Analysis of a polycomb group protein defines regions that link repressive activity on nucleosomal templates to in vivo function

Molecular and Cellular Biology

Volumn 25, Issue 15, 2005, Pages 6578-6591

  King, Ian F G ^a,b   Emmons, Richard B ^b   Francis, Nicole J ^a,b,d   Wild, Brigitte ^c   Müller, Jürg ^c   Kingston, Robert E ^a,b   Wu, Chao Ting ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCOMB GROUP PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; EMBRYO; GENE; GENE MUTATION; GENE REPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOSOME; PHENOTYPE; POSTERIOR SEX COMB GENE; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

ANIMALS; BINDING SITES; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MUTATION; NUCLEOSOMES; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC; WING;

EID: 22544485646     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.15.6578-6591.2005     Document Type: Article

References (62)

1. Adler, P. N., E. C. Martin, J. Charlton, and K. Jones. 1991. Phenotypic consequences and genetic interactions of a null mutation in the Drosophila Posterior Sex Combs gene. Dev. Genet. 12:349-361.
2. Ali, J., and W. Bender. 2004. Cross-regulation among the polycomb group genes in Drosophila melanogaster. Mol. Cell. Biol. 24:7737-7747.
3. Alkema, M. J., M. Bronk, E. Verhoeven, A. Otte, L. J. van't Veer, A. Berns, and M. van Lohuizen. 1997. Identification of Bmi1-interacting proteins as constituents of a multimeric mammalian polycomb complex. Genes Dev. 11:226-240.
4. Alkema, M. J., J. Jacobs, J. W. Voncken, N. A. Jenkins, N. G. Copeland, D. P. Satijn, A. P. Otte, A. Berns, and M. van Lohuizen. 1997. MPc2, a new murine homolog of the Drosophila polycomb protein is a member of the mouse polycomb transcriptional repressor complex. J. Mol. Biol. 273:993-1003.
5. Beuchle, D., G. Struhl, and J. Muller. 2001. Polycomb group proteins and heritable silencing of Drosophila Hox genes. Development 128:993-1004.
6. Brock, H. W., and M. van Lohuizen. 2001. The Polycomb group-no longer an exclusive club? Curr. Opin. Genet. Dev. 11:175-181.
7. Brunk, B. P., E. C. Martin, and P. N. Adler. 1991. Drosophila genes Posterior Sex Combs and Suppressor two of zeste encode proteins with homology to the murine bmi-1 oncogene. Nature 353:351-353.
8. Brunk, B. P., E. C. Martin, and P. N. Adler. 1991. Molecular genetics of the Posterior sex combs/Suppressor 2 of zeste region of Drosophila: aberrant expression of the Suppressor 2 of zeste gene results in abnormal bristle development. Genetics 128:119-132.
9. Bunker, C. A., and R. E. Kingston. 1994. Transcriptional repression by Drosophila and mammalian Polycomb group proteins in transfected mammalian cells. Mol. Cell. Biol. 14:1721-1732.
10. Cao, R., L. Wang, H. Wang, L. Xia, H. Erdjument-Bromage, P. Tempst, R. S. Jones, and Y. Zhang. 2002. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298:1039-1043.
11. Cao, R., and Y. Zhang. 2004. The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr. Opin. Genet. Dev. 14:155-164.
12. Cohen, K. J., J. S. Hanna, J. E. Frescott, and C. V. Dang. 1996. Transformation by the Bmi-1 oncoprotein correlates with its subnuclear localization but not its transcriptional suppression activity. Mol. Cell. Biol. 16:5527-5535.
13. Czermin, B., R. Melfi, D. McCabe, V. Seitz, A. Imhof, and V. Pirrotta. 2002. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyl-transferase activity that marks chromosomal Polycomb sites. Cell 111:185-196.
14. Dejardin, J., and G. Cavalli. 2004. Chromatin inheritance upon Zeste-mediated Brahma recruitment at a minimal cellular memory module. EMBO J. 23f:857-868.
15. Dellino, G. I., Y. B. Schwartz, G. Farkas, D. McCabe, S. C. Elgin, and V. Pirrotta. 2004. Polycomb silencing blocks transcription initiation. Mol. Cell 13:887-893.
16. de Napoles, M., J. E. Merrooud, R. Wakao, Y. A. Tang, M. Endoh, R. Appanah, T. B. Nesterova, J. Silva, A. P. Otte, M. Vidal, H. Koseki, and N. Brockdorff. 2004. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell 7:663-676.
17. Fang, J., T. Chen, B. Chadwick, E. Li, and Y. Zhang. 2004. Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J. Biol. Chem. 270:52812-52815.
18. Fang, S. M., K. L. Lorick, J. P. Jensen, and A. M. Weissman. 2003. RING finger ubiquitin protein ligases: implications for tumorigenesis, metastasis, and for molecular targets in cancer. Semin. Cancer Biol. 13:5-14.
19. Fitzgerald, D. P., and W. Bender. 2001. Polycomb group repression reduces DNA accessibility. Mol. Cell. Biol. 21:6585-6597.
20. Francis, N. J., and R. E. Kingston. 2001. Mechanisms of transcriptional memory. Nat. Rev. Mol. Cell Biol. 2:409-421.
21. Francis, N. J., R. E. Kingston, and C. L. Woodcock. 2004. Chromatin compaction by a polycomb group protein complex. Science 306:1574-1577.
22. Francis, N. J., A. J. Saurin, Z. Shao, and R. E. Kingston. 2001. Reconstitution of a functional core polycomb repressive complex. Mol. Cell 8:545-556.
23. Franke, A., M. DeCamillis, D. Zink, N. Cheng, H. W. Brock, and R. Paro. 1992. Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster. EMBO J. 11:2941-2950.
24. Fritsch, C., D. Beuchle, and J. Muller. 2003. Molecular and genetic analysis of the Polycomb group gene Sex combs extra/Ring in Drosophila. Mech. Dev. 120:949-954.
25. Fujisakia, S., Y. Ninomiyaa, H. Ishiharaa, M. Miyazakia, R. Kannoa, T. Asaharab, and M. Kanno. 2003. Dimerization of the Polycomb-group protein Mel-18 is regulated by PKC phosphorylation. Biochem. Biophys. Res. Commun. 300:135-140.
26. Gorfinkiel, N., L. Fanti, T. Melgar, E. Garcia, S. Pimpinelli, I. Guerrero, and M. Vidal. 2004. The Drosophila Polycomb group gene Sex combs extra encodes the ortholog of mammalian Ring1 proteins. Mech. Dev. 121:449-462.
27. Hur, M. W., J. D. Laney, S. H. Jeon, J. Ali, and M. D. Biggin. 2002. Zeste maintains repression of Ubx transgenes: support for a new model of Polycomb repression. Development 129:1339-1343.
28. Irminger-Finger, I., and R. Nothiger. 1995. The Drosophila melanogaster gene lethal(3)73Ah encodes a ring finger protein homologous to the oncoproteins MEL-18 and BMI-1. Gene 163:203-208.
29. Jurgens, G. 1985. A group of genes controlling the spatial expression of the bithorax complex of Drosophila. Nature 316:153-155.
30. King, I. F., N. J. Francis, and R. E. Kingston. 2002. Native and recombinant polycomb group complexes establish a selective block to template accessibility to repress transcription in vitro. Mol. Cell. Biol. 22:7919-7928.
31. Kuzmichev, A., K. Nishioka, H. Erdjument-Bromage, P. Tempst, and D. Reinberg. 2002. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 16:2893-2905.
32. Kyba, M., and H. W. Brock. 1998. The Drosophila polycomb group protein Psc contacts Ph and Pc through specific conserved domains. Mol. Cell. Biol. 18:2712-2720.
33. Lasko, P. F., and M. L. Pardue. 1988. Studies of the genetic organization of the vestigial microregion of Drosophila melanogaster. Genetics 120:495-502.
34. Lavigne, M., N. J. Francis, I. F. King, and R. E. Kingston. 2004. Propagation of silencing: recruitment and repression of naive chromatin in trans by Polycomb repressed chromatin. Mol. Cell 13:1-20.
35. Logic, C., and C. L. Peterson. 1997. Catalytic activity of the yeast SWI/SNF complex on reconstituted nucleosome arrays. EMBO J. 16:6772-6782.
36. Lund, A. H., and M. van Lohuizen. 2004. Polycomb complexes and silencing mechanisms. Curr. Opin. Cell Biol. 16:239-246.
37. Martin, E. C., and P. N. Adler. 1993. The Polycomb group gene Posterior Sex Combs encodes a chromosomal protein. Development 117:641-655.
38. McCall, K., and W. Bender. 1996. Probes of chromatin accessibility in the Drosophila bithorax complex respond differently to Polycomb-mediated repression. EMBO J. 15:569-580.
39. Mulholland, N. M., I. F. King, and R. E. Kingston. 2003. Regulation of Polycomb group complexes by the sequence-specific DNA binding proteins Zeste and GAGA. Genes Dev. 17:2741-2746.
40. Muller, J. 1995. Transcriptional silencing by the Polycomb protein in Drosophila embryos. EMBO J. 14:1209-1220.
41. Muller, J., C. M. Hart, N. J. Francis, M. L. Vargas, A. Sengupte, B. Wild, E. L. Miller, M. B. O'Connor, R. E. Kingston, and J. A. Simon. 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111:197-208.
42. Nusslein-Volhard, C., H. Kluding, and G. Jurgens. 1985. Genes affecting the segmental subdivision of the Drosophila embryo. Cold Spring Harbor Symp. Quant. Biol. 50:145-154.
43. Orlando, V. 2003. Polycomb, epigenomes, and control of cell identity. Cell 112:599-606.
44. Pare, R. 1990. Imprinting a determined state into the chromatin of Drosophila. Trends Genet. 6:416-421.
45. Pelegri, F., and R. Lehmann. 1994. A role of polycomb group genes in the regulation of gap gene expression in Drosophila. Genetics 136:1341-1353.
46. Pirrotta, V. 1991. The genetics and molecular biology of zeste in Drosophila melanogaster. Adv. Genet. 29:301-348.
47. Pirrotta, V. 1998. Polycombing the genome: PcG, trxG, and chromatin silencing. Cell 93:333-336.
48. Platero, J. S., E. J. Sharp, P. N. Adler, and J. C. Eissenberg. 1996. In vivo assay for protein-protein interactions using Drosophila chromosomes. Chromosoma 104:393-404.
49. Rastelli, L., C. S. Chan, and V. Pirrotta. 1993. Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function. EMBO J. 12:1513-1522.
50. Satijn, D. P., and A. P. Otte. 1999. RING1 interacts with multiple Polycomb-group proteins and displays tumorigenic activity. Mol. Cell. Biol. 19:57-68.
51. Saurin, A. J., Z. Shao, H. Erdjument-Bromage, P. Tempst, and R. E. Kingston. 2001. A Drosophila Polycomb group complex includes Zeste and dTAFII proteins. Nature 412:655-660.
52. Shao, Z., F. Raible, R. Mollaaghababa, J. R. Guyon, C. T. Wu, W. Bender, and R. E. Kingston. 1999. Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98:37-46.
53. Sharp, E. J., N. A. Abramova, W. J. Park, and P. N. Adler. 1997. The conserved HR domain of the Drosophila suppressor 2 of zeste [Su(z)2] and murine bmi-1 proteins constitutes a locus-specific chromosome binding domain. Chromosoma 106:70-80.
54. Sharp, E. J., E. C. Martin, and P. N. Adler. 1994. Directed overexpression of suppressor 2 of zeste and Posterior Sex Combs results in bristle abnormalities in Drosophila melanogaster. Dev. Biol. 161:379-392.
55. Simon, J., A. Chiang, and W. Bender. 1992. Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products. Development 114:493-505.
56. Simon, J. A., and J. W. Tamkun. 2002. Programming off and on states in chromatin; mechanisms of Polycomb and trithorax group complexes. Curr. Opin. Genet. Dev. 12:210-218.
57. Soto, M. C., T. B. Chou, and W. Bender. 1995. Comparison of germline mosaics of genes in the Polycomb group of Drosophila melanogaster. Genetics 140:231-243.
58. van der Knaap, J. A., B. R. Kumar, Y. M. Moshkin, K. Langenberg, J. Krijgsveld, A. J. Heck, F. Karch, and C. P. Verrijzer. 2005. GMP synthetase stimulates histone H2B deubiquitylation by the epigenetic silencer USP7. Mol. Cell 17:695-707.
59. van Lohuizen, M., M. Frasch, E. Wientjens, and A. Berns. 1991. Sequence similarity between the mammalian bmi-1 proto-oncogene and the Drosophila regulatory genes Psc and Su(z)2. Nature 353:353-355.
60. Wang, H., L. Wang, H. Edrdjument-Bromage, M. Vidal, P. Tempst, R. S. Jones, and Y. Zhang. 2004. Role of histone H2A ubiquitination in Polycomb silencing. Nature 431:873-878.
61. Wu, C.-T., R. S. Jones, P. F. Lasko, and W. M. Gelbart, 1989. Homeosis and the interaction of zeste and white in Drosophila. Mol. Gen. Genet. 218:559-564.
62. Wu, C. T., and M. Howe. 1995. A genetic analysis of the Suppressor 2 of zeste complex of Drosophila melanogaster. Genetics 140:139-181.