mSin3A corepressor regulates diverse transcriptional networks governing normal and neoplastic growth and survival

Genes and Development

Volumn 19, Issue 13, 2005, Pages 1581-1595

  Dannenberg, Jan Hermen ^a,b   David, Gregory ^a,b,d   Zhong, Sheng ^c   Van Der Torre, Jaco ^a,b   Wong, Wing H ^c   DePinho, Ronald A ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c STANFORD UNIVERSITY   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Histone modifications; Knock out; mSin3 complex; mSin3A; Transcriptional regulation; Tumorigenesis

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA; IMITATION SWITCH PROTEIN; MYC PROTEIN; PROTEIN; PROTEIN MAD; PROTEIN NODAL; PROTEIN P53; STAT PROTEIN; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR SIN3A; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BIOLOGICAL ACTIVITY; CANCER CELL; CANCER GROWTH; CARCINOGENESIS; CELL CYCLE; CELL IMMORTALIZATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; CHEMICAL ANALYSIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPUTER MODEL; CONTROLLED STUDY; CYTOLOGY; DATA BASE; DEACETYLATION; DEVELOPMENT; DNA REPAIR; DNA REPLICATION; EMBRYO; EMBRYO DEVELOPMENT; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; GENETIC REGULATION; GROWTH; MATHEMATICAL ANALYSIS; MATHEMATICAL COMPUTING; MITOCHONDRIAL RESPIRATION; MONITORING; MOUSE; NONHUMAN; NUCLEOSOME; NULL CELL; ONCOGENE MYC; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; REGULATORY MECHANISM; TIME; TRANSCRIPTION REGULATION; UPREGULATION; VALIDATION PROCESS;

ANIMALS; CELL CYCLE; CELL SURVIVAL; CELLS, CULTURED; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MICE; NEOPLASMS, EXPERIMENTAL; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION, GENETIC;

EID: 22344454807     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1286905     Document Type: Article

References (77)

1. Aggarwal, B.D. and Calvi, B.R. 2004. Chromatin regulates origin activity in Drosophila follicle cells. Nature 430: 372-376.
2. Aguirre, A.J., Bardeesy, N., Sinha, M., Lopez, L., Tuveson, D.A., Horner, J., Redston, M.S., and DePinho, R.A. 2003. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes & Dev. 17: 3112-3126.
3. Alland, L., David, G., Shen-Li, H., Potes, J., Muhle, R., Lee, H.C., Hou, H.J., Chen, K., and DePinho, R.A. 2002. Identification of mammalian Sds3 as an integral component of the Sin3/histone deacetylase corepressor complex. Mol. Cell. Biol. 22: 2743-2750.
4. Aparicio, J.G., Viggiani, C.J., Gibson, D.G., and Aparicio, O.M. 2004. The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae. Mol. Cell. Biol. 24: 4769-4780.
5. Ayer, D.E. 1999. Histone deacetylases: Transcriptional repression with siners and nurds. Trends Cell. Biol. 9: 193-198.
6. Ayer, D.E., Lawrence, Q.A., and Eisenman, R.N. 1995. Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3 Cell 80: 767-776.
7. Badenhorst, P., Voas, M., Rebay, I., and Wu, C. 2002. Biological functions of the ISWI chromatin remodeling complex NURF. Genes & Dev. 16: 3186-3198.
8. Bailey, T.L. and Elkan, C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2: 28-36.
9. Barak, O., Lazzaro, M.A., Lane, W.S., Speicher, D.W., Picketts, D.J., and Shiekhattar, R. 2003. Isolation of human NURF: A regulator of Engrailed gene expression. EMBO J. 22: 6089-6100.
10. Bowser, R., Giambrone, A., and Davies, P. 1995. FAC1, a novel gene identified with the monoclonal antibody Alz50, is developmentally regulated in human brain. Dev. Neurosci. 17: 20-37.
11. Brehm, A., Miska, E.A., McCance, D.J., Reid, J.L., Bannister, A.J., and Kouzarides, T. 1998. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 391: 597-601.
12. Cheng, H.L., Mostoslavsky, R., Saito, S., Manis, J.P., Gu, Y., Patel, P., Bronson, R., Appella, E., and Alt, F.W. 2003. Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice. Proc. Natl. Acad. Sci. 100: 10794-10799.
13. Cowley, S.M., Iritani, B.M., Mendrysa, S.M., Xu, T., Cheng, P.F., Yada, J., Liggitt, H.D., and Eisenman, R.N. 2005. The mSin3A chromatin modifying complex is essential for embryogenesis and T cell development. Mol. Cell. Biol. (in press).
14. Dang, V.D., Benedik, M.J., Ekwall, K., Choi, J., Allshire, R.C, and Levin, H.L. 1999. A new member of the Sin3 family of corepressors is essential for cell viability and required for retroelement propagation in fission yeast. Mol. Cell. Biol. 19: 2351-2365.
15. Dannenberg, J.-H., van Rossum, A., Schuijff, L., and te Riele, H. 2000. Ablation of the retinoblastoma gene family deregulates G(1) control causing immortalization and increased cell turnover under growth-restricting conditions. Genes & Dev. 14: 3051-3064.
16. David, G., Turner, G.M., Yao, Y., Protopopov, A., and DePinho, R.A. 2003. mSin3-associated protein, mSds3, is essential for pericentric heterochromatin formation and chromosome segregation in mammalian cells. Genes & Dev. 17: 2396-2405.
17. De Nadal, E., Zapater, M., Alepuz, P.M., Sumoy, L., Mas, G., and Posas, F. 2004. The MAPK Hog1 recruits Rpd3 histone deacetylase to activate osmoresponsive genes. Nature 427: 370-374.
18. Fan, M., Rhee, J., St-Pierre, J., Handschin, C., Puigserver, P., Lin, J., Jaeger, S., Erdjument-Bromage, H., Tempst, P., and Spiegelman, B.M. 2004. Suppression of mitochondrial respiration through recruitment of p160 myb binding protein to PGC-1α: Modulation by p38 MAPK. Genes & Dev. 18: 278-289.
19. Fernandez, P.C., Frank, S.R., Wang, L., Schroeder, M., Liu, S., Greene, J., Cocito, A., and Amati, B. 2003. Genomic targets of the human c-Myc protein. Genes & Dev. 17: 1115-1129.
20. Fischle, W., Wang, Y., and Allis, C.D. 2003. Histone and chromatin cross-talk. Curr. Opin. Cell. Biol. 15: 172-183.
21. Fleischer, T.C., Yun, U.J., and Ayer, D.E. 2003. Identification and characterization of three new components of the mSin3A corepressor complex. Mol. Cell. Biol. 23: 3456-3467.
22. Helbing, C.C., Veillette, C., Riabowol, K., Johnston, R.N., and Garkavtsev, I. 1997. A novel candidate tumor suppressor, ING1, is involved in the regulation of apoptosis. Cancer Res. 57: 1255-1258.
23. Huang, Y., Myers, S.J., and Dingledine, R. 1999. Transcriptional repression by REST: Recruitment of Sin3A and histone deactylase to neuronal genes. Nat. Neurosci. 8: 67-72.
24. Jazayeri, A., McAinsh, A.D., and Jackson, S.P. 2004. Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc. Natl. Acad. Sci. 101: 1644-1649.
25. Johnstone, R.W. and Licht, J.D. 2003. Histone deacetylase inhibitors in cancer therapy: Is transcription the primary target? Cancer Cell 4: 13-18.
26. Jones, M.H., Hamana, N., and Shimane, M. 2000. Identification and characterization of BPTF, a novel bromodomain transcription factor. Genomics 63: 35-39.
27. Jordan-Sciutto, K.L., Dragich, J.M., Rhodes, J.L., and Bowser, R. 1999. Fetal Alz-50 clone 1, a novel zinc finger protein, binds a specific DNA sequence and acts as a transcriptional regulator. J. Biol. Chem. 274: 35262-35268.
28. Juan, L.J., Shia, W.J., Chen, M.H., Yang, W.M., Seto, E., Lin, Y.S., and Wu, C.W. 2000. Histone deacetylases specifically downregulate p53-dependent gene activation. J. Biol. Chem. 275: 20436-20443.
29. Kim, H., Lee, J.E., Cho, E.J., Liu, J.O., and Youn, H.D. 2003. Menin, a tumor suppressor, represses JunD-mediated transcriptional activity by association with an mSin3A-histone deacetylase complex. Cancer Res. 63: 6135-6139.
30. Knoepfler, P.S. and Eisenman, R.N. 1999. Sin meets NuRD and other tails of repression. Cell 99: 447-450.
31. Koipally, J., Renold, A., Kim, J., and Georgopoulos, K. 1999. Repression by Ikaros and Aiolos is mediated through histone deacetylase complexes. EMBO J. 18: 3090-3100.
32. Kuzmichev, A., Zhang, Y., Erdjument-Bromage, H., Tempst, P., and Reinberg, D. 2002. Role of the Sin3-histone deacetylase complex in growth regulation by the candidate tumor suppressor p33(ING1). Mol. Cell. Biol. 22: 835-848.
33. Lagger, G., O'Carroll, D., Rembold, M., Khier, H., Tischler, J., Weitzer, G., Schuettengruber, B., Hauser, C., Brunmeir, R., Jenuwein, T., et al. 2002. Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J. 21: 2672-2681.
34. Lagger, G., Doetzlhofer, A., Schuettengruber, B., Haidweger, E., Simboeck, E., Tischler, J., Chiocca, S., Suske, G., Rotheneder, H., Wintersberger, E., et al. 2003. The tumor suppressor p53 and histone deacetylase 1 are antagonistic regulators of the cyclin-dependent kinase inhibitor p21/WAF1/CIP1 gene. Mol. Cell. Biol. 23: 2669-2679.
35. Laherty, C.D., Yang, W.M., Sun, J.M., Davie, J.R., Seto, E., and Eisenman, R.N. 1997. Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression. Cell 89: 349-356.
36. Lai, A, Kennedy, B.K., Barbie, D.A., Bertos, N.R., Yang, X.J., Theberge, M.C., Tsai, S.C., Seto, E., Zhang, Y., Kuzmichev, A., et al. 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. 8: 2918-2932.
37. Lakso, M., Pichel, J.G., Gorman, J.R., Sauer, B., Okamoto, Y., Lee, E., Alt, F.W., and Westphal, H. 1996. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. 93: 5860-5865.
38. Lee, S.K., Kim, J.H., Lee, Y.C., Cheong, J., and Lee, J.W. 2000. Silencing mediator of retinoic acid and thyroid hormone receptors, as a novel transcriptional corepressor molecule of activating protein-1, nuclear factor-κB, and serum response factor. J. Biol. Chem. 275: 12470-12474.
39. Li, C. and Wong, W. 2001. Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proc. Natl. Acad. Sci. 98: 31-36.
40. Luo, R.X., Postigo, A.A., and Dean, D.C. 1998. Rb interacts with histone deacetylase to repress transcription. Cell 92: 463-473.
41. Luo, J., Su, F., Chen, D., Shiloh, A., and Gu, W. 2000. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 408: 377-381.
42. Luo, J., Nikolaev, A.Y., Imai, S., Chen, D., Su, F., Shiloh, A., Guarente, L., and Gu, W. 2001. Negative control of p53 by Sir2 promotes cell survival under stress. Cell 107: 137-148.
43. Magnaghi-Jaulin, L., Groisman, R., Naguibneva, I., Robin, P., Lorain, S., Le Villain, J.P., Troalen, F., Trouche, D., and Harel-Bellan, A. 1998. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 391: 601-605.
44. Matys, V., Fricke, E., Geffers, R., Gossling, E., Haubrock, M., Hehl, R., Hornischer, K., Karas, D., Kel, A.E., Kel-Margoulis, O.V., et al. 2003. TRANSFAC®: Transcriptional regulation, from patterns to profiles. Nucleic Acids Res. 31: 374-378.
45. Meehan, W.J., Samant, R.S., Hopper, J.E., Carrozza, M.J., Shevde, L.A., Workman, J.L., Eckert, K.A., Verderame, M.F., and Welch, D.R. 2004. Breast cancer metastasis suppressor 1 (BRMS1) forms complexes with retinoblastoma- binding protein 1 (RBP1) and the mSin3 histone deacetylase complex and represses transcription. J. Biol. Chem. 279: 1562-1569.
46. Melnick, A. and Licht, J.D. 2002. Histone deacetylases as therapeutic targets in hematologic malignancies. Curr. Opin. Hematol. 9: 322-332.
47. Murphy, M., Ahn, J., Walker, K.K., Hoffman, W.H., Evans, R.M., Levine, A.J., and George, D.L. 1999. Transcriptional repression by wild-type p53 utilizes histone deacetylases, mediated by interaction with mSin3a. Genes & Dev. 13: 2490-2501.
48. Nakayama, J., Xiao, G., Noma, K., Malikzay, A., Bjerling, P., Ekwall, K., Kobayashi, R., and Grewal, S.I. 2003. Alp13, an MRG family protein, is a component of fission yeast Clr6 histone deacetylase required for genomic integrity. EMBO J. 22: 2776-2787.
49. Naviaux, R.K., Costanzi, E., Haas, M., and Verma, I.M. 1996. The pCL vector system: Rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70: 5701-5705.
50. Nicholson, D.W., Ali, A., Thornberry, N.A., Vaillancourt, J.P., Ding, C.K., Gallant, M., Gareau, Y., Griffin, P.R., Labelle, M., Lazebnik, Y.A., et al. 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376: 37-43.
51. Orian, A., van Steensel, B., Delrow, J., Bussemaker, H.J., Li, L., Sawado, T., Williams, E., Loo, L.W., Cowley, S.M., Yost, C., et al. 2003. Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. Genes & Dev. 17: 1101-1114.
52. Pile, L.A., Spellman, P.T., Katzenberger, R.J., and Wassarman, D.A. 2003. The SIN3 deacetylase complex represses genes encoding mitochondrial proteins: Implications for the regulation of energy metabolism. J. Biol. Chem. 278: 37840-37848.
53. Pothof, J., van Haaften, G., Thijssen, K., Kamath, R.S., Fraser, A.G., Ahringer, J., Plasterk, R.H., and Tijsterman, M. 2003. Identification of genes that protect the C. elegans genome against mutations by genome-wide RNAi. Genes & Dev. 17: 443-448.
54. Prasanth, S.G., Prasanth, K.V., Siddiqui, K., Spector, D.L., and Stillman, B. 2004. Human Orc2 localizes to centrosomes, centromeres and heterochromatin during chromosome inheritance. EMBO J. 23: 2651-2663.
55. Puigserver, P., Wu, Z., Park, C.W., Graves, R., Wright, M., and Spiegelman, B.M. 1998. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92: 829-839.
56. Rayman, J.B., Takahashi, Y., Indjeian, V.B., Dannenberg, J.-H., Catchpole, S., Watson, R.J., te Riele, H., and Dynlacht, B.D. 2002. E2F mediates cell cycle-dependent transcriptional repression in vivo by recruitment of an HDAC1/mSin3B corepressor complex. Genes & Dev. 16: 933-947.
57. Reiss, U., Oskouian, B., Zhou, J., Gupta, V., Sooriyakumaran, P., Kelly, S., Wang, E., Merrill Jr., A.H., and Saba, J.D. 2004. Sphingosine-phosphate lyase enhances stress-induced ceramide generation and apoptosis. J. Biol. Chem. 279: 1281-1290.
58. Ren, B., Cam, H., Takahashi, Y., Volkert, T., Terragni, J., Young, R.A., and Dynlacht, B.D. 2002. E2F integrates cell cycle progression with DNA repair, replication, and G(2)/M checkpoints. Genes & Dev. 16: 245-256.
59. Rodriguez, C.I., Buchholz, F., Galloway, J., Sequerra, R., Kasper, J., Ayala, R., Stewart, A.F., and Dymecki, S.M. 2000. Highefficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 2: 139-140.
60. Sakaguchi, K., Herrera, J.E., Saito, S., Miki, T., Bustin, M., Vassilev, A., Anderson, C.W., and Appella, E. 1998. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes & Dev. 12: 2831-2841.
61. Schreiber-Agus, N. and DePinho, R.A. 1998. Repression by the mad(mxi1)-sin3 complex. Bioessays 20: 808-818.
62. Schreiber-Agus, N., Chin, L., Chen, K., Torres, R., Rao, G., Guida, P., Skoultchi, A.I., and DePinho, R.A. 1995. An amino-terminal domain of Mxi1 mediates anti-Myc oncogenic activity and interacts with a homolog of the yeast repressor SIN3. Cell 80: 777-786.
63. Schuettengruber, B., Simboeck, E., Khier, H., and Seiser, C. 2003. Autoregulation of mouse histone deacetylase 1 expression. Mol. Cell. Biol. 19: 6993-7004.
64. Siepel, A. and Haussler, D. 2005. Phylogenetic hidden Markov models. In Statistical methods in molecular evolution (ed. R. Nielsen), pp. 325-351. Springer, New York.
65. Sif, S., Saurin A.J., Imbalzano, A.N., and Kingston, R.E. 2001. Purification and characterization of mSin3A-containing Brg1 and hBrm chromatin remodeling complexes. Genes & Dev. 15: 603-618.
66. Silverstein, R.A. and Ekwall, K. 2004. Sin3: A flexible regulator of global gene expression and genome instability. Curr. Genet. 47: 1-17.
67. Silverstein, R.A., Richardson, W., Levin, H., Allshire, R., and Ekwall, K. 2003. A new role for the transcriptional corepressor SIN3; regulation of centromeres. Curr. Biol. 13: 68-72.
68. Skowyra, D., Zeremski, M., Neznanov, N., Li, M., Choi, Y., Uesugi, M., Hauser, C.A., Gu, W., Gudkov, A.V., and Qin, J. 2001. Differential association of products of alternative transcripts of the candidate tumor suppressor ING1 with the mSin3/HDAC1 transcriptional corepressor complex. J. Biol. Chem. 276: 8734-8739.
69. Sternberg, P.W., Stern, M.J., Clark, I., and Herskowitz, I. 1987. Activation of the yeast HO gene by release from multiple negative controls. Cell 48: 567-577.
70. Vannier, D., Balderes, D., and Shore, D. 1996. Evidence that the transcriptional regulators SIN3 and RPD3, and a novel gene (SDS3) with similar functions, are involved in transcriptional silencing in S. cerevisiae. Genetics 144: 1343-1353.
71. Vaziri, H., Dessain, S.K., Ng Eaton, E., Imai, S.I., Frye, R.A., Pandita, T.K., Guarente, L., and Weinberg, R.A. 2001. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 107: 149-159.
72. Wang, R., Cherukuri, P., and Luo, J. 2005. Activation of Stat3 sequence-specific DNA binding and transcription by p300/CREB-binding protein-mediated acetylation. J. Biol. Chem. 280: 11528-11534.
73. Whitfield, M.L., Sherlock, G., Saldanha, A.J., Murray, J.I., Ball, C.A., Alexander, K.E., Matese, J.C., Perou, C.M., Hurt, M.M., Brown, P.O., et al. 2002. Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol. Biol. Cell. 6: 1977-2000.
74. Xiao, H., Sandaltzopoulos, R., Wang, H.M., Hamiche, A., Ranallo, R., Lee, K.M., Fu, D., and Wu, C. 2001. Dual functions of largest NURF subunit NURF301 in nucleosome sliding and transcription factor interactions. Mol. Cell. 8: 531-543.
75. Yang, X.J. 2004. Lysine acetylation and the bromodomain: A new partnership for signaling. Bioessays 26: 1076-1087.
76. Yuan, Z.L., Guan, Y.J., Chatterjee, D., and Chin, Y.E. 2005. Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science 307: 269-273.
77. Zilfou, J.T., Hoffman, W.H., Sank, M., George, D.L., and Murphy, M. 2001. The corepressor mSin3a interacts with the proline-rich domain of p53 and protects p53 from proteasome-mediated degradation. Mol. Cell. Biol. 21: 3974-3985.