Nuclear hormone receptor co-repressors: Structure and function

Molecular and Cellular Endocrinology

Volumn 348, Issue 2, 2012, Pages 440-449

  Watson, Peter J ^a   Fairall, Louise ^a   Schwabe, John W R ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Co repressor; GPS2; HDAC; Nuclear receptor; SMRT NCoR; TBL1

Indexed keywords

CELL NUCLEUS RECEPTOR; HISTONE; HISTONE DEACETYLASE 3; NUCLEAR RECEPTOR COREPRESSOR; SILENCING MEDIATOR OF RETINOID AND THYROID HORMONE RECEPTOR; TRANSCRIPTION FACTOR;

CARBOXY TERMINAL SEQUENCE; HISTONE MODIFICATION; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW;

ANIMALS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HUMANS; MULTIPROTEIN COMPLEXES; NUCLEAR RECEPTOR CO-REPRESSOR 1; NUCLEAR RECEPTOR CO-REPRESSOR 2; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 82655181792     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.08.033     Document Type: Review

References (108)

1. Aasland R., Stewart A.F., Gibson T. The SANT domain: a putative DNA-binding domain in the SWI-SNF and ADA complexes, the transcriptional co-repressor N-CoR and TFIIIB. Trends Biochem. Sci. 1996, 21:87-88.
2. Ahmad K.F., Melnick A., Lax S., Bouchard D., Liu J., Kiang C., Mayer S., Takahashi S., Licht J.D., Prive G.G. Mechanism of SMRT corepressor recruitment by the BCL6 BTB domain. Mol. Cell 2003, 12:1551-1564.
3. Amann J.M., Nip J., Strom D.K., Lutterbach B., Harada H., Lenny N., Downing J.R., Meyers S., Hiebert S.W. ETO, a target of t(8;21) in acute leukemia, makes distinct contacts with multiple histone deacetylases and binds mSin3A through its oligomerization domain. Mol. Cell. Biol. 2001, 21:6470-6483.
4. Ariyoshi M., Schwabe J.W.R. A conserved structural motif reveals the essential transcriptional repression function of Spen proteins and their role in developmental signaling. Genes Dev. 2003, 17:1909-1920.
5. Astapova I., Dordek M.F., Hollenberg A.N. The thyroid hormone receptor recruits NCoR via widely spaced receptor-interacting domains. Mol. Cell. Endocrinol. 2009, 307:83-88.
6. Baek S.H., Ohgi K.A., Rose D.W., Koo E.H., Glass C.K., Rosenfeld M.G. Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappaB and beta-amyloid precursor protein. Cell 2002, 110:55-67.
7. Cavaillès V., Dauvois S., L'Horset F., Lopez G., Hoare S., Kushner P.J., Parker M.G. Nuclear factor RIP140 modulates transcriptional activation by the estrogen receptor. EMBO J. 1995, 14:3741-3751.
8. Cerchietti L.C., Yang S.N., Shaknovich R., Hatzi K., Polo J.M., Chadburn A., Dowdy S.F., Melnick A. A peptomimetic inhibitor of BCL6 with potent antilymphoma effects in vitro and in vivo. Blood 2009, 113:3397-3405.
9. Cerna D., Wilson D.K. The structure of Sif2p, a WD repeat protein functioning in the SET3 corepressor complex. J. Mol. Biol. 2005, 351:923-935.
10. Chen J.D., Evans R.M. A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature 1995, 377:454-457.
11. Christian M., Tullet J.M.A., Parker M.G. Characterization of four autonomous repression domains in the corepressor receptor interacting protein 140. J. Biol. Chem. 2004, 279:15645-15651.
12. Codina A., Love J.D., Li Y., Lazar M.A., Neuhaus D., Schwabe J.W.R. Structural insights into the interaction and activation of histone deacetylase 3 by nuclear receptor corepressors. Proc. Natl. Acad. Sci. USA 2005, 102:6009-6014.
13. Cohen R.N., Putney A., Wondisford F.E., Hollenberg A.N. The nuclear corepressors recognize distinct nuclear receptor complexes. Mol. Endocrinol. 2000, 14:900-914.
14. Couture J., Collazo E., Trievel R.C. Molecular recognition of histone H3 by the WD40 protein WDR5. Nat. Struct. Mol. Biol. 2006, 13:698-703.
15. Darimont B.D., Wagner R.L., Apriletti J.W., Stallcup M.R., Kushner P.J., Baxter J.D., Fletterick R.J., Yamamoto K.R. Structure and specificity of nuclear receptor-coactivator interactions. Genes Dev. 1998, 12:3343-3356.
16. Dhordain P., Lin R.J., Quief S., Lantoine D., Kerckaert J.P., Evans R.M., Albagli O. The LAZ3(BCL-6) oncoprotein recruits a SMRT/mSIN3A/histone deacetylase containing complex to mediate transcriptional repression. Nucleic Acids Res. 1998, 26:4645-4651.
17. Fernandes I., Bastien Y., Wai T., Nygard K., Lin R., Cormier O., Lee H.S., Eng F., Bertos N.R., Pelletier N., Mader S., Han V.K.M., Yang X., White J.H. Ligand-dependent nuclear receptor corepressor LCoR functions by histone deacetylase-dependent and -independent mechanisms. Mol. Cell 2003, 11:139-150.
18. Fischle W., Dequiedt F., Hendzel M.J., Guenther M.G., Lazar M.A., Voelter W., Verdin E. Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Mol. Cell 2002, 9:45-57.
19. Fritah A., Christian M., Parker M.G. The metabolic coregulator RIP140: an update. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E335-40.
20. Fu M., Wang C., Wang J., Zhang X., Sakamaki T., Yeung Y.G., Chang C., Hopp T., Fuqua S.A.W., Jaffray E., Hay R.T., Palvimo J.J., Janne O.A., Pestell R.G. Androgen receptor acetylation governs trans activation and MEKK1-induced apoptosis without affecting in vitro SUMOylation and trans-repression function. Mol. Cell. Biol. 2002, 22:3373-3388.
21. Gelmetti V., Zhang J., Fanelli M., Minucci S., Pelicci P.G., Lazar M.A. Aberrant recruitment of the nuclear receptor corepressor-histone deacetylase complex by the acute myeloid leukemia fusion partner ETO. Mol. Cell. Biol. 1998, 18:7185-7191.
22. Ghetu A.F., Corcoran C.M., Cerchietti L., Bardwell V.J., Melnick A., Privé G.G. Structure of a BCOR corepressor peptide in complex with the BCL6 BTB domain dimer. Mol. Cell 2008, 29:384-391.
23. Glass C.K., Rosenfeld M.G. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 2000, 14:121-141.
24. Goodson M.L., Jonas B.A., Privalsky M.L. Alternative mRNA splicing of SMRT creates functional diversity by generating corepressor isoforms with different affinities for different nuclear receptors. J. Biol. Chem. 2005, 280:7493-7503.
25. Greschik H., Wurtz J., Sanglier S., Bourguet W., Van Dorsselaer A., Moras D., Renaud J. Structural and functional evidence for ligand-independent transcriptional activation by the estrogen-related receptor 3. Mol. Cell 2002, 21:6091-6101.
26. Guenther M.G., Lane W.S., Fischle W., Verdin E., Lazar M.A., Shiekhattar R. A core SMRT corepressor complex containing HDAC3 and TBL1, a WD40-repeat protein linked to deafness. Genes Dev. 2000, 14:1048-1057.
27. Guenther M.G., Orr B., Lazar M.A. The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Mol. Cell. Biol. 2001, 21:6091-6101.
28. Guenther M.G., Yu J., Kao G.D., Yen T.J., Lazar M.A. Assembly of the SMRT-histone deacetylase 3 repression complex requires the TCP-1 ring complex. Genes Dev. 2002, 16:3130-3135.
29. Hartman H.B., Yu J., Alenghat T., Ishizuka T., Lazar M.A. The histone-binding code of nuclear receptor co-repressors matches the substrate specificity of histone deacetylase 3. EMBO Rep. 2005, 6:445-451.
30. Haynes C., Oldfield C.J., Ji F., Klitgord N., Cusick M.E., Radivojac P., Uversky V.N., et al. Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput. Biol. 2006, 2:100.
31. Heery D.M., Kalkhoven E., Hoare S., Parker M.G. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 1997, 387:733-736.
32. Heinzel T., Lavinsky R.M., Mullen T.M., Söderström M., Laherty C.D., Torchia J., Yang W.M., Brad G., Ngo S.D., Davie J.R., Seto E., Eisenman R.N., Rose D.W., Glass C.K., Rosenfeld M.G. A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature 1997, 387:43-48.
33. Hermanson O., Glass C.K., Rosenfeld M.G. Nuclear receptor coregulators: multiple modes of modification. Trends Endocrinol. Metab. 2002, 13:55-60.
34. Herzog B., Hallberg M., Seth A., Woods A., White R., Parker M.G. The nuclear receptor cofactor, receptor-interacting protein 140, is required for the regulation of hepatic lipid and glucose metabolism by liver X receptor. Mol. Endocrinol. 2007, 21:2687-2697.
35. Hong S.H., Privalsky M.L. The SMRT corepressor is regulated by a MEK-1 kinase pathway: inhibition of corepressor function is associated with SMRT phosphorylation and nuclear export. Mol. Cell. Biol. 2000, 20:6612-6625.
36. Hörlein A.J., Näär A.M., Heinzel T., Torchia J., Gloss B., Kurokawa R., Ryan A., Kamei Y., Soderstrom M., Glass C.K. Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 1995, 377:397-404.
37. Hu X., Lazar M.A. The CoRNR motif controls the recruitment of corepressors by nuclear hormone receptors. Nature 1999, 402:93-96.
38. Huang E.Y., Zhang J., Miska E.A., Guenther M.G., Kouzarides T., Lazar M.A. Nuclear receptor corepressors partner with class II histone deacetylases in a Sin3-independent repression pathway. Genes Dev. 2000, 14:45-54.
39. Huynh K.D., Fischle W., Verdin E., Bardwell V.J. BCoR, a novel corepressor involved in BCL-6 repression. Genes Dev. 2000, 14:1810-1823.
40. Ishizuka T., Lazar M.A. The N-CoR/histone deacetylase 3 complex is required for repression by thyroid hormone receptor. Mol. Cell. Biol. 2003, 23:5122-5131.
41. Jayne S., Zwartjes C.G.M., van Schaik F.M.A., Timmers H.T.M. Involvement of the SMRT/NCoR-HDAC3 complex in transcriptional repression by the CNOT2 subunit of the human Ccr4-Not complex. Biochem. J. 2006, 398:461-467.
42. Jin L., Yong L. Structural and functional insights into nuclear receptor signaling. Adv. Drug Deliv. Rev. 2010, 62:1218-1226.
43. Kallenberger B.C., Love J.D., Chatterjee V.K.K., Schwabe J.W.R. A dynamic mechanism of nuclear receptor activation and its perturbation in a human disease. Nat. Struct. Mol. Biol. 2003, 10:136-140.
44. Kao H.Y., Ordentlich P., Koyano-Nakagawa N., Tang Z., Downes M., Kintner C.R., Evans R.M., Kadesch T. A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes. Dev. 1998, 12:2269-2277.
45. Kao H.Y., Downes M., Ordentlich P., Evans R.M. Isolation of a novel histone deacetylase reveals that class I and class II deacetylases promote SMRT-mediated repression. Genes Dev. 2000, 14:55-66.
46. Kelley L.A., Sternberg M.J.E. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 2009, 4:363-371.
47. Kim J.Y., Son Y.L., Kim J.-S., Lee Y.C. Molecular determinants required for selective interactions between the thyroid hormone receptor homodimer and the nuclear receptor corepressor N-CoR. J. Mol. Biol. 2010, 396:747-760.
48. Kiskinis E., Hallberg M., Christian M., Olofsson M., Dilworth S.M., White R., Parker M.G. RIP140 directs histone and DNA methylation to silence Ucp1 expression in white adipocytes. EMBO J. 2007, 26:4831-4840.
49. le Maire A., Teyssier C., Erb C., Grimaldi M., Alvarez S., de Lera A.R., Balaguer P., Gronemeyer H., Royer C.A., Germain P., Bourguet W. A unique secondary-structure switch controls constitutive gene repression by retinoic acid receptor. Nat. Struct. Mol. Biol. 2010, 17:801-807.
50. Lee J., Maskos K., Huber R. Structural and functional studies of the yeast class II Hda1 histone deacetylase complex. J. Mol. Biol. 2009, 391:744-757.
51. Lemercier C., Brocard M., Puvion-Dutilleul F., Kao H., Albagli O., Khochbin S. Class II histone deacetylases are directly recruited by BCL6 transcriptional repressor. J. Biol. Chem. 2002, 277:22045-22052.
52. Li J., Wang J., Wang J., Nawaz Z., Liu J.M., Qin J., Wong J. Both corepressor proteins SMRT and N-CoR exist in large protein complexes containing HDAC3. EMBO J. 2000, 19:4342-4350.
53. Li J., Lin Q., Wang W., Wade P., Wong J. Specific targeting and constitutive association of histone deacetylase complexes during transcriptional repression. Genes Dev. 2002, 16:687-692.
54. Liu Y., Chen W., Gaudet J., Cheney M.D., Roudaia L., Cierpicki T., Klet R.C., Hartman K., Laue T.M., Speck N.A., Bushweller J.H. Structural basis for recognition of SMRT/N-CoR by the MYND domain and its contribution to AML1/ETO's activity. Cancer Cell 2007, 11:483-497.
55. Lutterbach B., Westendorf J.J., Linggi B., Patten A., Moniwa M., Davie J.R., Huynh K.D., Bardwell V.J., Lavinsky R.M., Rosenfeld M.G., Glass G., Seto E., Hiebert S.W. ETO, a target of t(8;21) in acute leukemia, interacts with the N-CoR and mSin3 corepressors. Mol. Cell. Biol. 1998, 8:7176-7184.
56. Madauss K.P., Grygielko E.T., Deng S., Sulpizio A.C., Stanley T.B., Wu C., Short S.A., Thompson S.K., Stewart E.L., Laping N.l., Williams S.P., Bray J.D. A structural and in vitro characterization of asoprisnil: a selective progesterone receptor modulator. Mol. Endocrinol. 2007, 21:1066-1081.
57. Makde R.D., England J.R., Yennawar H.P., Tan S. Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature 2010, 467:562-566.
58. Makowski A., Brzostek S., Cohen R.N., Hollenberg A.N. Determination of nuclear receptor corepressor interactions with the thyroid hormone receptor. Mol. Endocrinol. 2003, 17:273-286.
59. Malartre M., Short S., Sharpe C. Alternative splicing generates multiple SMRT transcripts encoding conserved repressor domains linked to variable transcription factor interaction domains. Nucleic Acids Res. 2004, 32:4676-4686.
60. Malartre M., Short S., Sharpe C. Xenopus embryos lacking specific isoforms of the corepressor SMRT develop abnormal heads. Dev. Biol. 2006, 292:333-343.
61. Mangelsdorf D.J., Thummel C., Beato M., Herrlich P., Schütz G., Umesono K., Blumberg B., Kastner P., Mark M., Chambon P., Evans R.M. The nuclear receptor superfamily: the second decade. Cell 1995, 83:835-839.
62. Margueron R., Justin N., Ohno K., Sharpe M.L., Son J., Drury W.J., Voigt P., Martin S.R., Taylor W.R., De Marco V., Pirrotta V., Reinberg D., Gambin S.J. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 2009, 461:762-767.
63. McKenna N.J., Lanz R.B., O'Malley B.W. Nuclear receptor coregulators: cellular and molecular biology. Endocr. Rev. 1999, 20:321-344.
64. Melnick A., Carlile G., Ahmad K.F., Kiang C., Corcoran C., Bardwell V., Prive G., Licht J.D. Critical residues within the BTB domain of PLZF and Bcl-6 modulate interaction with corepressors. Mol. Cell. Biol. 2002, 22:1804-1818.
65. Miyoshi H., Kozu T., Shimizu K., Enomoto K., Maseki N., Kaneko Y., Kamada N., Ohki M. The t(8;21) translocation in acute myeloid leukemia results in production of an AML1-MTG8 fusion transcript. EMBO J. 1993, 2:2715-2721.
66. Murzina N.V., Pei X., Zhang W., Sparkes M., Vicente-Garcia J., Pratap J.V., McLaughlin S.H., Ben-Shahar T.R., Verreault A., Luisi B.F. Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 2008, 16:1077-1085.
67. Nagy L., Kao H.Y., Chakravarti D., Lin R.J., Hassig C.A., Ayer D.E., Schreiber S., Evans R.M. Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell 1997, 89:373-380.
68. Nagy L., Kao H.Y., Love J.D., Li C., Banayo E., Gooch J.T., Krishna V., Chatterjee K., Evans R.M., Schwabe J.W. Mechanism of corepressor binding and release from nuclear hormone receptors. Genes Dev. 1999, 13:3209-3216.
69. Niu H., Cattoretti G., Dalla-Favera R. BCL6 controls the expression of the B7-1/CD80 costimulatory receptor in germinal center B cells. J. Exp. Med. 2003, 198:211-221.
70. Nolte R.T., Wisely G.B., Westin S., Cobb J.E., Lambert M.H., Kurokawa R., Rosenfeld M.G., Willson T.M., Glass C.K., Milburn V.M. Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-gamma. Nature 1998, 395:137-143.
71. Oberoi J., Fairall L., Watson P.J., Yang J., Czimmerer Z., Kampmann T., Goult B.T., Greenwood J.A., Gooch J.T., Kallenberger B.C., Nagy L., Neuhaus D., Schwabe J.W.R. Structural basis for the assembly of the SMRT/NCoR core transcriptional repression machinery. Nat. Struct. Mol. Biol. 2011, 18:177-184.
72. Oswald F., Kostezka U., Astrahantseff K., Bourteele S., Dillinger K., Zechner U., Ludwig L., Wilda M., Hameister H., Knochel W., Liptay S., Schmid R.M. SHARP is a novel component of the Notch/RBP-Jkappa signalling pathway. EMBO J. 2002, 21:5417-5426.
73. Pashkova N., Gakhar L., Winistorfer S.C., Yu L., Ramaswamy S., Piper R.C. WD40 repeat propellers define a ubiquitin-binding domain that regulates turnover of F box proteins. Mol. Cell 2010, 40:433-443.
74. Perissi V., Rosenfeld M.G. Controlling nuclear receptors: the circular logic of cofactor cycles. Nat. Rev. Mol. Cell. Biol. 2005, 6:542-554.
75. Perissi V., Staszewski L.M., McInerney E.M., Kurokawa R., Krones A., Rose D.W., Lambert M.H., Milburn M.V., Glass C.K., Rosenfeld M.G. Molecular determinants of nuclear receptor-corepressor interaction. Genes Dev. 1999, 13:3198-3208.
76. Phelan C.A., Gampe R.T., Lambert M.H., Parks D.J., Montana V., Bynum J., Broderick T.M., Hu X., Williams S.P., Nolte R.T., Lazar M.A. Structure of Rev-erbalpha bound to N-CoR reveals a unique mechanism of nuclear receptor-co-repressor interaction. Nat. Struct. Mol. Biol. 2010, 17:808-814.
77. Picard F., Kurtev M., Chung N., Topark-Ngarm A., Senawong T., Machado De Oliveira R., Leid M., McBurney M.W., Guarente L. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 2004, 429:771-776.
78. Polo J.M., Dell'Oso T., Ranuncolo S.M., Cerchietti L., Beck D., Da Silva G.F., Prive G.G., Licht J.D., Melnick A. Specific peptide interference reveals BCL6 transcriptional and oncogenic mechanisms in B-cell lymphoma cells. Nat. Med. 2004, 10:1329-1335.
79. Sablin E.P., Krylova I.N., Fletterick R.J., Ingraham H.A. Structural basis for ligand-independent activation of the orphan nuclear receptor LRH-1. Mol. Cell 2003, 11:1575-1585.
80. Sakano D., Kato A., Parikh N., McKnight K., Terry D., Stefanovic B., Kato Y. BCL6 canalizes Notch-dependent transcription, excluding Mastermind-like1 from selected target genes during left-right patterning. Dev. Cell 2010, 18:450-462.
81. Schalch T., Duda S., Sargent D.F., Richmond T.J. X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature 2005, 436:138-141.
82. Shi Y., Downes M., Xie W., Kao H.Y., Ordentlich P., Tsai C.C., Hon M., Evans R.M. SHARP, an inducible cofactor that integrates nuclear receptor repression and activation. Genes Dev. 2001, 15:1140-1151.
83. Shiau A.K., Barstad D., Loria P.M., Cheng L., Kushner P.J., Agard D.A., Greene G.L. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 1998, 95:927-937.
84. Short S., Malartre M., Sharpe C. SMRT has tissue-specific isoform profiles that include a form containing one CoRNR box. Biochem. Biophys. Res. Commun. 2005, 334:845-852.
85. Singh G.P., Ganapathi M., Dash D. Role of intrinsic disorder in transient interactions of hub proteins. Proteins 2007, 66:761-765.
86. Song J., Garlick J.D., Kingston R.E. Structural basis of histone H4 recognition by p55. Genes Dev. 2008, 22:1313-1318.
87. Sprague E.R., Redd M.J., Johnson A.D., Wolberger C. Structure of the C-terminal domain of Tup1, a corepressor of transcription in yeast. EMBO J. 2000, 19:3016-3027.
88. Varlakhanova N., Snyder C., Jose S., Hahm J.B., Privalsky M.L. Estrogen receptors recruit SMRT and N-CoR corepressors through newly recognized contacts between the corepressor N terminus and the receptor DNA binding domain. Mol. Cell. Biol. 2010, 30:1434-1445.
89. Varlakhanova N., Hahm J.B., Privalsky M.L. Regulation of SMRT corepressor dimerization and composition by MAP kinase phosphorylation. Mol. Cell. Endocrinol. 2011, 322:180-188.
90. Vo N., Fjeld C., Goodman R.H. Acetylation of nuclear hormone receptor-interacting protein RIP140 regulates binding of the transcriptional corepressor CtBP. Mol. Cell. Biol. 2001, 21:6181-6188.
91. Wang J., Hoshino T., Redner R.L., Kajigaya S., Liu J.M. ETO, fusion partner in t(8;21) acute myeloid leukemia, represses transcription by interaction with the human N-CoR/mSin3/HDAC1 complex. Proc. Natl. Acad. Sci. USA 1998, 95:10860-10865.
92. Wang C., Fu M., Angeletti R.H., Siconolfi-Baez L., Reutens A.T., Albanese C., Lisanti M.P., Katzenellenbogen B.S., Kato S., Hopp T., Fuqua S.A.W., Lopez G.N., Kushner P.J., Pestell R.G. Direct acetylation of the estrogen receptor alpha hinge region by p300 regulates transactivation and hormone sensitivity. J. Biol. Chem. 2001, 276:18375-18383.
93. Wang L., Zuercher W.J., Consler T.G., Lambert M.H., Miller A.B., Orband-Miller L.A., McKee D.D., Wilson T.M. X-ray crystal structures of the estrogen-related receptor-gamma ligand binding domain in three functional states reveal the molecular basis of small molecule regulation. J. Biol. Chem. 2006, 281:37773-37781.
94. Wang Z., Zang C., Cui K., Schones D.E., Barski A., Peng W., Zhao K. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009, 138:1019-1031.
95. Watkins R.E., Wisely G.B., Moore L.B., Collins J.L., Lambert M.H., Williams S.P., Willson T.M., Kliewer S.A., Redinbo M.R. The human nuclear xenobiotic receptor PXR: structural determinants of directed promiscuity. Science 2001, 292:2329-2333.
96. Webb P., Anderson C.M., Valentine C., Nguyen P., Marimuthu A., West B.L., Baxter J.D., Kushner P.J. The nuclear receptor corepressor (N-CoR) contains three isoleucine motifs (I/LXXII) that serve as receptor interaction domains (IDs). Mol. Endocrinol. 2000, 14:1976-1985.
97. Wei L.N., Hu X., Chandra D., Seto E., Farooqui M. Receptor-interacting protein 140 directly recruits histone deacetylases for gene silencing. J. Biol. Chem. 2000, 275:40782-40787.
98. Wen Y.D., Perissi V., Staszewski L.M., Yang W.M., Krones A., Glass C.K., Rosenfeld M.G., Seto E. The histone deacetylase-3 complex contains nuclear receptor corepressors. Proc. Natl. Acad. Sci. USA 2000, 97:7202-7207.
99. Willson T.M., Moore J.T. Genomics versus orphan nuclear receptors - a half-time report. Mol. Endocrinol. 2002, 16:1135-1144.
100. Wong C.W., Privalsky M.L. Components of the SMRT corepressor complex exhibit distinctive interactions with the POZ domain oncoproteins PLZF, PLZF-RARalpha, and BCL-6. J. Biol. Chem. 1998, 273:27695-27702.
101. Wu X., Li H., Park E.J., Chen J.D. SMRTE inhibits MEF2C transcriptional activation by targeting HDAC4 and 5 to nuclear domains. J. Biol. Chem. 2001, 276:24177-24185.
102. Xu H.E., Stanley T.B., Montana V.G., Lambert M.H., Shearer B.G., Cobb J.E., McKee D.D., Galardi C.M., Plunket K.D., Nolte R.T., Parks D.J., Moore J.T., Kliewer S.A., Willson T.M., Stimmel J.B. Structural basis for antagonist-mediated recruitment of nuclear co-repressors by PPARalpha. Nature 2002, 415:813-817.
103. Yang W., Tsai S., Wen Y., Fejer G., Seto E. Functional domains of histone deacetylase-3. J. Biol. Chem. 2002, 277:9447-9454.
104. Yoon H., Chan D.W., Reynolds A.B., Qin J., Wong J. N-CoR mediates DNA methylation-dependent repression through a methyl CpG binding protein Kaiso. Mol. Cell 2003, 12:723-734.
105. Yu J., Li Y., Ishizuka T., Guenther M.G., Lazar M.A. A SANT motif in the SMRT corepressor interprets the histone code and promotes histone deacetylation. EMBO J. 2003, 22:3403-3410.
106. Zhang J., Kalkum M., Chait B.T., Roeder R.G. The N-CoR-HDAC3 nuclear receptor corepressor complex inhibits the JNK pathway through the integral subunit GPS2. Mol. Cell 2002, 9:611-623.
107. Zhang X., Ozawa Y., Lee H., Wen Y., Tan T., Wadzinski B.E., Seto E. Histone deacetylase 3 (HDAC3) activity is regulated by interaction with protein serine/threonine phosphatase 4. Genes Dev. 2005, 19:827-839.
108. Zhou Y., Gross W., Hong S.H., Privalsky M.L. The SMRT corepressor is a target of phosphorylation by protein kinase CK2 (casein kinase II). Mol. Cell. Biochem. 2001, 220:1-13.