Polycomb silencers control cell fate, development and cancer (original) (raw)
Jones, P. A. & Baylin, S. B. The fundamental role of epigenetic events in cancer. Nature Rev. Genet.3, 415–428 (2002). ArticleCASPubMed Google Scholar
Martinez, A. M. & Cavalli, G. The role of Polycomb group proteins in cell cycle regulation during development. Cell Cycle5, 1189–1197 (2006). ArticleCASPubMed Google Scholar
Valk-Lingbeek, M. E., Bruggeman, S. W. & van Lohuizen, M. Stem cells and cancer; the Polycomb connection. Cell118, 409–418 (2004). ArticleCASPubMed Google Scholar
Gil, J., Bernard, D. & Peters, G. Role of Polycomb group proteins in stem cell self-renewal and cancer. DNA Cell Biol.24, 117–125 (2005). ArticleCASPubMed Google Scholar
Ringrose, L. & Paro, R. Epigenetic regulation of cellular memory by the Polycomb and trithorax group proteins. Annu. Rev. Genet.38, 413–443 (2004). ArticleCASPubMed Google Scholar
Akasaka, T. et al. A role for mel-18, a Polycomb group-related vertebrate gene, during theanteroposterior specification of the axial skeleton. Development122, 1513–1522 (1996). ArticleCASPubMed Google Scholar
Core, N. et al. Altered cellular proliferation and mesoderm patterning in Polycomb-M33-deficient mice. Development124, 721–729 (1997). ArticleCASPubMed Google Scholar
del Mar Lorente, M. et al. Loss- and gain-of-function mutations show a Polycomb group function for Ring1A in mice. Development127, 5093–5100 (2000). ArticleCASPubMed Google Scholar
van der Lugt, N. M. et al. Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev.8, 757–769 (1994). ArticleCASPubMed Google Scholar
Levine, S. S., King, I. F. & Kingston, R. E. Division of labor in Polycomb group repression. Trends Biochem. Sci.29, 478–485 (2004). ArticleCASPubMed Google Scholar
Lund, A. H. & van Lohuizen, M. Polycomb complexes and silencing mechanisms. Curr. Opin. Cell Biol.16, 239–246 (2004). ArticleCASPubMed Google Scholar
Cao, R. et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science298, 1039–1043 (2002). ArticleCASPubMed Google Scholar
Czermin, B. et al. Drosophila Enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell111, 185–196 (2002). ArticleCASPubMed Google Scholar
Muller, J. et al. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell111, 197–208 (2002). ArticleCASPubMed Google Scholar
Fischle, W. et al. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev.17, 1870–1881 (2003). ArticleCASPubMedPubMed Central Google Scholar
Min, J., Zhang, Y. & Xu, R. M. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev.17, 1823–1828 (2003). ArticleCASPubMedPubMed Central Google Scholar
Wang, H. et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature431, 873–878 (2004). ArticleCASPubMed Google Scholar
Francis, N. J., Kingston, R. E. & Woodcock, C. L. Chromatin compaction by a Polycomb group protein complex. Science306, 1574–1577 (2004). ArticleCASPubMed Google Scholar
Papp, B. & Muller, J. Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev.20, 2041–2054 (2006). ArticleCASPubMedPubMed Central Google Scholar
Schwartz, Y. B. et al. Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nature Genet.38, 700–705 (2006). ArticleCASPubMed Google Scholar
Klymenko, T. et al. A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev.20, 1110–1122 (2006). ArticleCASPubMedPubMed Central Google Scholar
Grimaud, C. et al. RNAi components are required for nuclear clustering of Polycomb group response elements. Cell124, 957–971 (2006). ArticleCASPubMed Google Scholar
Otte, A. P. & Kwaks, T. H. Gene repression by Polycomb group protein complexes: a distinct complex for every occasion? Curr. Opin. Genet. Dev.13, 448–454 (2003). ArticleCASPubMed Google Scholar
Dellino, G. I. et al. Polycomb silencing blocks transcription initiation. Mol. Cell13, 887–893 (2004). ArticleCASPubMed Google Scholar
Francis, N. J. & Kingston, R. E. Mechanisms of transcriptional memory. Nature Rev. Mol. Cell Biol.2, 409–421 (2001). ArticleCAS Google Scholar
Wang, L. et al. Hierarchical recruitment of Polycomb group silencing complexes. Mol. Cell14, 637–646 (2004). ArticleCASPubMed Google Scholar
Cao, R., Tsukada, Y. & Zhang, Y. Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol. Cell20, 845–854 (2005). ArticleCASPubMed Google Scholar
Kuzmichev, A., Jenuwein, T., Tempst, P. & Reinberg, D. Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol. Cell14, 183–193 (2004). Data are presented to indicate that the substrate specificity of distinct 'PRC2-like' complexes is determined by association with different EED isoforms. ArticleCASPubMed Google Scholar
Daujat, S., Zeissler, U., Waldmann, T., Happel, N. & Schneider, R. HP1 binds specifically to Lys26-methylated histone H1.4, whereas simultaneous Ser27 phosphorylation blocks HP1 binding. J. Biol. Chem.280, 38090–38095 (2005). ArticleCASPubMed Google Scholar
Vire, E. et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature439, 871–874 (2006). The first demonstration of a direct link between PcG-mediated gene repression and DNA methylation, two key mechanisms of epigenetic silencing. ArticleCASPubMed Google Scholar
Haupt, Y., Alexander, W. S., Barri, G., Klinken, S. P. & Adams, J. M. Novel zinc finger gene implicated as myc collaborator by retrovirally accelerated lymphomagenesis in E mu-myc transgenic mice. Cell65, 753–763 (1991). ArticleCASPubMed Google Scholar
van Lohuizen, M. et al. Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell65, 737–752 (1991). ArticleCASPubMed Google Scholar
Jacobs, J. J., Kieboom, K., Marino, S., DePinho, R. A. & van Lohuizen, M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature397, 164–168 (1999). ArticleCASPubMed Google Scholar
Jacobs, J. J. et al. Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ARF. Genes Dev.13, 2678–2690 (1999). References 33 and 34 identify theCdkn2alocus as a crucial target of BMI1. ArticleCASPubMedPubMed Central Google Scholar
Sherr, C. J. The INK4a/ARF network in tumour suppression. Nature Rev. Mol. Cell Biol.2, 731–737 (2001). ArticleCAS Google Scholar
Lowe, S. W. & Sherr, C. J. Tumor suppression by Ink4a–Arf: progress and puzzles. Curr. Opin. Genet. Dev.13, 77–83 (2003). ArticleCASPubMed Google Scholar
Gil, J., Bernard, D., Martinez, D. & Beach, D. Polycomb CBX7 has a unifying role in cellular lifespan. Nature Cell Biol.6, 67–72 (2004). ArticleCASPubMed Google Scholar
Voncken, J. W. et al. RNF2 (RING1b) deficiency causes gastrulation arrest and cell cycle inhibition. Proc. Natl Acad. Sci. USA100, 2468–2473 (2003). ArticleCASPubMedPubMed Central Google Scholar
Lessard, J. et al. Functional antagonism of the Polycomb-group genes eed and _Bmi_1 in hemopoietic cell proliferation. Genes Dev.13, 2691–2703 (1999). ArticleCASPubMedPubMed Central Google Scholar
Ohta, H. et al. Polycomb group gene rae28 is required for sustaining activity of hematopoietic stem cells. J. Exp. Med.195, 759–770 (2002). ArticleCASPubMedPubMed Central Google Scholar
Kirmizis, A., Bartley, S. M. & Farnham, P. J. Identification of the Polycomb group protein SU(Z)12 as a potential molecular target for human cancer therapy. Mol. Cancer Ther.2, 113–121 (2003). CASPubMed Google Scholar
van Kemenade, F. J. et al. Coexpression of BMI-1 and EZH2 Polycomb-group proteins is associated with cycling cells and degree of malignancy in B-cell non-Hodgkin lymphoma. Blood97, 3896–3901 (2001). ArticleCASPubMed Google Scholar
Raaphorst, F. M. et al. Coexpression of BMI-1 and EZH2 Polycomb group genes in Reed–Sternberg cells of Hodgkin's disease. Am. J. Pathol.157, 709–715 (2000). ArticleCASPubMedPubMed Central Google Scholar
Visser, H. P. et al. The Polycomb group protein EZH2 is upregulated in proliferating, cultured human mantle cell lymphoma. Br. J. Haematol.112, 950–958 (2001). ArticleCASPubMed Google Scholar
Bracken, A. P. et al. EZH2 is downstream of the pRB–E2F pathway, essential for proliferation and amplified in cancer. EMBO J.22, 5323–5335 (2003). ArticleCASPubMedPubMed Central Google Scholar
Kleer, C. G. et al. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc. Natl Acad. Sci. USA100, 11606–11611 (2003). ArticleCASPubMedPubMed Central Google Scholar
Varambally, S. et al. The Polycomb group protein EZH2 is involved in progression of prostate cancer. Nature419, 624–629 (2002). ArticleCASPubMed Google Scholar
Su, I. H. et al. Polycomb group protein EZH2 controls actin polymerization and cell signaling. Cell121, 425–436 (2005). ArticleCASPubMed Google Scholar
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.20, 1123–1136 (2006). ArticleCASPubMedPubMed Central Google Scholar
Kuzmichev, A. et al. Composition and histone substrates of Polycomb repressive group complexes change during cellular differentiation. Proc. Natl Acad. Sci. USA102, 1859–1864 (2005). Based on data obtained in a mouse model for prostate cancer, the authors speculate that changes in PcG complex composition reset gene expression patterns, thereby promoting tumour progression. ArticleCASPubMedPubMed Central Google Scholar
Boyer, L. A. et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature441, 349–353 (2006). ArticleCASPubMed Google Scholar
Lee, T. I. et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell125, 301–313 (2006). References 49, 52 and 53 globally map PcG binding sites in mammalian embryonic cell lines and analyse changes at PcG target genes during differentiation. ArticleCASPubMedPubMed Central Google Scholar
Pardal, R., Clarke, M. F. & Morrison, S. J. Applying the principles of stem-cell biology to cancer. Nature Rev. Cancer3, 895–902 (2003). ArticleCAS Google Scholar
Meshorer, E. & Misteli, T. Chromatin in pluripotent embryonic stem cells and differentiation. Nature Rev. Mol. Cell Biol.7, 540–546 (2006). ArticleCAS Google Scholar
Azuara, V. et al. Chromatin signatures of pluripotent cell lines. Nature Cell Biol.8, 532–538 (2006). ArticleCASPubMed Google Scholar
Bernstein, B. E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell125, 315–326 (2006). ArticleCASPubMed Google Scholar
Shumacher, A., Faust, C. & Magnuson, T. Positional cloning of a global regulator of anterior–posterior patterning in mice. Nature383, 250–253 (1996). ArticleCASPubMed Google Scholar
Takihara, Y. et al. Targeted disruption of the mouse homologue of the Drosophila polyhomeotic gene leads to altered anteroposterior patterning and neural crest defects. Development124, 3673–3682 (1997). ArticleCASPubMed Google Scholar
Tolhuis, B. et al. Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nature Genet.38, 694–699 (2006). ArticleCASPubMed Google Scholar
Hombria, J. C. & Lovegrove, B. Beyond homeosis — HOX function in morphogenesis and organogenesis. Differentiation71, 461–476 (2003). ArticlePubMed Google Scholar
Burch, J. B. Regulation of GATA gene expression during vertebrate development. Semin. Cell Dev. Biol.16, 71–81 (2005). ArticleCASPubMed Google Scholar
Schepers, G. E., Teasdale, R. D. & Koopman, P. Twenty pairs of Sox: extent, homology, and nomenclature of the mouse and human Sox transcription factor gene families. Dev. Cell3, 167–170 (2002). ArticleCASPubMed Google Scholar
Loebel, D. A., Watson, C. M., De Young, R. A. & Tam, P. P. Lineage choice and differentiation in mouse embryos and embryonic stem cells. Dev. Biol.264, 1–14 (2003). ArticleCASPubMed Google Scholar
Boyer, L. A. et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell122, 947–956 (2005). First comprehensive description of the core transcriptional network regulated by the pluripotency factors OCT4, SOX2 and Nanog in human ES cells. ArticleCASPubMedPubMed Central Google Scholar
Chambers, I. et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell113, 643–655 (2003). ArticleCASPubMed Google Scholar
Mitsui, K. et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell113, 631–642 (2003). ArticleCASPubMed Google Scholar
Nichols, J. et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell95, 379–391 (1998). ArticleCASPubMed Google Scholar
Caretti, G., Di Padova, M., Micales, B., Lyons, G. E. & Sartorelli, V. The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Genes Dev.18, 2627–2638 (2004). This study shows that EZH2 inhibits muscle cell differentiation in a histone methyltransferase-dependent manner by repressing muscle-specific genes. ArticleCASPubMedPubMed Central Google Scholar
Chen, X., Hiller, M., Sancak, Y. & Fuller, M. T. Tissue-specific TAFs counteract Polycomb to turn on terminal differentiation. Science310, 869–872 (2005). ArticleCASPubMed Google Scholar
Klose, R. J. et al. The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature442, 312–316 (2006). ArticleCASPubMed Google Scholar
Shi, Y. et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell119, 941–953 (2004). ArticleCASPubMed Google Scholar
Tsukada, Y. et al. Histone demethylation by a family of JmjC domain-containing proteins. Nature439, 811–816 (2006). ArticleCASPubMed Google Scholar
Voncken, J. W. et al. Chromatin-association of the Polycomb group protein BMI1 is cell cycle-regulated and correlates with its phosphorylation status. J. Cell Sci.112, 4627–4639 (1999). ArticleCASPubMed Google Scholar
Hernandez-Munoz, I. et al. Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. Proc. Natl Acad. Sci. USA102, 7635–7640 (2005). ArticleCASPubMedPubMed Central Google Scholar
Gunster, M. J. et al. Identification and characterization of interactions between the vertebrate Polycomb-group protein BMI1 and human homologs of polyhomeotic. Mol. Cell. Biol.17, 2326–2335 (1997). ArticleCASPubMedPubMed Central Google Scholar
Kagey, M. H., Melhuish, T. A. & Wotton, D. The Polycomb protein Pc2 is a SUMO E3. Cell113, 127–137 (2003). ArticleCASPubMed Google Scholar
Collins, C. A. et al. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell122, 289–301 (2005). ArticleCASPubMed Google Scholar
Kim, C. F. et al. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell121, 823–835 (2005). ArticleCASPubMed Google Scholar
Montarras, D. et al. Direct isolation of satellite cells for skeletal muscle regeneration. Science309, 2064–2067 (2005). ArticleCASPubMed Google Scholar
Shackleton, M. et al. Generation of a functional mammary gland from a single stem cell. Nature439, 84–88 (2006). ArticleCASPubMed Google Scholar
Stingl, J. et al. Purification and unique properties of mammary epithelial stem cells. Nature439, 993–997 (2006). ArticleCASPubMed Google Scholar
Iwama, A. et al. Enhanced self-renewal of hematopoietic stem cells mediated by the Polycomb gene product Bmi-1. Immunity21, 843–851 (2004). ArticleCASPubMed Google Scholar
Lessard, J. & Sauvageau, G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature423, 255–260 (2003). An elegant study demonstrating that BMI1 is required for the proliferation of leukaemic stem cells. ArticleCASPubMed Google Scholar
Leung, C. et al. Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature428, 337–341 (2004). The authors show that BMI1 is essential for SHH-induced proliferation of cerebellar precursor cells and is implicated in medullablastoma pathogenesis. ArticleCASPubMed Google Scholar
Molofsky, A. V. et al. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature425, 962–967 (2003). ArticleCASPubMedPubMed Central Google Scholar
Park, I. K. et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature423, 302–305 (2003). ArticleCASPubMed Google Scholar
Chagraoui, J. et al. E4F1: a novel candidate factor for mediating BMI1 function in primitive hematopoietic cells. Genes Dev.20, 2110–2120 (2006). ArticleCASPubMedPubMed Central Google Scholar
Lee, N., Maurange, C., Ringrose, L. & Paro, R. Suppression of Polycomb group proteins by JNK signalling induces transdetermination in Drosophila imaginal discs. Nature438, 234–237 (2005). ArticleCASPubMed Google Scholar
Liu, S. et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res.66, 6063–6071 (2006). ArticleCASPubMedPubMed Central Google Scholar
Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J. & Clarke, M. F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA100, 3983–3988 (2003). ArticleCASPubMedPubMed Central Google Scholar
Singh, S. K. et al. Identification of a cancer stem cell in human brain tumors. Cancer Res.63, 5821–5828 (2003). CASPubMed Google Scholar
Pasca di Magliano, M. & Hebrok, M. Hedgehog signalling in cancer formation and maintenance. Nature Rev. Cancer3, 903–911 (2003). Article Google Scholar
Ferres-Marco, D. et al. Epigenetic silencers and Notch collaborate to promote malignant tumours by Rb silencing. Nature439, 430–436 (2006). A genetic screen identifying two epigenetic repressors as collaborators of Notch-induced tumour development. ArticleCASPubMed Google Scholar
Bruggeman, S. W. & van Lohuizen, M. Controlling stem cell proliferation: CKIs at work. Cell Cycle5, 1281–1285 (2006). ArticleCASPubMed Google Scholar
Glinsky, G. V., Berezovska, O. & Glinskii, A. B. Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. J. Clin. Invest.115, 1503–21 (2005). ArticleCASPubMedPubMed Central Google Scholar
van't Veer, L. J. et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature415, 530–536 (2002). ArticleCAS Google Scholar
Strahl, B. D. & Allis, C. D. The language of covalent histone modifications. Nature403, 41–45 (2000). ArticleCASPubMed Google Scholar
Kanno, M., Hasegawa, M., Ishida, A., Isono, K. & Taniguchi, M. mel-18, a Polycomb group-related mammalian gene, encodes a transcriptional negative regulator with tumor suppressive activity. EMBO J.14, 5672–5678 (1995). ArticleCASPubMedPubMed Central Google Scholar
Dejardin, J. et al. Recruitment of Drosophila Polycomb group proteins to chromatin by DSP1. Nature434, 533–538 (2005). ArticleCASPubMed Google Scholar
Klymenko, T. & Muller, J. The histone methyltransferases Trithorax and Ash1 prevent transcriptional silencing by Polycomb group proteins. EMBO Rep.5, 373–377 (2004). ArticleCASPubMedPubMed Central Google Scholar
Raman, J. D. et al. Increased expression of the Polycomb group gene, EZH2, in transitional cell carcinoma of the bladder. Clin. Cancer Res.11, 8570–8576 (2005). ArticleCASPubMed Google Scholar
Arisan, S. et al. Increased expression of EZH2, a Polycomb group protein, in bladder carcinoma. Urol. Int.75, 252–257 (2005). ArticleCASPubMed Google Scholar
Weikert, S. et al. Expression levels of the EZH2 Polycomb transcriptional repressor correlate with aggressiveness and invasive potential of bladder carcinomas. Int. J. Mol. Med.16, 349–353 (2005). CASPubMed Google Scholar
Bachmann, I. M. et al. EZH2 expression is associated with high proliferation rate and aggressive tumor subgroups in cutaneous melanoma and cancers of the endometrium, prostate, and breast. J. Clin. Oncol.24, 268–273 (2006). ArticleCASPubMed Google Scholar
Raaphorst, F. M. et al. Poorly differentiated breast carcinoma is associated with increased expression of the human Polycomb group EZH2 gene. Neoplasia5, 481–488 (2003). ArticleCASPubMedPubMed Central Google Scholar
Collett, K. et al. Expression of enhancer of zeste homologue 2 is significantly associated with increased tumor cell proliferation and is a marker of aggressive breast cancer. Clin. Cancer Res.12, 1168–1174 (2006). ArticleCASPubMed Google Scholar
Mimori, K. et al. Clinical significance of enhancer of zeste homolog 2 expression in colorectal cancer cases. Eur. J. Surg. Oncol.31, 376–380 (2005). ArticleCASPubMed Google Scholar
Sudo, T. et al. Clinicopathological significance of EZH2 mRNA expression in patients with hepatocellular carcinoma. Br. J. Cancer92, 1754–1758 (2005). ArticleCASPubMedPubMed Central Google Scholar
Sawa, M. et al. BMI-1 is highly expressed in M0-subtype acute myeloid leukemia. Int. J. Hematol.82, 42–47 (2005). ArticleCASPubMed Google Scholar
Bea, S. et al. BMI-1 gene amplification and overexpression in hematological malignancies occur mainly in mantle cell lymphomas. Cancer Res.61, 2409–2412 (2001). CASPubMed Google Scholar
Nowak, K. et al. BMI1 is a target gene of E2F-1 and is strongly expressed in primary neuroblastomas. Nucleic Acids Res.34, 1745–1754 (2006). ArticleCASPubMedPubMed Central Google Scholar
Vonlanthen, S. et al. The bmi-1 oncoprotein is differentially expressed in non-small cell lung cancer and correlates with INK4A–ARF locus expression. Br. J. Cancer84, 1372–1376 (2001). ArticleCASPubMedPubMed Central Google Scholar
Wang, S., Robertson, G. P. & Zhu, J. A novel human homologue of Drosophila Polycomblike gene is up-regulated in multiple cancers. Gene343, 69–78 (2004). ArticleCASPubMed Google Scholar
Tokimasa, S. et al. Lack of the Polycomb-group gene rae28 causes maturation arrest at the early B-cell developmental stage. Exp. Hematol.29, 93–103 (2001). ArticleCASPubMed Google Scholar
Gilbert, S. F. in Developmental Biology 6th edn (Sinauer Associates, Sunderland, 2000). Google Scholar
Moazed, D. & O'Farrell, P. H. Maintenance of the engrailed expression pattern by Polycomb group genes in Drosophila. Development, 116, 805–810 (1992). ArticleCASPubMed Google Scholar