KAP1 Represses Differentiation-Inducible Genes in Embryonic Stem Cells through Cooperative Binding with PRC1 and Derepresses Pluripotency-Associated Genes

REFERENCES

• Kerppola TK. 2009. Polycomb group complexes—many combinations, many functions. Trends Cell Biol. 19:692–704. http://dx.doi.org/10.1016/j.tcb.2009.10.001.
   PubMed Web of Science ®Google Scholar
• Ogawa H, Ishiguro K, Gaubatz S, Livingston DM, Nakatani Y. 2002. A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in G(0) cells. Science 296:1132–1136. http://dx.doi.org/10.1126/science.1069861.
   PubMed Web of Science ®Google Scholar
• Gearhart MD, Corcoran CM, Wamstad JA, Bardwell VJ. 2006. Polycomb group and SCF ubiquitin ligases are found in a novel BCOR complex that is recruited to BCL6 targets. Mol. Cell. Biol. 26:6880–6889. http://dx.doi.org/10.1128/MCB.00630-06.
   PubMed Web of Science ®Google Scholar
• Sánchez C, Sánchez I, Demmers JAA, 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. http://dx.doi.org/10.1074/mcp.M600275-MCP200.
   PubMedGoogle Scholar
• Boukarabila H, Saurin AJ, Batsche E, Mossadegh N, van Lohuizen M, Otte AP, Pradel J, Muchardt C, Sieweke M, Duprez E. 2009. The PRC1 polycomb group complex interacts with PLZF/RARA to mediate leukemic transformation. Genes Dev. 23:1195–1206. http://dx.doi.org/10.1101/gad.512009.
   PubMed Web of Science ®Google Scholar
• Ren X, Kerppola TK. 2011. REST interacts with Cbx proteins and regulates polycomb repressive complex 1 occupancy at RE1 elements. Mol. Cell. Biol. 31:2100–2110. http://dx.doi.org/10.1128/MCB.05088-11.
   PubMedGoogle Scholar
• Vandamme J, Volkel P, Rosnoblet C, Le Faou P, Angrand PO. 2011. Interaction proteomics analysis of polycomb proteins defines distinct PRC1 complexes in mammalian cells. Mol. Cell. Proteomics 10:M110.002642. http://dx.doi.org/10.1074/mcp.M110.002642.
   PubMed Web of Science ®Google Scholar
• Endoh M, Endo TA, Endoh T, Fujimura YI, Ohara O, Toyoda T, Otte AP, Okano M, Brockdorff N, Vidal M, Koseki H. 2008. Polycomb group proteins Ring1A/B are functionally linked to the core transcriptional regulatory circuitry to maintain ES cell identity. Development 135:1513–1524. http://dx.doi.org/10.1242/dev.014340.
   PubMedGoogle Scholar
• Dietrich N, Lerdrup M, Landt E, Agrawal-Singh S, Bak M, Tommerup N, Rappsilber J, Sodersten E, Hansen K. 2012. REST-mediated recruitment of polycomb repressor complexes in mammalian cells. PLoS Genet. 8:e1002494. http://dx.doi.org/10.1371/journal.pgen.1002494.
   PubMed Web of Science ®Google Scholar
• Farcas AM, Blackledge NP, Sudbery I, Long HK, McGouran JF, Rose NR, Lee S, Sims D, Cerase A, Sheahan TW, Koseki H, Brockdorff N, Ponting CP, Kessler BM, Klose RJ. 2012. KDM2B links the polycomb repressive complex 1 (PRC1) to recognition of CpG islands. eLife 1:e00205. http://dx.doi.org/10.7554/eLife.00205.
   PubMed Web of Science ®Google Scholar
• Wu X, Johansen Jens V, Helin K. 2013. Fbxl10/Kdm2b recruits polycomb repressive complex 1 to CpG islands and regulates H2A ubiquitylation. Mol. Cell 49:1134–1146. http://dx.doi.org/10.1016/j.molcel.2013.01.016.
   PubMed Web of Science ®Google Scholar
• He J, Shen L, Wan M, Taranova O, Wu H, Zhang Y. 2013. Kdm2b maintains murine embryonic stem cell status by recruiting PRC1 complex to CpG islands of developmental genes. Nat. Cell Biol. 15:373–384. http://dx.doi.org/10.1038/ncb2702.
   PubMed Web of Science ®Google Scholar
• Schoeftner S, Sengupta AK, Kubicek S, Mechtler K, Spahn L, Koseki H, Jenuwein T, Wutz A. 2006. Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J. 25:3110–3122. http://dx.doi.org/10.1038/sj.emboj.7601187.
   PubMed Web of Science ®Google Scholar
• Vincenz C, Kerppola TK. 2008. Different polycomb group CBX family proteins associate with distinct regions of chromatin using nonhomologous protein sequences. Proc. Natl. Acad. Sci. U. S. A. 105:16572–16577. http://dx.doi.org/10.1073/pnas.0805317105.
   PubMedGoogle Scholar
• Puschendorf M, Terranova R, Boutsma E, Mao XH, Isono KI, Brykczynska U, Kolb C, Otte AP, Koseki H, Orkin SH, van Lohuizen M, Peters AHFM. 2008. PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat. Genet. 40:411–420. http://dx.doi.org/10.1038/ng.99.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1016/j.cell.2011.12.029.
   PubMed Web of Science ®Google Scholar
• Hu G, Kim J, Xu Q, Leng Y, Orkin SH, Elledge SJ. 2009. A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal. Genes Dev. 23:837–848. http://dx.doi.org/10.1101/gad.1769609.
   PubMed Web of Science ®Google Scholar
• Friedman JR, Fredericks WJ, Jensen DE, Speicher DW, Huang XP, Neilson EG, Rauscher FJIII. 1996. KAP-1, a novel corepressor for the highly conserved KRAB repression domain. Genes Dev. 10:2067–2078. http://dx.doi.org/10.1101/gad.10.16.2067.
   PubMed Web of Science ®Google Scholar
• Kim SS, Chen YM, O'Leary E, Witzgall R, Vidal M, Bonventre JV. 1996. A novel member of the RING finger family, KRIP-1, associates with the KRAB-A transcriptional repressor domain of zinc finger proteins. Proc. Natl. Acad. Sci. U. S. A. 93:15299–15304. http://dx.doi.org/10.1073/pnas.93.26.15299.
   PubMedGoogle Scholar
• Ryan RF, Schultz DC, Ayyanathan K, Singh PB, Friedman JR, Fredericks WJ, Rauscher FJIII. 1999. KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Krüppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol. Cell. Biol. 19:4366–4378.
   PubMed Web of Science ®Google Scholar
• Wang C, Rauscher FJIII, Cress WD, Chen J. 2007. Regulation of E2F1 function by the nuclear corepressor KAP1. J. Biol. Chem. 282:29902–29909. http://dx.doi.org/10.1074/jbc.M704757200.
   PubMedGoogle Scholar
• Cammas F, Mark M, Dolle P, Dierich A, Chambon P, Losson R. 2000. Mice lacking the transcriptional corepressor TIF1beta are defective in early postimplantation development. Development 127:2955–2963.
   PubMed Web of Science ®Google Scholar
• Voncken JW, Roelen BA, Roefs M, de Vries S, Verhoeven E, Marino S, Deschamps J, van Lohuizen M. 2003. Rnf2 (Ring1b) deficiency causes gastrulation arrest and cell cycle inhibition. Proc. Natl. Acad. Sci. U. S. A. 100:2468–2473. http://dx.doi.org/10.1073/pnas.0434312100.
   PubMed Web of Science ®Google Scholar
• Leeb M, Wutz A. 2007. Ring1B is crucial for the regulation of developmental control genes and PRC1 proteins but not X inactivation in embryonic cells. J. Cell Biol. 178:219–229. http://dx.doi.org/10.1083/jcb.200612127.
   PubMedGoogle Scholar
• van der Stoop P, Boutsma EA, Hulsman D, Noback S, Heimerikx M, Kerkhoven RM, Voncken JW, Wessels LF, van Lohuizen M. 2008. Ubiquitin E3 ligase Ring1b/Rnf2 of polycomb repressive complex 1 contributes to stable maintenance of mouse embryonic stem cells. PLoS One 3:e2235. http://dx.doi.org/10.1371/journal.pone.0002235.
   PubMedGoogle Scholar
• Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, Maillard PV, Layard-Liesching H, Verp S, Marquis J, Spitz F, Constam DB, Trono D. 2010. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463:237–240. http://dx.doi.org/10.1038/nature08674.
   PubMed Web of Science ®Google Scholar
• Leeb M, Pasini D, Novatchkova M, Jaritz M, Helin K, Wutz A. 2010. Polycomb complexes act redundantly to repress genomic repeats and genes. Genes Dev. 24:265–276. http://dx.doi.org/10.1101/gad.544410.
   PubMed Web of Science ®Google Scholar
• Maksakova IA, Thompson PJ, Goyal P, Jones SJ, Singh PB, Karimi MM, Lorincz MC. 2013. Distinct roles of KAP1, HP1 and G9a/GLP in silencing of the two-cell-specific retrotransposon MERVL in mouse ES cells. Epigenetics Chromatin 6:15. http://dx.doi.org/10.1186/1756-8935-6-15.
   PubMed Web of Science ®Google Scholar
• Herzog M, Wendling O, Guillou F, Chambon P, Mark M, Losson R, Cammas F. 2011. TIF1beta association with HP1 is essential for post-gastrulation development, but not for Sertoli cell functions during spermatogenesis. Dev. Biol. 350:548–558. http://dx.doi.org/10.1016/j.ydbio.2010.12.014.
   PubMedGoogle Scholar
• Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ. 2003. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 425:962–967. http://dx.doi.org/10.1038/nature02060.
   PubMed Web of Science ®Google Scholar
• Park IK, Qian DL, Kiel M, Becker MW, Pihalja M, Weissman IL, Morrison SJ, Clarke MF. 2003. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 423:302–305. http://dx.doi.org/10.1038/nature01587.
   PubMed Web of Science ®Google Scholar
• Iwama A, Oguro H, Negishi M, Kato Y, Morita Y, Tsukui H, Ema H, Kamijo T, Katoh-Fukui Y, Koseki H, van Lohuizen M, Nakauchi H. 2004. Enhanced self-renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity 21:843–851. http://dx.doi.org/10.1016/j.immuni.2004.11.004.
   PubMed Web of Science ®Google Scholar
• Pietersen AM, Evers B, Prasad AA, Tanger E, Cornelissen-Steijger P, Jonkers J, van Lohuizen M. 2008. Bmi1 regulates stem cells and proliferation and differentiation of committed cells in mammary epithelium. Curr. Biol. 18:1094–1099. http://dx.doi.org/10.1016/j.cub.2008.06.070.
   PubMed Web of Science ®Google Scholar
• Zhou X-F, Yu J, Chang M, Zhang M, Zhou D, Cammas F, Sun S-C. 2012. TRIM28 mediates chromatin modifications at the TCRα enhancer and regulates the development of T and natural killer T cells. Proc. Natl. Acad. Sci. U. S. A. 109:20083–20088. http://dx.doi.org/10.1073/pnas.1214704109.
   PubMedGoogle Scholar
• Barde I, Rauwel B, Marin-Florez RM, Corsinotti A, Laurenti E, Verp S, Offner S, Marquis J, Kapopoulou A, Vanicek J, Trono D. 2013. A KRAB/KAP1-miRNA cascade regulates erythropoiesis through stage-specific control of mitophagy. Science 340:350–353. http://dx.doi.org/10.1126/science.1232398.
   PubMedGoogle Scholar
• Santoni de Sio FR, Massacand J, Barde I, Offner S, Corsinotti A, Kapopoulou A, Bojkowska K, Dagklis A, Fernandez M, Ghia P, Thomas JH, Pinschewer D, Harris N, Trono D. 2012. KAP1 regulates gene networks controlling mouse B-lymphoid cell differentiation and function. Blood 119:4675–4685. http://dx.doi.org/10.1182/blood-2011-12-401117.
   PubMedGoogle Scholar
• Bojkowska K, Aloisio F, Cassano M, Kapopoulou A, Santoni de Sio F, Zangger N, Offner S, Cartoni C, Thomas C, Quenneville S, Johnsson K, Trono D. 2012. Liver-specific ablation of Krüppel-associated box-associated protein 1 in mice leads to male-predominant hepatosteatosis and development of liver adenoma. Hepatology 56:1279–1290. http://dx.doi.org/10.1002/hep.25767.
   PubMedGoogle Scholar
• Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, Bell GW, Otte AP, Vidal M, Gifford DK, Young RA, Jaenisch R. 2006. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441:349–353. http://dx.doi.org/10.1038/nature04733.
   PubMed Web of Science ®Google Scholar
• Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, Mikkelsen TS, Presser A, Nusbaum C, Xie X, Chi AS, Adli M, Kasif S, Ptaszek LM, Cowan CA, Lander ES, Koseki H, Bernstein BE. 2008. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4:e1000242. http://dx.doi.org/10.1371/journal.pgen.1000242.
   PubMed Web of Science ®Google Scholar
• Iyengar S, Ivanov AV, Jin VX, Rauscher FJIII, Farnham PJ. 2011. Functional analysis of KAP1 genomic recruitment. Mol. Cell. Biol. 31:1833–1847. http://dx.doi.org/10.1128/MCB.01331-10.
   PubMedGoogle Scholar
• Quenneville S, Verde G, Corsinotti A, Kapopoulou A, Jakobsson J, Offner S, Baglivo I, Pedone PV, Grimaldi G, Riccio A, Trono D. 2011. In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Mol. Cell 44:361–372. http://dx.doi.org/10.1016/j.molcel.2011.08.032.
   PubMed Web of Science ®Google Scholar
• Yu M, Mazor T, Huang H, Huang HT, Kathrein KL, Woo AJ, Chouinard CR, Labadorf A, Akie TE, Moran TB, Xie H, Zacharek S, Taniuchi I, Roeder RG, Kim CF, Zon LI, Fraenkel E, Cantor AB. 2012. Direct recruitment of polycomb repressive complex 1 to chromatin by core binding transcription factors. Mol. Cell 45:330–343. http://dx.doi.org/10.1016/j.molcel.2011.11.032.
   PubMed Web of Science ®Google Scholar
• Ziv Y, Bielopolski D, Galanty Y, Lukas C, Taya Y, Schultz DC, Lukas J, Bekker-Jensen S, Bartek J, Shiloh Y. 2006. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat. Cell Biol. 8:870–876. http://dx.doi.org/10.1038/ncb1446.
   PubMed Web of Science ®Google Scholar
• Ren X, Vincenz C, Kerppola TK. 2008. Changes in the distributions and dynamics of polycomb repressive complexes during embryonic stem cell differentiation. Mol. Cell. Biol. 28:2884–2895. http://dx.doi.org/10.1128/MCB.00949-07.
   PubMed Web of Science ®Google Scholar
• Elderkin S, Maertens GN, Endoh M, Mallery DL, Morrice N, Koseki H, Peters G, Brockdorff N, Hiom K. 2007. A phosphorylated form of mel-18 targets the Ring1B histone H2A ubiquitin ligase to chromatin. Mol. Cell 28:107–120. http://dx.doi.org/10.1016/j.molcel.2007.08.009.
   PubMed Web of Science ®Google Scholar
• Katoh-Fukui Y, Tsuchiya R, Shiroishi T, Nakahara Y, Hashimoto N, Noguchi K, Higashinakagawa T. 1998. Male-to-female sex reversal in M33 mutant mice. Nature 393:688–692. http://dx.doi.org/10.1038/31482.
   PubMed Web of Science ®Google Scholar
• 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. http://dx.doi.org/10.1016/j.molcel.2012.01.002.
   PubMed Web of Science ®Google Scholar
• Hu CD, Chinenov Y, Kerppola TK. 2002. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9:789–798. http://dx.doi.org/10.1016/S1097-2765(02)00496-3.
   PubMed Web of Science ®Google Scholar
• Doss M, Chen S, Winkler J, Hippler-Altenburg R, Odenthal M, Wickenhauser C, Balaraman S, Schulz H, Hummel O, Hubner N, Ghosh-Choudhury N, Sotiriadou I, Hescheler J, Sachinidis A. 2007. Transcriptomic and phenotypic analysis of murine embryonic stem cell derived BMP2+ lineage cells: an insight into mesodermal patterning. Genome Biol. 8:R184. http://dx.doi.org/10.1186/gb-2007-8-9-r184.
   PubMedGoogle Scholar
• Rowe HM, Kapopoulou A, Corsinotti A, Fasching L, Macfarlan TS, Tarabay Y, Viville S, Jakobsson J, Pfaff SL, Trono D. 2013. TRIM28 repression of retrotransposon-based enhancers is necessary to preserve transcriptional dynamics in embryonic stem cells. Genome Res. 23:452–461. http://dx.doi.org/10.1101/gr.147678.112.
   PubMed Web of Science ®Google Scholar
• Meylan S, Groner AC, Ambrosini G, Malani N, Quenneville S, Zangger N, Kapopoulou A, Kauzlaric A, Rougemont J, Ciuffi A, Bushman FD, Bucher P, Trono D. 2011. A gene-rich, transcriptionally active environment and the pre-deposition of repressive marks are predictive of susceptibility to KRAB/KAP1-mediated silencing. BMC Genomics 12:378. http://dx.doi.org/10.1186/1471-2164-12-378.
   PubMed Web of Science ®Google Scholar
• Hosoya T, Clifford M, Losson R, Tanabe O, Engel JD. 2013. TRIM28 is essential for erythroblast differentiation in the mouse. Blood 122:3798–3807. http://dx.doi.org/10.1182/blood-2013-04-496166.
   PubMedGoogle Scholar