p55, the Drosophila ortholog of RbAp46/RbAp48, is required for the repression of dE2F2/RBF-regulated genes

Molecular and Cellular Biology

Volumn 24, Issue 20, 2004, Pages 9124-9136

  Taylor Harding, Barbie ^a   Binné, Ulrich K ^a   Korenjak, Michael ^b   Brehm, Alexander ^b   Dyson, Nicholas J ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; HISTONE DEACETYLASE; PROTEIN P55; PROTEIN SWI; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F2;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CHROMATIN; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE CONTROL; GENE REPRESSION; GENE TARGETING; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE;

ANIMALIA; ARACHNIDA; DROSOPHILA; DROSOPHILA MELANOGASTER; HEXAPODA; MAMMALIA; MELANOGASTER;

EID: 4744362120     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.20.9124-9136.2004     Document Type: Article

References (68)

1. Ait-Si-Ali, S., V. Guasconi, L. Fritsch, H. Yahi, R. Sekhri, I. Naguibneva, P. Robin, F. Cabon, A. Polesskaya, and A. Harel-Bellan. 2004. A Suv39h-dependent mechanism for silencing S-phase genes in differentiating but not in cycling cells. EMBO J. 23:605-615.
2. Ayer, D. E. 1999. Histone deacetylases: transcriptional repression with SINers and NuRDs. Trends Cell Biol. 9:193-198.
3. Bouazoune, K., A. Mitterweger, G. Langst, A. Imhof, A. Akhtar, P. B. Becker, and A. Brehm. 2002. The dMi-2 chromodomains are DNA binding modules important for ATP-dependent nucleosome mobilization. EMBO J. 21:2430-2440.
4. Boutillier, A. L., E. Trinh, and J. P. Loeffler. 2002. Constitutive repression of E2F1 transcriptional activity through HDAC proteins is essential for neuronal survival. Ann. N. Y. Acad. Sci. 973:438-442.
5. Brehm, A., G. Langst, J. Kehle, C. R. Clapier, A. Imhof, A. Eberharter, J. Muller, and P. B. Becker. 2000. dMi-2 and ISWI chromatin remodelling factors have distinct nucleosome binding and mobilization properties. EMBO J. 19:4332-4341.
6. Brehm, A., E. A. Miska, D. J. McCance, J. L. Reid, A. J. Bannister, and T. Kouzarides. 1998. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 391:597-601.
7. Chellappan, S. P., S. Hiehert, M. Mudryj, J. M. Horowitz, and J. R. Nevins. 1991. The E2F transcription factor is a cellular target for the RB protein. Cell 65:1053-1061.
8. Classon, M., and N. Dyson. 2001. p107 and p130: versatile proteins with interesting pockets. Exp. Cell Res. 264:135-147.
9. Dahiya, A., S. Wong, S. Gonzalo, M. Gavin, and D. C. Dean. 2001. Linking the Rb and polycomb pathways. Mol. Cell 8:557-569.
10. de Bruin, A., B. Maiti, L. Jakoi, C. Timmers, R. Buerki, and G. Leone. 2003. Identification and characterization of E2F7, a novel mammalian E2F family member capable of blocking cellular proliferation. J. Biol. Chem. 278:42041-42049.
11. Dimova, D. K., O. Stevaux, M. V. Frolov, and N. J. Dyson. 2003. Cell cycle-dependent and cell cycle-independent control of transcription by the Drosophila E2F/RB pathway. Genes Dev. 17:2308-2320.
12. Di Stefano, L., M. R. Jensen, and K. Helin. 2003. E2F7, a novel E2F featuring DP-independent repression of a subset of E2F-regulated genes. EMBO J. 22:6289-6298.
13. Dunaief, J. L., B. E. Strober, S. Guha, P. A. Khavari, K. Alin, J. Luban, M. Begemann, G. R. Crabtree, and S. P. Goff. 1994. The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest. Cell 79:119-130.
14. Dyson, N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12:2245-2262.
15. Ferreira, R., L. Magnaghi-Jaulin, P. Robin, A. Harel-Bellan, and D. Trouche. 1998. The three members of the pocket proteins family share the ability to repress E2F activity through recruitment of a histone deacetylase. Proc. Natl. Acad. Sci. USA 95:10493-10498.
16. Frolov, M. V., D. S. Huen, O. Stevaux, D. Dimova, K. Balczarek-Strang, M. Elsdon, and N. J. Dyson. 2001. Functional antagonism between E2F family members. Genes Dev. 15:2146-2160.
17. Frolov, M. V., O. Stevaux, N. S. Moon, D. Dimova, E. J. Kwon, E. J. Morris, and N. J. Dyson. 2003. G1 cyclin-dependent kinases are insufficient to reverse dE2F2-mediated repression. Genes Dev. 17:723-728.
18. 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.
19. Gaubatz, S., G. J. Lindeman, S. Ishida, L. Jakoi, J. R. Nevins, D. M. Livingston, and R. E. Rempel. 2000. E2F4 and E2F5 play an essential role in pocket protein-mediated G1 control. Mol. Cell 6:729-735.
20. Helin, K., E. Harlow, and A. Fattaey. 1993. Inhibition of E2F-1 transactivation by direct binding of the retinoblastoma protein. Mol. Cell. Biol. 13: 6501-6508.
21. Hiebert, S. W. 1993. Regions of the retinoblastoma gene product required for its interaction with the E2F transcription factor are necessary for E2 promoter repression and pRB-mediated growth suppression. Mol. Cell. Biol. 13:3384-3391.
22. Ishida, S., E. Huang, H. Zuzan, R. Spang, G. Leone, M. West, and J. R. Nevins. 2001. Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol. Cell. Biol. 21: 4684-4699.
23. Kehle, J., D. Beuchle, S. Treuheit, B. Christen, J. A. Kennison, M. Bienz, and J. Muller. 1998. dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 282:1897-1900.
24. Kennedy, B. K., O. W. Liu, F. A. Dick, N. Dyson, E. Harlow, and M. Vidal. 2001. Histone deacetylase-dependent transcriptional repression by pRB in yeast occurs independently of interaction through the LXCXE binding cleft. Proc. Natl. Acad. Sci. USA 98:8720-8725.
25. Lai, A., B. K. Kennedy, D. A. Barbie, N. R. Bertos, X. J. Yang, M. C. Theberge, S. C. Tsai, E. Seto, Y. Zhang, A. Kuzmichev, W. S. Lane, D. Reinberg, E. Harlow, and P. E. Branton. 2001. RBP1 recruits the mSIN3-histone deacetylase complex to the pocket of retinoblastoma tumor suppressor family proteins found in limited discrete regions of the nucleus at growth arrest. Mol. Cell. Biol. 21:2918-2932.
26. Lam, E. W., and N. B. La Thangue. 1994. DP and E2F proteins: coordinating transcription with cell cycle progression. Curr. Opin. Cell Biol. 6:859-866.
27. Liu, K., Y. Luo, F. T. Lin, and W. C. Lin. 2004. TopBP1 recruits Brg1/Brm to repress E2F1-induced apoptosis, a novel pRB-independent and E2F1-specific control for cell survival. Genes Dev. 18:673-686.
28. Loyola, A., and G. Almouzni. 2004. Histone chaperones, a supporting role in the limelight. Biochim. Biophys. Acta 1677:3-11.
29. Lu, X., and H. R. Horvitz. 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 95:981-991.
30. Luo, R. X., A. A. Postigo, and D. C. Dean. 1998. Rb interacts with histone deacetylase to repress transcription. Cell 92:463-473.
31. Magnaghi-Jaulin, L., R. Groisman, I. Naguibneva, P. Robin, S. Lorain, J. P. Le Villain, F. Troalen, D. Trouche, and A. Harel-Bellan. 1998. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 391:601-605.
32. Meloni, A. R., E. J. Smith, and J. R. Nevins. 1999. A mechanism for Rb/ p130-mediated transcription repression involving recruitment of the CtBP corepressor. Proc. Natl. Acad. Sci. USA 96:9574-9579.
33. Mizzen, C. A., X. J. Yang, T. Kokuho, J. E. Brownell, A. J. Bannister, T. Owen-Hughes, J. Workman, L. Wang, S. L. Berger, T. Kouzarides, Y. Nakatani, and C. D. Allis. 1996. The TAF(II)250 subunit of TFIID has histone acetyltransferase activity. Cell 87:1261-1270.
34. Morrison, A. J., C. Sardet, and R. E. Herrera. 2002. Retinoblastoma protein transcriptional repression through histone deacetylation of a single nucleosome. Mol. Cell. Biol. 22:856-865.
35. 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.
36. Nevins, J. R. 1992. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science 258:424-429.
37. Nicolas, E., S. Ait-Si-Ali, and D. Trouche. 2001. The histone deacetylase HDAC3 targets RbAp48 to the retinoblastoma protein. Nucleic Acids Res. 29:3131-3136.
38. Nielsen, S. J., R. Schneider, U. M. Bauer, A. J. Bannister, A. Morrison, D. O'Carroll, R. Firestein, M. Cleary, T. Jenuwein, R. E. Herrera, and T. Kouzarides. 2001. Rb targets histone H3 methylation and HP1 to promoters. Nature 412:561-565.
39. Ogawa, H., K. Ishiguro, S. Gaubatz, D. M. Livingston, and Y. Nakatani. 2002. A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in G0 cells. Science 296:1132-1136.
40. Pile, L. A., and D. A. Wassarman. 2000. Chromosomal localization links the SIN3-RPD3 complex to the regulation of chromatin condensation, histone acetylation and gene expression. EMBO J. 19:6131-6140.
41. Qian, Y. W., Y. C. Wang, R. E. Hollingsworth, Jr., D. Jones, N. Ling, and E. Y. Lee. 1993. A retinoblastoma-binding protein related to a negative regulator of Ras in yeast. Nature 364:648-652.
42. Rayman, J. B., Y. Takahashi, V. B. Indjeian, J. H. Dannenberg, S. Catchpole, R. J. Watson, H. te Riele, and B. D. Dynlacht. 2002. E2F mediates cell cycle-dependent transcriptional repression in vivo by recruitment of an HDAC1/mSin3B corepressor complex. Genes Dev. 16:933-947.
43. Ren, B., H. Cam, Y. Takahashi, T. Volkert, J. Terragni, R. A. Young, and B. D. Dynlacht. 2002. E2F integrates cell cycle progression with DNA repair, replication, and G(2)/M checkpoints. Genes Dev. 16:245-256.
44. Ridgway, P., and G. Almouzni. 2000. CAF-1 and the inheritance of chromatin states: at the crossroads of DNA replication and repair. J. Cell Sci. 113:2647-2658.
45. Robertson, K. D., S. Ait-Si-Ali, T. Yokochi, P. A. Wade, P. L. Jones, and A. P. Wolffe. 2000. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat. Genet. 25:338-342.
46. Ross, J. F., X. Liu, and B. D. Dynlacht. 1999. Mechanism of transcriptional repression of E2F by the retinoblastoma tumor suppressor protein. Mol. Cell 3:195-205.
47. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
48. 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.
49. Secombe, J., J. Pispa, R. Saint, and H. Richardson. 1998. Analysis of a Drosophila cyclin E hypomorphic mutation suggests a novel role for cyclin E in cell proliferation control during eye imaginal disc development. Genetics 149:1867-1882.
50. Shao, Z., S. Ruppert, and P. D. Robbins. 1995. The retinoblastoma- susceptibility gene product binds directly to the human TATA-binding protein-associated factor TAFII250. Proc. Natl. Acad. Sci. USA 92:3115-3119.
51. Siddiqui, H., D. A. Solomon, R. W. Gunawardena, Y. Wang, and E. S. Knudsen. 2003. Histone deacetylation of RB-responsive promoters: requisite for specific gene repression but dispensable for cell cycle inhibition. Mol. Cell. Biol. 23:7719-7731.
52. Staehling-Hampton, K., P. J. Ciampa, A. Brook, and N. Dyson. 1999. A genetic screen for modifiers of E2F in Drosophila melanogaster. Genetics 153:275-287.
53. Stevaux, O., D. Dimova, M. V. Frolov, B. Taylor-Harding, E. Morris, and N. Dyson. 2002. Distinct mechanisms of E2F regulation by Drosophila RBF1 and RBF2. EMBO J. 21:4927-4937.
54. Stevaux, O., and N. J. Dyson. 2002. A revised picture of the E2F transcriptional network and RB function. Curr. Opin. Cell Biol. 14:684-691.
55. Takahashi, Y., J. B. Rayman, and B. D. Dynlacht. 2000. Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression. Genes Dev. 14:804-816.
56. Tevosian, S. G., H. H. Shih, K. G. Mendelson, K. A. Sheppard, K. E. Paulson, and A. S. Yee. 1997. HBP1: a HMG box transcriptional repressor that is targeted by the retinoblastoma family. Genes Dev. 11:383-396.
57. 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.
58. Trouche, D., C. Le Chalony, C. Muchardt, M. Yaniv, and T. Kouzarides. 1997. RB and hbrm cooperate to repress the activation functions of E2F1. Proc. Natl. Acad. Sci. USA 94:11268-11273.
59. Tsukiyama, T., C. Daniel, J. Tamkun, and C. Wu. 1995. ISWI, a member of the SWI2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor. Cell 83:1021-1026.
60. Tyler, J. K., K. A. Collins, J. Prasad-Sinha, E. Amiott, M. Bulger, P. J. Harte, R. Kobayashi, and J. T. Kadonaga. 2001. Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol. Cell. Biol. 21:6574-6584.
61. Tyler, J. K., M. Bulger, R. T. Kamakaka, R. Kobayashi, and J. T. Kadonaga. 1996. The p55 subunit of Drosophila chromatin assembly factor 1 is homologous to a histone deacetylase-associated protein. Mol. Cell. Biol. 16:6149-6159.
62. Vaute, O., E. Nicolas, L. Vandel, and D. Trouche. 2002. Functional and physical interaction between the histone methyl transferase Suv39H1 and histone deacetylases. Nucleic Acids Res. 30:475-481.
63. Verreault, A., P. D. Kaufman, R. Kobayashi, and B. Stillman. 1996. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87:95-104.
64. Weinmann, A. S., P. S. Yan, M. J. Oberley, T. H. Huang, and P. J. Farnham. 2002. Isolating human transcription factor targets by coupling chromatin immunoprecipitation and CpG island microarray analysis. Genes Dev. 16: 235-244.
65. Wells, J., K. E. Boyd, C. J. Fry, S. M. Bartley, and P. J. Farnham. 2000. Target gene specificity of E2F and pocket protein family members in living cells. Mol. Cell. Biol. 20:5797-5807.
66. Wu, L., C. Timmers, B. Maiti, H. I. Saavedra, L. Sang, G. T. Chong, F. Nuckolls, P. Giangrande, F. A. Wright, S. J. Field, M. E. Greenberg, S. Orkin, J. R. Nevins, M. L. Robinson, and G. Leone. 2001. The E2F1-3 transcription factors are essential for cellular proliferation. Nature 414:457-462.
67. Xue, Y., J. Wong, G. T. Moreno, M. K. Young, J. Cote, and W. Wang. 1998. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol. Cell 2:851-861.
68. Zhang, H. S., M. Gavin, A. Dahiya, A. A. Postigo, D. Ma, R. X. Luo, J. W. Harbour, and D. C. Dean. 2000. Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell 101:79-89.