 2015, 105:108-115.
62. Dietrich N., et al. REST-mediated recruitment of Polycomb repressor complexes in mammalian cells. PLoS Genet. 2012, 8:e1002494.
63. Ren X., Kerppola T.K. REST interacts with Cbx proteins and regulates Polycomb repressive complex 1 occupancy at RE1 elements. Mol. Cell Biol. 2011, 31:2100-2110.
64. Yu M., et al. Direct recruitment of Polycomb repressive complex 1 to chromatin by core binding transcription factors. Mol. Cell 2012, 45:330-343.
65. Attwooll C., et al. A novel repressive E2F6 complex containing the Polycomb group protein, EPC1, that interacts with EZH2 in a proliferation-specific manner. J. Biol. Chem. 2005, 280:1199-1208.
66. Ogawa H., et al. A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in G0 cells. Science 2002, 296:1132-1136.
67. Trimarchi J.M., et al. The E2F6 transcription factor is a component of the mammalian Bmi1-containing Polycomb complex. Proc. Natl. Acad Sci. U.S.A. 2001, 98:1519-1524.
68. Herranz N., et al. Polycomb complex 2 is required for E-cadherin repression by the Snail1 transcription factor. Mol. Cell Biol. 2008, 28:4772-4781.
69. Londhe P., Davie J.K. Interferon-gamma resets muscle cell fate by stimulating the sequential recruitment of JARID2 and PRC2 to promoters to repress myogenesis. Sci. Signal 2013, 6:ra107.
70. Ku M., et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 2008, 4:e1000242.
71. Vella P., et al. Yin Yang 1 extends the Myc-related transcription factors network in embryonic stem cells. Nucleic Acids Res. 2012, 40:3403-3418.
72. Matharu N.K., et al. Vertebrate homologue of Drosophila GAGA factor. J. Mol. Biol. 2010, 400:434-447.
73. Bauer M., et al. The quest for mammalian Polycomb response elements: are we there yet?. Chromosoma 2015.
74. Brockdorff N. Noncoding RNA and Polycomb recruitment. RNA 2013, 19:429-442.
75. Pengelly A.R., et al. A histone mutant reproduces the phenotype caused by loss of histone-modifying factor Polycomb. Science 2013, 339:698-699.
76. Chopra V.S., et al. The Polycomb group mutant esc leads to augmented levels of paused Pol II in the Drosophila embryo. Mol. Cell 2011, 42:837-844.
77. Nakagawa T., et al. Deubiquitylation of histone H2A activates transcriptional initiation via trans-histone cross-talk with H3K4 di- and trimethylation. Genes Dev. 2008, 22:37-49.
78. Zhou W., et al. Histone H2A monoubiquitination represses transcription by inhibiting RNA polymerase II transcriptional elongation. Mol. Cell 2008, 29:69-80.
79. Stock J.K., et al. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat. Cell Biol. 2007, 9:1428-1435.
80. Pengelly A.R., et al. Transcriptional repression by PRC1 in the absence of H2A monoubiquitylation. Genes Dev. 2015, 29:1487-1492.
81. Tie F., et al. Polycomb inhibits histone acetylation by CBP by binding directly to its catalytic domain. Proc. Natl. Acad Sci. U.S.A. 2016, 113:E744-E753.
82. Francis N.J., et al. Chromatin compaction by a Polycomb group protein complex. Science 2004, 306:1574-1577.
83. Eskeland R., et al. Histone acetylation and the maintenance of chromatin compaction by Polycomb repressive complexes. Cold Spring Harb Symp. Quant. Biol. 2010, 75:71-78.
84. Yuan W., et al. Dense chromatin activates Polycomb repressive complex 2 to regulate H3 lysine 27 methylation. Science 2012, 337:971-975.
85. Ebert A., et al. Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes Dev. 2004, 18:2973-2983.
86. Ferrari K.J., et al. Polycomb-dependent H3K27me1 and H3K27me2 regulate active transcription and enhancer fidelity. Mol. Cell 2014, 53:49-62.
87. Jung H.R., et al. Quantitative mass spectrometry of histones H3.2 and H3.3 in Suz12-deficient mouse embryonic stem cells reveals distinct, dynamic post-translational modifications at Lys-27 and Lys-36. Mol. Cell Proteomics 2010, 9:838-850.
88. Peters A.H., et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 2003, 12:1577-1589.
89. Voigt P., et al. Asymmetrically modified nucleosomes. Cell 2012, 151:181-193.
90. Lee H.G., et al. Genome-wide activities of Polycomb complexes control pervasive transcription. Genome Res. 2015, 25:1170-1181.
91. Lanzuolo C., et al. Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Nat. Cell Biol. 2007, 9:1167-1174.
92. Comet I., et al. A chromatin insulator driving three-dimensional Polycomb Response Element (PRE) contacts and Polycomb association with the chromatin fiber. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:2294-2299.
93. Gonzalez I., et al. Identification of regulators of the three-dimensional Polycomb organization by a microscopy-based genome-wide RNAi screen. Mol. Cell 2014, 54:485-499.
94. Hernandez-Munoz I., et al. Association of BMI1 with Polycomb bodies is dynamic and requires PRC2/EZH2 and the maintenance DNA methyltransferase DNMT1. Mol. Cell Biol. 2005, 25:11047-11058.
95. Cheutin T., Cavalli G. Polycomb silencing: from linear chromatin domains to 3D chromosome folding. Curr. Opin. Genet. Dev. 2014, 25C:30-37.
96. Tiwari V.K., et al. PcG proteins, DNA methylation, and gene repression by chromatin looping. PLoS Biol. 2008, 6:2911-2927.
97. Bantignies F., et al. Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila. Cell 2011, 144:214-226.
98. Schuettengruber B., Cavalli G. Polycomb domain formation depends on short and long distance regulatory cues. PLoS ONE 2013, 8:e56531.
99. Bantignies F., et al. Inheritance of Polycomb-dependent chromosomal interactions in Drosophila. Genes Dev. 2003, 17:2406-2420.
100. Li H.B., et al. Insulators target active genes to transcription factories and Polycomb-repressed genes to Polycomb bodies. PLoS Genet. 2013, 9:e1003436.
101. Denholtz M., et al. Long-range chromatin contacts in embryonic stem cells reveal a role for pluripotency factors and Polycomb proteins in genome organization. Cell Stem Cell 2013, 13:602-616.
102. Vieux-Rochas M., et al. Clustering of mammalian Hox genes with other H3K27me3 targets within an active nuclear domain. Proc. Natl. Acad Sci. U.S.A. 2015, 112:4672-4677.
103. Joshi O., et al. Dynamic reorganization of extremely long-range promoter-promoter interactions between two states of pluripotency. Cell Stem Cell 2015, 17:748-757.
104. Schoenfelder S., et al. Polycomb repressive complex PRC1 spatially constrains the mouse embryonic stem cell genome. Nat. Genet. 2015, 47:1179-1186.
105. Kondo T., et al. Polycomb in transcriptional phase transition of developmental genes. Trends Biochem. Sci. 2016, 41:9-19.
106. Sanborn A.L., et al. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc. Natl. Acad Sci. U.S.A. 2015, 112:E6456-E6465.
107. Dixon J.R., et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
108. Vietri Rudan M., et al. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep. 2015, 10:1297-1309.
109. Dowen J.M., et al. Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 2014, 159:374-387.
110. Sexton T., et al. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 2012, 148:458-472.
111. Narendra V., et al. CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science 2015, 347:1017-1021.
112. Noordermeer D., et al. Temporal dynamics and developmental memory of 3D chromatin architecture at Hox gene loci. Elife 2014, 3:e02557.
113. Noordermeer D., et al. The dynamic architecture of Hox gene clusters. Science 2011, 334:222-225.
114. Nora E.P., et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012, 485:381-385.
115. Wijchers P.J., et al. Cause and consequence of tethering a subTAD to different nuclear compartments. Mol. Cell 2016, 61:461-473.
116. Isono K., et al. SAM domain polymerization links subnuclear clustering of PRC1 to gene silencing. Dev. Cell 2013, 26:565-577.
117. Wani A.H., et al. Chromatin topology is coupled to Polycomb group protein subnuclear organization. Nat. Commun. 2016, 7:10291.
118. Gambetta M.C., Muller J. O-GlcNAcylation prevents aggregation of the Polycomb group repressor Polyhomeotic. Dev. Cell 2014, 31:629-639.
119. Boettiger A.N., et al. Super-resolution imaging reveals distinct chromatin folding for different epigenetic states. Nature 2016, 529:418-422.
120. Follmer N.E., et al. A Polycomb group protein is retained at specific sites on chromatin in mitosis. PLoS Genet. 2012, 8:e1003135.
121. Fiedler T., Rehmsmeier M. jPREdictor: a versatile tool for the prediction of cis-regulatory elements. Nucleic Acids Res. 2006, 34:W546-W550.
122. Ringrose L., et al. Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster. Dev. Cell 2003, 5:759-771.
123. Schuettengruber B., et al. Functional anatomy of Polycomb and Trithorax chromatin landscapes in Drosophila embryos. PLoS Biol. 2009, 7:e13.
124. Brookes E., et al. Polycomb associates genome-wide with a specific RNA polymerase II variant, and regulates metabolic genes in ESCs. Cell Stem Cell 2012, 10:157-170.
125. Frangini A., et al. The Aurora B kinase and the Polycomb protein ring1B combine to regulate active promoters in quiescent lymphocytes. Mol. Cell 2013, 51:647-661.
126. Kaneko S., et al. PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells. Nat. Struct. Mol. Biol. 2013, 20:1258-1264.
127. Mousavi K., et al. Polycomb protein Ezh1 promotes RNA polymerase II elongation. Mol. Cell 2012, 45:255-262.
128. van den Boom V., et al. Non-canonical PRC1.1 targets active genes independent of H3K27me3 and is essential for leukemogenesis. Cell Rep. 2016, 14:332-346.
129. Creppe C., et al. A Cbx8-containing Polycomb complex facilitates the transition to gene activation during ES cell differentiation. PLoS Genet. 2014, 10:e1004851.
130. Morey L., et al. Polycomb regulates mesoderm cell fate-specification in embryonic stem cells through activation and repression mechanisms. Cell Stem Cell 2015, 17:300-315.
131. Gao Z., et al. An AUTS2-Polycomb complex activates gene expression in the CNS. Nature 2014, 516:349-354.
132. Lv X., et al. A positive role for Polycomb in transcriptional regulation via H4K20me1. Cell Res. 2016, 2016.
133. Arora M., et al. RING1A and BMI1 bookmark active genes via ubiquitination of chromatin-associated proteins. Nucleic Acids Res. 2016, 44:2136-2144.