Cooperative activation of cyclin D1 and progesterone receptor gene expression by the SRC-3 coactivator and SMRT corepressor

Molecular Endocrinology

Volumn 24, Issue 6, 2010, Pages 1187-1202

  Karmakar, Sudipan ^a   Gao, Tong ^a   Pace, Margaret C ^a   Oesterreich, Steffi ^a,b   Smith, Carolyn L ^a,b  

^a Molecular and Cellular Biology   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; PROGESTERONE RECEPTOR; PROTEIN P160; SILENCING MEDIATOR OF RETINOID AND THYROID HORMONE RECEPTOR; STEROID RECEPTOR COACTIVATOR 3;

ARTICLE; BREAST CARCINOGENESIS; BREAST TUMOR; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CORRELATION ANALYSIS; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

BREAST NEOPLASMS; CELL LINE, TUMOR; CYCLIN D1; ENHANCER ELEMENTS, GENETIC; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NUCLEAR RECEPTOR CO-REPRESSOR 2; NUCLEAR RECEPTOR COACTIVATOR 2; NUCLEAR RECEPTOR COACTIVATOR 3; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, PROGESTERONE; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 77954823526     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2009-0480     Document Type: Article

References (82)

1. Katzenellenbogen BS 1996 Estrogen receptors: bioactivities and interactions with cell signaling pathways. Biol Reprod 54:287-293
2. Sarrel PM, Lufkin EG, Oursler MJ, Keefe D 1994 Estrogen actions in arteries, bone and brain. Sci Am Sci Med 1:44-53
3. Henderson BE, Ross R, Bernstein L 1988 Estrogens as a cause of human cancer: the Richard and Hinda Rosenthal Foundation Award Lecture. Cancer Res 48:246-253 (Pubitemid 18045752)
4. Glass CK 1994 Differential recognition of target genes by nuclear receptor monomers, dimers, and heterodimers. Endocr Rev 15:391-407
5. Oñate SA, Tsai SY, Tsai MJ, O'Malley BW 1995 Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science 270:1354-1357
6. Voegel JJ, Heine MJ, Zechel C, Chambon P, Gronemeyer H 1996 TIF2, a 160 kDa transcriptional mediator for the ligand-dependent activation function AF-2 of nuclear receptors. EMBO J 15:3667-3675 (Pubitemid 26239779)
7. Oh Y, Müller HL, Ng L, Rosenfeld RG 1995 Transforming growth factor-β-induced cell growth inhibition in human breast cancer cells is mediated through insulin-like growth factor-binding protein-3 action. J Biol Chem 270:13589-13592
8. Kamei Y, Xu L, Heinzel T, Torchia J, Kurokawa R, Gloss B, Lin SC, Heyman RA, Rose DW, Glass CK, Rosenfeld MG 1996 A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell 85:403-414
9. Chakravarti D, LaMorte VJ, Nelson MC, Nakajima T, Schulman IG, Juguilon H, Montminy M, Evans RM 1996 Role of CBP/P300 in nuclear receptor signalling. Nature 383:99-103
10. Chen D, Ma H, Hong H, Koh SS, Huang SM, Schurter BT, Aswad DW, Stallcup MR 1999 Regulation of transcription by a protein methyltransferase. Science 284:2174-2177
11. Karmakar S, Foster EA, Smith CL 2009 Unique roles of p160 coactivators for regulation of breast cancer cell proliferation and estrogen receptor-α transcriptional activity. Endocrinology 150:1588-1596
12. Hudelist G, Czerwenka K, Kubista E, Marton E, Pischinger K, Singer CF 2003 Expression of sex steroid receptors and their cofactors in normal and malignant breast tissue: AIB1 is a carcinomaspecific co-activator. Breast Cancer Res Treat 78:193-204
13. List HJ, Reiter R, Singh B, Wellstein A, Riegel AT 2001 Expression of the nuclear coactivator AIB1 in normal and malignant breast tissue. Breast Cancer Res Treat 68:21-28 (Pubitemid 32928267)
14. Osborne CK, Bardou V, Hopp TA, Chamness GC, Hilsenbeck SG, Fuqua SA, Wong J, Allred DC, Clark GM, Schiff R 2003 Role of the estrogen receptor coactivator AIB1 (SRC-3) and HER-2/neu in tamoxifen resistance in breast cancer. J Natl Cancer Inst 95:353-361 (Pubitemid 36395255)
15. Harigopal M, Heymann J, Ghosh S, Anagnostou V, Camp RL, Rimm DL 2009 Estrogen receptor co-activator (AIB1) protein expression by automated quantitative analysis (AQUA) in a breast cancer tissue microarray and association with patient outcome. Breast Cancer Res Treat 115:77-85
16. Fereshteh MP, Tilli MT, Kim SE, Xu J, O'Malley BW, Wellstein A, Furth PA, Riegel AT 2008 The nuclear receptor coactivator amplified in breast cancer-1 is required for Neu (ErbB2/HER2) activation, signaling, and mammary tumorigenesis in mice. Cancer Res 68:3697-3706
17. Chen JD, Evans RM 1995 A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature 377:454-457
18. Hörlein AJ, Näär AM, Heinzel T, Torchia J, Gloss B, Kurokawa R, Ryan A, Kamei Y, Söderström M, Glass CK 1995 Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 377:397-404
19. Jepsen K, Rosenfeld MG 2002 Biological roles and mechanistic actions of co-repressor complexes. J Cell Sci 115:689-698
20. Li J, Wang J, Wang J, Nawaz Z, Liu JM, Qin J, Wong J 2000 Both corepressor proteins SMRT and N-CoR exist in large protein complexes containing HDAC3. EMBO J 19:4342-4350
21. Guenther MG, Lane WS, Fischle W, Verdin E, Lazar MA, Shiekhattar R 2000 A core SMRT corepressor complex containing HDAC3 and TBL1, a WD40-repeat protein linked to deafness. Genes Dev 14:1048-1057
22. Zhang J, Kalkum M, Chait BT, Roeder RG 2002 The N-CoRHDAC3 nuclear receptor corepressor complex inhibits the JNK pathway through the integral subunit GPS2. Mol Cell 9:611-623
23. Nagy L, Kao HY, Chakravarti D, Lin RJ, Hassig CA, Ayer DE, Schreiber SL, Evans RM 1997 Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell 89:373-380
24. Nettles KW, Greene GL 2005 Ligand control of coregulator recruitment to nuclear receptors. Annu Rev Physiol 67:309-333
25. Privalsky ML 2004 The role of corepressors in transcriptional regulation by nuclear hormone receptors. Annu Rev Physiol 66:315-360 (Pubitemid 40614447)
26. Peterson TJ, Karmakar S, Pace MC, Gao T, Smith CL 2007 The silencing mediator of retinoic acid and thyroid hormone receptor (SMRT) corepressor is required for full estrogen receptor-α transcriptional activity. Mol Cell Biol 27:5933-5948
27. Smith CL, Nawaz Z, O'Malley BW 1997 Coactivator and corepressor regulation of the agonist/antagonist activity of the mixed antiestrogen, 4-hydroxytamoxifen. Mol Endocrinol 11:657-666
28. Métivier R, Stark A, Flouriot G, Hübner MR, Brand H, Penot G, Manu D, Denger S, Reid G, Kos M, Russell RB, Kah O, Pakdel F, Gannon F 2002 A dynamic structural model for estrogen receptor-α activation by ligands, emphasizing the role of interactions between distant A and E domains. Mol Cell 10:1019-1032
29. Hodgson MC, Astapova I, Cheng S, Lee LJ, Verhoeven MC, Choi E, Balk SP, Hollenberg AN 2005 The androgen receptor recruits nuclear receptor corepressor (N-CoR) in the presence of mifepristone via its N and C termini revealing a novel molecular mechanism for androgen receptor antagonists. J Biol Chem 280:6511-6519
30. Yoon HG, Wong J 2006 The corepressors silencing mediator of retinoid and thyroid hormone receptor and nuclear receptor corepressor are involved in agonist- and antagonist-regulated transcription by androgen receptor. Mol Endocrinol 20:1048-1060
31. Wang D, Wang Q, Awasthi S, Simons Jr SS 2007 Amino-terminal domain of TIF2 is involved in competing for corepressor binding to glucocorticoid and progesterone receptors. Biochemistry 46:8036-8049
32. Sankar N, Baluchamy S, Kadeppagari RK, Singhal G, Weitzman S, Thimmapaya B 2008 p300 provides a corepressor function by cooperating with YY1 and HDAC3 to repress c-Myc. Oncogene 27:5717-5728
33. Guidez F, Howell L, Isalan M, Cebrat M, Alani RM, Ivins S, Hormaeche I, McConnell MJ, Pierce S, Cole PA, Licht J, Zelent A 2005 Histone acetyltransferase activity of p300 is required for transcriptional repression by the promyelocytic leukemia zinc finger protein. Mol Cell Biol 25:5552-5566
34. Li X, Kimbrel EA, Kenan DJ, McDonnell DP 2002 Direct interactions between corepressors and coactivators permit the integration of nuclear receptor-mediated repression and activation. Mol Endocrinol 16:1482-1491
35. Perissi V, Aggarwal A, Glass CK, Rose DW, Rosenfeld MG 2004 A corepressor/coactivator exchange complex required for transcriptional activation by nuclear receptors and other regulated transcription factors. Cell 116:511-526 (Pubitemid 38264429)
36. Yoon HG, Choi Y, Cole PA, Wong J 2005 Reading and function of a histone code involved in targeting corepressor complexes for repression. Mol Cell Biol 25:324-335
37. Qiu Y, Zhao Y, Becker M, John S, Parekh BS, Huang S, Hendarwanto A, Martinez ED, Chen Y, Lu H, Adkins NL, Stavreva DA, Wiench M, Georgel PT, Schiltz RL, Hager GL 2006 HDAC1 acetylation is linked to progressive modulation of steriod receptor-induced gene transcription. Mol Cell 22:669-679
38. Welsbie DS, Xu J, Chen Y, Borsu L, Scher HI, Rosen N, Sawyers CL 2009 Histone deacetylases are required for androgen receptor function in hormone-sensitive and castrate-resistant prostate cancer. Cancer Res 69:958-966
39. Rogatsky I, Luecke HF, Leitman DC, Yamamoto KR 2002 Alternate surfaces of transcriptional coregulator GRIP1 function in different glucocorticoid receptor activation and repression contexts. Proc Natl Acad Sci USA 99:16701-16706
40. Eeckhoute J, Carroll JS, Geistlinger TR, Torres-Arzayus MI, Brown M 2006 A cell-type-specific transcriptional network required for estrogen regulation of cyclin D1 and cell cycle progression in breast cancer. Genes Dev 20:2513-2526
41. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J, Brodsky AS, Keeton EK, Fertuck KC, Hall GF, Wang Q, Bekiranov S, Sementchenko V, Fox EA, Silver PA, Gingeras TR, Liu XS, Brown M 2006 Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38:1289-1297
42. Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H, Mohamed YB, Orlov YL, Velkov S, Ho A, Mei PH, Chew EG, Huang PY, Welboren WJ, Han Y, Ooi HS, Ariyaratne PN, Vega VB, Luo Y, Tan PY, Choy PY, Wansa KD, Zhao B, Lim KS, Leow SC, Yow JS, Joseph R, Li H, Desai KV, Thomsen JS, Lee YK, Karuturi RK, Herve T, Bourque G, Stunnenberg HG, Ruan X, Cacheux-Rataboul V, Sung WK, Liu ET, Wei CL, Cheung E, Ruan Y 2009 An oestrogen-receptor-γ-bound human chromatin interactome. Nature 462:58-64
43. Bonéy-Montoya J, Ziegler YS, Curtis CD, Montoya JA, Nardulli AM 2010 Long-range transcriptional control of progesterone receptor gene expression. Mol Endocrinol 24:346-358
44. Yamamoto Y, Wada O, Suzawa M, Yogiashi Y, Yano T, Kato S, Yanagisawa J 2001 The tamoxifen-responsive estrogen receptor α mutant D351Y shows reduced tamoxifen-dependent interaction with corepressor complexes. J Biol Chem 276:42684-42691
45. Webb P, Nguyen P, Kushner PJ 2003 Differential SERM effects on corepressor binding dictate ERα activity in vivo. J Biol Chem 278:6912-6920
46. Webb P, Nguyen P, Shinsako J, Anderson C, Feng W, Nguyen MP, Chen D, Huang SM, Subramanian S, McKinerney E, Katzenellenbogen BS, Stallcup MR, Kushner PJ 1998 Estrogen receptor activation function 1 works by binding p160 coactivator proteins. Mol Endocrinol 12:1605-1618
47. Werbajh S, Nojek I, Lanz R, Costas MA 2000 RAC-3 is a NF-κB coactivator. FEBS Lett 485:195-199
48. Louie MC, Zou JX, Rabinovich A, Chen HW 2004 ACTR/AIB1 functions as an E2F1 coactivator to promote breast cancer cell proliferation and antiestrogen resistance. Mol Cell Biol 24:5157-5171
49. Yan J, Yu CT, Ozen M, Ittmann M, Tsai SY, Tsai MJ 2006 Steroid receptor coactivator-3 and activator protein-1 coordinately regulate the transcription of components of the insulin-like growth factor/AKT signaling pathway. Cancer Res 66:11039-11046
50. Smith CL, O'Malley BW 2004 Coregulator function: a key to understanding tissue specificity of selective receptor modulators. Endocr Rev 25:45-71
51. Hurtado A, Holmes KA, Geistlinger TR, Hutcheson IR, Nicholson RI, Brown M, Jiang J, Howat WJ, Ali S, Carroll JS 2008 Regulation of ERBB2 by oestrogen receptor-PAX2 determines response to tamoxifen. Nature 456:663-666
52. Montano MM, Ekena K, Delage-Mourroux R, Chang W, Martini P, Katzenellenbogen BS 1999 An estrogen receptor-selective coregulator that potentiates the effectiveness of antiestrogens and represses the activity of estrogens. Proc Natl Acad Sci USA 96:6947-6952 (Pubitemid 29274990)
53. Delage-Mourroux R, Martini PG, Choi I, Kraichely DM, Hoeksema J, Katzenellenbogen BS 2000 Analysis of estrogen receptor interaction with a repressor of estrogen receptor activity (REA) and the regulation of estrogen receptor transcriptional activity by REA. J Biol Chem 275:35848-35856
54. Sánchez-Martínez R, Zambrano A, Castillo AI, Aranda A 2008 Vitamin D-dependent recruitment of corepressors to vitamin D/retinoid X receptor heterodimers. Mol Cell Biol 28:3817-3829
55. Wang Q, Anzick S, Richter WF, Meltzer P, Simons Jr SS 2004 Modulation of transcriptional sensitivity on mineralocorticoid and estrogen receptors. J Steroid Biochem Mol Biol 91:197-210
56. Szapary D, Huang Y, Simons Jr SS 1999 Opposing effects of corepressor and coactivators in determining the dose-response curve of agonist, and residual agonist activity of antagonists, for glucocorticoid receptor-regulated gene expression. Mol Endocrinol 13:2108-2121 (Pubitemid 30637270)
57. Leong GM, Subramaniam N, Issa LL, Barry JB, Kino T, Driggers PH, Hayman MJ, Eisman JA, Gardiner EM 2004 Ski-interacting protein, a bifunctional nuclear receptor coregulator that interacts with N-CoR/SMRT and p300. Biochem Biophys Res Commun 315:1070-1076
58. Métivier R, Penot G, Carmouche RP, Hübner MR, Reid G, Denger S, Manu D, Brand H, Kos M, Benes V, Gannon F 2004 Transcriptional complexes engaged by apo-estrogen receptor-α isoforms have divergent outcomes. EMBO J 23:3653-3666
59. Shang Y, Brown M 2002 Molecular determinants for the tissue specificity of SERMs. Science 295:2465-2468
60. Shang Y, Hu X, DiRenzo J, Lazar MA, Brown M 2000 Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103:843-852
61. Suen CS, Berrodin TJ, Mastroeni R, Cheskis BJ, Lyttle CR, Frail DE 1998 A transcriptional coactivator, steroid receptor coactivator-3, selectively augments steroid receptor transcriptional activity. J Biol Chem 273:27645-27653
62. Li H, Gomes PJ, Chen JD 1997 RAC3, a steroid/nuclear receptor-associated coactivator that is related to SRC-1 and TIF2. Proc Natl Acad Sci USA 94:8479-8484
63. Zhao Y, Takeyama K, Sawatsubashi S, Ito S, Suzuki E, Yamagata K, Tanabe M, Kimura S, Fujiyama S, Ueda T, Murata T, Matsukawa H, Shirode Y, Kouzmenko AP, Li F, Tabata T, Kato S 2009 Corepressive action of CBP on androgen receptor transactivation in pericentric heterochromatin in a Drosophila experimental model system. Mol Cell Biol 29:1017-1034
64. Cvoro A, Tzagarakis-Foster C, Tatomer D, Paruthiyil S, Fox MS, Leitman DC 2006 Distinct roles of unliganded estrogen receptors in transcriptional repression. Mol Cell 21:555-564 (Pubitemid 43228010)
65. Lonard DM, Lanz RB, O'Malley BW 2007 Nuclear receptor coreguators and human disease. Endocr Rev 28:575-587
66. Anzick SL, Kononen J, Walker RL, Azorsa DO, Tanner MM, Guan XY, Sauter G, Kallioniemi OP, Trent JM, Meltzer PS 1997 AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science 277:965-968
67. Kirkegaard T, McGlynn LM, Campbell FM, Müller S, Tovey SM, Dunne B, Nielsen KV, Cooke TG, Bartlett JM 2007 Amplified in breast cancer 1 in human epidermal growth factor receptor-positive tumors of tamoxifen-treated cancer patients. Clin Cancer Res 13:1405-1411
68. Lavinsky RM, Jepsen K, Heinzel T, Torchia J, Mullen TM, Schiff R, Del-Rio AL, Ricote M, Ngo S, Gemsch J, Hilsenbeck SG, Osborne CK, Glass CK, Rosenfeld MG, Rose DW 1998 Diverse signaling pathways modulate nuclear receptor recruitment of NCoR and SMRT complexes. Proc Natl Acad Sci USA 95:2920-2925
69. Girault I, Lerebours F, Amarir S, Tozlu S, Tubiana-Hulin M, Lidereau R, Bièche I 2003 Expression analysis of estrogen receptor α coregulators in breast carcinoma: evidence that NCOR1 expression is predictive of the response to tamoxifen. Clin Cancer Res 9:1259-1266
70. Chan CM, Lykkesfeldt AE, Parker MG, Dowsett M 1999 Expression of nuclear receptor interacting proteins TIF-1, SUG-1, receptor interacting protein 140, and corepressor SMRT in tamoxifen-resistant breast cancer. Clin Cancer Res 5:3460-3467
71. Chan CM, Martin LA, Johnston SR, Ali S, Dowsett M 2002 Molecular changes associated with the acquisition of oestrogen hypersensitivity in MCF-7 breast cancer cells on long-term oestrogen deprivation. J Steroid Biochem Mol Biol 81:333-341 (Pubitemid 35279118)
72. Sarvilinna N, Eronen H, Miettinen S, Vienonen A, Ylikomi T 2006 Steroid hormone receptors and coregulators in endocrine-resistant and estrogen-independent breast cancer cells. Int J Cancer 118:832-840
73. Green AR, Burney C, Granger CJ, Paish EC, El-Sheikh S, Rakha EA, Powe DG, Macmillan RD, Ellis IO, Stylianou E 2008 The prognostic significance of steroid receptor co-regulators in breast cancer: co-repressor NCOR2/SMRT is an independent indicator of poor outcome. Breast Cancer Res Treat 110:427-437
74. Labhart P, Karmakar S, Salicru EM, Egan BS, Alexiadis V, O'Malley BW, Smith CL 2005 Identification of target genes in breast cancer cells directly regulated by the SRC-3/AIB1 coactivator. Proc Natl Acad Sci USA 102:1339-1344
75. Nawaz Z, Lonard DM, Smith CL, Lev-Lehman E, Tsai SY, Tsai MJ, O'Malley BW 1999 The Angelman syndrome-associated protein, E6-AP, is a coactivator for the nuclear hormone receptor superfamily. Mol Cell Biol 19:1182-1189
76. Nawaz Z, Lonard DM, Dennis AP, Smith CL, O'Malley BW 1999 Proteasome-dependent degradation of the human estrogen receptor. Proc Natl Acad Sci USA 96:1858-1862
77. Park EJ, Schroen DJ, Yang M, Li H, Li L, Chen JD 1999 SMRTe, a silencing mediator for retinoid and thyroid hormone receptors-extended isoform that is more related to the nuclear receptor corepressor. Proc Natl Acad Sci USA 96:3519-3524
78. Goodson ML, Jonas BA, Privalsky ML 2005 Alternative mRNA splicing of SMRT creates functional diversity by generating corepressor isoforms with different affinities for different nuclear receptors. J Biol Chem 280:7493-7503
79. Dutertre M, Smith CL 2003 Ligand-independent interactions of p160/steroid receptor coactivators and CREB-binding protein (CBP) with estrogen receptor-α: regulation by phosphorylation sites in the A/B region depends on other receptor domains. Mol Endocrinol 17:1296-1314
80. Lonard DM, Nawaz Z, Smith CL, O'Malley BW 2000 The 26S proteasome is required for estrogen receptor-α and coactivator turn-over and for efficient estrogen receptor-α transactivation. Mol Cell 5:939-948
81. Wu RC, Qin J, Yi P, Wong J, Tsai SY, Tsai MJ, O'Malley BW 2004 Selective phosphorylations of the SRC-3/AIBI coactivator integrate genomic responses to multiple cellular signaling pathways. Mol Cell 15:937-949
82. Yi P, Wu RC, Sandquist J, Wong J, Tsai SY, Tsai MJ, Means AR, O'Malley BW 2005 Peptidyl-prolyl isomerase 1 (Pin1) serves as a coactivator of steroid receptor by regulating the activity of phosphorylated steroid receptor coactivator 3 (SRC-3/AIB1). Mol Cell Biol 25:9687-9699