From Flies to Mice: The Emerging Role of Non-Canonical PRC1 Members in Mammalian Development
Abstract
:1. Introduction
1.1. Discovery of the Polycomb Repressor System
1.2. Evolutionarily Conserved Domains in PcG Proteins
1.3. Discovery of Polycomb Repressive Complexes
2. Mammalian PRC Complexes
2.1. Mammalian PcG Gene Functions: Parallels and Differences between Mammals and Fruit Fly
2.2. Classification of Mammalian PRC Complexes
3. Canonical PRC1 Complexes
4. Studying Mammalian PcG Functions with Embryonic Stem Cell and Mouse Models
4.1. Advantages of Mouse Models in Studying Gene Function during Development
- Mice are experimentally tractable mammalian model systems.
- Mice have short reproducing time, easy to breed and maintain.
- Mice have relatively short gestation (20 days) and big litter size (5 to 15 pups), brief time for sexual maturity and rapid generation time, which makes an ideal model for studying embryonic development.
- Mice have small size and are easy to handle.
- Mice have close similarities with human development and disease.
- The genome size, number of genes and genomic organization of mice are similar to humans.
- Mice are suitable for derivation of stem cells, such as ES cells, which can be re-introduced to the mouse germline.
4.2. Advantages of ES Cells in Studying Gene Function during Development
- If required, ES cells lines can be newly established from mice or other species (e.g., bovine, pig) by isolating morula or blastocyst stage embryos [198].
- There are reproducible experimental conditions and a more serum/animal free environment (small molecules, inhibitors and proteins).
- Well scalable thus high throughput experiments can be executed.
- There is no limitation of starting material due to unlimited self-renewal.
- ES cells can be differentiated to all cell types of the body.
- Differentiation conditions can be tightly controlled, which is highly desired for industrial applications.
- Culture conditions for maintaining ES cells and for differentiating them could be internationally standardized conferring high reproducibility to the experimental systems.
- Finally, studying human development by the utilization of existing and approved human ES cell lines [199] circumvents the ethical barriers, as it does not require destruction of preimplantation human embryos.
5. General Description of Mammalian ncPRC1s
6. Core Subunits of ncPRCs
6.1. Core Members of ncPRCs
6.2. The Function of Yy1
6.3. Detailed Description of the Composition and Function of Different ncPRC1 Type Complexes
6.3.1. ncPRC1.1
6.3.2. ncPRC1.2 and ncPRC1.4
6.3.3. ncPRC1.3 and ncPRC1.5
6.3.4. ncPRC1.6
7. Targeting of Different ncPRC1 Complexes
8. Conclusions and Future Questions
8.1. There Are Profound Differences in PRC Function between Fly and Mice
8.2. The Function of ncPRC1 Subunits Are often Essential for Mammalian Development
8.3. The Dosage and Interactions of ncPRC1 Subunits Is Critical for Mammalian Development
8.4. The Assembly of ncPRC1 Subunits Is still under Debate
8.5. The Activator Function of ncPRC1s Opens New Perspectives in Gene Regulation
8.6. More Emphasis Is Placed on Integrative Approaches to Analyze ncPRC1 Functions in Differentiation
8.7. NcPRCs Have a Profound Role in Extraembryonic Lineage Commitment
8.8. The Role of ccPRCs in Initiating and Maintaining Naïve vs. Primed Pluripotent States Are Not Established
9. Concluding Remarks
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Lewis, P.H. New mutants. Drosoph. Inf. Serv. 1947, 21, 69. [Google Scholar]
- Lewis, P.H. Pc: Polycomb. Drosoph. Inf. Serv. 1949, 21, 69. [Google Scholar]
- Schuettengruber, B.; Bourbon, H.-M.; Di Croce, L.; Cavalli, G. Genome Regulation by Polycomb and Trithorax: 70 Years and Counting. Cell 2017, 171, 34–57. [Google Scholar] [CrossRef] [PubMed]
- Lewis, E.B. A gene complex controlling segmentation in Drosophila. Nature 1978, 276, 565–570. [Google Scholar] [CrossRef] [PubMed]
- Sánchez-Herrero, E.; Vernós, I.; Marco, R.; Morata, G. Genetic organization of Drosophila bithorax complex. Nature 1985, 313, 108–113. [Google Scholar] [CrossRef] [PubMed]
- Tiong, S.; Bone, L.M.; Whittle, J.R. Recessive lethal mutations within the bithorax-complex in Drosophila. Mol. Gen. Genet. 1985, 200, 335–342. [Google Scholar] [CrossRef] [PubMed]
- Karch, F.; Weiffenbach, B.; Peifer, M.; Bender, W.; Duncan, I.; Celniker, S.; Crosby, M.; Lewis, E.B. The abdominal region of the bithorax complex. Cell 1985, 43, 81–96. [Google Scholar] [CrossRef]
- Peifer, M.; Karch, F.; Bender, W. The Bithorax complex: Control of segmental identity. Genes Dev. 1987, 1, 891–898. [Google Scholar] [CrossRef]
- Bowman, S.K.; Deaton, A.M.; Domingues, H.; Wang, P.I.; Sadreyev, R.I.; Kingston, R.E.; Bender, W. H3K27 modifications define segmental regulatory domains in the Drosophila bithorax complex. eLife 2014, 3, e02833. [Google Scholar] [CrossRef] [PubMed]
- Maeda, R.K.; Karch, F. The open for business model of the bithorax complex in Drosophila. Chromosoma 2015, 124, 293–307. [Google Scholar] [CrossRef] [PubMed]
- Maeda, R.K.; Karch, F. The ABC of the BX-C: The bithorax complex explained. Development 2006, 133, 1413–1422. [Google Scholar] [CrossRef] [PubMed]
- Bajusz, I.; Sipos, L.; Pirity, M.K. Nucleotide substitutions revealing specific functions of Polycomb group genes. Mol. Genet. Metab. 2015, 114, 547–556. [Google Scholar] [CrossRef] [PubMed]
- Geisler, S.J.; Paro, R. Trithorax and Polycomb group-dependent regulation: A tale of opposing activities. Development 2015, 142, 2876–2887. [Google Scholar] [CrossRef] [PubMed]
- Schuettengruber, B.; Ganapathi, M.; Leblanc, B.; Portoso, M.; Jaschek, R.; Tolhuis, B.; van Lohuizen, M.; Tanay, A.; Cavalli, G. Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLoS Biol. 2009, 7, e13. [Google Scholar] [CrossRef] [PubMed]
- Denell, R.E.; Frederick, R.D. Homoeosis in Drosophila: A description of the Polycomb lethal syndrome. Dev. Biol. 1983, 97, 34–47. [Google Scholar] [CrossRef]
- Simon, J.; Chiang, A.; Bender, W. Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products. Development 1992, 114, 493–505. [Google Scholar] [PubMed]
- Landecker, H.L.; Sinclair, D.A.R.; Brock, H.W. Screen for enhancers of Polycomb and Polycomblike in Drosophila melanogaster. Dev. Genet. 1994, 15, 425–434. [Google Scholar] [CrossRef] [PubMed]
- Nüsslein-Volhard, C.; Wieschaus, E.; Kluding, H. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster—I. Zygotic loci on the second chromosome. Wilhelm Roux’s Arch. Dev. Biol. 1984, 193, 267–282. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [PubMed]
- Kennison, J.A.; Tamkun, J.W. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc. Natl. Acad. Sci. USA 1988, 85, 8136–8140. [Google Scholar] [CrossRef] [PubMed]
- Jürgens, G. A group of genes controlling the spatial expression of the bithorax complex in Drosophila. Nature 1985, 316, 153–155. [Google Scholar] [CrossRef]
- Struhl, G. A gene product required for correct initiation of segmental determination in Drosophila. Nature 1981, 293, 36–41. [Google Scholar] [CrossRef] [PubMed]
- Struhl, G. Role of the esc+ gene product in ensuring the selective expression of segment-specific homeotic genes in Drosophila. J. Embryol. Exp. Morphol. 1983, 76, 297–331. [Google Scholar] [PubMed]
- Gehring, W. A recessive lethal [l(4)29] with a homeotic effect in D. melanogaster. Drosoph. Inf. Serv. 1970, 45, 5. [Google Scholar]
- Phillips, M.D.; Shearn, A. Mutations in polycombeotic, a Drosophila polycomb-group gene, cause a wide range of maternal and zygotic phenotypes. Genetics 1990, 125, 91–101. [Google Scholar] [PubMed]
- Jones, R.S.; Gelbart, W.M. Genetic analysis of the enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster. Genetics 1990, 126, 185–199. [Google Scholar] [PubMed]
- Ingham, P.W. A gene that regulates the bithorax complex differentially in larval and adult cells of Drosophila. Cell 1984, 37, 815–823. [Google Scholar] [CrossRef]
- Santamaría, P.; Randsholt, N.B. Characterization of a region of the X chromosome of Drosophila including multi sex combs (mxc), a Polycomb group gene which also functions as a tumour suppressor. Mol. Gen. Genet. 1995, 246, 282–290. [Google Scholar] [CrossRef] [PubMed]
- Campbell, R.B.; Sinclair, D.A.; Couling, M.; Brock, H.W. Genetic interactions and dosage effects of Polycomb group genes of Drosophila. Mol. Gen. Genet. 1995, 246, 291–300. [Google Scholar] [CrossRef] [PubMed]
- Dura, J.M.; Brock, H.W.; Santamaria, P. Polyhomeotic: A gene of Drosophila melanogaster required for correct expression of segmental identity. Mol. Gen. Genet. 1985, 198, 213–220. [Google Scholar] [CrossRef] [PubMed]
- Sato, T.; Russell, M.A.; Denell, R.E. Homoeosis in Drosophila: A new enhancer of polycomb and related homoeotic mutations. Genetics 1983, 105, 357–370. [Google Scholar] [PubMed]
- Bejarano, F.; González, I.; Vidal, M.; Busturia, A. The Drosophila RYBP gene functions as a Polycomb-dependent transcriptional repressor. Mech. Dev. 2005, 122, 1118–1129. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez, I.; Aparicio, R.; Busturia, A. Functional Characterization of the dRYBP Gene in Drosophila. Genetics 2008, 179, 1373–1388. [Google Scholar] [CrossRef] [PubMed]
- Brunk, B.P.; Martin, E.C.; Adler, P.N. Drosophila genes Posterior Sex Combs and Suppressor two of zeste encode proteins with homology to the murine bmi-1 oncogene. Nature 1991, 353, 351–353. [Google Scholar] [CrossRef] [PubMed]
- Soto, M.C.; Chou, T.B.; Bender, W. Comparison of germline mosaics of genes in the Polycomb group of Drosophila melanogaster. Genetics 1995, 140, 231–243. [Google Scholar] [PubMed]
- Beuchle, D.; Struhl, G.; Müller, J. Polycomb group proteins and heritable silencing of Drosophila Hox genes. Development 2001, 128, 993–1004. [Google Scholar] [PubMed]
- de Ayala Alonso, A.G.; Gutierrez, L.; Fritsch, C.; Papp, B.; Beuchle, D.; Muller, J. A Genetic Screen Identifies Novel Polycomb Group Genes in Drosophila. Genetics 2007, 176, 2099–2108. [Google Scholar] [CrossRef] [PubMed]
- Gutiérrez, L.; Oktaba, K.; Scheuermann, J.C.; Gambetta, M.C.; Ly-Hartig, N.; Müller, J. The role of the histone H2A ubiquitinase Sce in Polycomb repression. Development 2012, 139, 117–127. [Google Scholar] [CrossRef] [PubMed]
- Yamamoto, Y.; Girard, F.; Bello, B.; Affolter, M.; Gehring, W.J. The cramped gene of Drosophila is a member of the Polycomb-group, and interacts with mus209, the gene encoding Proliferating Cell Nuclear Antigen. Development 1997, 124, 3385–3394. [Google Scholar] [PubMed]
- Klymenko, T.; Papp, B.; Fischle, W.; Köcher, T.; Schelder, M.; Fritsch, C.; Wild, B.; Wilm, M.; Müller, J. A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev. 2006, 20, 1110–1122. [Google Scholar] [CrossRef] [PubMed]
- Birve, A.; Sengupta, A.K.; Beuchle, D.; Larsson, J.; Kennison, J.A.; Rasmuson-Lestander, A.; Müller, J. Su(z)12, a novel Drosophila Polycomb group gene that is conserved in vertebrates and plants. Development 2001, 128, 3371–3379. [Google Scholar] [PubMed]
- Schwartz, Y.B.; Pirrotta, V. Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 2007, 8, 9–22. [Google Scholar] [CrossRef] [PubMed]
- Paro, R. Mechanisms of heritable gene repression during development of Drosophila. Curr. Opin. Cell Biol. 1993, 5, 999–1005. [Google Scholar] [CrossRef]
- Struhl, G.; Akam, M. Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J. 1985, 4, 3259–3264. [Google Scholar] [PubMed]
- Wedeen, C.; Harding, K.; Levine, M. Spatial regulation of Antennapedia and bithorax gene expression by the Polycomb locus in Drosophila. Cell 1986, 44, 739–748. [Google Scholar] [CrossRef]
- Dura, J.M.; Ingham, P. Tissue- and stage-specific control of homeotic and segmentation gene expression in Drosophila embryos by the polyhomeotic gene. Development 1988, 103, 733–741. [Google Scholar] [PubMed]
- Paro, R. Imprinting a determined state into the chromatin of Drosophila. Trends Genet. 1990, 6, 416–421. [Google Scholar] [CrossRef]
- Ji, J.-Y.; Miles, W.O.; Korenjak, M.; Zheng, Y.; Dyson, N.J. In Vivo Regulation of E2F1 by Polycomb Group Genes in Drosophila. G3 Genes|Genomes|Genetics 2012, 2, 1651–1660. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martinez, A.-M.; Colomb, S.; Déjardin, J.; Bantignies, F.; Cavalli, G. Polycomb group-dependent Cyclin A repression in Drosophila. Genes Dev. 2006, 20, 501–513. [Google Scholar] [CrossRef] [PubMed]
- Levine, S.S.; Weiss, A.; Erdjument-Bromage, H.; Shao, Z.; Tempst, P.; Kingston, R.E. The core of the polycomb repressive complex is compositionally and functionally conserved in flies and humans. Mol. Cell. Biol. 2002, 22, 6070–6078. [Google Scholar] [CrossRef] [PubMed]
- Vandamme, J.; Völkel, P.; Rosnoblet, C.; Le Faou, P.; Angrand, P.-O. Interaction Proteomics Analysis of Polycomb Proteins Defines Distinct PRC1 Complexes in Mammalian Cells. Mol. Cell. Proteom. 2011, 10, M110.002642. [Google Scholar] [CrossRef] [PubMed]
- Gao, Z.; Zhang, J.; Bonasio, R.; Strino, F.; Sawai, A.; Parisi, F.; Kluger, Y.; Reinberg, D. PCGF Homologs, CBX Proteins, and RYBP Define Functionally Distinct PRC1 Family Complexes. Mol. Cell 2012, 45, 344–356. [Google Scholar] [CrossRef] [PubMed]
- Paro, R.; Hogness, D.S. The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc. Natl. Acad. Sci. USA 1991, 88, 263–267. [Google Scholar] [CrossRef] [PubMed]
- Festenstein, R.; Sharghi-Namini, S.; Fox, M.; Roderick, K.; Tolaini, M.; Norton, T.; Saveliev, A.; Kioussis, D.; Singh, P. Heterochromatin protein 1 modifies mammalian PEV in a dose- and chromosomal-context-dependent manner. Nat. Genet. 1999, 23, 457–461. [Google Scholar] [CrossRef] [PubMed]
- Muller, H.J. Types of visible variations induced by X-rays in Drosophila. J. Genet. 1930, 22, 299–334. [Google Scholar] [CrossRef]
- Gowen, J.W.; Gay, E.H. Eversporting as a Function of the Y-Chromosome in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 1933, 19, 122–126. [Google Scholar] [CrossRef] [PubMed]
- Messmer, S.; Franke, A.; Paro, R. Analysis of the functional role of the Polycomb chromo domain in Drosophila melanogaster. Genes Dev. 1992, 6, 1241–1254. [Google Scholar] [CrossRef] [PubMed]
- Fitzgerald, D.P.; Bender, W. Polycomb group repression reduces DNA accessibility. Mol. Cell. Biol. 2001, 21, 6585–6597. [Google Scholar] [CrossRef] [PubMed]
- Boettiger, A.N.; Bintu, B.; Moffitt, J.R.; Wang, S.; Beliveau, B.J.; Fudenberg, G.; Imakaev, M.; Mirny, L.A.; Wu, C.; Zhuang, X. Super-resolution imaging reveals distinct chromatin folding for different epigenetic states. Nature 2016, 529, 418–422. [Google Scholar] [CrossRef] [PubMed]
- Kundu, S.; Ji, F.; Sunwoo, H.; Jain, G.; Lee, J.T.; Sadreyev, R.I.; Dekker, J.; Kingston, R.E. Polycomb Repressive Complex 1 Generates Discrete Compacted Domains that Change during Differentiation. Mol. Cell 2017, 65, 432–446.e5. [Google Scholar] [CrossRef] [PubMed]
- Platero, J.S.; Hartnett, T.; Eissenberg, J.C. Functional analysis of the chromo domain of HP1. EMBO J. 1995, 14, 3977–3986. [Google Scholar] [PubMed]
- Tschiersch, B.; Hofmann, A.; Krauss, V.; Dorn, R.; Korge, G.; Reuter, G. The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J. 1994, 13, 3822–3831. [Google Scholar] [PubMed]
- Orlando, V. Polycomb, epigenomes, and control of cell identity. Cell 2003, 112, 599–606. [Google Scholar] [CrossRef]
- Alvarez-Venegas, R.; Avramova, Z. SET-domain proteins of the Su(var)3-9, E(z) and trithorax families. Gene 2002, 285, 25–37. [Google Scholar] [CrossRef]
- Tachibana, M.; Sugimoto, K.; Fukushima, T.; Shinkai, Y. SET Domain-containing Protein, G9a, Is a Novel Lysine-preferring Mammalian Histone Methyltransferase with Hyperactivity and Specific Selectivity to Lysines 9 and 27 of Histone H3. J. Biol. Chem. 2001, 276, 25309–25317. [Google Scholar] [CrossRef] [PubMed]
- Czermin, B.; Melfi, R.; McCabe, D.; Seitz, V.; Imhof, A.; Pirrotta, V. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 2002, 111, 185–196. [Google Scholar] [CrossRef]
- Müller, 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. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 2002, 111, 197–208. [Google Scholar] [CrossRef]
- Kuzmichev, A.; Nishioka, K.; Erdjument-Bromage, H.; Tempst, P.; Reinberg, D. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 2002, 16, 2893–2905. [Google Scholar] [CrossRef] [PubMed]
- van Lohuizen, M.; Frasch, M.; Wientjens, E.; Berns, A. Sequence similarity between the mammalian bmi-1 proto-oncogene and the Drosophila regulatory genes Psc and Su(z)2. Nature 1991, 353, 353–355. [Google Scholar] [CrossRef] [PubMed]
- Asano, H.; Ishida, A.; Hasegawa, M.; Ono, T.; Yoshida, M.C.; Taniguchi, M.; Kanno, M. The mouse Mel-18 “RING-finger” gene: Genomic organization, promoter analysis and chromosomal assignment. DNA Seq. 1993, 3, 369–377. [Google Scholar] [CrossRef] [PubMed]
- Martinez-Noel, G.; Niedenthal, R.; Tamura, T.; Harbers, K. A family of structurally related RING finger proteins interacts specifically with the ubiquitin-conjugating enzyme UbcM4. FEBS Lett. 1999, 454, 257–261. [Google Scholar] [PubMed]
- Lorick, K.L.; Jensen, J.P.; Fang, S.; Ong, A.M.; Hatakeyama, S.; Weissman, A.M. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl. Acad. Sci. USA 1999, 96, 11364–11369. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Wang, L.; Erdjument-Bromage, H.; Vidal, M.; Tempst, P.; Jones, R.S.; Zhang, Y. Role of histone H2A ubiquitination in Polycomb silencing. Nature 2004, 431, 873–878. [Google Scholar] [CrossRef] [PubMed]
- Peterson, A.J.; Kyba, M.; Bornemann, D.; Morgan, K.; Brock, H.W.; Simon, J. A domain shared by the Polycomb group proteins Scm and ph mediates heterotypic and homotypic interactions. Mol. Cell. Biol. 1997, 17, 6683–6692. [Google Scholar] [CrossRef] [PubMed]
- Kim, C.A.; Gingery, M.; Pilpa, R.M.; Bowie, J.U. The SAM domain of polyhomeotic forms a helical polymer. Nat. Struct. Biol. 2002, 9, 453–457. [Google Scholar] [CrossRef] [PubMed]
- Gambetta, M.C.; Müller, J. O-GlcNAcylation prevents aggregation of the Polycomb group repressor polyhomeotic. Dev. Cell 2014, 31, 629–639. [Google Scholar] [CrossRef] [PubMed]
- Robinson, A.K.; Leal, B.Z.; Chadwell, L.V.; Wang, R.; Ilangovan, U.; Kaur, Y.; Junco, S.E.; Schirf, V.; Osmulski, P.A.; Gaczynska, M.; et al. The Growth-Suppressive Function of the Polycomb Group Protein Polyhomeotic Is Mediated by Polymerization of Its Sterile Alpha Motif (SAM) Domain. J. Biol. Chem. 2012, 287, 8702–8713. [Google Scholar] [CrossRef] [PubMed]
- Wani, A.H.; Boettiger, A.N.; Schorderet, P.; Ergun, A.; Münger, C.; Sadreyev, R.I.; Zhuang, X.; Kingston, R.E.; Francis, N.J. Chromatin topology is coupled to Polycomb group protein subnuclear organization. Nat. Commun. 2016, 7, 10291. [Google Scholar] [CrossRef] [PubMed]
- Qiao, F.; Bowie, J.U. The many faces of SAM. Sci. STKE 2005, 2005, re7. [Google Scholar] [CrossRef] [PubMed]
- Akasaka, T.; Kanno, M.; Balling, R.; Mieza, M.A.; Taniguchi, M.; Koseki, H. A role for mel-18, a Polycomb group-related vertebrate gene, during theanteroposterior specification of the axial skeleton. Development 1996, 122, 1513–1522. [Google Scholar] [PubMed]
- Gould, A. Functions of mammalian Polycomb group and trithorax group related genes. Curr. Opin. Genet. Dev. 1997, 7, 488–494. [Google Scholar] [CrossRef]
- 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. Identification and characterization of interactions between the vertebrate polycomb-group protein BMI1 and human homologs of polyhomeotic. Mol. Cell. Biol. 1997, 17, 2326–2335. [Google Scholar] [CrossRef] [PubMed]
- Fisher, C.L.; Lee, I.; Bloyer, S.; Bozza, S.; Chevalier, J.; Dahl, A.; Bodner, C.; Helgason, C.D.; Hess, J.L.; Humphries, R.K.; et al. Additional sex combs-like 1 belongs to the enhancer of trithorax and polycomb group and genetically interacts with Cbx2 in mice. Dev. Biol. 2010, 337, 9–15. [Google Scholar] [CrossRef] [PubMed]
- Lanzuolo, C.; Orlando, V. Memories from the Polycomb Group Proteins. Annu. Rev. Genet. 2012, 46, 561–589. [Google Scholar] [CrossRef] [PubMed]
- Grossniklaus, U.; Paro, R. Transcriptional Silencing by Polycomb-Group Proteins. Cold Spring Harb. Perspect. Biol. 2014, 6, a019331. [Google Scholar] [CrossRef] [PubMed]
- Goodrich, J.; Puangsomlee, P.; Martin, M.; Long, D.; Meyerowitz, E.M.; Coupland, G. A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 1997, 386, 44–51. [Google Scholar] [CrossRef] [PubMed]
- Springer, N.M.; Danilevskaya, O.N.; Hermon, P.; Helentjaris, T.G.; Phillips, R.L.; Kaeppler, H.F.; Kaeppler, S.M. Sequence Relationships, Conserved Domains, and Expression Patterns for Maize Homologs of the Polycomb Group Genes E(z), esc, and E(Pc). PLANT Physiol. 2002, 128, 1332–1345. [Google Scholar] [CrossRef] [PubMed]
- Köhler, C.; Makarevich, G. Epigenetic mechanisms governing seed development in plants. EMBO Rep. 2006, 7, 1223–1227. [Google Scholar] [CrossRef] [PubMed]
- Derkacheva, M.; Hennig, L. Variations on a theme: Polycomb group proteins in plants. J. Exp. Bot. 2014, 65, 2769–2784. [Google Scholar] [CrossRef] [PubMed]
- Calonje, M. PRC1 Marks the Difference in Plant PcG Repression. Mol. Plant 2014, 7, 459–471. [Google Scholar] [CrossRef] [PubMed]
- Pu, L.; Sung, Z.R. PcG and trxG in plants—Friends or foes. Trends Genet. 2015, 31, 252–262. [Google Scholar] [CrossRef] [PubMed]
- Köhler, C.; Villar, C.B.R. Programming of gene expression by Polycomb group proteins. Trends Cell Biol. 2008, 18, 236–243. [Google Scholar] [CrossRef] [PubMed]
- Roure, V.; Bantignies, F. Polycomb group-mediated gene silencing mechanisms: Stability versus flexibility. Epigenomics 2009, 1, 301–318. [Google Scholar] [CrossRef] [PubMed]
- Morey, L.; Helin, K. Polycomb group protein-mediated repression of transcription. Trends Biochem. Sci. 2010, 35, 323–332. [Google Scholar] [CrossRef] [PubMed]
- Trask, M.C.; Mager, J. Complexity of polycomb group function: Diverse mechanisms of target specificity. J. Cell. Physiol. 2011, 226, 1719–1721. [Google Scholar] [CrossRef] [PubMed]
- Franke, A.; DeCamillis, M.; Zink, D.; Cheng, N.; Brock, H.W.; Paro, R. Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster. EMBO J. 1992, 11, 2941–2950. [Google Scholar] [PubMed]
- Tie, F.; Furuyama, T.; Harte, P.J. The Drosophila Polycomb Group proteins ESC and E(Z) bind directly to each other and co-localize at multiple chromosomal sites. Development 1998, 125, 3483–3496. [Google Scholar] [PubMed]
- Saurin, A.J.; Shao, Z.; Erdjument-Bromage, H.; Tempst, P.; Kingston, R.E. A Drosophila Polycomb group complex includes Zeste and dTAFII proteins. Nature 2001, 412, 655–660. [Google Scholar] [CrossRef] [PubMed]
- Simon, J.A.; Kingston, R.E. Mechanisms of Polycomb gene silencing: Knowns and unknowns. Nat. Rev. Mol. Cell Biol. 2009, 10, 697–708. [Google Scholar] [CrossRef] [PubMed]
- Bárdos, J.I.; Saurin, A.J.; Tissot, C.; Duprez, E.; Freemont, P.S. HPC3 Is a New Human Polycomb Orthologue That Interacts and Associates with RING1 and Bmi1 and Has Transcriptional Repression Properties. J. Biol. Chem. 2000, 275, 28785–28792. [Google Scholar] [CrossRef] [PubMed]
- Satijn, D.P.; Otte, A.P. Polycomb group protein complexes: Do different complexes regulate distinct target genes? Biochim. Biophys. Acta 1999, 1447, 1–16. [Google Scholar] [CrossRef]
- Francis, N.J.; Saurin, A.J.; Shao, Z.; Kingston, R.E. Reconstitution of a functional core polycomb repressive complex. Mol. Cell 2001, 8, 545–556. [Google Scholar] [CrossRef]
- King, I.F.G.; Emmons, R.B.; Francis, N.J.; Wild, B.; Müller, J.; Kingston, R.E.; Wu, C.-T. Analysis of a polycomb group protein defines regions that link repressive activity on nucleosomal templates to in vivo function. Mol. Cell. Biol. 2005, 25, 6578–6591. [Google Scholar] [CrossRef] [PubMed]
- Francis, N.J.; Kingston, R.E.; Woodcock, C.L. Chromatin Compaction by a Polycomb Group Protein Complex. Science 2004, 306, 1574–1577. [Google Scholar] [CrossRef] [PubMed]
- Buchwald, G.; van der Stoop, P.; Weichenrieder, O.; Perrakis, A.; van Lohuizen, M.; Sixma, T.K. Structure and E3-ligase activity of the Ring–Ring complex of Polycomb proteins Bmi1 and Ring1b. EMBO J. 2006, 25, 2465–2474. [Google Scholar] [CrossRef] [PubMed]
- Eskeland, R.; Leeb, M.; Grimes, G.R.; Kress, C.; Boyle, S.; Sproul, D.; Gilbert, N.; Fan, Y.; Skoultchi, A.I.; Wutz, A.; et al. Ring1B Compacts Chromatin Structure and Represses Gene Expression Independent of Histone Ubiquitination. Mol. Cell 2010, 38, 452–464. [Google Scholar] [CrossRef] [PubMed]
- Gearhart, M.D.; Corcoran, C.M.; Wamstad, J.A.; Bardwell, V.J. 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. [Google Scholar] [CrossRef] [PubMed]
- Sánchez, C.; Sánchez, I.; Demmers, J.A.A.; Rodriguez, P.; Strouboulis, J.; Vidal, M. Proteomics Analysis of Ring1B/Rnf2 Interactors Identifies a Novel Complex with the Fbxl10/Jhdm1B Histone Demethylase and the Bcl6 Interacting Corepressor. Mol. Cell. Proteom. 2007, 6, 820–834. [Google Scholar] [CrossRef] [PubMed]
- Lagarou, A.; Mohd-Sarip, A.; Moshkin, Y.M.; Chalkley, G.E.; Bezstarosti, K.; Demmers, J.A.A.; Verrijzer, C.P. dKDM2 couples histone H2A ubiquitylation to histone H3 demethylation during Polycomb group silencing. Genes Dev. 2008, 22, 2799–2810. [Google Scholar] [CrossRef] [PubMed]
- Cao, R.; Wang, L.; Wang, H.; Xia, L.; Erdjument-Bromage, H.; Tempst, P.; Jones, R.S.; Zhang, Y. Role of Histone H3 Lysine 27 Methylation in Polycomb-Group Silencing. Science. 2002, 298, 1039–1043. [Google Scholar] [CrossRef] [PubMed]
- Rea, S.; Eisenhaber, F.; O’Carroll, D.; Strahl, B.D.; Sun, Z.-W.; Schmid, M.; Opravil, S.; Mechtler, K.; Ponting, C.P.; Allis, C.D.; et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 2000, 406, 593–599. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Pasini, D.; Bracken, A.P.; Jensen, M.R.; Lazzerini Denchi, E.; Helin, K. Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J. 2004, 23, 4061–4071. [Google Scholar] [CrossRef] [PubMed]
- Ketel, C.S.; Andersen, E.F.; Vargas, M.L.; Suh, J.; Strome, S.; Simon, J.A. Subunit contributions to histone methyltransferase activities of fly and worm polycomb group complexes. Mol. Cell. Biol. 2005, 25, 6857–6868. [Google Scholar] [CrossRef] [PubMed]
- Nekrasov, M.; Wild, B.; Müller, J. Nucleosome binding and histone methyltransferase activity of Drosophila PRC2. EMBO Rep. 2005, 6, 348–353. [Google Scholar] [CrossRef] [PubMed]
- Montgomery, N.D.; Yee, D.; Chen, A.; Kalantry, S.; Chamberlain, S.J.; Otte, A.P.; Magnuson, T. The Murine Polycomb Group Protein Eed Is Required for Global Histone H3 Lysine-27 Methylation. Curr. Biol. 2005, 15, 942–947. [Google Scholar] [CrossRef] [PubMed]
- Nekrasov, M.; Klymenko, T.; Fraterman, S.; Papp, B.; Oktaba, K.; Köcher, T.; Cohen, A.; Stunnenberg, H.G.; Wilm, M.; Müller, J. Pcl-PRC2 is needed to generate high levels of H3-K27 trimethylation at Polycomb target genes. EMBO J. 2007, 26, 4078–4088. [Google Scholar] [CrossRef] [PubMed]
- Li, G.; Margueron, R.; Ku, M.; Chambon, P.; Bernstein, B.E.; Reinberg, D. Jarid2 and PRC2, partners in regulating gene expression. Genes Dev. 2010, 24, 368–380. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.; Kang, K.; Kim, J. AEBP2 as a potential targeting protein for Polycomb Repression Complex PRC2. Nucleic Acids Res. 2009, 37, 2940–2950. [Google Scholar] [CrossRef] [PubMed]
- Aldiri, I.; Vetter, M.L. PRC2 during vertebrate organogenesis: A complex in transition. Dev. Biol. 2012, 367, 91–99. [Google Scholar] [CrossRef] [PubMed]
- Veneti, Z.; Gkouskou, K.; Eliopoulos, A. Polycomb Repressor Complex 2 in Genomic Instability and Cancer. Int. J. Mol. Sci. 2017, 18, 1657. [Google Scholar] [CrossRef] [PubMed]
- Moritz, L.E.; Trievel, R.C. Structure, mechanism, and regulation of polycomb repressive complex 2. J. Biol. Chem. 2017. [Google Scholar] [CrossRef] [PubMed]
- Fischle, W.; Wang, Y.; Jacobs, S.A.; Kim, Y.; Allis, C.D.; Khorasanizadeh, S. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 2003, 17, 1870–1881. [Google Scholar] [CrossRef] [PubMed]
- Blackledge, N.P.; Farcas, A.M.; Kondo, T.; King, H.W.; McGouran, J.F.; Hanssen, L.L. P.; Ito, S.; Cooper, S.; Kondo, K.; Koseki, Y.; et al. Variant PRC1 Complex-Dependent H2A Ubiquitylation Drives PRC2 Recruitment and Polycomb Domain Formation. Cell 2014, 157, 1445–1459. [Google Scholar] [CrossRef] [PubMed]
- Cooper, S.; Dienstbier, M.; Hassan, R.; Schermelleh, L.; Sharif, J.; Blackledge, N.P.; De Marco, V.; Elderkin, S.; Koseki, H.; Klose, R.; 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. [Google Scholar] [CrossRef] [PubMed]
- Kalb, R.; Latwiel, S.; Baymaz, H.I.; Jansen, P.W.T.C.; Müller, C.W.; Vermeulen, M.; Müller, J. Histone H2A monoubiquitination promotes histone H3 methylation in Polycomb repression. Nat. Struct. Mol. Biol. 2014, 21, 569–571. [Google Scholar] [CrossRef] [PubMed]
- Müller, J.; Bienz, M. Long range repression conferring boundaries of Ultrabithorax expression in the Drosophila embryo. EMBO J. 1991, 10, 3147–3155. [Google Scholar] [PubMed]
- Simon, J.; Chiang, A.; Bender, W.; Shimell, M.J.; O’Connor, M. Elements of the Drosophila Bithorax Complex That Mediate Repression by Polycomb Group Products. Dev. Biol. 1993, 158, 131–144. [Google Scholar] [CrossRef] [PubMed]
- Chan, C.S.; Rastelli, L.; Pirrotta, V. A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J. 1994, 13, 2553–2564. [Google Scholar] [PubMed]
- Chiang, A.; O’Connor, M.B.; Paro, R.; Simon, J.; Bender, W. Discrete Polycomb-binding sites in each parasegmental domain of the bithorax complex. Development 1995, 121, 1681–1689. [Google Scholar] [PubMed]
- Schuettengruber, B.; Oded Elkayam, N.; Sexton, T.; Entrevan, M.; Stern, S.; Thomas, A.; Yaffe, E.; Parrinello, H.; Tanay, A.; Cavalli, G. Cooperativity, Specificity, and Evolutionary Stability of Polycomb Targeting in Drosophila. Cell Rep. 2014, 9, 219–233. [Google Scholar] [CrossRef] [PubMed]
- Ringrose, L.; Rehmsmeier, M.; Dura, J.-M.; Paro, R. Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster. Dev. Cell 2003, 5, 759–771. [Google Scholar] [CrossRef]
- Müller, J.; Kassis, J.A. Polycomb response elements and targeting of Polycomb group proteins in Drosophila. Curr. Opin. Genet. Dev. 2006, 16, 476–484. [Google Scholar] [CrossRef] [PubMed]
- Fritsch, C.; Brown, J.L.; Kassis, J.A.; Müller, J. The DNA-binding polycomb group protein pleiohomeotic mediates silencing of a Drosophila homeotic gene. Development 1999, 126, 3905–3913. [Google Scholar] [PubMed]
- Mihaly, J.; Mishra, R.K.; Karch, F. A conserved sequence motif in Polycomb-response elements. Mol. Cell 1998, 1, 1065–1066. [Google Scholar] [CrossRef]
- Poux, S.; Melfi, R.; Pirrotta, V. Establishment of Polycomb silencing requires a transient interaction between PC and ESC. Genes Dev. 2001, 15, 2509–2514. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Brown, J.L.; Cao, R.; Zhang, Y.; Kassis, J.A.; Jones, R.S. Hierarchical Recruitment of Polycomb Group Silencing Complexes. Mol. Cell 2004, 14, 637–646. [Google Scholar] [CrossRef] [PubMed]
- Brown, J.L.; Fritsch, C.; Mueller, J.; Kassis, J.A. The Drosophila pho-like gene encodes a YY1-related DNA binding protein that is redundant with pleiohomeotic in homeotic gene silencing. Development 2003, 130, 285–294. [Google Scholar] [CrossRef] [PubMed]
- Grimm, C.; Matos, R.; Ly-Hartig, N.; Steuerwald, U.; Lindner, D.; Rybin, V.; Müller, J.; Müller, C.W. Molecular recognition of histone lysine methylation by the Polycomb group repressor dSfmbt. EMBO J. 2009, 28, 1965–1977. [Google Scholar] [CrossRef] [PubMed]
- Frey, F.; Sheahan, T.; Finkl, K.; Stoehr, G.; Mann, M.; Benda, C.; Müller, J. Molecular basis of PRC1 targeting to Polycomb response elements by PhoRC. Genes Dev. 2016, 30, 1116–1127. [Google Scholar] [CrossRef] [PubMed]
- Kang, H.; McElroy, K.A.; Jung, Y.L.; Alekseyenko, A.A.; Zee, B.M.; Park, P.J.; Kuroda, M.I. Sex comb on midleg (Scm) is a functional link between PcG-repressive complexes in Drosophila. Genes Dev. 2015, 29, 1136–1150. [Google Scholar] [CrossRef] [PubMed]
- Scheuermann, J.C.; de Ayala Alonso, A.G.; Oktaba, K.; Ly-Hartig, N.; McGinty, R.K.; Fraterman, S.; Wilm, M.; Muir, T.W.; Müller, J. Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB. Nature 2010, 465, 243–247. [Google Scholar] [CrossRef] [PubMed]
- Dey, A.; Seshasayee, D.; Noubade, R.; French, D.M.; Liu, J.; Chaurushiya, M.S.; Kirkpatrick, D.S.; Pham, V.C.; Lill, J.R.; Bakalarski, C.E.; et al. Loss of the Tumor Suppressor BAP1 Causes Myeloid Transformation. Science 2012, 337, 1541–1546. [Google Scholar] [CrossRef] [PubMed]
- Müller, J.; Gaunt, S.; Lawrence, P.A. Function of the Polycomb protein is conserved in mice and flies. Development 1995, 121, 2847–2852. [Google Scholar] [PubMed]
- Gorfinkiel, N.; Fanti, L.; Melgar, T.; Garcı́a, E.; Pimpinelli, S.; Guerrero, I.; Vidal, M. The Drosophila Polycomb group gene Sex combs extra encodes the ortholog of mammalian Ring1 proteins. Mech. Dev. 2004, 121, 449–462. [Google Scholar] [CrossRef] [PubMed]
- Atchison, L.; Ghias, A.; Wilkinson, F.; Bonini, N.; Atchison, M.L. Transcription factor YY1 functions as a PcG protein in vivo. EMBO J. 2003, 22, 1347–1358. [Google Scholar] [CrossRef] [PubMed]
- Coré, N.; Bel, S.; Gaunt, S.J.; Aurrand-Lions, M.; Pearce, J.; Fisher, A.; Djabali, M. Altered cellular proliferation and mesoderm patterning in Polycomb-M33-deficient mice. Development 1997, 124, 721–729. [Google Scholar] [PubMed]
- van der Lugt, N.M.; Domen, J.; Linders, K.; van Roon, M.; Robanus-Maandag, E.; te Riele, H.; van der Valk, M.; Deschamps, J.; Sofroniew, M.; van Lohuizen, M. Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev. 1994, 8, 757–769. [Google Scholar] [CrossRef] [PubMed]
- Alkema, M.J.; van der Lugt, N.M.T.; Bobeldijk, R.C.; Berns, A.; van Lohuizen, M. Transformation of axial skeleton due to overexpression of bmi-1 in transgenic mice. Nature 1995, 374, 724–727. [Google Scholar] [CrossRef] [PubMed]
- Hanson, R.D.; Hess, J.L.; Yu, B.D.; Ernst, P.; van Lohuizen, M.; Berns, A.; van der Lugt, N.M.; Shashikant, C.S.; Ruddle, F.H.; Seto, M.; et al. Mammalian Trithorax and polycomb-group homologues are antagonistic regulators of homeotic development. Proc. Natl. Acad. Sci. USA 1999, 96, 14372–14377. [Google Scholar] [CrossRef] [PubMed]
- del Mar Lorente, M.; Marcos-Gutiérrez, C.; Pérez, C.; Schoorlemmer, J.; Ramírez, A.; Magin, T.; Vidal, M. Loss- and gain-of-function mutations show a polycomb group function for Ring1A in mice. Development 2000, 127, 5093–5100. [Google Scholar] [PubMed]
- Suzuki, M.; Mizutani-Koseki, Y.; Fujimura, Y.-I.; Miyagishima, H.; Kaneko, T.; Takada, Y.; Akasaka, T.; Tanzawa, H.; Takihara, Y.; Nakano, M.; Masumoto, H.; Vidal, M.; Isono, K.-I.; Koseki, H. Involvement of the Polycomb-group gene Ring1B in the specification of the anterior-posterior axis in mice. Development 2002, 129, 4171–4183. [Google Scholar] [PubMed]
- Lorente, M.; Pérez, C.; Sánchez, C.; Donohoe, M.; Shi, Y.; Vidal, M. Homeotic transformations of the axial skeleton of YY1 mutant mice and genetic interaction with the Polycomb group gene Ring1/Ring1A. Mech. Dev. 2006, 123, 312–320. [Google Scholar] [CrossRef] [PubMed]
- Takihara, Y.; Tomotsune, D.; Shirai, M.; Katoh-Fukui, Y.; Nishii, K.; Motaleb, M.A.; Nomura, M.; Tsuchiya, R.; Fujita, Y.; Shibata, Y.; et al. Targeted disruption of the mouse homologue of the Drosophila polyhomeotic gene leads to altered anteroposterior patterning and neural crest defects. Development 1997, 124, 3673–3682. [Google Scholar] [PubMed]
- Isono, K.-I.; Fujimura, Y.-I.; Shinga, J.; Yamaki, M.; O-Wang, J.; Takihara, Y.; Murahashi, Y.; Takada, Y.; Mizutani-Koseki, Y.; Koseki, H. Mammalian Polyhomeotic Homologues Phc2 and Phc1 Act in Synergy To Mediate Polycomb Repression of Hox Genes. Mol. Cell. Biol. 2005, 25, 6694–6706. [Google Scholar] [CrossRef] [PubMed]
- Bel, S.; Coré, N.; Djabali, M.; Kieboom, K.; Van der Lugt, N.; Alkema, M.J.; Van Lohuizen, M. Genetic interactions and dosage effects of Polycomb group genes in mice. Development 1998, 125, 3543–3551. [Google Scholar] [PubMed]
- Whitcomb, S.J.; Basu, A.; Allis, C.D.; Bernstein, E. Polycomb Group proteins: An evolutionary perspective. Trends Genet. 2007, 23, 494–502. [Google Scholar] [CrossRef] [PubMed]
- Schumacher, A.; Magnuson, T. Murine Polycomb- and trithorax-group genes regulate homeotic pathways and beyond. Trends Genet. 1997, 13, 167–170. [Google Scholar] [CrossRef]
- Prezioso, C.; Orlando, V. Polycomb proteins in mammalian cell differentiation and plasticity. FEBS Lett. 2011, 585, 2067–2077. [Google Scholar] [CrossRef] [PubMed]
- Ohta, H.; Sawada, A.; Kim, J.Y.; Tokimasa, S.; Nishiguchi, S.; Humphries, R.K.; Hara, J.; Takihara, Y. Polycomb group gene rae28 is required for sustaining activity of hematopoietic stem cells. J. Exp. Med. 2002, 195, 759–770. [Google Scholar] [CrossRef] [PubMed]
- Raaphorst, F.M. Self-renewal of hematopoietic and leukemic stem cells: A central role for the Polycomb-group gene Bmi-1. Trends Immunol. 2003, 24, 522–524. [Google Scholar] [CrossRef]
- Andricovich, J.; Kai, Y.; Peng, W.; Foudi, A.; Tzatsos, A. Histone demethylase KDM2B regulates lineage commitment in normal and malignant hematopoiesis. J. Clin. Investig. 2016, 126, 905–920. [Google Scholar] [CrossRef] [PubMed]
- Searle, N.E.; Pillus, L. Critical genomic regulation mediated by Enhancer of Polycomb. Curr. Genet. 2017. [Google Scholar] [CrossRef] [PubMed]
- Takihara, Y.; Hara, J. Polycomb-group genes and hematopoiesis. Int. J. Hematol. 2000, 72, 165–172. [Google Scholar] [PubMed]
- Vidal, M.; Starowicz, K. Polycomb complexes PRC1 and their function in hematopoiesis. Exp. Hematol. 2017, 48, 12–31. [Google Scholar] [CrossRef] [PubMed]
- Pirity, M.K.; Locker, J.; Schreiber-Agus, N. Rybp/DEDAF Is Required for Early Postimplantation and for Central Nervous System Development. Mol. Cell. Biol. 2005, 25, 7193–7202. [Google Scholar] [CrossRef] [PubMed]
- Corley, M.; Kroll, K.L. The roles and regulation of Polycomb complexes in neural development. Cell Tissue Res. 2015, 359, 65–85. [Google Scholar] [CrossRef] [PubMed]
- Kim, T.-G.; Chen, J.; Sadoshima, J.; Lee, Y. Jumonji represses atrial natriuretic factor gene expression by inhibiting transcriptional activities of cardiac transcription factors. Mol. Cell. Biol. 2004, 24, 10151–10160. [Google Scholar] [CrossRef] [PubMed]
- He, A.; Ma, Q.; Cao, J.; von Gise, A.; Zhou, P.; Xie, H.; Zhang, B.; Hsing, M.; Christodoulou, D.C.; Cahan, P.; et al. Polycomb Repressive Complex 2 Regulates Normal Development of the Mouse Heart. Circ. Res. 2012, 110, 406–415. [Google Scholar] [CrossRef] [PubMed]
- Beketaev, I.; Zhang, Y.; Kim, E.Y.; Yu, W.; Qian, L.; Wang, J. Critical role of YY1 in cardiac morphogenesis. Dev. Dyn. 2015, 244, 669–680. [Google Scholar] [CrossRef] [PubMed]
- Kee, H.J.; Kim, J.-R.; Nam, K.-I.; Park, H.Y.; Shin, S.; Kim, J.C.; Shimono, Y.; Takahashi, M.; Jeong, M.H.; Kim, N.; et al. Enhancer of Polycomb1, a Novel Homeodomain Only Protein-binding Partner, Induces Skeletal Muscle Differentiation. J. Biol. Chem. 2007, 282, 7700–7709. [Google Scholar] [CrossRef] [PubMed]
- Mu, W.; Starmer, J.; Fedoriw, A.M.; Yee, D.; Magnuson, T. Repression of the soma-specific transcriptome by Polycomb-repressive complex 2 promotes male germ cell development. Genes Dev. 2014, 28, 2056–2069. [Google Scholar] [CrossRef] [PubMed]
- Endoh, M.; Endo, T.A.; Shinga, J.; Hayashi, K.; Farcas, A.; Ma, K.-W.; Ito, S.; Sharif, J.; Endoh, T.; Onaga, N.; et al. PCGF6-PRC1 suppresses premature differentiation of mouse embryonic stem cells by regulating germ cell-related genes. Elife 2017, 6. [Google Scholar] [CrossRef]
- Eun, S.H.; Feng, L.; Cedeno-Rosario, L.; Gan, Q.; Wei, G.; Cui, K.; Zhao, K.; Chen, X. Polycomb Group Gene E(z) Is Required for Spermatogonial Dedifferentiation in Drosophila Adult Testis. J. Mol. Biol. 2017, 429, 2030–2041. [Google Scholar] [CrossRef] [PubMed]
- Feng, L.; Shi, Z.; Chen, X. Enhancer of polycomb coordinates multiple signaling pathways to promote both cyst and germline stem cell differentiation in the Drosophila adult testis. PLOS Genet. 2017, 13, e1006571. [Google Scholar] [CrossRef] [PubMed]
- Faust, C.; Schumacher, A.; Holdener, B.; Magnuson, T. The eed mutation disrupts anterior mesoderm production in mice. Development 1995, 121, 273–285. [Google Scholar] [PubMed]
- Bracken, A.P.; Dietrich, N.; Pasini, D.; Hansen, K.H.; Helin, K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 2006, 20, 1123–1136. [Google Scholar] [CrossRef] [PubMed]
- Junco, S.E.; Wang, R.; Gaipa, J.C.; Taylor, A.B.; Schirf, V.; Gearhart, M.D.; Bardwell, V.J.; Demeler, B.; Hart, P.J.; Kim, C.A. Structure of the polycomb group protein PCGF1 in complex with BCOR reveals basis for binding selectivity of PCGF homologs. Structure 2013, 21, 665–671. [Google Scholar] [CrossRef] [PubMed]
- Hauri, S.; Comoglio, F.; Seimiya, M.; Gerstung, M.; Glatter, T.; Hansen, K.; Aebersold, R.; Paro, R.; Gstaiger, M.; Beisel, C. A High-Density Map for Navigating the Human Polycomb Complexome. Cell Rep. 2016, 17, 583–595. [Google Scholar] [CrossRef] [PubMed]
- Zhao, W.; Huang, Y.; Zhang, J.; Liu, M.; Ji, H.; Wang, C.; Cao, N.; Li, C.; Xia, Y.; Jiang, Q.; et al. Polycomb group RING finger protein 3/5 activate transcription via an interaction with the pluripotency factor Tex10 in embryonic stem cells. J. Biol. Chem. 2017. [Google Scholar] [CrossRef] [PubMed]
- Maeda, I.; Okamura, D.; Tokitake, Y.; Ikeda, M.; Kawaguchi, H.; Mise, N.; Abe, K.; Noce, T.; Okuda, A.; Matsui, Y. Max is a repressor of germ cell-related gene expression in mouse embryonic stem cells. Nat. Commun. 2013, 4, 1754. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, A.; Hirasaki, M.; Hishida, T.; Wu, J.; Okamura, D.; Ueda, A.; Nishimoto, M.; Nakachi, Y.; Mizuno, Y.; Okazaki, Y.; et al. Loss of MAX results in meiotic entry in mouse embryonic and germline stem cells. Nat. Commun. 2016, 7, 11056. [Google Scholar] [CrossRef] [PubMed]
- Luis, N.M.; Morey, L.; Di Croce, L.; Benitah, S.A. Polycomb in Stem Cells: PRC1 Branches Out. Cell Stem Cell 2012, 11, 16–21. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [CrossRef] [PubMed]
- Richly, H.; Aloia, L.; Di Croce, L. Roles of the Polycomb group proteins in stem cells and cancer. Cell Death Dis. 2011, 2, e204. [Google Scholar] [CrossRef] [PubMed]
- Ma, R.; Zhang, Y.; Sun, T.; Cheng, B. Epigenetic regulation by polycomb group complexes: Focus on roles of CBX proteins. J. Zhejiang Univ. Sci. B 2014, 15, 412–428. [Google Scholar] [CrossRef] [PubMed]
- Gil, J.; O’Loghlen, A. PRC1 complex diversity: Where is it taking us? Trends Cell Biol. 2014, 24, 632–641. [Google Scholar] [CrossRef] [PubMed]
- Simon, J.A.; Kingston, R.E. Occupying Chromatin: Polycomb Mechanisms for Getting to Genomic Targets, Stopping Transcriptional Traffic, and Staying Put. Mol. Cell 2013, 49, 808–824. [Google Scholar] [CrossRef] [PubMed]
- Morey, L.; Pascual, G.; Cozzuto, L.; Roma, G.; Wutz, A.; Benitah, S.A.; Di Croce, L. Nonoverlapping Functions of the Polycomb Group Cbx Family of Proteins in Embryonic Stem Cells. Cell Stem Cell 2012, 10, 47–62. [Google Scholar] [CrossRef] [PubMed]
- O’Loghlen, A.; Muñoz-Cabello, A.M.; Gaspar-Maia, A.; Wu, H.-A.; Banito, A.; Kunowska, N.; Racek, T.; Pemberton, H.N.; Beolchi, P.; Lavial, F.; et al. MicroRNA Regulation of Cbx7 Mediates a Switch of Polycomb Orthologs during ESC Differentiation. Cell Stem Cell 2012, 10, 33–46. [Google Scholar] [CrossRef] [PubMed]
- Klauke, K.; Radulović, V.; Broekhuis, M.; Weersing, E.; Zwart, E.; Olthof, S.; Ritsema, M.; Bruggeman, S.; Wu, X.; Helin, K.; et al. Polycomb Cbx family members mediate the balance between haematopoietic stem cell self-renewal and differentiation. Nat. Cell Biol. 2013, 15, 353–362. [Google Scholar] [CrossRef] [PubMed]
- Brockdorff, N. Noncoding RNA and Polycomb recruitment. RNA 2013, 19, 429–442. [Google Scholar] [CrossRef] [PubMed]
- Yap, K.L.; Li, S.; Muñoz-Cabello, A.M.; Raguz, S.; Zeng, L.; Mujtaba, S.; Gil, J.; Walsh, M.J.; Zhou, M.-M. Molecular Interplay of the Noncoding RNA ANRIL and Methylated Histone H3 Lysine 27 by Polycomb CBX7 in Transcriptional Silencing of INK4a. Mol. Cell 2010, 38, 662–674. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.; Lin, C.; Liu, W.; Zhang, J.; Ohgi, K.A.; Grinstein, J.D.; Dorrestein, P.C.; Rosenfeld, M.G. ncRNA- and Pc2 Methylation-Dependent Gene Relocation between Nuclear Structures Mediates Gene Activation Programs. Cell 2011, 147, 773–788. [Google Scholar] [CrossRef] [PubMed]
- Hu, X.; Feng, Y.; Zhang, D.; Zhao, S.D.; Hu, Z.; Greshock, J.; Zhang, Y.; Yang, L.; Zhong, X.; Wang, L.-P.; et al. A Functional Genomic Approach Identifies FAL1 as an Oncogenic Long Noncoding RNA that Associates with BMI1 and Represses p21 Expression in Cancer. Cancer Cell 2014, 26, 344–357. [Google Scholar] [CrossRef] [PubMed]
- Boiani, M.; Schöler, H.R. Developmental cell biology: Regulatory networks in embryo-derived pluripotent stem cells. Nat. Rev. Mol. Cell Biol. 2005, 6, 872–881. [Google Scholar] [CrossRef] [PubMed]
- Joyner, A.L. Gene Targeting: A Practical Approach; Oxford University Press: Oxford, UK, 2000; ISBN 9780199637928. [Google Scholar]
- Brook, F.A.; Gardner, R.L. The origin and efficient derivation of embryonic stem cells in the mouse. Proc. Natl. Acad. Sci. USA 1997, 94, 5709–5712. [Google Scholar] [CrossRef] [PubMed]
- Sivarajah, S.; Raj, G.S.; Mathews, A.J.V.; Sahib, N.B.E.; Hwang, W.S.; Crook, J.M. The generation of GLP-grade human embryonic stem cell banks from four clinical-grade cell lines for preclinical research. Vitr. Cell. Dev. Biol. Anim. 2010, 46, 210–216. [Google Scholar] [CrossRef] [PubMed]
- Aloia, L.; Di Stefano, B.; Di Croce, L. Polycomb complexes in stem cells and embryonic development. Development 2013, 140, 2525–2534. [Google Scholar] [CrossRef] [PubMed]
- Mas, G.; Di Croce, L. The role of Polycomb in stem cell genome architecture. Curr. Opin. Cell Biol. 2016, 43, 87–95. [Google Scholar] [CrossRef] [PubMed]
- Sauvageau, M.; Sauvageau, G. Polycomb group proteins: Multi-faceted regulators of somatic stem cells and cancer. Cell Stem Cell 2010, 7, 299–313. [Google Scholar] [CrossRef] [PubMed]
- Surface, L.E.; Thornton, S.R.; Boyer, L.A. Polycomb group proteins set the stage for early lineage commitment. Cell Stem Cell 2010, 7, 288–298. [Google Scholar] [CrossRef] [PubMed]
- Ku, M.; Koche, R.P.; Rheinbay, E.; Mendenhall, E.M.; Endoh, M.; Mikkelsen, T.S.; Presser, A.; Nusbaum, C.; Xie, X.; Chi, A.S.; et al. Genomewide Analysis of PRC1 and PRC2 Occupancy Identifies Two Classes of Bivalent Domains. PLoS Genet. 2008, 4, e1000242. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Creppe, C.; Palau, A.; Malinverni, R.; Valero, V.; Buschbeck, M. A Cbx8-Containing Polycomb Complex Facilitates the Transition to Gene Activation during ES Cell Differentiation. PLoS Genet. 2014, 10, e1004851. [Google Scholar] [CrossRef] [PubMed]
- Kloet, S.L.; Makowski, M.M.; Baymaz, H.I.; van Voorthuijsen, L.; Karemaker, I.D.; Santanach, A.; Jansen, P.W.T.C.; Di Croce, L.; Vermeulen, M. The dynamic interactome and genomic targets of Polycomb complexes during stem-cell differentiation. Nat. Struct. Mol. Biol. 2016, 23, 682–690. [Google Scholar] [CrossRef] [PubMed]
- Mantsoki, A.; Devailly, G.; Joshi, A. CpG island erosion, polycomb occupancy and sequence motif enrichment at bivalent promoters in mammalian embryonic stem cells. Sci. Rep. 2015, 5, 16791. [Google Scholar] [CrossRef] [PubMed]
- Stock, J.K.; Giadrossi, S.; Casanova, M.; Brookes, E.; Vidal, M.; Koseki, H.; Brockdorff, N.; Fisher, A.G.; Pombo, A. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat. Cell Biol. 2007, 9, 1428–1435. [Google Scholar] [CrossRef] [PubMed]
- Bernstein, B.E.; Mikkelsen, T.S.; Xie, X.; Kamal, M.; Huebert, D.J.; Cuff, J.; Fry, B.; Meissner, A.; Wernig, M.; Plath, K.; et al. A Bivalent Chromatin Structure Marks Key Developmental Genes in Embryonic Stem Cells. Cell 2006, 125, 315–326. [Google Scholar] [CrossRef] [PubMed]
- Brookes, E.; Pombo, A. Modifications of RNA polymerase II are pivotal in regulating gene expression states. EMBO Rep. 2009, 10, 1213–1219. [Google Scholar] [CrossRef] [PubMed]
- Harikumar, A.; Meshorer, E. Chromatin remodeling and bivalent histone modifications in embryonic stem cells. EMBO Rep. 2015, 16, 1609–1619. [Google Scholar] [CrossRef] [PubMed]
- Tavares, L.; Dimitrova, E.; Oxley, D.; Webster, J.; Poot, R.; Demmers, J.; Bezstarosti, K.; Taylor, S.; Ura, H.; Koide, H.; et al. RYBP-PRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell 2012, 148, 664–678. [Google Scholar] [CrossRef] [PubMed]
- Ogawa, H.; Ishiguro, K.-I.; Gaubatz, S.; Livingston, D.M.; Nakatani, Y. A Complex with Chromatin Modifiers That Occupies E2F- and Myc-Responsive Genes in G0 Cells. Science 2002, 296, 1132–1136. [Google Scholar] [CrossRef] [PubMed]
- Trojer, P.; Cao, A.R.; Gao, Z.; Li, Y.; Zhang, J.; Xu, X.; Li, G.; Losson, R.; Erdjument-Bromage, H.; Tempst, P.; et al. L3MBTL2 Protein Acts in Concert with PcG Protein-Mediated Monoubiquitination of H2A to Establish a Repressive Chromatin Structure. Mol. Cell 2011, 42, 438–450. [Google Scholar] [CrossRef] [PubMed]
- Qin, J.; Whyte, W.A.; Anderssen, E.; Apostolou, E.; Chen, H.-H.; Akbarian, S.; Bronson, R.T.; Hochedlinger, K.; Ramaswamy, S.; Young, R.A.; et al. The Polycomb Group Protein L3mbtl2 Assembles an Atypical PRC1-Family Complex that Is Essential in Pluripotent Stem Cells and Early Development. Cell Stem Cell 2012, 11, 319–332. [Google Scholar] [CrossRef] [PubMed]
- Sanchez-Pulido, L.; Devos, D.; Sung, Z.R.; Calonje, M. RAWUL: A new ubiquitin-like domain in PRC1 Ring finger proteins that unveils putative plant and worm PRC1 orthologs. BMC Genom. 2008, 9, 308. [Google Scholar] [CrossRef] [PubMed]
- Wang, R.; Taylor, A.B.; Leal, B.Z.; Chadwell, L.V.; Ilangovan, U.; Robinson, A.K.; Schirf, V.; Hart, P.J.; Lafer, E.M.; Demeler, B.; et al. Polycomb group targeting through different binding partners of RING1B C-terminal domain. Structure 2010, 18, 966–975. [Google Scholar] [CrossRef] [PubMed]
- Boyer, L.A.; Plath, K.; Zeitlinger, J.; Brambrink, T.; Medeiros, L.A.; Lee, T.I.; Levine, S.S.; Wernig, M.; Tajonar, A.; Ray, M.K.; et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006, 441, 349–353. [Google Scholar] [CrossRef] [PubMed]
- Kahn, T.G.; Dorafshan, E.; Schultheis, D.; Zare, A.; Stenberg, P.; Reim, I.; Pirrotta, V.; Schwartz, Y.B. Interdependence of PRC1 and PRC2 for recruitment to Polycomb Response Elements. Nucleic Acids Res. 2016, 44, 10132–10149. [Google Scholar] [CrossRef] [PubMed]
- Schoeftner, S.; Sengupta, A.K.; Kubicek, S.; Mechtler, K.; Spahn, L.; Koseki, H.; Jenuwein, T.; Wutz, A. Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J. 2006, 25, 3110–3122. [Google Scholar] [CrossRef] [PubMed]
- Puschendorf, M.; Terranova, R.; Boutsma, E.; Mao, X.; Isono, K.; Brykczynska, U.; Kolb, C.; Otte, A.P.; Koseki, H.; Orkin, S.H.; et al. PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat. Genet. 2008, 40, 411–420. [Google Scholar] [CrossRef] [PubMed]
- Richly, H.; Rocha-Viegas, L.; Ribeiro, J.D.; Demajo, S.; Gundem, G.; Lopez-Bigas, N.; Nakagawa, T.; Rospert, S.; Ito, T.; Di Croce, L. Transcriptional activation of polycomb-repressed genes by ZRF1. Nature 2010, 468, 1124–1128. [Google Scholar] [CrossRef] [PubMed]
- Morey, L.; Aloia, L.; Cozzuto, L.; Benitah, S.A.; Di Croce, L. RYBP and Cbx7 Define Specific Biological Functions of Polycomb Complexes in Mouse Embryonic Stem Cells. Cell Rep. 2013, 3, 60–69. [Google Scholar] [CrossRef] [PubMed]
- Lovering, R.; Hanson, I.M.; Borden, K.L.; Martin, S.; O’Reilly, N.J.; Evan, G.I.; Rahman, D.; Pappin, D.J.; Trowsdale, J.; Freemont, P.S. Identification and preliminary characterization of a protein motif related to the zinc finger. Proc. Natl. Acad. Sci. USA 1993, 90, 2112–2116. [Google Scholar] [CrossRef] [PubMed]
- Schoorlemmer, J.; Marcos-Gutiérrez, C.; Were, F.; Martínez, R.; García, E.; Satijn, D.P.E.; Otte, A.P.; Vidal, M. Ring1A is a transcriptional repressor that interacts with the Polycomb-M33 protein and is expressed at rhombomere boundaries in the mouse hindbrain. EMBO J. 1997, 16, 5930–5942. [Google Scholar] [CrossRef] [PubMed]
- Voncken, J.W.; Roelen, B.A.J.; Roefs, M.; de Vries, S.; Verhoeven, E.; Marino, S.; Deschamps, J.; van Lohuizen, M. Rnf2 (Ring1b) deficiency causes gastrulation arrest and cell cycle inhibition. Proc. Natl. Acad. Sci. USA 2003, 100, 2468–2473. [Google Scholar] [CrossRef] [PubMed]
- Cales, C.; Roman-Trufero, M.; Pavon, L.; Serrano, I.; Melgar, T.; Endoh, M.; Perez, C.; Koseki, H.; Vidal, M. Inactivation of the Polycomb Group Protein Ring1B Unveils an Antiproliferative Role in Hematopoietic Cell Expansion and Cooperation with Tumorigenesis Associated with Ink4a Deletion. Mol. Cell. Biol. 2008, 28, 1018–1028. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- de Napoles, M.; Mermoud, J.E.; Wakao, R.; Tang, Y.A.; Endoh, M.; Appanah, R.; Nesterova, T.B.; Silva, J.; Otte, A.P.; Vidal, 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. [Google Scholar] [CrossRef] [PubMed]
- Fujimura, Y.-I.; Isono, K.-I.; Vidal, M.; Endoh, M.; Kajita, H.; Mizutani-Koseki, Y.; Takihara, Y.; van Lohuizen, M.; Otte, A.; Jenuwein, T.; et al. Distinct roles of Polycomb group gene products in transcriptionally repressed and active domains of Hoxb8. Development 2006, 133, 2371–2381. [Google Scholar] [CrossRef] [PubMed]
- Leeb, M.; Wutz, A. Ring1B is crucial for the regulation of developmental control genes and PRC1 proteins but not X inactivation in embryonic cells. J. Cell Biol. 2007, 178, 219–229. [Google Scholar] [CrossRef] [PubMed]
- van der Stoop, P.; Boutsma, E.A.; Hulsman, D.; Noback, S.; Heimerikx, M.; Kerkhoven, R.M.; Voncken, J.W.; Wessels, L.F.A.; van Lohuizen, M. Ubiquitin E3 Ligase Ring1b/Rnf2 of Polycomb Repressive Complex 1 Contributes to Stable Maintenance of Mouse Embryonic Stem Cells. PLoS ONE 2008, 3, e2235. [Google Scholar] [CrossRef] [PubMed]
- Román-Trufero, M.; Méndez-Gómez, H.R.; Pérez, C.; Hijikata, A.; Fujimura, Y.; Endo, T.; Koseki, H.; Vicario-Abejón, C.; Vidal, M. Maintenance of Undifferentiated State and Self-Renewal of Embryonic Neural Stem Cells by Polycomb Protein Ring1B. Stem Cells 2009, 27, 1559–1570. [Google Scholar] [CrossRef] [PubMed]
- Wei, M.; Jiao, D.; Han, D.; Wu, J.; Wei, F.; Zheng, G.; Guo, Z.; Xi, W.; Yang, F.; Xie, P.; et al. Knockdown of RNF2 induces cell cycle arrest and apoptosis in prostate cancer cells through the upregulation of TXNIP. Oncotarget 2017, 8, 5323–5338. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Sun, Z.; Han, Y.; Yao, R.; Yue, L.; Xu, Y.; Zhang, J. Rnf2 knockdown reduces cell viability and promotes cell cycle arrest in gastric cancer cells. Oncol. Lett. 2017, 13, 3817–3822. [Google Scholar] [CrossRef] [PubMed]
- Endoh, M.; Endo, T.A.; Endoh, T.; Fujimura, Y. I.; Ohara, O.; Toyoda, T.; Otte, A.P.; Okano, M.; Brockdorff, N.; Vidal, M.; et al. Polycomb group proteins Ring1A/B are functionally linked to the core transcriptional regulatory circuitry to maintain ES cell identity. Development 2008, 135, 1513–1524. [Google Scholar] [CrossRef] [PubMed]
- Bravo, M.; Nicolini, F.; Starowicz, K.; Barroso, S.; Cales, C.; Aguilera, A.; Vidal, M. Polycomb RING1A- and RING1B-dependent histone H2A monoubiquitylation at pericentromeric regions promotes S-phase progression. J. Cell Sci. 2015, 128, 3660–3671. [Google Scholar] [CrossRef] [PubMed]
- Lapthanasupkul, P.; Feng, J.; Mantesso, A.; Takada-Horisawa, Y.; Vidal, M.; Koseki, H.; Wang, L.; An, Z.; Miletich, I.; Sharpe, P.T. Ring1a/b polycomb proteins regulate the mesenchymal stem cell niche in continuously growing incisors. Dev. Biol. 2012, 367, 140–153. [Google Scholar] [CrossRef] [PubMed]
- Neira, J.L.; Román-Trufero, M.; Contreras, L.M.; Prieto, J.; Singh, G.; Barrera, F.N.; Renart, M.L.; Vidal, M. The Transcriptional Repressor RYBP Is a Natively Unfolded Protein Which Folds upon Binding to DNA †. Biochemistry 2009, 48, 1348–1360. [Google Scholar] [CrossRef] [PubMed]
- Garcia, E.; Marcos-Gutiérrez, C.; del Mar Lorente, M.; Moreno, J.C.; Vidal, M. RYBP, a new repressor protein that interacts with components of the mammalian Polycomb complex, and with the transcription factor YY1. EMBO J. 1999, 18, 3404–3418. [Google Scholar] [CrossRef] [PubMed]
- Pirity, M.K.; Wang, W.-L.; Wolf, L.V.; Tamm, E.R.; Schreiber-Agus, N.; Cvekl, A. Rybp, a polycomb complex-associated protein, is required for mouse eye development. BMC Dev. Biol. 2007, 7, 39. [Google Scholar] [CrossRef] [PubMed]
- Wei, W.; He, H.-B.; Zhang, W.-Y.; Zhang, H.-X.; Bai, J.-B.; Liu, H.-Z.; Cao, J.-H.; Chang, K.-C.; Li, X.-Y.; Zhao, S.-H. miR-29 targets Akt3 to reduce proliferation and facilitate differentiation of myoblasts in skeletal muscle development. Cell Death Dis. 2013, 4, e668. [Google Scholar] [CrossRef] [PubMed]
- Zhao, J.-L.; Huang, F.; He, F.; Gao, C.-C.; Liang, S.-Q.; Ma, P.-F.; Dong, G.-Y.; Han, H.; Qin, H.-Y. Forced Activation of Notch in Macrophages Represses Tumor Growth by Upregulating miR-125a and Disabling Tumor-Associated Macrophages. Cancer Res. 2016, 76, 1403–1415. [Google Scholar] [CrossRef] [PubMed]
- Calés, C.; Pavón, L.; Starowicz, K.; Pérez, C.; Bravo, M.; Ikawa, T.; Koseki, H.; Vidal, M. Role of Polycomb RYBP in Maintaining the B-1-to-B-2 B-Cell Lineage Switch in Adult Hematopoiesis. Mol. Cell. Biol. 2016, 36, 900–912. [Google Scholar] [CrossRef] [PubMed]
- Ujhelly, O.; Szabo, V.; Kovacs, G.; Vajda, F.; Mallok, S.; Prorok, J.; Acsai, K.; Hegedus, Z.; Krebs, S.; Dinnyes, A.; et al. Lack of Rybp in Mouse Embryonic Stem Cells Impairs Cardiac Differentiation. Stem Cells Dev. 2015, 24, 2193–2205. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kovacs, G.; Szabo, V.; Pirity, M.K. Absence of Rybp Compromises Neural Differentiation of Embryonic Stem Cells. Stem Cells Int. 2016, 2016, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Kalenik, J.L.; Chen, D.; Bradley, M.E.; Chen, S.J.; Lee, T.C. Yeast two-hybrid cloning of a novel zinc finger protein that interacts with the multifunctional transcription factor YY1. Nucleic Acids Res. 1997, 25, 843–849. [Google Scholar] [CrossRef] [PubMed]
- Bannasch, D.; Mädge, B.; Schwab, M. Functional interaction of Yaf2 with the central region of MycN. Oncogene 2001, 20, 5913–5919. [Google Scholar] [CrossRef] [PubMed]
- Mädge, B.; Geisen, C.; Möröy, T.; Schwab, M. Yaf2 inhibits Myc biological function. Cancer Lett. 2003, 193, 171–176. [Google Scholar] [CrossRef]
- Kaneko, T.; Miyagishima, H.; Hasegawa, T.; Mizutani-Koseki, Y.; Isono, K.; Koseki, H. The mouse YAF2 gene generates two distinct transcripts and is expressed in pre-and postimplantation embryos. Gene 2003, 315, 183–192. [Google Scholar] [CrossRef]
- Sawa, C.; Yoshikawa, T.; Matsuda-Suzuki, F.; Deléhouzée, S.; Goto, M.; Watanabe, H.; Sawada, J.; Kataoka, K.; Handa, H. YEAF1/RYBP and YAF-2 are functionally distinct members of a cofactor family for the YY1 and E4TF1/hGABP transcription factors. J. Biol. Chem. 2002, 277, 22484–22490. [Google Scholar] [CrossRef] [PubMed]
- Wilkinson, F.; Pratt, H.; Atchison, M.L. PcG recruitment by the YY1 REPO domain can be mediated by Yaf2. J. Cell. Biochem. 2009, 109. [Google Scholar] [CrossRef] [PubMed]
- Basu, A.; Wilkinson, F.H.; Colavita, K.; Fennelly, C.; Atchison, M.L. YY1 DNA binding and interaction with YAF2 is essential for Polycomb recruitment. Nucleic Acids Res. 2014, 42, 2208–2223. [Google Scholar] [CrossRef] [PubMed]
- Yant, S.R.; Zhu, W.; Millinoff, D.; Slightom, J.L.; Goodman, M.; Gumucio, D.L. High affinity YY1 binding motifs: Identification of two core types (ACAT and CCAT) and distribution of potential binding sites within the human beta globin cluster. Nucleic Acids Res. 1995, 23, 4353–4362. [Google Scholar] [CrossRef] [PubMed]
- Shi, Y.; Seto, E.; Chang, L.S.; Shenk, T. Transcriptional repression by YY1, a human GLI-Krüppel-related protein, and relief of repression by adenovirus E1A protein. Cell 1991, 67, 377–388. [Google Scholar] [CrossRef]
- Park, K.; Atchison, M.L. Isolation of a candidate repressor/activator, NF-E1 (YY-1, delta), that binds to the immunoglobulin kappa 3’ enhancer and the immunoglobulin heavy-chain mu E1 site. Proc. Natl. Acad. Sci. USA 1991, 88, 9804–9808. [Google Scholar] [CrossRef] [PubMed]
- Donohoe, M.E.; Zhang, X.; McGinnis, L.; Biggers, J.; Li, E.; Shi, Y. Targeted disruption of mouse Yin Yang 1 transcription factor results in peri-implantation lethality. Mol. Cell. Biol. 1999, 19, 7237–7244. [Google Scholar] [CrossRef] [PubMed]
- Kurisaki, K.; Kurisaki, A.; Valcourt, U.; Terentiev, A.A.; Pardali, K.; Ten Dijke, P.; Heldin, C.-H.; Ericsson, J.; Moustakas, A. Nuclear factor YY1 inhibits transforming growth factor beta- and bone morphogenetic protein-induced cell differentiation. Mol. Cell. Biol. 2003, 23, 4494–4510. [Google Scholar] [CrossRef] [PubMed]
- He, Y.; Kim, J.Y.; Dupree, J.; Tewari, A.; Melendez-Vasquez, C.; Svaren, J.; Casaccia, P. Yy1 as a molecular link between neuregulin and transcriptional modulation of peripheral myelination. Nat. Neurosci. 2010, 13, 1472–1480. [Google Scholar] [CrossRef] [PubMed]
- Trask, M.C.; Tremblay, K.D.; Mager, J. Yin-Yang1 is required for epithelial-to-mesenchymal transition and regulation of Nodal signaling during mammalian gastrulation. Dev. Biol. 2012, 368, 273–282. [Google Scholar] [CrossRef] [PubMed]
- Yan, X.; Pan, J.; Xiong, W.; Cheng, M.; Sun, Y.; Zhang, S.; Chen, Y. Yin Yang 1 (YY1) synergizes with Smad7 to inhibit TGF-β signaling in the nucleus. Sci. China Life Sci. 2014, 57, 128–136. [Google Scholar] [CrossRef] [PubMed]
- Wallingford, M.C.; Hiller, J.; Zhang, K.; Mager, J. YY1 Is Required for Posttranscriptional Stability of SOX2 and OCT4 Proteins. Cell. Reprogram. 2017, 19, 263–269. [Google Scholar] [CrossRef] [PubMed]
- Affar, E.B.; Gay, F.; Shi, Y.; Liu, H.; Huarte, M.; Wu, S.; Collins, T.; Li, E.; Shi, Y. Essential Dosage-Dependent Functions of the Transcription Factor Yin Yang 1 in Late Embryonic Development and Cell Cycle Progression. Mol. Cell. Biol. 2006, 26, 3565–3581. [Google Scholar] [CrossRef] [PubMed]
- Gregoire, S.; Karra, R.; Passer, D.; Deutsch, M.-A.; Krane, M.; Feistritzer, R.; Sturzu, A.; Domian, I.; Saga, Y.; Wu, S.M. Essential and Unexpected Role of Yin Yang 1 to Promote Mesodermal Cardiac Differentiation. Circ. Res. 2013, 112, 900–910. [Google Scholar] [CrossRef] [PubMed]
- Yan, Y.; Zhao, W.; Huang, Y.; Tong, H.; Xia, Y.; Jiang, Q.; Qin, J. Loss of Polycomb Group Protein Pcgf1 Severely Compromises Proper Differentiation of Embryonic Stem Cells. Sci. Rep. 2017, 7, 46276. [Google Scholar] [CrossRef] [PubMed]
- Farcas, A.M.; Blackledge, N.P.; Sudbery, I.; Long, H.K.; McGouran, J.F.; Rose, N.R.; Lee, S.; Sims, D.; Cerase, A.; Sheahan, T.W.; et al. KDM2B links the polycomb repressive complex 1 (PRC1) to recognition of CpG islands. Elife 2012, 2012. [Google Scholar] [CrossRef] [PubMed]
- Wu, X.; Johansen, J.V.; Helin, K. Fbxl10/Kdm2b recruits polycomb repressive complex 1 to CpG islands and regulates H2A ubiquitylation. Mol. Cell 2013, 49, 1134–1146. [Google Scholar] [CrossRef] [PubMed]
- Turner, S.A.; Bracken, A.P. A “complex” issue: Deciphering the role of variant PRC1 in ESCs. Cell Stem Cell 2013, 12, 145–146. [Google Scholar] [CrossRef] [PubMed]
- Nunes, M.; Blanc, I.; Maes, J.; Fellous, M.; Robert, B.; McElreavey, K. NSPc1, a novel mammalian Polycomb gene, is expressed in neural crest-derived structures of the peripheral nervous system. Mech. Dev. 2001, 102, 219–222. [Google Scholar] [CrossRef]
- Oliviero, G.; Munawar, N.; Watson, A.; Streubel, G.; Manning, G.; Bardwell, V.; Bracken, A.P.; Cagney, G. The variant Polycomb Repressor Complex 1 component PCGF1 interacts with a pluripotency sub-network that includes DPPA4, a regulator of embryogenesis. Sci. Rep. 2015, 5, 18388. [Google Scholar] [CrossRef] [PubMed]
- Wu, X.; Gong, Y.; Yue, J.; Qiang, B.; Yuan, J.; Peng, X. Cooperation between EZH2, NSPc1-mediated histone H2A ubiquitination and Dnmt1 in HOX gene silencing. Nucleic Acids Res. 2008, 36, 3590–3599. [Google Scholar] [CrossRef] [PubMed]
- Huynh, K.D.; Fischle, W.; Verdin, E.; Bardwell, V.J. BCoR, a novel corepressor involved in BCL-6 repression. Genes Dev. 2000, 14, 1810–1823. [Google Scholar] [PubMed]
- Wamstad, J.A.; Corcoran, C.M.; Keating, A.M.; Bardwell, V.J. Role of the Transcriptional Corepressor Bcor in Embryonic Stem Cell Differentiation and Early Embryonic Development. PLoS ONE 2008, 3, e2814. [Google Scholar] [CrossRef] [PubMed]
- Cox, B.J.; Vollmer, M.; Tamplin, O.; Lu, M.; Biechele, S.; Gertsenstein, M.; van Campenhout, C.; Floss, T.; Kuhn, R.; Wurst, W.; et al. Phenotypic annotation of the mouse X chromosome. Genome Res. 2010, 20, 1154–1164. [Google Scholar] [CrossRef] [PubMed]
- Grossmann, V.; Tiacci, E.; Holmes, A.B.; Kohlmann, A.; Martelli, M.P.; Kern, W.; Spanhol-Rosseto, A.; Klein, H.-U.; Dugas, M.; Schindela, S.; et al. Whole-exome sequencing identifies somatic mutations of BCOR in acute myeloid leukemia with normal karyotype. Blood 2011, 118, 6153–6163. [Google Scholar] [CrossRef] [PubMed]
- Temming, P.; Corson, T.W.; Lohmann, D.R. Retinoblastoma tumorigenesis: Genetic and epigenetic changes walk hand in hand. Future Oncol. 2012, 8, 525–528. [Google Scholar] [CrossRef] [PubMed]
- Pugh, T.J.; Weeraratne, S.D.; Archer, T.C.; Pomeranz Krummel, D.A.; Auclair, D.; Bochicchio, J.; Carneiro, M.O.; Carter, S.L.; Cibulskis, K.; Erlich, R.L.; et al. Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 2012, 488, 106–110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kenny, C.; Bausenwein, S.; Lazaro, A.; Furtwängler, R.; Gooskens, S.L.; van den Heuvel Eibrink, M.; Vokuhl, C.; Leuschner, I.; Graf, N.; Gessler, M.; et al. Mutually exclusive BCOR internal tandem duplications and YWHAE-NUTM2 fusions in clear cell sarcoma of kidney: Not the full story. J. Pathol. 2016, 238, 617–620. [Google Scholar] [CrossRef] [PubMed]
- Kao, Y.-C.; Sung, Y.-S.; Zhang, L.; Huang, S.-C.; Argani, P.; Chung, C.T.; Graf, N.S.; Wright, D.C.; Kellie, S.J.; Agaram, N.P.; et al. Recurrent BCOR Internal Tandem Duplication and YWHAE-NUTM2B Fusions in Soft Tissue Undifferentiated Round Cell Sarcoma of Infancy. Am. J. Surg. Pathol. 2016, 40, 1009–1020. [Google Scholar] [CrossRef] [PubMed]
- Cao, Q.; Gearhart, M.D.; Gery, S.; Shojaee, S.; Yang, H.; Sun, H.; Lin, D.; Bai, J.; Mead, M.; Zhao, Z.; et al. BCOR regulates myeloid cell proliferation and differentiation. Leukemia 2016, 30, 1155–1165. [Google Scholar] [CrossRef] [PubMed]
- Fukuda, T.; Tokunaga, A.; Sakamoto, R.; Yoshida, N. Fbxl10/Kdm2b deficiency accelerates neural progenitor cell death and leads to exencephaly. Mol. Cell. Neurosci. 2011, 46, 614–624. [Google Scholar] [CrossRef] [PubMed]
- He, J.; Kallin, E.M.; Tsukada, Y.; Zhang, Y. The H3K36 demethylase Jhdm1b/Kdm2b regulates cell proliferation and senescence through p15Ink4b. Nat. Struct. Mol. Biol. 2008, 15, 1169–1175. [Google Scholar] [CrossRef] [PubMed]
- He, J.; Shen, L.; Wan, M.; Taranova, O.; Wu, H.; Zhang, Y. Kdm2b maintains murine embryonic stem cell status by recruiting PRC1 complex to CpG islands of developmental genes. Nat. Cell Biol. 2013, 15, 373–384. [Google Scholar] [CrossRef] [PubMed]
- Kottakis, F.; Foltopoulou, P.; Sanidas, I.; Keller, P.; Wronski, A.; Dake, B.T.; Ezell, S.A.; Shen, Z.; Naber, S.P.; Hinds, P.W.; et al. NDY1/KDM2B Functions as a Master Regulator of Polycomb Complexes and Controls Self-Renewal of Breast Cancer Stem Cells. Cancer Res. 2014, 74, 3935–3946. [Google Scholar] [CrossRef] [PubMed]
- Lu, L.; Gao, Y.; Zhang, Z.; Cao, Q.; Zhang, X.; Zou, J.; Cao, Y. Kdm2a/b Lysine Demethylases Regulate Canonical Wnt Signaling by Modulating the Stability of Nuclear β-Catenin. Dev. Cell 2015, 33, 660–674. [Google Scholar] [CrossRef] [PubMed]
- Boulard, M.; Edwards, J.R.; Bestor, T.H. FBXL10 protects Polycomb-bound genes from hypermethylation. Nat. Genet. 2015, 47, 479–485. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Kobayashi, R.; Galaktionov, K.; Beach, D. p19Skp1 and p45Skp2 are essential elements of the cyclin A-CDK2 S phase kinase. Cell 1995, 82, 915–925. [Google Scholar] [CrossRef]
- Bai, C.; Sen, P.; Hofmann, K.; Ma, L.; Goebl, M.; Harper, J.W.; Elledge, S.J. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 1996, 86, 263–274. [Google Scholar] [CrossRef]
- Connelly, C.; Hieter, P. Budding yeast SKP1 encodes an evolutionarily conserved kinetochore protein required for cell cycle progression. Cell 1996, 86, 275–285. [Google Scholar] [CrossRef]
- Piva, R.; Liu, J.; Chiarle, R.; Podda, A.; Pagano, M.; Inghirami, G. In vivo interference with Skp1 function leads to genetic instability and neoplastic transformation. Mol. Cell. Biol. 2002, 22, 8375–8387. [Google Scholar] [CrossRef] [PubMed]
- Mandel, S.A.; Fishman-Jacob, T.; Youdim, M.B.H. Modeling sporadic Parkinson’s disease by silencing the ubiquitin E3 ligase component, SKP1A. Parkinsonism Relat. Disord. 2009, 15, S148–S151. [Google Scholar] [CrossRef]
- Everett, R.D.; Meredith, M.; Orr, A.; Cross, A.; Kathoria, M.; Parkinson, J. A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein. EMBO J. 1997, 16, 1519–1530. [Google Scholar] [CrossRef] [PubMed]
- Cummins, J.M.; Rago, C.; Kohli, M.; Kinzler, K.W.; Lengauer, C.; Vogelstein, B. Tumour suppression: Disruption of HAUSP gene stabilizes p53. Nature 2004, 428. [Google Scholar] [CrossRef] [PubMed]
- Li, M.; Brooks, C.L.; Kon, N.; Gu, W. A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol. Cell 2004, 13, 879–886. [Google Scholar] [CrossRef]
- Kon, N.; Kobayashi, Y.; Li, M.; Brooks, C.L.; Ludwig, T.; Gu, W. Inactivation of HAUSP in vivo modulates p53 function. Oncogene 2010, 29, 1270–1279. [Google Scholar] [CrossRef] [PubMed]
- Kon, N.; Zhong, J.; Kobayashi, Y.; Li, M.; Szabolcs, M.; Ludwig, T.; Canoll, P.D.; Gu, W. Roles of HAUSP-mediated p53 regulation in central nervous system development. Cell Death Differ. 2011, 18, 1366–1375. [Google Scholar] [CrossRef] [PubMed]
- Huang, Z.; Wu, Q.; Guryanova, O.A.; Cheng, L.; Shou, W.; Rich, J.N.; Bao, S. Deubiquitylase HAUSP stabilizes REST and promotes maintenance of neural progenitor cells. Nat. Cell Biol. 2011, 13, 142–152. [Google Scholar] [CrossRef] [PubMed]
- Hao, Y.-H.; Fountain, M.D.; Fon Tacer, K.; Xia, F.; Bi, W.; Kang, S.-H.L.; Patel, A.; Rosenfeld, J.A.; Le Caignec, C.; et al. USP7 Acts as a Molecular Rheostat to Promote WASH-Dependent Endosomal Protein Recycling and Is Mutated in a Human Neurodevelopmental Disorder. Mol. Cell 2015, 59, 956–969. [Google Scholar] [CrossRef] [PubMed]
- Tang, Y.; Lv, L.; Li, W.; Zhang, X.; Jiang, Y.; Ge, W.; Zhou, Y. Protein deubiquitinase USP7 is required for osteogenic differentiation of human adipose-derived stem cells. Stem Cell Res. Ther. 2017, 8, 186. [Google Scholar] [CrossRef] [PubMed]
- Akasaka, T.; van Lohuizen, M.; van der Lugt, N.; Mizutani-Koseki, Y.; Kanno, M.; Taniguchi, M.; Vidal, M.; Alkema, M.; Berns, A.; Koseki, H. Mice doubly deficient for the Polycomb Group genes Mel18 and Bmi1 reveal synergy and requirement for maintenance but not initiation of Hox gene expression. Development 2001, 128, 1587–1597. [Google Scholar] [PubMed]
- Tagawa, M.; Sakamoto, T.; Shigemoto, K.; Matsubara, H.; Tamura, Y.; Ito, T.; Nakamura, I.; Okitsu, A.; Imai, K.; Taniguchi, M. Expression of novel DNA-binding protein with zinc finger structure in various tumor cells. J. Biol. Chem. 1990, 265, 20021–20026. [Google Scholar] [PubMed]
- Akasaka, T.; Tsuji, K.; Kawahira, H.; Kanno, M.; Harigaya, K.; Hu, L.; Ebihara, Y.; Nakahata, T.; Tetsu, O.; Taniguchi, M.; et al. The role of mel-18, a mammalian Polycomb group gene, during IL-7-dependent proliferation of lymphocyte precursors. Immunity 1997, 7, 135–146. [Google Scholar] [CrossRef]
- Miyazaki, M.; Kawamoto, H.; Kato, Y.; Itoi, M.; Miyazaki, K.; Masuda, K.; Tashiro, S.; Ishihara, H.; Igarashi, K.; Amagai, T.; et al. Polycomb group gene mel-18 regulates early T progenitor expansion by maintaining the expression of Hes-1, a target of the Notch pathway. J. Immunol. 2005, 174, 2507–2516. [Google Scholar] [CrossRef] [PubMed]
- Hod-Dvorai, R.; Jacob, E.; Boyko, Y.; Avni, O. The binding activity of Mel-18 at the Il17a promoter is regulated by the integrated signals of the TCR and polarizing cytokines. Eur. J. Immunol. 2011, 41, 2424–2435. [Google Scholar] [CrossRef] [PubMed]
- Won, H.-Y.; Lee, J.-Y.; Shin, D.-H.; Park, J.-H.; Nam, J.-S.; Kim, H.-C.; Kong, G. Loss of Mel-18 enhances breast cancer stem cell activity and tumorigenicity through activating Notch signaling mediated by the Wnt/TCF pathway. FASEB J. 2012, 26, 5002–5013. [Google Scholar] [CrossRef] [PubMed]
- Morey, L.; Santanach, A.; Blanco, E.; Aloia, L.; Nora, E.P.; Bruneau, B.G.; Di Croce, L. Polycomb Regulates Mesoderm Cell Fate-Specification in Embryonic Stem Cells through Activation and Repression Mechanisms. Cell Stem Cell 2015, 17, 300–315. [Google Scholar] [CrossRef] [PubMed]
- Oguro, H.; Yuan, J.; Ichikawa, H.; Ikawa, T.; Yamazaki, S.; Kawamoto, H.; Nakauchi, H.; Iwama, A. Poised Lineage Specification in Multipotential Hematopoietic Stem and Progenitor Cells by the Polycomb Protein Bmi1. Cell Stem Cell 2010, 6, 279–286. [Google Scholar] [CrossRef] [PubMed]
- Smith, L.-L.; Yeung, J.; Zeisig, B.B.; Popov, N.; Huijbers, I.; Barnes, J.; Wilson, A.J.; Taskesen, E.; Delwel, R.; Gil, J.; et al. Functional Crosstalk between Bmi1 and MLL/Hoxa9 Axis in Establishment of Normal Hematopoietic and Leukemic Stem Cells. Cell Stem Cell 2011, 8, 649–662. [Google Scholar] [CrossRef] [PubMed]
- Bruggeman, S.W.M.; Valk-Lingbeek, M.E.; van der Stoop, P.P.M.; Jacobs, J.J.L.; Kieboom, K.; Tanger, E.; Hulsman, D.; Leung, C.; Arsenijevic, Y.; Marino, S.; et al. Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice. Genes Dev. 2005, 19, 1438–1443. [Google Scholar] [CrossRef] [PubMed]
- Zencak, D.; Lingbeek, M.; Kostic, C.; Tekaya, M.; Tanger, E.; Hornfeld, D.; Jaquet, M.; Munier, F.L.; Schorderet, D.F.; van Lohuizen, M.; et al. Bmi1 Loss Produces an Increase in Astroglial Cells and a Decrease in Neural Stem Cell Population and Proliferation. J. Neurosci. 2005, 25, 5774–5783. [Google Scholar] [CrossRef] [PubMed]
- Molofsky, A.V.; Pardal, R.; Iwashita, T.; Park, I.-K.; Clarke, M.F.; Morrison, S.J. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003, 425, 962–967. [Google Scholar] [CrossRef] [PubMed]
- Almeida, M.; Pintacuda, G.; Masui, O.; Koseki, Y.; Gdula, M.; Cerase, A.; Brown, D.; Mould, A.; Innocent, C.; Nakayama, M.; et al. PCGF3/5-PRC1 initiates Polycomb recruitment in X chromosome inactivation. Science 2017, 356, 1081–1084. [Google Scholar] [CrossRef] [PubMed]
- Si, S.; Nakajima-Takagi, Y.; Aoyama, K.; Oshima, M.; Saraya, A.; Sugishita, H.; Nakayama, M.; Ishikura, T.; Koseki, H.; Iwama, A. Loss of Pcgf5 Affects Global H2A Monoubiquitination but Not the Function of Hematopoietic Stem and Progenitor Cells. PLoS ONE 2016, 11, e0154561. [Google Scholar] [CrossRef] [PubMed]
- Gao, Z.; Lee, P.; Stafford, J.M.; von Schimmelmann, M.; Schaefer, A.; Reinberg, D. An AUTS2-Polycomb complex activates gene expression in the CNS. Nature 2014, 516, 349–354. [Google Scholar] [CrossRef] [PubMed]
- Buchou, T.; Vernet, M.; Blond, O.; Jensen, H.H.; Pointu, H.; Olsen, B.B.; Cochet, C.; Issinger, O.-G.; Boldyreff, B. Disruption of the regulatory beta subunit of protein kinase CK2 in mice leads to a cell-autonomous defect and early embryonic lethality. Mol. Cell. Biol. 2003, 23, 908–915. [Google Scholar] [CrossRef] [PubMed]
- Cozza, G.; Meggio, F.; Moro, S. The dark side of protein kinase CK2 inhibition. Curr. Med. Chem. 2011, 18, 2867–2884. [Google Scholar] [CrossRef] [PubMed]
- Cozza, G.; Pinna, L.A.; Moro, S. Kinase CK2 inhibition: An update. Curr. Med. Chem. 2013, 20, 671–693. [Google Scholar] [CrossRef] [PubMed]
- Huillard, E.; Ziercher, L.; Blond, O.; Wong, M.; Deloulme, J.-C.; Souchelnytskyi, S.; Baudier, J.; Cochet, C.; Buchou, T. Disruption of CK2beta in embryonic neural stem cells compromises proliferation and oligodendrogenesis in the mouse telencephalon. Mol. Cell. Biol. 2010, 30, 2737–2749. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seldin, D.C.; Xu, X.; Toselli, P.A.; Russell, L.D. Globozoospermia in mice lacking the casein kinase II alpha’ catalytic subunit. Nat. Genet. 1999, 23, 118–121. [Google Scholar] [CrossRef] [PubMed]
- Escalier, D.; Silvius, D.; Xu, X. Spermatogenesis of mice lacking CK2alpha’: Failure of germ cell survival and characteristic modifications of the spermatid nucleus. Mol. Reprod. Dev. 2003, 66, 190–201. [Google Scholar] [CrossRef] [PubMed]
- Lou, D.Y.; Dominguez, I.; Toselli, P.; Landesman-Bollag, E.; O’Brien, C.; Seldin, D.C. The Alpha Catalytic Subunit of Protein Kinase CK2 Is Required for Mouse Embryonic Development. Mol. Cell. Biol. 2008, 28, 131–139. [Google Scholar] [CrossRef] [PubMed]
- Alvarez, L.M.; Revuelta-Cervantes, J.; Dominguez, I. CK2 in Embryonic Development. In Protein Kinase CK2; John Wiley & Sons, Inc.: Oxford, UK, 2013; pp. 129–168. ISBN 9781118482490. [Google Scholar]
- Sultana, R.; Yu, C.-E.; Yu, J.; Munson, J.; Chen, D.; Hua, W.; Estes, A.; Cortes, F.; de la Barra, F.; Yu, D.; et al. Identification of a novel gene on chromosome 7q11.2 interrupted by a translocation breakpoint in a pair of autistic twins. Genomics 2002, 80, 129–134. [Google Scholar] [CrossRef] [PubMed]
- Oksenberg, N.; Ahituv, N. The role of AUTS2 in neurodevelopment and human evolution. Trends Genet. 2013, 29, 600–608. [Google Scholar] [CrossRef] [PubMed]
- Rothkoff, G.; Reisman, M.; Tal, N.; Shani, O.; Nissim-Rafinia, M.; Meshorer, E.; Shifman, S. Isoform Dependent Functions of AUTS2 During Neuronal Differentiation. Eur. Neuropsychopharmacol. 2017, 27, S372–S373. [Google Scholar] [CrossRef]
- Prakash, S.; Robbins, P.W. Cloning and Analysis of the cDNA for Human Fibrosin, a Novel Fibrogenic Lymphokine. DNA Cell Biol. 1998, 17, 879–884. [Google Scholar] [CrossRef] [PubMed]
- Trimarchi, J.M.; Lees, J.A. Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 2002, 3, 11–20. [Google Scholar] [CrossRef] [PubMed]
- Cam, H.; Dynlacht, B.D. Emerging roles for E2F: Beyond the G1/S transition and DNA replication. Cancer Cell 2003, 3, 311–316. [Google Scholar] [CrossRef]
- Polager, S.; Ginsberg, D. E2F—at the crossroads of life and death. Trends Cell Biol. 2008, 18, 528–535. [Google Scholar] [CrossRef] [PubMed]
- Bandara, L.R.; Buck, V.M.; Zamanian, M.; Johnston, L.H.; La Thangue, N.B. Functional synergy between DP-1 and E2F-1 in the cell cycle-regulating transcription factor DRTF1/E2F. EMBO J. 1993, 12, 4317–4324. [Google Scholar] [PubMed]
- Helin, K.; Wu, C.L.; Fattaey, A.R.; Lees, J.A.; Dynlacht, B.D.; Ngwu, C.; Harlow, E. Heterodimerization of the transcription factors E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev. 1993, 7, 1850–1861. [Google Scholar] [CrossRef] [PubMed]
- Krek, W.; Livingston, D.M.; Shirodkar, S. Binding to DNA and the retinoblastoma gene product promoted by complex formation of different E2F family members. Science 1993, 262, 1557–1560. [Google Scholar] [CrossRef] [PubMed]
- Grandori, C.; Cowley, S.M.; James, L.P.; Eisenman, R.N. The Myc/Max/Mad Network and the Transcriptional Control of Cell Behavior. Annu. Rev. Cell Dev. Biol. 2000, 16, 653–699. [Google Scholar] [CrossRef] [PubMed]
- Hurlin, P.J.; Steingrìmsson, E.; Copeland, N.G.; Jenkins, N.A.; Eisenman, R.N. Mga, a dual-specificity transcription factor that interacts with Max and contains a T-domain DNA-binding motif. EMBO J. 1999, 18, 7019–7028. [Google Scholar] [CrossRef] [PubMed]
- Brown, S.E.; Campbell, R.D.; Sanderson, C.M. Novel NG36/G9a gene products encoded within the human and mouse MHC class III regions. Mamm. Genome 2001, 12, 916–924. [Google Scholar] [CrossRef] [PubMed]
- Jones, D.O.; Mattei, M.G.; Horsley, D.; Cowell, I.G.; Singh, P.B. The gene and pseudogenes of Cbx3/mHP1 gamma. DNA Seq. 2001, 12, 147–160. [Google Scholar] [CrossRef] [PubMed]
- Trimarchi, J.M.; Fairchild, B.; Wen, J.; Lees, J.A. The E2F6 transcription factor is a component of the mammalian Bmi1-containing polycomb complex. Proc. Natl. Acad. Sci. USA 2001, 98, 1519–1524. [Google Scholar] [CrossRef] [PubMed]
- Schlisio, S.; Halperin, T.; Vidal, M.; Nevins, J.R. Interaction of YY1 with E2Fs, mediated by RYBP, provides a mechanism for specificity of E2F function. EMBO J. 2002, 21, 5775–5786. [Google Scholar] [CrossRef] [PubMed]
- Zdzieblo, D.; Li, X.; Lin, Q.; Zenke, M.; Illich, D.J.; Becker, M.; Müller, A.M. Pcgf6, a Polycomb Group Protein, Regulates Mesodermal Lineage Differentiation in Murine ESCs and Functions in iPS Reprogramming. Stem Cells 2014, 32, 3112–3125. [Google Scholar] [CrossRef] [PubMed]
- Zhao, W.; Tong, H.; Huang, Y.; Yan, Y.; Teng, H.; Xia, Y.; Jiang, Q.; Qin, J. Essential Role for Polycomb Group Protein Pcgf6 in Embryonic Stem Cell Maintenance and a Noncanonical Polycomb Repressive Complex 1 (PRC1) Integrity. J. Biol. Chem. 2017, 292, 2773–2784. [Google Scholar] [CrossRef] [PubMed]
- Yang, C.-S.; Chang, K.-Y.; Dang, J.; Rana, T.M. Polycomb Group Protein Pcgf6 Acts as a Master Regulator to Maintain Embryonic Stem Cell Identity. Sci. Rep. 2016, 6, 26899. [Google Scholar] [CrossRef] [PubMed]
- Sun, J.; Wang, J.; He, L.; Lin, Y.; Wu, J. Knockdown of polycomb-group RING finger 6 modulates mouse male germ cell differentiation in vitro. Cell. Physiol. Biochem. 2015, 35, 339–352. [Google Scholar] [CrossRef] [PubMed]
- Stielow, C.; Stielow, B.; Finkernagel, F.; Scharfe, M.; Jarek, M.; Suske, G. SUMOylation of the polycomb group protein L3MBTL2 facilitates repression of its target genes. Nucleic Acids Res. 2014, 42, 3044–3058. [Google Scholar] [CrossRef] [PubMed]
- Shen-Li, H.; O’Hagan, R.C.; Hou, H.; Horner, J.W.; Lee, H.W.; DePinho, R.A. Essential role for Max in early embryonic growth and development. Genes Dev. 2000, 14, 17–22. [Google Scholar] [PubMed]
- Washkowitz, A.J.; Schall, C.; Zhang, K.; Wurst, W.; Floss, T.; Mager, J.; Papaioannou, V.E. Mga is essential for the survival of pluripotent cells during peri-implantation development. Development 2015, 142, 31–40. [Google Scholar] [CrossRef] [PubMed]
- Storre, J.; Elsässer, H.-P.; Fuchs, M.; Ullmann, D.; Livingston, D.M.; Gaubatz, S. Homeotic transformations of the axial skeleton that accompany a targeted deletion of E2f6. EMBO Rep. 2002, 3, 695–700. [Google Scholar] [CrossRef] [PubMed]
- Pohlers, M.; Truss, M.; Frede, U.; Scholz, A.; Strehle, M.; Kuban, R.-J.; Hoffmann, B.; Morkel, M.; Birchmeier, C.; Hagemeier, C. A Role for E2F6 in the Restriction of Male-Germ-Cell-Specific Gene Expression. Curr. Biol. 2005, 15, 1051–1057. [Google Scholar] [CrossRef] [PubMed]
- Kohn, M.J.; Bronson, R.T.; Harlow, E.; Dyson, N.J.; Yamasaki, L. Dp1 is required for extra-embryonic development. Development 2003, 130, 1295–1305. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, A.; Hirasaki, M.; Okuda, A. Does MAX open up a new avenue for meiotic research? Dev. Growth Differ. 2017, 59, 61–69. [Google Scholar] [CrossRef] [PubMed]
- Leeb, M.; Pasini, D.; Novatchkova, M.; Jaritz, M.; Helin, K.; Wutz, A. Polycomb complexes act redundantly to repress genomic repeats and genes. Genes Dev. 2010, 24, 265–276. [Google Scholar] [CrossRef] [PubMed]
- Blackledge, N.P.; Rose, N.R.; Klose, R.J. Targeting Polycomb systems to regulate gene expression: Modifications to a complex story. Nat. Rev. Mol. Cell Biol. 2015, 16, 643–649. [Google Scholar] [CrossRef] [PubMed]
- Eid, A.; Torres-Padilla, M.-E. Characterization of non-canonical Polycomb Repressive Complex 1 subunits during early mouse embryogenesis. Epigenetics 2016, 11, 389–397. [Google Scholar] [CrossRef] [PubMed]
- Woo, C.J.; Kharchenko, P.V.; Daheron, L.; Park, P.J.; Kingston, R.E. A Region of the Human HOXD Cluster that Confers Polycomb-Group Responsiveness. Cell 2010, 140, 99–110. [Google Scholar] [CrossRef] [PubMed]
- Yu, M.; Mazor, T.; Huang, H.; Huang, H.-T.; Kathrein, K.L.; Woo, A.J.; Chouinard, C.R.; Labadorf, A.; Akie, T.E.; Moran, T.B.; et al. Direct Recruitment of Polycomb Repressive Complex 1 to Chromatin by Core Binding Transcription Factors. Mol. Cell 2012, 45, 330–343. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Birchler, J.A.; Veitia, R.A. The gene balance hypothesis: Implications for gene regulation, quantitative traits and evolution. New Phytol. 2010, 186, 54–62. [Google Scholar] [CrossRef] [PubMed]
- Strübbe, G.; Popp, C.; Schmidt, A.; Pauli, A.; Ringrose, L.; Beisel, C.; Paro, R. Polycomb purification by in vivo biotinylation tagging reveals cohesin and Trithorax group proteins as interaction partners. Proc. Natl. Acad. Sci. USA 2011, 108, 5572–5577. [Google Scholar] [CrossRef] [PubMed]
- Chittock, E.C.; Latwiel, S.; Miller, T.C.R.; Müller, C.W. Molecular architecture of polycomb repressive complexes. Biochem. Soc. Trans. 2017, 45, 193–205. [Google Scholar] [CrossRef] [PubMed]
- Wong, S.J.; Gearhart, M.D.; Taylor, A.B.; Nanyes, D.R.; Ha, D.J.; Robinson, A.K.; Artigas, J.A.; Lee, O.J.; Demeler, B.; Hart, P.J.; et al. KDM2B Recruitment of the Polycomb Group Complex, PRC1.1, Requires Cooperation between PCGF1 and BCORL1. Structure 2016, 24, 1795–1801. [Google Scholar] [CrossRef] [PubMed]
- Rose, N.R.; King, H.W.; Blackledge, N.P.; Fursova, N.A.; Ember, K.J.; Fischer, R.; Kessler, B.M.; Klose, R.J. RYBP stimulates PRC1 to shape chromatin-based communication between Polycomb repressive complexes. Elife 2016, 5. [Google Scholar] [CrossRef] [PubMed]
- Maezawa, S.; Hasegawa, K.; Yukawa, M.; Sakashita, A.; Alavattam, K.G.; Andreassen, P.R.; Vidal, M.; Koseki, H.; Barski, A.; Namekawa, S.H. Polycomb directs timely activation of germline genes in spermatogenesis. Genes Dev. 2017, 31, 1693–1703. [Google Scholar] [CrossRef] [PubMed]
- Brookes, E.; de Santiago, I.; Hebenstreit, D.; Morris, K.J.; Carroll, T.; Xie, S.Q.; Stock, J.K.; Heidemann, M.; Eick, D.; Nozaki, N.; 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. [Google Scholar] [CrossRef] [PubMed]
- Kar, G.; Kim, J.K.; Kolodziejczyk, A.A.; Natarajan, K.N.; Torlai Triglia, E.; Mifsud, B.; Elderkin, S.; Marioni, J.C.; Pombo, A.; Teichmann, S.A. Flipping between Polycomb repressed and active transcriptional states introduces noise in gene expression. Nat. Commun. 2017, 8, 36. [Google Scholar] [CrossRef] [PubMed]
- Shan, Y.; Liang, Z.; Xing, Q.; Zhang, T.; Wang, B.; Tian, S.; Huang, W.; Zhang, Y.; Yao, J.; Zhu, Y.; et al. PRC2 specifies ectoderm lineages and maintains pluripotency in primed but not naïve ESCs. Nat. Commun. 2017, 8, 672. [Google Scholar] [CrossRef] [PubMed]
- Blakeley, P.; Fogarty, N.M.E.; del Valle, I.; Wamaitha, S.E.; Hu, T.X.; Elder, K.; Snell, P.; Christie, L.; Robson, P.; Niakan, K.K. Defining the three cell lineages of the human blastocyst by single-cell RNA-seq. Development 2015, 142, 3151–3165. [Google Scholar] [CrossRef] [PubMed]
Short Name of Mouse Homolog | Synonyms | ID Numbers (MGI, UNIPROT) | Chromosomal Localization | Drosophila Orthologs | Protein Domains and Conserved Regions | Complex |
---|---|---|---|---|---|---|
Auts2 | - | MGI:1919847 UniProt Q8VDM3 | Ch: 5 | TAY limited similarity | None predicted | ncPRC 1.3/1.5 |
Bcor | - | MGI:1918708 UniProt: Q8CGN4 | Ch: X | CG14073 limited similarity | PFUD:PCGF1 binding domain, Ankyrin repeat: protein interaction Blc6 non ankyrin domain | ncPRC1.1 and BCOR |
Cbx3 | Hp1γ | MGI:109372 UniProt Q61686 | Ch: 15 | HP1 | Chromo domain: H3K27 binding Chromo shadow: dimerization, protein binding | ncPRC 1.6 |
Csnk2a2 | Ck2 | MGI:88547 UniProt O54833 | Ch: 8 | CKIIalfa | Protein kinase domain: catalytic, phosphorylation | ncPRC 1.3/1.5 |
E2f6 | - | MGI:1354159 UniProt O54917 | Ch: 12 | No homolog identified | Winged helix-like: DNA binding CC-MB domain: E2F-DP1 dimerization | ncPRC1.6 |
Fbrs | Fbs, Fbs1 | MGI:104648 UniProt Q8R089 | Ch: 7 | TAY has limited similarity | None predicted | ncPRC 1.3/1.5 |
Hdac1 | Rpd3, Hd1 | MGI:108086 UniProt O09106 | Ch: 4 | HDAC1/RPD3 | Histone deacetylase domain: removing acetyl group from histones | ncPRC 1.6 |
Hdac2 | Yaf1, Yy1bp | MGI:1097691 UniProt P70288 | Ch: 10 | HDAC1/RPD3 | Histone deacetylase domain: removing acetyl group from histones | ncPRC 1.6 |
Kdm2b | Fbxl10, Jhdm1b, Cxxc2, | MGI:1354737 UniProt Q6P1G2 | Ch: 5 | dKDM2 | Ring domain: protein interaction JMJC domain: histone demethylation FBOX: protein interaction with SKP1 Zn finger CXXC: CpG binding | ncPRC1.1 and BCOR |
L3mbtl2 | M4mbt | MGI:2443584 UniProt P59178 | Ch: 15 | L3MBT | FCS-type Zn finger: 4 MBT: mono-, dimethylated histone binding | ncPRC 1.6 |
Max | bHLHd4 | MGI:96921 UniProt P28574 | Ch: 12 | MAX | HLH: DNA binding | ncPRC 1.6 |
Mga | Cdrap, Mia1 | MGI:109615 UnidKDM2Prot Q61865 | Ch: 7 | BYN/TRG limited similarity | T-box: DNA binding CDD, HLH: DNA binding | ncPRC 1.6 |
Pcgf1 | Nspc1, Rnf68 | MGI:1917087 UniProt Q8R023 | Ch: 6 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: BCOR binding | ncPRC1.1 |
Pcgf2 | Mel18 | MGI:99161 UniProt P23798 | Ch: 11 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: protein interaction | ncPRC1.2/1.4 |
Pcgf3 | Dong1, Rnf3 | MGI:1916837 UniProt Q8BTQ0 | Ch: 5 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: protein interaction | ncPRC 1.3/1.5 |
Pcgf4 | Bmi1, Rnf51 | MGI:88174 UniProt P25916 | Ch: 2 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: protein interaction | ncPRC 1.2/1.4 |
Pcgf5 | Rnf159 | MGI:1923505 UniProt Q3UK78 | Ch: 19 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: protein interaction | ncPRC 1.3/1.5 |
Pcgf6 | Mblr, Rnf134 | MGI:1918291 UniProt Q99NA9 | Ch: 19 | PSC, SU(Z)2 | Ring domain: dimerization RAWUL: protein interaction | ncPRC 1.6 |
Ring1 | Ring1A | MGI:1101770 UniProt: O35730 | Ch: 17 | SCE/dRING | Ring domain: dimerization RAWUL: Cbx, Rybp binding | CORE |
Rnf2 | Ring2, Ring1B, dinG | MGI:1101759 UniProt Q9CQJ4 | Ch: 1 | SCE/dRING | Ring domain: dimerization RAWUL: Cbx, Rybp binding | CORE |
Rybp | Dedaf, Yeaf1 | MGI:1929059 UniProt Q8CCI5 | Ch: 6 | dRYBP | RanBP2-type Zn finger: YAF2/RYBP C-terminal binding: RING binding | CORE |
Skp1a | Skp1, p19 | MGI:103575 UniProt Q9WTX5 | Ch: 11 | dSKPA | POZ domain, dimerization domain | ncPRC1.1 |
Tfdp1 | Dp1, Drtf1 | MGI:101934 UniProt Q08639 | Ch: 8 | dDP | Winged helix-like: DNA binding Dimerization domain: E2F-DP1 dimerization | ncPRC1.6 |
Usp7 | Hausp | MGI:2182061 UniProt Q6A4J8 | Ch: 16 | USP7 | MATH/TRAF, ubiquitin protease | ncPRC1.1 |
Wdr5 | Big, Big3 | MGI:2155884 UniProt P61965 | Ch: 2 | WDS | WD repeats | ncPRC1.6 |
Yaf2 | - | MGI:1914307 UniProt Q99LW6 | Ch: 15 | Only RYBP present | RanBP2-type Zn finger: YAF2/RYBP C-terminal binding: RING binding | CORE |
Yy1 | - | MGI:99150 UniProt Q00899 | Ch: 12 | PHO | CH2 Zn-finger: DNA binding REPO: Recruitment of PC | INTERACTOR of Rybp/Yaf2 |
Gene Name | Embryonic Phenotype | Extra-Embryonic Phenotype | ES Cell Phenotype | Role in Lineage Commitment | Ref. | ||||
---|---|---|---|---|---|---|---|---|---|
NEU | CAR | HEM | GER | MISC | |||||
Ring1 | Ring1−/− viable | ND | No | No | No | No | No | Homeotic transformation of the axial skeleton | [151] |
Rnf2 | Rnf2−/− E6.5–E7.0 lethal Rnf2+/− mice are viable with homeotic transformations | Defects | No | Premature differentiation | Premature differentiation | ND | ND | ND | [226,227,228,229,230] |
Ring1-Rnf2 double knockout | ND | ND | Proliferation arrest | ND | ND | ND | ND | ND | [235] |
Rybp | Rybp−/− E5.0–E6.0 lethal; Rybp+/−semipenetrant lethal at birth due to NTDs | ND | No | Impairment in terminal phase of differentiation | Impairment in contractile cardiomyocyte formation | Increased number of B-1 progenitors and loss of B-2 progenitors | ND | ND | [166,240,243,244,245] |
Yaf2 | Yaf2−/− ND | ND | ND | ND | ND | ND | ND | ND | - |
Gene Name | Embryonic Phenotype | Extra-Embryonic Phenotype | ES Cell Phenotype | Role in Lineage Commitment | Ref. | ||||
---|---|---|---|---|---|---|---|---|---|
NEU | CAR | HEM | GERM | MISC | |||||
Pcgf1 | ND | ND | Impaired differentiation | Promotes ectodermal lineage specification | Promotes mesodermal lineage specification | Promotes mesodermal lineage specification | No | Promotes ectodermal lineage specification | [264] |
Kdm2b | Kdm2b−/− semipenetrant lethal at birth due to NTDs | ND | Premature differentiation | Altered cell-cycle processes in neural precursors | Induces early mesoderm differentiation | Impaired hematopoiesis | Reduced number of spermatozoa | Induces early endoderm differentiation | [162,280,282] |
Bcor | Bcor−/− E5–E6.5 male lethal | Defect in extraembryonic tissues | ND | Delayed activation of genes responsible for ectodermal lineage specification | Delayed activation of genes responsible for mesodermal lineage specification; failure of heart looping | Impaired mesodermal lineage specification; and primitive erythrocyte formation | ND | ND | [272,273] |
Skp1 | Skp1−/− ND | ND | ND | Increases susceptibility to cell death in neuronal cells in mice | ND | Reduced proliferation in the lymphoid organs | ND | Hypoplasia | [289,290] |
Usp7 | Usp7−/− E6.5–E7.5 lethal | Defect in extraembryonic tissues | ND | Promotes neuronal differentiation and disrupts self-renewal | ND | ND | ND | Compromised osteogenic differentiation | [294,296,298] |
Gene Name | Embryonic Phenotype | Extra-Embryonic Phenotype | ES Cell Phenotype | Role in Lineage Commitment | Ref. | ||||
---|---|---|---|---|---|---|---|---|---|
NEU | CAR | HEM | GERM | MISC | |||||
Pcgf2 | Pcgf2−/− viable, but growth retardation, posterior transformations of the axial skeleton | No | No | ND | Impairs proper cardiac differentiation | Compromised T and B lymphocyte development | ND | Hypertrophy of intestinal smooth muscle, obstruction of the lower intestine | [80,301,305] |
Pcgf4 | Pcgf4−/− viable | No | Defect in postnatal stem cell maintenance in hematopoietic and neural tissues | Postnatal stem cell maintenance in neural tissues; neurological abnormalities | Represses cardio-myocyte fate | Postnatal stem cell maintenance in hematopoietic tissues; defect in hematopoiesis | ND | ND | [148,306,307,310] |
Gene Name | Embryonic Phenotype | Extra-Embryonic | ES Cell Phenotype | Role in Lineage Commitment | Ref. | ||||
---|---|---|---|---|---|---|---|---|---|
NEU | CAR | HEM | GERM | MISC | |||||
Pcgf3 | Pcgf3−/− viable | No | No | No | No | No | No | Impairs mesoderm differentiation, absent spleen | [180,311] |
Pcgf5 | Pcgf5−/− viable | No | No | No | No | No | No | Impairs mesoderm differentiation | [31,32] |
Pcgf3-Pcgf5 double knockout | Pcgf3−/−/Pcgf5−/− female-specific embryo lethality at mid-gestation | Placental defects; lack of throphoblast and labirynth cell layers | No | No | No | No | No | Impairs mesoderm differentiation | [311] |
Auts2 | Auts2−/− ND | ND | ND | Defects in CNS development in mice; Auts2+/− ES cells have premature neuronal differentiation during in vitro corticogenesis | Mesodermal genes are upregulated in Auts2+/− ES cells during in vitro corticogenesis | ND | ND | ND | [311,313] |
Fbrs | Fbrs−/− ND | ND | ND | ND | ND | ND | ND | ND | - |
Ck2 β * | Ck2 β−/− E3.5 lethal | ND | CK2β is required for stem cell maintenance | In NES conditional mutants defect in oligodendrogenesis in telencephalon; NTDs | ND | Improper hematopoietic differentiation | Male mice are infertile | Improper adipogenic and osteogenic differentiation | [317,318,319,320] |
CK2α * | CK2α−/− E9.5–10.5 lethal | ND | ND | ND | NTDs. improper branchial arch and heart development | ND | ND | ND | [318,319,320] |
CK2α’ * | CK2α’−/− viable but infertile | ND | ND | ND | ND | ND | Defect in germ cell development | ND | [318,319,320] |
Gene Name | Embryonic Phenotype | Extra-Embryonic Phenotype | ES Cell Phenotype | Role in Lineage Commitment | Ref. | ||||
---|---|---|---|---|---|---|---|---|---|
NEU | CAR | HEM | GERM | MISC | |||||
Pcgf6 | Pcgf6−/− ND | ND | Decreased proliferation; required for maintaining ES cell pluripotency | ND | ND | Suppresses dendritic cell activation | Suppress premature differentiation; Ectopic male germ cell specific gene expression | Ectopic mesodermal specific gene expression | [173,338,339,340,341] |
E2f6 | E2f6−/− viable with homeotic transformations | No | ND | No | No | No | Oligozospermia, ectopic male germ cell specific gene expression | ND | [345,346] |
Tfdp1 | Tfdp1−/− E10.5–E11.5 lethal | Defect in trophectoderm development, disorganized ectoplacental cone | ND | ND | ND | ND | ND | ND | [347] |
L3mbtl2 | L3mbtl2−/− E6.5 lethal | No distinct pro-amniotic cavity, chorion or amnion | Compromised proliferation of ES cells | ND | ND | ND | ND | No EB formation | [215] |
Max | Max−/− E5.0–E5.5 lethal | Growth arrest | Compromised proliferation of ES cells | ND | ND | ND | Early meiotic entry in vitro ectopic expression of germ cell related genes | ND | [181,182,343] |
Mga | Mga−/− E5.0–E5.5 lethal | Empty decidua capsularis | Not viable | ND | ND | ND | ND | ND | [344] |
Cbx3 | Cbx3−/− viable | No | ND | ND | ND | ND | Compromised spermatogenesis, male infertility, small testis | ND | [335] |
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Bajusz, I.; Kovács, G.; Pirity, M.K. From Flies to Mice: The Emerging Role of Non-Canonical PRC1 Members in Mammalian Development. Epigenomes 2018, 2, 4. https://doi.org/10.3390/epigenomes2010004
Bajusz I, Kovács G, Pirity MK. From Flies to Mice: The Emerging Role of Non-Canonical PRC1 Members in Mammalian Development. Epigenomes. 2018; 2(1):4. https://doi.org/10.3390/epigenomes2010004
Chicago/Turabian StyleBajusz, Izabella, Gergő Kovács, and Melinda K. Pirity. 2018. "From Flies to Mice: The Emerging Role of Non-Canonical PRC1 Members in Mammalian Development" Epigenomes 2, no. 1: 4. https://doi.org/10.3390/epigenomes2010004