Alternative ESC and ESC-like subunits of a polycomb group histone methyltransferase complex are differentially deployed during Drosophila development

Molecular and Cellular Biology

Volumn 26, Issue 7, 2006, Pages 2637-2647

  Wang, Liangjun ^a   Jahren, Neal ^b   Vargas, Marcus L ^b   Andersen, Erica F ^b   Benes, Judith ^a   Zhang, Junyu ^a   Miller, Ellen L ^b   Jones, Richard S ^a,c   Simon, Jeffrey A ^b,c  

^a SOUTHERN METHODIST UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EMBRYONIC ECTODERM DEVELOPMENT PROTEIN; EXTRA SEX COMBS PROTEIN; HISTONE H3; HISTONE METHYLTRANSFERASE; POLYCOMB PROTEIN; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; ENHANCER REGION; ENZYME ANALYSIS; GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; REGULATOR GENE; UBX GENE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; CHROMATIN; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC ENHANCEMENT; HISTONE-LYSINE N-METHYLTRANSFERASE; HOMEODOMAIN PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN SUBUNITS; REGULATORY SEQUENCES, NUCLEIC ACID; TRANSCRIPTION FACTORS; WING;

ANIMALIA;

EID: 33645214914     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.7.2637-2647.2006     Document Type: Article

References (61)

1. Bender, L. B., R. Cao, Y. Zhang, and S. Strome. 2004. The MES-2/MES-3/MES-6 complex and regulation of histone H3 methylation in C. elegans. Curr. Biol. 14:1639-1643.
2. Beuchle, D., G. Struhl, and J. Muller. 2001. Polycomb group proteins and heritable silencing of Drosophila Hox genes. Development 128:993-1004.
3. Brown, J. L., C. Fritsch, J. Mueller, and J. A. Kassis. 2003. The Drosophila pho-like gene encodes a YY1-related DNA binding protein that is redundant with pleiohomeotic in homeotic gene silencing. Development 130:285-294.
4. Busturia, A., C. D. Wightman, and S. Sakonju. 1997. A silencer is required for maintenance of transcriptional repression throughout Drosophila development. Development 124:4343-4350.
5. 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.
6. Cao, R., and Y. Zhang. 2004. SUZ12 is required for both the histone methyltransferase activity and the silencing function of the EED-EZH2 complex. Mol. Cell 15:57-67.
7. Carrington, E. A., and R. S. Jones. 1996. The Drosophila Enhancer of zeste gene encodes a chromosomal protein: examination of wild-type and mutant protein distribution. Development 122:4073-4083.
8. Currie, D. A., M. J. Milner, and C. W. Evans. 1988. The growth and differentiation in vitro of leg and wing imaginal disc cells from Drosophila melanogaster. Development 102:805-814.
9. Czermin, B., R. Melfi, D. McCabe, V. Seitz, A. Imhof, and V. Pirrotta. 2002. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111:185-196.
10. Fischle, W., Y. Wang, S. A. Jacobs, Y. Kim, C. D. Allis, and S. Khorasanizadeh. 2003. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 17:1870-1881.
11. Francis, N. J., and R. E. Kingston. 2001. Mechanisms of transcriptional memory. Nat. Rev. Mol. Cell. Biol. 2:409-421.
12. 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.
13. 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.
14. Frei, E., D. Bopp, M. Burri, S. Baumgartner, J. E. Edström, and M. Noll. 1985. Isolation and structural analysis of the extra sex combs gene of Drosophila. Cold Spring Harbor Symp. Quant. Biol. 50:127-134.
15. Frei, E., R. Schuh, S. Baumgartner, M. Burri, M. Noll, G. Jurgens, E. Seifert, U. Nauber, and H. Jackle. 1988. Molecular characterization of spalt, a homeotic gene required for head and tail development in the Drosophila embryo. EMBO J. 7:197-204.
16. Furuyama, T., R. Banerjee, T. R. Breen, and P. J. Harte. 2004. SIR2 is required for polycomb silencing and is associated with an E(Z) histone methyltransferase complex. Curr. Biol. 14:1812-1821.
17. Furuyama, T., F. Tie, and P. J. Harte. 2003. Polycomb group proteins ESC and E(Z) are present in multiple distinct complexes that undergo dynamic changes during development. Genesis 35:114-124.
18. Glicksman, M. A., and D. L. Brower. 1988. Misregulation of homeotic gene expression in Drosophila larvae resulting from mutations at the extra sex combs locus. Dev. Biol. 126:219-227.
19. Goodrich, J., P. Puangsomlee, M. Martin, D. Long, E. M. Meyerowitz, and G. Coupland. 1997. A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386:44-51.
20. Gutjahr, T., E. Frei, C. Spicer, S. Baumgartner, R. A. White, and M. Noll. 1995. The Polycomb-group gene, extra sex combs, encodes a nuclear member of the WD-40 repeat family. EMBO J. 14:4296-4306.
21. Holdeman, R., S. Nehrt, and S. Strome. 1998. MES-2, a maternal protein essential for viability of the germline in Caenorhabditis elegans, is homologous to a Drosophila Polycomb group protein. Development 125:2457-2467.
22. Jones, C. A., J. Ng, A. J. Peterson, K. Morgan, J. Simon, and R. S. Jones. 1998. The Drosophila Esc and E(z) proteins are direct partners in polycomb group-mediated repression. Mol. Cell. Biol. 18:2825-2834.
23. Jones, R. S., and W. M. Gelbart. 1990. Genetic analysis of the enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster. Genetics 126:185-199.
24. Ketel, C. S., E. F. Andersen, M. L. Vargas, J. Suh, S. Strome, and J. A. Simon. 2005. Subunit contributions to histone methyltransferase activities of fly and worm polycomb group complexes. Mol. Cell. Biol. 25:6857-6868.
25. Korf, I., Y. Fan, and S. Strome. 1998. The Polycomb group in Caenorhabditis elegans and maternal control of germline development. Development 125:2469-2478.
26. Kuzmichev, A., T. Jenuwein, P. Tempst, and D. Reinberg. 2004. Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol. Cell 14:183-193.
27. 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.
28. McKeon, J., and H. W. Brock. 1991. Interactions of the Polycomb group of genes with homeotic loci of Drosophila. Roux's Arch. Dev. Biol. 199:387-396.
29. Min, J., Y. Zhang, and R, M. Xu. 2003. Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev. 17:1823-1828.
30. Moazed, D., and P. H. O'Farrell. 1992. Maintenance of the engrailed expression pattern by Polycomb group genes in Drosophila. Development 116:805-810.
31. Montgomery, N. D., D. Yee, A. Chen, S. Kalantry, S. J. Chamberlain, A. P. Otte, and T. Magnuson. 2005. The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation. Curr. Biol. 15:942-947.
32. Muller, J., C. M. Hart, N. J. Francis, M. L. Vargas, A. Sengupta, 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.
33. Nekrasov, M., B. Wild, and J. Muller. 2005. Nucleosome binding and histone methyltransferase activity of Drosophila PRC2. EMBO Rep. 6:348-353.
34. Ng, J., C. M. Hart, K. Morgan, and J. A. Simon. 2000. A Drosophila ESC-E(Z) protein complex is distinct from other polycomb group complexes and contains covalently modified ESC. Mol. Cell. Biol. 20:3069-3078.
35. Ng, J., R. Li, K. Morgan, and J. Simon. 1997. Evolutionary conservation and predicted structure of the Drosophila extra sex combs repressor protein. Mol. Cell. Biol. 17:6663-6672.
36. O'Connell, S., L. Wang, S. Robert, C. A. Jones, R. Saint, and R. S. Jones. 2001. Polycomblike PHD Fingers Mediate Conserved Interaction with Enhancer of Zeste Protein. J. Biol. Chem. 276:43065-43073.
37. Plath, K., J. Fang, S. K. Mlynarczyk-Evans, R. Cao, K. A. Worringer, H. Wang, C. C. de la Cruz, A. P. Otte, B. Panning, and Y. Zhang. 2003. Role of histone H3 lysine 27 methylation in X inactivation. Science 300:131-135.
38. Ringrose, L., and R. Paro. 2004. Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu. Rev. Genet. 38:413-443.
39. Ringrose, L., M. Rehmsmeier, J. M. Dura, and R. Paro. 2003. Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster. Dev. Cell 5:759-771.
40. Sathe, S. S., and P. J. Harte. 1995. The Drosophila extra sex combs protein contains WD motifs essential for its function as a repressor of homeotic genes. Mech. Dev. 52:77-87.
41. 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.
42. Schumacher, A., C. Faust, and T. Magnuson. 1996. Positional cloning of a global regulator of anterior-posterior patterning in mice. Nature 383:250-253.
43. 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.
44. Silva, J., W. Mak, I. Zvetkova, R. Appanah, T. B. Nesterova, Z. Webster, A. H. Peters, T. Jenuwein, A. P. Otte, and N. Brockdorff. 2003. Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev. Cell 4:481-495.
45. Simon, J., D. Bornemann, K. Lunde, and C. Schwartz. 1995. The extra sex combs product contains WD40 repeats and its time of action implies a role distinct from other Polycomb group products. Mech. Dev. 53:197-208.
46. 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.
47. Simon, J. A. 2003. Polycomb group proteins. Curr. Biol. 13:R79-80.
48. 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.
49. Spillane, C., C. MacDougall, C. Stock, C. Kohler, J. P. Vielle-Calzada, S. M. Nunes, U. Grossniklaus, and J. Goodrich. 2000. Interaction of the Arabidopsis polycomb group proteins FIE and MEA mediates their common phenotypes. Curr. Biol. 10:1535-1538.
50. Struhl, G. 1981. A gene product required for correct initiation of segmental determination in Drosophila. Nature 293:36-41.
51. Struhl, G. 1983. Role of the esc+ gene product in ensuring the selective expression of segment-specific homeotic genes in Drosophila. J. Embryol. Exp. Morphol. 76:297-331.
52. Struhl, G., and M. Akam. 1985. Altered distributions of Ultrabithorax transcripts in extra sex combs mutant embryos of Drosophila. EMBO J. 4:3259-3264.
53. + gene product in the determination of segments in Drosophila. Cell 31:285-292.
54. Tie, F., T. Furuyama, and P. J. Harte. 1998. The Drosophila Polycomb Group proteins ESC and E(Z) bind directly to each other and co-localize at multiple chromosomal sites. Development 125:3483-3496.
55. Tie, F., T. Furuyama, J. Prasad-Sinha, E. Jane, and P. J. Harte. 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 128:275-286.
56. Tokunaga, C., and C. Stern. 1965. The developmental autonomy of extra sex combs in Drosophila melanogaster. Dev. Biol. 11:50-81.
57. van Der Vlag, J., and A. P. Otte. 1999. Transcriptional repression mediated by the human polycomb-group protein EED involves histone deacetylation. Nat. Genet. 23:474-478.
58. 2. Cell 83:1047-1058.
59. Wang, J., J. Mager, Y. Chen, E. Schneider, J. C. Cross, A. Nagy, and T. Magnuson. 2001. Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat. Genet. 28:371-375.
60. Wang, L., J. L. Brown, R. Cao, Y. Zhang, J. A. Kassis, and R. S. Jones. 2004. Hierarchical recruitment of polycomb group silencing complexes. Mol. Cell 14:637-646.
61. Yoshida, N., Y. Yanai, L. Chen, Y. Kato, J. Hiratsuka, T. Miwa, Z. R. Sung, and S. Takahashi. 2001. EMBRYONIC FLOWER2, a novel polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. Plant Cell 13:2471-2481.