Crossref journal-article
The Company of Biologists
Development (237)
Abstract

ABSTRACT The Drosophila Polycomb Group (PcG) proteins are required for stable long term transcriptional silencing of the homeotic genes. Among PcG genes, esc is unique in being critically required for establishment of PcG-mediated silencing during early embryogenesis, but not for its subsequent maintenance throughout development. We previously showed that ESC is physically associated in vivo with the PcG protein E(Z). We report here that ESC, together with E(Z), is present in a 600 kDa complex that is distinct from complexes containing other PcG proteins. We have purified this ESC complex and show that it also contains the histone deacetylase RPD3 and the histone-binding protein p55, which is also a component of the chromatin remodeling complex NURF and the chromatin assembly complex CAF-1. The association of ESC and E(Z) with p55 and RPD3 is conserved in mammals. We show that RPD3 is required for silencing mediated by a Polycomb response element (PRE) in vivo and that E(Z) and RPD3 are bound to the Ubx PRE in vivo, suggesting that they act directly at the PRE. We propose that histone deacetylation by this complex is a prerequisite for establishment of stable long-term silencing by other continuously required PcG complexes.

Bibliography

Tie, F., Furuyama, T., Prasad-Sinha, J., Jane, E., & J. Harte, P. (2001). The Drosophila Polycomb Group proteins ESC and E(Z) are present in a complex containing the histone-binding protein p55 and the histone deacetylase RPD3. Development, 128(2), 275–286.

Authors 5
  1. Feng Tie (first)
  2. Takehito Furuyama (additional)
  3. Jayashree Prasad-Sinha (additional)
  4. Esther Jane (additional)
  5. Peter J. Harte (additional)
References 91 Referenced 211
  1. {'key': '2023022722551391800_', 'first-page': '1595', 'article-title': 'A conserved family of WD-40 proteins binds to the retinoblastoma protein in both plants and animals', 'volume': '9', 'author': 'Ach', 'year': '1997', 'journal-title': 'Plant Cell'} / Plant Cell / A conserved family of WD-40 proteins binds to the retinoblastoma protein in both plants and animals by Ach (1997)
  2. 10.1126/science.287.5461.2185 / Science / The genome sequence of Drosophila melanogaster by Adams (2000)
  3. 10.1101/gad.11.2.226 / Genes Dev / Identification of Bmi1-interacting proteins as constituents of a multimeric mammalian Polycomb complex by Alkema (1997)
  4. 10.1006/jmbi.1997.1372 / J. Mol. Biol / MPc2, a new murine homolog of the Drosophila Polycomb protein is a member of the mouse Polycomb transcriptional repressor complex by Alkema (1997)
  5. 10.1016/S0022-2836(05)80360-2 / J. Mol. Biol / Basic local alignment search tool by Altschul (1990)
  6. 10.1093/nar/25.17.3389 / Nucleic Acids Res / Gapped BLAST and PSI-BLAST: a new generation of protein database search programs by Altschul (1997)
  7. 10.1242/dev.122.5.1621 / Development / The Drosophila Polycomb group gene Sex comb on midleg (Scm) encodes a zinc finger protein with similarity to polyhomeotic protein by Bornemann (1996)
  8. 10.1128/MCB.19.12.8451 / Mol. Cell. Biol / The Drosophila Polycomb protein interacts with nucleosomal core particles In vitro via its repression domain by Breiling (1999)
  9. 10.1016/S1097-2765(00)80106-9 / Mol. Cell / The Drosophila Polycomb group gene pleiohomeotic encodes a DNA binding protein with homology to the transcription factor YY1 by Brown (1998)
  10. 10.1038/353351a0 / Nature / Drosophila genes Posterior Sex Combs and Suppressor two of zeste encode proteins with homology to the murine bmi-1 oncogene by Brunk (1991)
  11. {'key': '2023022722551391800_', 'first-page': '1721', 'article-title': 'Transcriptional repression by Drosophila and mammalian Polycomb group proteins in transfected mammalian cells', 'volume': '14', 'author': 'Bunker', 'year': '1994', 'journal-title': 'Mol. Cell. Biol'} / Mol. Cell. Biol / Transcriptional repression by Drosophila and mammalian Polycomb group proteins in transfected mammalian cells by Bunker (1994)
  12. 10.1242/dev.122.12.4073 / Development / The Drosophila Enhancer of zeste gene encodes a chromosomal protein: examination of wild-type and mutant protein distribution by Carrington (1996)
  13. 10.1126/science.286.5441.955 / Science / Epigenetic inheritance of active chromatin after removal of the main transactivator by Cavalli (1999)
  14. 10.1002/j.1460-2075.1994.tb06545.x / EMBO J / A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression by Chan (1994)
  15. 10.1101/gad.13.17.2218 / Genes Dev / A functional interaction between the histone deacetylase Rpd3 and the corepressor Groucho in Drosophila development by Chen (1999)
  16. 10.1002/j.1460-2075.1995.tb07197.x / EMBO J / The Drosophila trithorax protein binds to specific chromosomal sites and is co-localized with Polycomb at many sites by Chinwalla (1995)
  17. 10.1021/bi981042r / Biochemistry / Rabbit beta-globin is extended beyond its UGA stop codon by multiple suppressions and translational reading gaps by Chittum (1998)
  18. 10.1101/gad.6.2.223 / Genes Dev / The polyhomeotic gene of Drosophila encodes a chromatin protein that shares polytene chromosome-binding sites with Polycomb by DeCamillis (1992)
  19. 10.1128/MCB.18.10.5634 / Mol. Cell. Biol / Point mutations in the WD40 domain of Eed block its interaction with Ezh2 by Denisenko (1998)
  20. 10.1038/384589a0 / Nature / The histone deacetylase RPD3 counteracts genomic silencing in Drosophila and yeast by DeRubertis (1996)
  21. 10.1091/mbc.6.7.777 / Mol. Biol. Cell / The Drosophila snr1 and brm proteins are related to yeast SWI/SNF proteins and are components of a large protein complex by Dingwall (1995)
  22. 10.1016/1044-0305(94)80016-2 / J. Am. Soc. Mass Spect / An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database by Eng (1994)
  23. {'key': '2023022722551391800_', 'first-page': '2941', 'volume': '11', 'author': 'Franke', 'year': '1992', 'journal-title': 'Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster. EMBO J'} / Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster. EMBO J by Franke (1992)
  24. 10.1002/j.1460-2075.1985.tb03727.x / EMBO J / Cloning of the extra sex combs gene of Drosophila and its identification by P element-mediated gene transfer by Frei (1985)
  25. 10.1128/MCB.17.4.2326 / Mol. Cell. Biol / Identification and characterization of interactions between the vertebrate Polycomb-Group protein BMI1 and human homologs of polyhomeotic by Gunster (1997)
  26. 10.1002/j.1460-2075.1995.tb00104.x / EMBO J / The Polycomb-group gene, extra sex combs, encodes a nuclear member of the WD-40 repeat family by Gutjahr (1995)
  27. 10.1006/bbrc.1998.8438 / Biochem. Biophys. Res. Commun / RAE28, BMI1, and M33 are members of heterogeneous multimeric mammalian Polycomb group complexes by Hashimoto (1998)
  28. 10.1016/S0092-8674(00)80214-7 / Cell / Histone deacetylase activity is required for full transcriptional repression by mSin3A by Hassig (1997)
  29. 10.1038/350160a0 / Nature / A cellular protein that competes with SV40 T antigen for binding to the retinoblastoma gene product by Huang (1991)
  30. 10.1016/S0378-1119(98)00435-1 / Gene / Molecular cloning of Drosophila melanogaster cDNAs that encode a novel histone deacetylase dHDAC3 by Johnson (1998)
  31. 10.1128/MCB.18.5.2825 / Mol. Cell. Biol / The Drosophila esc and E(z) proteins are direct partners in Polycomb Group-mediated repression by Jones (1998)
  32. {'key': '2023022722551391800_', 'first-page': '6357', 'article-title': 'The Drosophila Polycomb-Group gene Enhancer of zeste shares a domain of sequence similarity with trithorax', 'volume': '13', 'author': 'Jones', 'year': '1993', 'journal-title': 'Mol. Cell. Biol'} / Mol. Cell. Biol / The Drosophila Polycomb-Group gene Enhancer of zeste shares a domain of sequence similarity with trithorax by Jones (1993)
  33. 10.1038/316153a0 / Nature / A group of genes controlling the spatial expression of the Bithorax Complex in Drosophila by Jürgens (1985)
  34. 10.1128/MCB.18.9.5121 / Mol. Cell. Biol / Targeted recruitment of the Sin3-Rpd3 histone deacetylase complex generates a highly localized domain of repressed chromatin in vivo by Kadosh (1998)
  35. 10.1073/pnas.88.3.1024 / Proc. Natl. Acad. Sci. USA / Accurate and efficient RNA polymerase II transcription with a soluble nuclear fraction derived from Drosophila embryos by Kamakaka (1991)
  36. 10.1128/MCB.18.5.2712 / Mol. Cell. Biol / The Drosophila Polycomb group protein PSC contacts PH and PC through specific conserved domains by Kyba (1998)
  37. 10.1002/(SICI)1520-6408(1998)22:1<74::AID-DVG8>3.0.CO;2-4 / Dev. Genet / The SAM domain of Polyhomeotic, RAE28, and Scm mediates specific interactions through conserved residues by Kyba (1998)
  38. 10.1002/dvg.1020150505 / Dev. Genet / Screen for enhancers of Polycomb and Polycomblike in Drosophila melanogaster by Landecker (1994)
  39. 10.1101/gad.13.20.2691 / Genes Dev / Functional antagonism of the Polycomb-Group genes eed and Bmi1 in hemopoietic cell proliferation by Lessard (1999)
  40. 10.1242/dev.120.9.2629 / Development / Molecular characterization of the Polycomblike gene of Drosophila melanogaster, a transacting negative regulator of homeotic gene expression by Lonie (1994)
  41. {'key': '2023022722551391800_', 'first-page': '981', 'article-title': 'lin-35 and lin-53, two genes that antagonize a C. elegans Ras pathway, encode proteins similar to Rb and its binding protein RbAp48. Cell', 'volume': '95', 'author': 'Lu', 'year': '1998'} / lin-35 and lin-53, two genes that antagonize a C. elegans Ras pathway, encode proteins similar to Rb and its binding protein RbAp48. Cell by Lu (1998)
  42. 10.1073/pnas.96.12.6797 / Proc. Natl. Acad. Sci. USA / The Rpd3 histone deacetylase is required for segmentation of the Drosophila embryo by Mannervik (1999)
  43. 10.1242/dev.117.2.641 / Development / The Polycomb group gene Posterior Sex Combs encodes a chromosomal protein by Martin (1993)
  44. 10.1073/pnas.95.1.132 / Proc. Natl. Acad. Sci. USA / Drosophila NURF-55, a WD repeat protein involved in histone metabolism by Martinez-Balbas (1998)
  45. 10.1002/j.1460-2075.1996.tb00389.x / EMBO J / Probes for chromatin accessibility in the Drosophila Bithorax Complex respond differently to Polycomb-mediated repression by McCall (1996)
  46. 10.1007/BF01705848 / Roux Arch. Dev. Biol / Interactions of the Polycomb group of genes with homeotic loci of Drosophila by McKeon (1991)
  47. 10.1093/genetics/154.2.657 / Genetics / Mutational analysis of a histone deacetylase in Drosophila melanogaster. Missense mutations suppress gene silencing associated with position effect variegation by Mottus (2000)
  48. 10.1002/j.1460-2075.1995.tb07104.x / EMBO J / Transcriptional silencing by the Polycomb protein in Drosophila embryos by Muller (1995)
  49. 10.1128/MCB.20.9.3069-3078.2000 / Mol. Cell. Biol / A Drosophila ESC-E(Z) protein complex is distinct from other Polycomb group complexes and contains covalently modified ESC by Ng (2000)
  50. 10.1093/emboj/17.17.5141 / EMBO J / Binding of Trithorax and Polycomb proteins to the bithorax complex: dynamic changes during early Drosophila embryogenesis by Orlando (1998)
  51. 10.1073/pnas.88.1.263 / Proc. Natl. Acad. Sci. USA / The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila by Paro (1991)
  52. 10.1016/S0092-8674(00)81325-2 / Cell / The major cytoplasmic histone acetyltransferase in yeast: links to chromatin replication and histone metabolism by Parthun (1996)
  53. 10.1093/genetics/144.4.1681 / Genetics / Zygotic lethal mutations with maternal effect phenotypes in Drosophila melanogaster. II. Loci on the second and third chromosomes identified by P-element-induced mutations by Perrimon (1996)
  54. 10.1128/MCB.17.11.6683 / Mol. Cell. Biol / A domain shared by the Polycomb group proteins Scm and ph mediates heterotypic and homotypic interactions by Peterson (1997)
  55. 10.1016/S0959-437X(97)80135-9 / Curr. Opin. Genet. Dev / PcG complexes and chromatin silencing by Pirrotta (1997)
  56. 10.1007/978-3-540-69111-2_10 / Results Probl. Cell. Differ / Polycomb silencing and the maintenance of stable chromatin states by Pirrotta (1999)
  57. 10.1002/bies.950160808 / BioEssays / white gene expression, repressive chromatin domains, and homeotic gene regulation in Drosophila by Pirrotta (1994)
  58. 10.1074/jbc.270.43.25507 / J. Biol. Chem / Dual retinoblastoma-binding proteins with properties related to a negative regulator of ras in yeast by Qian (1995)
  59. 10.1038/364648a0 / Nature / A retinoblastoma-binding protein related to a negative regulator of Ras in yeast by Qian (1993)
  60. 10.4049/jimmunol.164.1.1 / J. Immunol / Polycomb gene expression patterns reflect distinct B cell differentiation stages in human germinal centers by Raaphorst (2000)
  61. 10.1002/j.1460-2075.1993.tb05795.x / EMBO J / Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function by Rastelli (1993)
  62. 10.1126/science.287.5461.2222 / Science / A Drosophila complementary DNA resource by Rubin (2000)
  63. 10.1038/33952 / Nature / Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3 by Rundlett (1998)
  64. 10.1016/0925-4773(95)00392-E / Mech. Dev / The Drosophila Extra sex combs protein contains WD repeats essential for its function as a repressor of homeotic genes by Sathe (1995)
  65. 10.1128/MCB.17.7.4105 / Mol. Cell. Biol / RING1 is associated with the Polycomb Group protein complex and acts as a transcriptional repressor by Satijn (1997)
  66. 10.1128/MCB.17.10.6076 / Mol. Cell. Biol / Interference with the expression of a novel human Polycomb protein, hPc2, results in cellular transformation and apoptosis by Satijn (1997)
  67. 10.1038/383250a0 / Nature / Positional cloning of a global regulator of anterior-posterior patterning in mice by Schumacher (1996)
  68. 10.1128/MCB.18.6.3586 / Mol. Cell. Biol / Characterization of interactions between the mammalian Polycomb-Group proteins Enx1/EZH2 and EED suggests the existence of different mammalian Polycomb-Group protein complexes by Sewalt (1998)
  69. 10.1016/S0092-8674(00)80604-2 / Cell / Stabilization of chromatin structure by PRC1, a Polycomb complex by Shao (1999)
  70. 10.1242/dev.114.2.493 / Development / Ten different Polycomb group genes are required for spatial control of the abd-A and Abd-B homeotic products by Simon (1992)
  71. 10.1016/0925-4773(95)00434-3 / Mech. Dev / The extra sex combs product contains WD40 repeats and its time of action implies a role distinct from other Polycomb group products by Simon (1995)
  72. 10.1242/dev.125.7.1207 / Development / The Additional sex combs gene of Drosophila encodes a chromatin protein that binds to shared and unique Polycomb group sites on polytene chromosomes by Sinclair (1998)
  73. 10.1093/genetics/140.1.231 / Genetics / Comparison of germline mosaics of genes in the Polycomb group of Drosophila melanogaster by Soto (1995)
  74. 10.1242/dev.125.20.4055 / Development / The Enhancer of Polycomb gene of Drosophila encodes a chromatin protein conserved in yeast and mammals by Stankunas (1998)
  75. {'key': '2023022722551391800_', 'first-page': '297', 'article-title': 'Role of the esc+ gene product in ensuring the selective expression of segment-specific homeotic genes in Drosophila', 'volume': '76', 'author': 'Struhl', 'year': '1983', 'journal-title': 'J. Embryol. Exp. Morphol'} / J. Embryol. Exp. Morphol / Role of the esc+ gene product in ensuring the selective expression of segment-specific homeotic genes in Drosophila by Struhl (1983)
  76. 10.1016/0092-8674(82)90428-7 / Cell / Early role of the esc+ gene product in the determination of segments in Drosophila by Struhl (1982)
  77. 10.1128/MCB.17.12.6773 / Mol. Cell. Biol / The Polycomb group protein complex of Drosophila melanogaster has different compositions at different target genes by Strutt (1997)
  78. 10.1126/science.272.5260.408 / Science / A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p by Taunton (1996)
  79. 10.1242/dev.125.17.3483 / Development / The Drosophila Polycomb-Group proteins ESC and E(Z) bind directly to each other and co-localize at multiple chromosomal sites by Tie (1998)
  80. 10.1016/0012-1606(65)90037-0 / Dev. Biol / The developmental autonomy of extra sex combs in Drosophila melanogaster by Tokunaga (1965)
  81. 10.1046/j.1432-0436.1999.6540229.x / Differentiation / A novel member of murine Polycomb-group proteins, Sex comb on midleg homolog protein, is highly conserved, and interacts with RAE28/mph1 in vitro by Tomotsune (1999)
  82. 10.1128/MCB.16.11.6149 / Mol. Cell. Biol / The p55 subunit of Drosophila chromatin assembly factor 1 is homologous to a histone deacetylase-associated protein by Tyler (1996)
  83. 10.1038/70602 / Nat. Genet / Transcriptional repression mediated by the human Polycomb-Group protein EED involves histone deacetylation by van der Vlag (1999)
  84. 10.1038/353353a0 / Nature / Sequence similarity between the mammalian bmi-1 proto-oncogene and the Drosophila regulatory genes Psc and Su(z)2 by van Lohuizen (1991)
  85. 10.1128/MCB.18.6.3572 / Mol. Cell. Biol / Interaction of mouse polycomb-group (Pc-G) proteins Enx1 and Enx2 with Eed: indication for separate Pc-G complexes by van Lohuizen (1998)
  86. 10.1128/MCB.19.9.5847 / Mol. Cell. Biol / Functional analysis of the SIN3-histone deacetylase RPD3-RbAp48-histone H4 connection in the Xenopus oocyte by Vermaak (1999)
  87. 10.1016/S0092-8674(00)81326-4 / Cell / Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4 by Verreault (1996)
  88. 10.1016/S0960-9822(98)70040-5 / Curr. Biol / Nucleosomal DNA regulates the core-histone-binding subunit of the human Hat1 acetyltransferase by Verreault (1998)
  89. 10.1016/S0960-9822(98)70328-8 / Curr. Biol / A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase by Wade (1998)
  90. 10.1016/S0092-8674(00)80216-0 / Cell / Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex by Zhang (1997)
  91. 10.1101/gad.13.15.1924 / Genes Dev / Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation by Zhang (1999)
Dates
Type When
Created 4 years, 4 months ago (April 26, 2021, 12:32 a.m.)
Deposited 2 years, 6 months ago (Feb. 27, 2023, 5:55 p.m.)
Indexed 3 weeks, 2 days ago (Aug. 6, 2025, 8:32 a.m.)
Issued 24 years, 7 months ago (Jan. 15, 2001)
Published 24 years, 7 months ago (Jan. 15, 2001)
Published Online 24 years, 7 months ago (Jan. 15, 2001)
Published Print 24 years, 7 months ago (Jan. 15, 2001)
Funders 0

None

@article{Tie_2001, title={The Drosophila Polycomb Group proteins ESC and E(Z) are present in a complex containing the histone-binding protein p55 and the histone deacetylase RPD3}, volume={128}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.128.2.275}, DOI={10.1242/dev.128.2.275}, number={2}, journal={Development}, publisher={The Company of Biologists}, author={Tie, Feng and Furuyama, Takehito and Prasad-Sinha, Jayashree and Jane, Esther and J. Harte, Peter}, year={2001}, month=jan, pages={275–286} }