Small molecule inhibition of the steroid receptor coactivators, SRC-3 and SRC-1

Molecular Endocrinology

Volumn 25, Issue 12, 2011, Pages 2041-2053

  Wang, Ying ^a   Lonard, David M ^a   Yu, Yang ^a   Chow, Dar Chone ^a   Palzkill, Timothy G ^a   O'Malley, Bert W ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; GOSSYPOL; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN P300; STEROID RECEPTOR COACTIVATOR 1; STEROID RECEPTOR COACTIVATOR 3;

ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; LIVER CANCER; LUNG CANCER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; SMALL MOLECULE INHIBITION;

ANIMALS; ANTINEOPLASTIC AGENTS; BENZIMIDAZOLES; CELL LINE, TUMOR; CELL SURVIVAL; DOWN-REGULATION; DRUG SYNERGISM; ESTROGEN RECEPTOR ALPHA; GOSSYPOL; HUMANS; INHIBITORY CONCENTRATION 50; LEUPEPTINS; MALE; MAP KINASE KINASE 1; MICE; NUCLEAR RECEPTOR COACTIVATOR 1; NUCLEAR RECEPTOR COACTIVATOR 2; NUCLEAR RECEPTOR COACTIVATOR 3; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; TRANSCRIPTION, GENETIC;

EID: 82055185689     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2011-1222     Document Type: Article

References (69)

1. 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
2. Hong H, Kohli K, Garabedian MJ, Stallcup MR 1997 GRIP1, a transcriptional coactivator for the AF-2 transactivation domain of steroid, thyroid, retinoid, and vitamin D receptors. Mol Cell Biol 17:2735-2744
3. 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
4. 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
5. Chen H, Lin RJ, Schiltz RL, Chakravarti D, Nash A, Nagy L, Privalsky ML, Nakatani Y, Evans RM 1997 Nuclear receptor coacti-vator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 90: 569-580
6. Li H, Gomes PJ, Chen JD 1997 RAC3, a steroid/nuclear receptorassociated coactivator that is related to SRC-1 and TIF2. Proc Natl Acad Sci USA 94:8479-8484
7. Torchia J, Rose DW, Inostroza J, Kamei Y, Westin S, Glass CK, Rosenfeld MG 1997 The transcriptional co-activator p/CIP binds CBP and mediates nuclear-receptor function. Nature 387:677-684
8. Oh A, List HJ, Reiter R, Mani A, Zhang Y, Gehan E, Wellstein A, Riegel AT 2004 The nuclear receptor coactivator AIB1 mediates insulin-like growth factor I-induced phenotypic changes in human breast cancer cells. Cancer Res 64:8299-8308
9. Gao Z, Chiao P, Zhang X, Zhang X, Lazar MA, Seto E, Young HA, Ye J 2005 Coactivators and corepressors of NF-κB in IκBα gene promoter. J Biol Chem 280:21091-21098
10. 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
11. Fleming FJ, Myers E, Kelly G, Crotty TB, McDermott EW, O'Higgins NJ, Hill AD, Young LS 2004 Expression of SRC-1, AIB1, and PEA3 in HER2 mediated endocrine resistant breast cancer; a predictive role for SRC-1. J Clin Pathol 57:1069-1074
12. Myers E, Hill AD, Kelly G, McDermott EW, O'Higgins NJ, Buggy Y, Young LS 2005 Associations and interactions between Ets-1 and Ets-2 and coregulatory proteins, SRC-1, AIB1, and NCoR in breast cancer. Clin Cancer Res 11:2111-2122
13. Wang S, Yuan Y, Liao L, Kuang SQ, Tien JC, O'Malley BW, Xu J 2009 Disruption of the SRC-1 gene in mice suppresses breast cancer metastasis without affecting primary tumor formation. Proc Natl Acad Sci USA 106:151-156
14. Torres-Arzayus MI, Font de Mora J, Yuan J, Vazquez F, Bronson R, Rue M, Sellers WR, Brown M 2004 High tumor incidence and activation of the PI3K/AKT pathway in transgenic mice define AIB1 as an oncogene. Cancer Cell 6:263-274
15. 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
16. Kuang SQ, Liao L, Wang S, Medina D, O'Malley BW, Xu J 2005 Mice lacking the amplified in breast cancer 1/steroid receptor coactivator- 3 are resistant to chemical carcinogen-induced mammary tumorigenesis. Cancer Res 65:7993-8002
17. Kuang SQ, Liao L, Zhang H, Lee AV, O'Malley BW, Xu J 2004 AIB1/SRC-3 deficiency affects insulin-like growth factor I signaling pathway and suppresses v-Ha-ras-induced breast cancer initiation and progression in mice. Cancer Res 64:1875-1885
18. Qin L, Liao L, Redmond A, Young L, Yuan Y, Chen H, O'Malley BW, Xu J 2008 The AIB1 oncogene promotes breast cancer metastasis by activation of PEA3-mediated matrix metalloproteinase 2 (MMP2) and MMP9 expression. Mol Cell Biol 28:5937-5950
19. Bautista S, Vallés H, Walker RL, Anzick S, Zeillinger R, Meltzer P, Theillet C 1998 In breast cancer, amplification of the steroid receptor coactivator gene AIB1 is correlated with estrogen and progesterone receptor positivity. Clin Cancer Res 4:2925-2929
20. Kershah SM, Desouki MM, Koterba KL, Rowan BG 2004 Expression of estrogen receptor coregulators in normal and malignant human endometrium. Gynecol Oncol 92:304-313
21. Fujimoto N, Mizokami A, Harada S, Matsumoto T 2001 Different expression of androgen receptor coactivators in human prostate. Urology 58:289-294
22. Gnanapragasam VJ, Leung HY, Pulimood AS, Neal DE, Robson CN 2001 Expression of RAC 3, a steroid hormone receptor coactivator in prostate cancer. Br J Cancer 85:1928-1936
23. Mäki HE, Waltering KK, Walle ́n MJ, Martikainen PM, Tammela TL, van Weerden WM, Vessella RL, Visakorpi T 2006 Screening of genetic and expression alterations of SRC1 gene in prostate cancer. Prostate 66:1391-1398
24. Wang Y, Wu MC, Sham JS, Zhang W, Wu WQ, Guan XY 2002 Prognostic significance of c-myc and AIB1 amplification in hepatocellular carcinoma. A broad survey using high-throughput tissue microarray. Cancer 95:2346-2352
25. Henke RT, Haddad BR, Kim SE, Rone JD, Mani A, Jessup JM, et al 2004 Overexpression of the nuclear receptor coactivator AIB1 (SRC-3) during progression of pancreatic adenocarcinoma. Clin Cancer Res 10(Pt 1):6134-6142
26. Xie D, Sham JS, Zeng WF, Lin HL, Bi J, Che LH, Hu L, Zeng YX, Guan XY 2005 Correlation of AIB1 overexpression with advanced clinical stage of human colorectal carcinoma. Hum Pathol 36:777-783
27. Cai D, Shames DS, Raso MG, Xie Y, Kim YH, Pollack JR, Girard L, Sullivan JP, Gao B, Peyton M, Nanjundan M, Byers L, Heymach J, Mills G, Gazdar AF, Wistuba I, Kodadek T, Minna JD 2010 Steroid receptor coactivator-3 expression in lung cancer and its role in the regulation of cancer cell survival and proliferation. Cancer Res 70:6477-6485
28. Shang Y, Brown M 2002 Molecular determinants for the tissue specificity of SERMs. Science 295:2465-2468
29. Shou J, Massarweh S, Osborne CK, Wakeling AE, Ali S, Weiss H, Schiff R 2004 Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer. J Natl Cancer Inst 96:926-935
30. Lahusen T, Henke RT, Kagan BL, Wellstein A, Riegel AT 2009 The role and regulation of the nuclear receptor co-activator AIB1 in breast cancer. Breast Cancer Res Treat 116:225-237
31. Lahusen T, Fereshteh M, Oh A, Wellstein A, Riegel AT 2007 Epidermal growth factor receptor tyrosine phosphorylation and signaling controlled by a nuclear receptor coactivator, amplified in breast cancer 1. Cancer Res 67:7256-7265
32. Wells JA, McClendon CL 2007 Reaching for high-hanging fruit in drug discovery at protein-protein interfaces. Nature 450:1001-1009
33. Rosania GR, Crippen G, Woolf P, States D, Shedden K 2007 A cheminformatic toolkit for mining biomedical knowledge. Pharm Res 24:1791-1802
34. Lonard DM, Tsai SY, O'Malley BW 2004 Selective estrogen receptor modulators 4-hydroxytamoxifen and raloxifene impact the stability and function of SRC-1 and SRC-3 coactivator proteins. Mol Cell Biol 24:14-24
35. Lonard DM, Nawaz Z, Smith CL, O'Malley BW 2000 The 26S proteasome is required for estrogen receptor-α and coactivator turnover and for efficient estrogen receptor-[1] transactivation. Mol Cell 5:939-948
36. Hadley MA, Burgos MH 1986 Gossypol injected in the rat epididymal fat pad inhibits epididymal sperm motility. Microsc Electron Biol Celular 10:133-143
37. Oko R, Hrudka F 1984 Comparison of the effects of gossypol, estradiol-17β and testosterone compensation on male rat reproductive organs. Biol Reprod 30:1198-1207
38. Gilbert NE, O'Reilly JE, Chang CJ, Lin YC, Brueggemeier RW 1995 Antiproliferative activity of gossypol and gossypolone on human breast cancer cells. Life Sci 57:61-67
39. Tuszynski GP, Cossu G 1984 Differential cytotoxic effect of gossypol on human melanoma, colon carcinoma, and other tissue culture cell lines. Cancer Res 44:768-771
40. Wolter KG, Wang SJ, Henson BS, Wang S, Griffith KA, Kumar B, Chen J, Carey TE, Bradford CR, Dsilva NJ 2006 (-)-Gossypol inhibits growth and promotes apoptosis of human head and neck squamous cell carcinoma in vivo. Neoplasia 8:163-172
41. Zhang M, Liu H, Guo R, Ling Y, Wu X, Li B, Roller PP, Wang S, Yang D 2003 Molecular mechanism of gossypol-induced cell growth inhibition and cell death of HT-29 human colon carcinoma cells. Biochem Pharmacol 66:93-103
42. Feng Q, Yi P, Wong J, O'Malley BW 2006 Signaling within a coactivator complex: methylation of SRC-3/AIB1 is a molecular switch for complex disassembly. Mol Cell Biol 26:7846-7857
43. Liu Z, Wong J, Tsai SY, Tsai MJ, O'Malley BW 2001 Sequential recruitment of steroid receptor coactivator-1 (SRC-1) and p300 enhances progesterone receptor-dependent initiation and reinitiation of transcription from chromatin. Proc Natl Acad Sci USA 98: 12426-12431
44. Huang YW, Wang LS, Chang HL, Ye W, Dowd MK, Wan PJ, et al. 2006 Molecular mechanisms of (-)-gossypol-induced apoptosis in human prostate cancer cells. Anticancer Res 26(3A):1925-1933
45. Wu RC, Feng Q, Lonard DM, O'Malley BW 2007 SRC-3 coactivator functional lifetime is regulated by a phospho-dependent ubiquitin time clock. Cell 129:1125-1140
46. Epps DE, Raub TJ, Caiolfa V, Chiari A, Zamai M 1999 Determination of the affinity of drugs toward serum albumin by measurement of the quenching of the intrinsic tryptophan fluorescence of the protein. J Pharm Pharmacol 51:41-48
47. Velazquez-Campoy A, Ohtaka H, Nezami A, Muzammil S, Freire E 2004 Isothermal titration calorimetry. Curr Protoc Cell Biol Chapter 17:Unit 17 8
48. Kao J, Salari K, Bocanegra M, Choi YL, Girard L, Gandhi J, Kwei KA, Hernandez-Boussard T, Wang P, Gazdar AF, Minna JD, Pollack JR 2009 Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLoS One 4:e6146
49. Márquez-Garbán DC, Chen HW, Fishbein MC, Goodglick L, Pietras RJ 2007 Estrogen receptor signaling pathways in human nonsmall cell lung cancer. Steroids 72:135-143
50. Yeow WS, Baras A, Chua A, Nguyen DM, Sehgal SS, Schrump DS, Nguyen DM 2006 Gossypol, a phytochemical with BH3-mimetic property, sensitizes cultured thoracic cancer cells to Apo2 ligand/ tumor necrosis factor-related apoptosis-inducing ligand. J Thorac Cardiovasc Surg 132:1356-1362
51. Wu RC, Qin J, Yi P, Wong J, Tsai SY, Tsai MJ, Omalley BW 2004 Selective phosphorylations of the SRC-3/AIB1 coactivator integrate genomic reponses to multiple cellular signaling pathways. Mol Cell 15:937-949
52. Font de Mora J, Brown M 2000 AIB1 is a conduit for kinasemediated growth factor signaling to the estrogen receptor. Mol Cell Biol 20:5041-5047
53. Wong KK 2009 Recent developments in anti-cancer agents targeting the Ras/Raf/ MEK/ERK pathway. Recent Pat Anticancer Drug Discov 4:28-35
54. Lyons JF, Wilhelm S, Hibner B, Bollag G 2001 Discovery of a novel Raf kinase inhibitor. Endocr Relat Cancer 8:219-225
55. Suzuki T, Nakagawa T, Endo H, Mitsudomi T, Masuda A, Yatabe Y, Sugiura T, Takahashi T, Hida T 2003 The sensitivity of lung cancer cell lines to the EGFR-selective tyrosine kinase inhibitor ZD1839 ('Iressa') is not related to the expression of EGFR or HER-2 or to K-ras gene status. Lung Cancer 42:35-41
56. Lenferink AE, Simpson JF, Shawver LK, Coffey RJ, Forbes JT, Arteaga CL 2000 Blockade of the epidermal growth factor receptor tyrosine kinase suppresses tumorigenesis in MMTV/Neu+ MMTV/TGF-α bigenic mice. Proc Natl Acad Sci USA 97:9609-9614
57. Wen B, Deutsch E, Marangoni E, Frascona V, Maggiorella L, Abdulkarim B, Chavaudra N, Bourhis J 2001 Tyrphostin AG 1024 modulates radiosensitivity in human breast cancer cells. Br J Cancer 85:2017-2021
58. List HJ, Lauritsen KJ, Reiter R, Powers C, Wellstein A, Riegel AT 2001 Ribozyme targeting demonstrates that the nuclear receptor coactivator AIB1 is a rate-limiting factor for estrogen-dependent growth of human MCF-7 breast cancer cells. J Biol Chem 276: 23763-23768
59. Yan F, Gao X, Lonard DM, Nawaz Z 2003 Specific ubiquitinconjugating enzymes promote degradation of specific nuclear receptor coactivators. Mol Endocrinol 17:1315-1331
60. Han SJ, Lonard DM, O'Malley BW 2009 Multi-modulation of nuclear receptor coactivators through posttranslational modifications. Trends Endocrinol Metab 20:8-15
61. Lonard DM, Kumar R, O'Malley BW 2010 Minireview: the SRC family of coactivators: an entree to understanding a subset of polygenic diseases? Mol Endocrinol 24:279-285
62. Xu J, Liao L, Ning G, Yoshida-Komiya H, Deng C, O'Malley BW 2000 The steroid receptor coactivator SRC-3 (p/CIP/RAC3/AIB1/ACTR/TRAM-1) is required for normal growth, puberty, female reproductive function, and mammary gland development. Proc Natl Acad Sci USA 97:6379-6384
63. Xu J, Qiu Y, DeMayo FJ, Tsai SY, Tsai MJ, O'Malley BW 1998 Partial hormone resistance in mice with disruption of the steroid receptor coactivator-1 (SRC-1) gene. Science 279:1922-1925
64. Meng Y, Tang W, Dai Y, Wu X, Liu M, Ji Q, Ji M, Pienta K, Lawrence T, Xu L 2008 Natural BH3 mimetic (-)-gossypol chemosensitizes human prostate cancer via Bcl-xL inhibition accompanied by increase of Puma and Noxa. Mol Cancer Ther 7:2192-2202
65. Kitada S, Leone M, Sareth S, Zhai D, Reed JC, Pellecchia M 2003 Discovery, characterization, and structure-activity relationships studies of proapoptotic polyphenols targeting B-cell lymphocyte/ leukemia-2 proteins. J Med Chem 46:4259-4264
66. Wang G, Nikolovska-Coleska Z, Yang CY, Wang R, Tang G, Guo J, Shangary S, Qiu S, Gao W, Yang D, Meagher J, Stuckey J, Krajewski K, Jiang S, Roller PP, Abaan HO, Tomita Y, Wang S 2006 Structure-based design of potent small-molecule inhibitors of antiapoptotic Bcl-2 proteins. J Med Chem 49:6139-6142
67. Lanz RB, Bulynko Y, Malovannaya A, Labhart P, Wang L, Li W, Qin J, Harper M, O'Malley BW 2010 Global characterization of transcriptional impact of the SRC-3 coregulator. Mol Endocrinol 24:859-872
68. 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
69. Louet JF, Chopra AR, Sagen JV, An J, York B, Tannour-Louet M, Saha PK, Stevens RD, Wenner BR, Ilkayeva OR, Bain JR, Zhou S, DeMayo F, Xu J, Newgard CB, O'Malley BW 2010 The coactivator SRC-1 is an essential coordinator of hepatic glucose production. Cell Metab 12:606-618