Histone Deacetylation of RB-Responsive Promoters: Requisite for Specific Gene Repression but Dispensable for Cell Cycle Inhibition

Molecular and Cellular Biology

Volumn 23, Issue 21, 2003, Pages 7719-7731

  Siddiqui, Hasan ^a   Solomon, David A ^a   Gunawardena, Ranjaka W ^a   Wang, Ying ^a   Knudsen, Erik S ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; DNA TOPOISOMERASE; HISTONE DEACETYLASE; PROTEIN KINASE; THYMIDYLATE SYNTHASE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE; CHROMATIN STRUCTURE; COMPLEX FORMATION; DEACETYLATION; DNA DAMAGE; DNA METHYLATION; GENE REPRESSION; GENE SILENCING; GENE TARGETING; GENETIC ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; TARGET CELL; TRANSCRIPTION REGULATION;

ACETYLATION; ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE; DOXYCYCLINE; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HISTONES; HUMANS; HYDROXAMIC ACIDS; MULTIENZYME COMPLEXES; PROMOTER REGIONS (GENETICS); RATS; REPRESSOR PROTEINS; RETINOBLASTOMA PROTEIN; TRANSCRIPTION, GENETIC;

ANIMALIA;

EID: 0142123190     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.21.7719-7731.2003     Document Type: Article

References (83)

1. 1/S inhibition. Exp. Cell Res. 276:201-213.
2. Bartek, J., J. Bartkova, and J. Lukas. 1997. The retinoblastoma protein pathway in cell cycle control and cancer. Exp. Cell Res. 237:1-6.
3. 1/S-regulating genes in human cancer. Prog. Cell Cycle Res. 3:211-220.
4. Boeger, H., J. Griesenbeck, J. S. Strattan, and R. D. Kornberg. 2003. Nucleosomes unfold completely at a transcriptionally active promoter. Mol. Cell 11:1587-1598.
5. Botz, J., K. Zerfass-Thome, D. Spitkovsky, H. Delius, B. Vogt, M. Eilers, A. Hatzigeorgiou, and P. Jansen-Durr. 1996. Cell cycle regulation of the murine cyclin E gene depends on an E2F binding site in the promoter. Mol. Cell. Biol. 16:3401-3409.
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. Bremner, R., B. L. Cohen, M. Sopta, P. A. Hamel, C. J. Ingles, B. L. Gallie, and R. A. Phillips. 1995. Direct transcriptional repression by pRB and its reversal by specific cyclins. Mol. Cell. Biol. 15:3256-3265.
8. Chellappan, S. P., S. Hiebert, 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.
9. Chen, T. T., and J. Y. Wang. 2000. Establishment of irreversible growth arrest in myogenic differentiation requires the RB LXCXE-binding function. Mol. Cell. Biol. 20:5571-5580.
10. Classon, M., and E. Harlow. 2002. The retinoblastoma tumour suppressor in development and cancer. Nat. Rev. Cancer 2:910-917.
11. Dahlya, A., M. R. Gavin, R. X. Luo, and D. C. Dean. 2000. Role of the LXCXE binding site in Rb function. Mol. Cell. Biol. 20:6799-6805.
12. Dalton, S. 1992. Cell cycle regulation of the human cdc2 gene. EMBO J. 11:1797-1804.
13. de la Serna, I. L., K. A. Carlson, D. A. Hill, C. J. Guidi, R. O. Stephenson, S. Sif, R. E. Kingston, and A. N. Imbalzano. 2000. Mammalian SWI-SNF complexes contribute to activation of the hsp70 gene. Mol. Cell. Biol. 20: 2839-2851.
14. de la Serna, I. L., K. A. Carlson, and A. N. Imbalzano. 2001. Mammalian SWI/SNF complexes promote MyoD-mediated muscle differentiation. Nat. Genet. 27:187-190.
15. 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.
16. Dyson, N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12:2245-2262.
17. Flemington, E. K., S. H. Speck, and W. G. Kaelin, Jr. 1993. E2F-1-mediated transactivation is inhibited by complex formation with the retinoblastoma susceptibility gene product. Proc. Natl. Acad. Sci. USA 90:6914-6918.
18. Furukawa, Y., Y. Terui, K. Sakoe, M. Ohta, and M. Saito. 1994. The role of cellular transcription factor E2F in the regulation of cdc2 mRNA expression and cell cycle control of human hematopoietic cells. J. Biol. Chem. 269: 26249-26258.
19. Furuno, N., N. den Elzen, and J. Pines. 1999. Human cyclin A is required for mitosis until mid prophase. J. Cell Biol. 147:295-306.
20. Geng, Y., E. N. Eaton, M. Picon, J. M. Roberts, A. S. Lundberg, A. Gifford, C. Sardet, and R. A. Weinberg. 1996. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene 12:1173-1180.
21. Grunstein, M. 1997. Histone acetylation in chromatin structure and transcription. Nature 389:349-352.
22. Harbour, J. W., and D. C. Dean. 2000. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev. 14:2393-2409.
23. 1. Cell 98:859-869.
24. Hassig, C. A., T. C. Fleischer, A. N. Billin, S. L. Schreiber, and D. E. Ayer. 1997. Histone deacetylase activity is required for full transcriptional repression by mSin3A. Cell 89:341-347.
25. Hassig, C. A., and S. L. Schreiber. 1997. Nuclear histone acetylases and deacetylases and transcriptional regulation: HATs off to HDACs. Curr. Opin. Chem. Biol. 1:300-308.
26. Heinzel, T., R. M. Lavinsky, T. M. Mullen, M. Soderstrom, C. D. Laherty, J. Torchia, W. M. Yang, G. Brard, S. D. Ngo, J. R. Davie, E. Seto, R. N. Eisenman, D. W. Rose, C. K. Glass, and M. G. Rosenfeld. 1997. A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature 387:43-48.
27. Helin, K., C. L. Wu, A. R. Fattaey, J. A. Lees, B. D. Dynlacht, C. Ngwu, and E. Harlow. 1993. Heterodimerization of the transcription factors E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev. 7:1850-1861.
28. Herrera, R. E., T. P. Makela, and R. A. Weinberg. 1996. TGF-β-induced growth inhibition in primary fibroblasts requires the retinoblastoma protein. Mol. Biol. Cell 7:1335-1342.
29. Huet, X., J. Rech, A. Plet, A. Vie, and J. M. Blanchard. 1996. Cyclin A expression is under negative transcriptional control during the cell cycle. Mol. Cell. Biol. 16:3789-3798.
30. Kaelin, W. G., Jr. 1997. Recent insights into the functions of the retinoblastoma susceptibility gene product. Cancer Investig. 15:243-254.
31. Karlseder, J., H. Rotheneder, and E. Wintersberger. 1996. Interaction of Sp1 with the growth- and cell cycle-regulated transcription factor E2F. Mol. Cell. Biol. 16:1659-1667.
32. 1/S transition and S-phase progression. Genes Dev. 12:2278-2292.
33. Kramer, O. H., M. Gottlicher, and T. Heinzel. 2001. Histone deacetylase as a therapeutic target. Trends Endocrinol. Metab. 12:294-300.
34. Lachner, M., D. O'Carroll, S. Rea, K. Mechtler, and T. Jenuwein. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116-120.
35. Laherty, C. D., W. M. Yang, J. M. Sun, J. R. Davie, E. Seto, and R. N. Eisenman. 1997. Histone deacetylases associated with the mSin3 corepressor mediate Mad transcriptional repression. Cell 89:349-356.
36. Lai, A., J. M. Lee, W. M. Yang, J. A. DeCaprio, W. G. Kaelin, Jr., E. Seto, and P. E. Branton. 1999. RBP1 recruits both histone deacetylase-dependent and -independent repression activities to retinoblastoma family proteins. Mol. Cell. Biol. 19:6632-6641.
37. Lai, A., R. C. Marcellus, H. B. Corbeil, and P. E. Branton. 1999. RBP1 induces growth arrest by repression of E2F-dependent transcription. Oncogene 18:2091-2100.
38. Lee, Y., and L. F. Johnson. 2000. Transcriptional control elements of the rat thymidylate synthase promoter: evolutionary conservation of regulatory features. Exp. Cell Res. 258:53-64.
39. Luo, R. X., A. A. Postigo, and D. C. Dean. 1998. Rb interacts with histone deacetylase to repress transcription. Cell 92:463-473.
40. 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.
41. Mal, A., and M. L. Harter. 2003. MyoD is functionally linked to the silencing of a muscle-specific regulatory gene prior to skeletal myogenesis. Proc. Natl. Acad. Sci. USA 100:1735-1739.
42. Markey, M. P., S. P. Angus, M. W. Strobeck, S. L. Williams, R. W. Gunawardena, B. J. Aronow, and E. S. Knudsen. 2002. Unbiased analysis of RB-mediated transcriptional repression identifies novel targets and distinctions from E2F action. Cancer Res. 62:6587-6597.
43. Marks, P., R. A. Rifkind, V. M. Richon, R. Breslow, T. Miller, and W. K. Kelly. 2001. Histone deacetylases and cancer: causes and therapies. Nat. Rev. Cancer 1:194-202.
44. 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.
45. Merlo, A., J. G. Herman, L. Mao, D. J. Lee, E. Gabrielson, P. C. Burger, S. B. Baylin, and D. Sidransky. 1995. 5′ CpG island methylation is associated with transcriptional silencing of the tumour suppressor p16/CDKN2/MTS1 in human cancers. Nat. Med. 1:686-692.
46. Morris, E. J., and N. J. Dyson. 2001. Retinoblastoma protein partners. Adv. Cancer Res. 82:1-54.
47. 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.
48. Narita, M., S. Nunez, E. Heard, M. Narita, A. W. Lin, S. A. Hearn, D. L. Spector, G. J. Hannon, and S. W. Lowe. 2003. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113:703-716.
49. Nevins, J. R. 1998. Toward an understanding of the functional complexity of the E2F and retinoblastoma families. Cell Growth Differ. 9:585-593.
50. Nguyen, C. T., D. J. Weisenberger, M. Velicescu, F. A. Gonzales, J. C. Lin, G. Liang, and P. A. Jones. 2002. Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-aza-2′-deoxcytidine. Cancer Res. 62:6456-6461.
51. Nicolas, E., V. Morales, L. Magnaghi-Jaulin, A. Harel-Bellan, H. Richard-Foy, and D. Trouche. 2000. RbAp48 belongs to the histone deacetylase complex that associates with the retinoblastoma protein. J. Biol. Chem. 275: 9797-9804.
52. 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.
53. Ogris, E., I. Mudrak, and E. Wintersberger. 1993. Distinct amounts of polyomavirus large T antigen are required for different functions of the protein. Oncogene 8:1277-1283.
54. Ohtani, K., J. DeGregori, and J. R. Nevins. 1995. Regulation of the cyclin E gene by transcription factor E2F1. Proc. Natl. Acad. Sci. USA 92:12146-12150.
55. Pagano, M., R. Pepperkok, F. Verde, W. Ansorge, and G. Draetta. 1992. Cyclin A is required at two points in the human cell cycle. EMBO J. 11:961-971.
56. Pattenden, S. G., R. Klose, E. Karaskov, and R. Bremner. 2002. Interferon-γ-induced chromatin remodeling at the CIITA locus is BRG1 dependent. EMBO J. 21:1978-1986.
57. Pearson, B. E., H. P. Nasheuer, and T. S. Wang. 1991. Human DNA polymerase α gene: sequences controlling expression in cycling and serum-stimulated cells. Mol. Cell. Biol. 11:2081-2095.
58. 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.
59. 1/S transition. Cancer Surv. 29:7-23.
60. Rietveld, L. E., E. Caldenhoven, and H. G. Stunnenberg. 2002. In vivo repression of an erythroid-specific gene by distinct corepressor complexes. EMBO J. 21:1389-1397.
61. Schulze, A., K. Zerfass, D. Spitkovsky, S. Middendorp, J. Berges, K. Helin, P. Jansen-Durr, and B. Henglein. 1995. Cell cycle regulation of the cyclin A gene promoter is mediated by a variant E2F site. Proc. Natl. Acad. Sci. USA 92:11264-11268.
62. Sellers, W. R., and W. G. Kaelin, Jr. 1997. Role of the retinoblastoma protein in the pathogenesis of human cancer. J. Clin. Oncol. 15:3301-3312.
63. Sellers, W. R., J. W. Rodgers, and W. G. Kaelin, Jr. 1995. A potent transrepression domain in the retinoblastoma protein induces a cell cycle arrest when bound to E2F sites. Proc. Natl. Acad. Sci. USA 92:11544-11548.
64. Shan, B., T. Durfee, and W. H. Lee. 1996. Disruption of RB/E2F-1 interaction by single point mutations in E2F-1 enhances S-phase entry and apoptosis. Proc. Natl. Acad. Sci. USA 93:679-684.
65. Sherr, C. J. 1996. Cancer cell cycles. Science 274:1672-1677.
66. 1/S boundary-specific enhancer of the rat cdc2 promoter. Mol. Cell. Biol. 15:2882-2892.
67. Shimizu, M., Y. Nomura, H. Suzuki, E. Ichikawa, A. Takeuchi, M. Suzuki, T. Nakamura, T. Nakajima, and K. Oda. 1998. Activation of the rat cyclin A promoter by ATF2 and Jun family members and its suppression by ATF4. Exp. Cell Res. 239:93-103.
68. Singh, P., J. Coe, and W. Hong. 1995. A role for retinoblastoma protein in potentiating transcriptional activation by the glucocorticoid receptor. Nature 374:562-565.
69. Slansky, J. E., and P. J. Farnham. 1996. Transcriptional regulation of the dihydrofolate reductase gene. Bioessays 18:55-62.
70. Strobeck, M. W., K. E. Knudsen, A. F. Fribourg, M. F. DeCristofaro, B. E. Weissman, A. N. Imbalzano, and E. S. Knudsen. 2000. BRG-1 is required for RB-mediated cell cycle arrest. Proc. Natl. Acad. Sci. USA 97:7748-7753.
71. Strobeck, M. W., D. N. Reisman, R. W. Gunawardena, B. L. Betz, S. P. Angus, K. E. Knudsen, T. F. Kowalik, B. E. Weissman, and E. S. Knudsen. 2002. Compensation of BRG-1 function by Brm: insight into the role of the core SWI-SNF subunits in retinoblastoma tumor suppressor signaling. J. Biol. Chem. 277:4782-4789.
72. 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.
73. Tommasi, S., and G. P. Pfeifer. 1995. In vivo structure of the human cdc2 promoter: release of a p130-E2F-4 complex from sequences immediately upstream of the transcription initiation site coincides with induction of cdc2 expression. Mol. Cell. Biol. 15:6901-6913.
74. Trouche, D., A. Cook, and T. Kouzarides. 1996. The CBP co-activator stimulates E2F1/DP1 activity. Nucleic Acids Res. 24:4139-4145.
75. Wang, J. Y., E. S. Knudsen, and P. J. Welch. 1994. The retinoblastoma tumor suppressor protein. Adv. Cancer Res. 64:25-85.
76. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
77. Weintraub, S. J., K. N. Chow, R. X. Luo, S. H. Zhang, S. He, and D. C. Dean. 1995. Mechanism of active transcriptional repression by the retinoblastoma protein. Nature 375:812-815.
78. 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.
79. Yoon, J. H., J. K. Kim, G. B. Rha, M. Oh, S. H. Park, R. H. Seong, S. H. Hong, and S. D. Park. 1999. Sp1 mediates cell proliferation-dependent regulation of rat DNA topoisomerase IIα gene promoter. Biochem. J. 344: 367-374.
80. Zhang, C. L., T. A. McKinsey, and E. N. Olson. 2002. Association of class II histone deacetylases with heterochromatin protein 1: potential role for histone methylation in control of muscle differentiation. Mol. Cell. Biol. 22: 7302-7312.
81. 1 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.
82. 1 arrest triggered by p16INK4a, TGFβ, and contact inhibition. Cell 97:53-61.
83. Zhang, Y., and M. L. Dufau. 2002. Silencing of transcription of the human luteinizing hormone receptor gene by histone deacetylase-mSin3A complex. J. Biol. Chem. 277:33431-33438.