The Role of Steroid Receptor Coactivators in Hormone Dependent Cancers and Their Potential as Therapeutic Targets

Hormones and Cancer

Volumn 7, Issue 4, 2016, Pages 229-235

  Wang, Lei ^a   Lonard, David M ^a   O’Malley, Bert W ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR RECEPTOR COACTIVATOR 2; STEROID RECEPTOR COACTIVATOR 1; STEROID RECEPTOR COACTIVATOR 3; ANTINEOPLASTIC AGENT; NUCLEAR RECEPTOR COACTIVATOR;

BREAST CANCER; CANCER GROWTH; ENDOMETRIUM CANCER; FEMALE; GENETIC TRANSCRIPTION; HUMAN; MALE; NEOPLASM; OVARY CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN FAMILY; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASMS, HORMONE-DEPENDENT;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MOLECULAR TARGETED THERAPY; NEOPLASMS, HORMONE-DEPENDENT; NUCLEAR RECEPTOR COACTIVATORS; SIGNAL TRANSDUCTION;

EID: 84964425536     PISSN: 18688497     EISSN: 18688500     Source Type: Journal    
DOI: 10.1007/s12672-016-0261-6     Document Type: Review

References (77)

1. Onate 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, Trivedi A, Johnson DL, Stallcup MR (1996) GRIP1, a novel mouse protein that serves as a transcriptional coactivator in yeast for the hormone binding domains of steroid receptors. Proc Natl Acad Sci U S A 93:4948–4952
3. 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
4. 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
5. 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
6. Chen H, Lin RJ, Schiltz RL, Chakravarti D, Nash A, Nagy L, Privalsky ML, Nakatani Y, Evans RM (1997) Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 90:569–580
7. 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 U S A 94:8479–8484
8. Takeshita A, Cardona GR, Koibuchi N, Suen CS, Chin WW (1997) TRAM-1, a novel 160-kDa thyroid hormone receptor activator molecule, exhibits distinct properties from steroid receptor coactivator-1. J Biol Chem 272:27629–27634
9. 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
10. Xu J, Wu RC, O’Malley BW (2009) Normal and cancer-related functions of the p160 steroid receptor co-activator (SRC) family. Nat Rev Cancer 9:615–630
11. Johnson AB, O’Malley BW (2012) Steroid receptor coactivators 1, 2, and 3: critical regulators of nuclear receptor activity and steroid receptor modulator (SRM)-based cancer therapy. Mol Cell Endocrinol 348:430–439
12. 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
13. Koh SS, Chen D, Lee YH, Stallcup MR (2001) Synergistic enhancement of nuclear receptor function by p160 coactivators and two coactivators with protein methyltransferase activities. J Biol Chem 276:1089–1098
14. Foulds CE, Feng Q, Ding C, Bailey S, Hunsaker TL, Malovannaya A, Hamilton RA, Gates LA, Zhang Z, Li C, Chan D, Bajaj A, Callaway CG, Edwards DP, Lonard DM, Tsai SY, Tsai MJ, Qin J, O’Malley BW (2013) Proteomic analysis of coregulators bound to ERalpha on DNA and nucleosomes reveals coregulator dynamics. Mol Cell 51:185–199
15. York B, O’Malley BW (2010) Steroid receptor coactivator (SRC) family: masters of systems biology. J Biol Chem 285:38743–38750
16. Han SJ, Lonard DM, O’Malley BW (2009) Multi-modulation of nuclear receptor coactivators through posttranslational modifications. Trends Endocrinol Metab 20:8–15
17. Lonard DM, O’Malley BW (2007) Nuclear receptor coregulators: judges, juries, and executioners of cellular regulation. Mol Cell 27:691–700
18. Bautista S, Valles 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
19. Bouras T, Southey MC, Venter DJ (2001) Overexpression of the steroid receptor coactivator AIB1 in breast cancer correlates with the absence of estrogen and progesterone receptors and positivity for p53 and HER2/neu. Cancer Res 61:903–907
20. Glaeser M, Floetotto T, Hanstein B, Beckmann MW, Niederacher D (2001) Gene amplification and expression of the steroid receptor coactivator SRC3 (AIB1) in sporadic breast and endometrial carcinomas. Horm Metab Res 33:121–126
21. Hudelist G, Czerwenka K, Kubista E, Marton E, Pischinger K, Singer CF (2003) Expression of sex steroid receptors and their co-factors in normal and malignant breast tissue: AIB1 is a carcinoma-specific co-activator. Breast Cancer Res Treat 78:193–204
22. Zhao C, Yasui K, Lee CJ, Kurioka H, Hosokawa Y, Oka T, Inazawa J (2003) Elevated expression levels of NCOA3, TOP1, and TFAP2C in breast tumors as predictors of poor prognosis. Cancer 98:18–23
23. Planas-Silva MD, Shang Y, Donaher JL, Brown M, Weinberg RA (2001) AIB1 enhances estrogen-dependent induction of cyclin D1 expression. Cancer Res 61:3858–3862
24. 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
25. 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
26. 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
27. 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
28. 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
29. 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
30. Li LB, Louie MC, Chen HW, Zou JX (2008) Proto-oncogene ACTR/AIB1 promotes cancer cell invasion by up-regulating specific matrix metalloproteinase expression. Cancer Lett 261:64–73
31. 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
32. Long W, Yi P, Amazit L, LaMarca HL, Ashcroft F, Kumar R, Mancini MA, Tsai SY, Tsai MJ, O’Malley BW (2010) SRC-3Delta4 mediates the interaction of EGFR with FAK to promote cell migration. Mol Cell 37:321–332
33. 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
34. Myers E, Fleming FJ, Crotty TB, Kelly G, McDermott EW, O’Higgins NJ, Hill AD, Young LS (2004) Inverse relationship between ER-beta and SRC-1 predicts outcome in endocrine-resistant breast cancer. Br J Cancer 91:1687–1693
35. Fleming FJ, Hill AD, McDermott EW, O’Higgins NJ, Young LS (2004) Differential recruitment of coregulator proteins steroid receptor coactivator-1 and silencing mediator for retinoid and thyroid receptors to the estrogen receptor-estrogen response element by beta-estradiol and 4-hydroxytamoxifen in human breast cancer. J Clin Endocrinol Metab 89:375–383
36. McBryan J, Theissen SM, Byrne C, Hughes E, Cocchiglia S, Sande S, O’Hara J, Tibbitts P, Hill AD, Young LS (2012) Metastatic progression with resistance to aromatase inhibitors is driven by the steroid receptor coactivator SRC-1. Cancer Res 72:548–559
37. Tai H, Kubota N, Kato S (2000) Involvement of nuclear receptor coactivator SRC-1 in estrogen-dependent cell growth of MCF-7 cells. Biochem Biophys Res Commun 267:311–316
38. Kishimoto H, Wang Z, Bhat-Nakshatri P, Chang D, Clarke R, Nakshatri H (2005) The p160 family coactivators regulate breast cancer cell proliferation and invasion through autocrine/paracrine activity of SDF-1alpha/CXCL12. Carcinogenesis 26:1706–1715
39. 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 U S A 106:151–156
40. Qin L, Liu Z, Chen H, Xu J (2009) The steroid receptor coactivator-1 regulates twist expression and promotes breast cancer metastasis. Cancer Res 69:3819–3827
41. Cavarretta IT, Mukopadhyay R, Lonard DM, Cowsert LM, Bennett CF, O’Malley BW, Smith CL (2002) Reduction of coactivator expression by antisense oligodeoxynucleotides inhibits ERalpha transcriptional activity and MCF-7 proliferation. Mol Endocrinol 16:253–270
42. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, Arora VK, Kaushik P, Cerami E, Reva B, Antipin Y, Mitsiades N, Landers T, Dolgalev I, Major JE, Wilson M, Socci ND, Lash AE, Heguy A, Eastham JA, Scher HI, Reuter VE, Scardino PT, Sander C, Sawyers CL, Gerald WL (2010) Integrative genomic profiling of human prostate cancer. Cancer Cell 18:11–22
43. Agoulnik IU, Vaid A, Nakka M, Alvarado M, Bingman WE 3rd, Erdem H, Frolov A, Smith CL, Ayala GE, Ittmann MM, Weigel NL (2006) Androgens modulate expression of transcription intermediary factor 2, an androgen receptor coactivator whose expression level correlates with early biochemical recurrence in prostate cancer. Cancer Res 66:10594–10602
44. Agoulnik IU, Weigel NL (2008) Androgen receptor coactivators and prostate cancer. Adv Exp Med Biol 617:245–255
45. Gregory CW, He B, Johnson RT, Ford OH, Mohler JL, French FS, Wilson EM (2001) A mechanism for androgen receptor-mediated prostate cancer recurrence after androgen deprivation therapy. Cancer Res 61:4315–4319
46. Chopra AR, Louet JF, Saha P, An J, Demayo F, Xu J, York B, Karpen S, Finegold M, Moore D, Chan L, Newgard CB, O’Malley BW (2008) Absence of the SRC-2 coactivator results in a glycogenopathy resembling Von Gierke’s disease. Science 322:1395–1399
47. Chopra AR, Kommagani R, Saha P, Louet JF, Salazar C, Song J, Jeong J, Finegold M, Viollet B, DeMayo F, Chan L, Moore DD, O’Malley BW (2011) Cellular energy depletion resets whole-body energy by promoting coactivator-mediated dietary fuel absorption. Cell Metab 13:35–43
48. Picard F, Gehin M, Annicotte J, Rocchi S, Champy MF, O’Malley BW, Chambon P, Auwerx J (2002) SRC-1 and TIF2 control energy balance between white and brown adipose tissues. Cell 111:931–941
49. Stashi E, Lanz RB, Mao J, Michailidis G, Zhu B, Kettner NM, Putluri N, Reineke EL, Reineke LC, Dasgupta S, Dean A, Stevenson CR, Sivasubramanian N, Sreekumar A, Demayo F, York B, Fu L, O’Malley BW (2014) SRC-2 is an essential coactivator for orchestrating metabolism and circadian rhythm. Cell Rep 6:633–645
50. Dasgupta S, Putluri N, Long W, Zhang B, Wang J, Kaushik AK, Arnold JM, Bhowmik SK, Stashi E, Brennan CA, Rajapakshe K, Coarfa C, Mitsiades N, Ittmann MM, Chinnaiyan AM, Sreekumar A, O’Malley BW (2015) Coactivator SRC-2-dependent metabolic reprogramming mediates prostate cancer survival and metastasis. J Clin Invest 125:1174–1188
51. Gnanapragasam VJ, Leung HY, Pulimood AS, Neal DE, Robson CN (2001) Expression of RAC 3, a steroid hormone receptor co-activator in prostate cancer. Br J Cancer 85:1928–1936
52. Zhou HJ, Yan J, Luo W, Ayala G, Lin SH, Erdem H, Ittmann M, Tsai SY, Tsai MJ (2005) SRC-3 is required for prostate cancer cell proliferation and survival. Cancer Res 65:7976–7983
53. Zhou G, Hashimoto Y, Kwak I, Tsai SY, Tsai MJ (2003) Role of the steroid receptor coactivator SRC-3 in cell growth. Mol Cell Biol 23:7742–7755
54. Yan J, Erdem H, Li R, Cai Y, Ayala G, Ittmann M, Yu-Lee LY, Tsai SY, Tsai MJ (2008) Steroid receptor coactivator-3/AIB1 promotes cell migration and invasiveness through focal adhesion turnover and matrix metalloproteinase expression. Cancer Res 68:5460–5468
55. Agoulnik IU, Vaid A, Bingman WE 3rd, Erdeme H, Frolov A, Smith CL, Ayala G, Ittmann MM, Weigel NL (2005) Role of SRC-1 in the promotion of prostate cancer cell growth and tumor progression. Cancer Res 65:7959–7967
56. 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
57. Sakaguchi H, Fujimoto J, Sun WS, Tamaya T (2007) Clinical implications of steroid receptor coactivator (SRC)-3 in uterine endometrial cancers. J Steroid Biochem Mol Biol 104:237–240
58. Balmer NN, Richer JK, Spoelstra NS, Torkko KC, Lyle PL, Singh M (2006) Steroid receptor coactivator AIB1 in endometrial carcinoma, hyperplasia and normal endometrium: correlation with clinicopathologic parameters and biomarkers. Mod Pathol 19:1593–1605
59. Yoshida H, Liu J, Samuel S, Cheng W, Rosen D, Naora H (2005) Steroid receptor coactivator-3, a homolog of Taiman that controls cell migration in the Drosophila ovary, regulates migration of human ovarian cancer cells. Mol Cell Endocrinol 245:77–85
60. Wu RC, Qin J, Hashimoto Y, Wong J, Xu J, Tsai SY, Tsai MJ, O’Malley BW (2002) Regulation of SRC-3 (pCIP/ACTR/AIB-1/RAC-3/TRAM-1) Coactivator activity by I kappa B kinase. Mol Cell Biol 22:3549–3561
61. Wu RC, Qin J, Yi P, Wong J, Tsai SY, Tsai MJ, O’Malley BW (2004) Selective phosphorylations of the SRC-3/AIB1 coactivator integrate genomic reponses to multiple cellular signaling pathways. Mol Cell 15:937–949
62. Giamas G, Castellano L, Feng Q, Knippschild U, Jacob J, Thomas RS, Coombes RC, Smith CL, Jiao LR, Stebbing J (2009) CK1delta modulates the transcriptional activity of ERalpha via AIB1 in an estrogen-dependent manner and regulates ERalpha-AIB1 interactions. Nucleic Acids Res 37:3110–3123
63. Oh AS, Lahusen JT, Chien CD, Fereshteh MP, Zhang X, Dakshanamurthy S, Xu J, Kagan BL, Wellstein A, Riegel AT (2008) Tyrosine phosphorylation of the nuclear receptor coactivator AIB1/SRC-3 is enhanced by Abl kinase and is required for its activity in cancer cells. Mol Cell Biol 28:6580–6593
64. Rowan BG, Weigel NL, O’Malley BW (2000) Phosphorylation of steroid receptor coactivator-1. Identification of the phosphorylation sites and phosphorylation through the mitogen-activated protein kinase pathway. J Biol Chem 275:4475–4483
65. Ueda T, Mawji NR, Bruchovsky N, Sadar MD (2002) Ligand-independent activation of the androgen receptor by interleukin-6 and the role of steroid receptor coactivator-1 in prostate cancer cells. J Biol Chem 277:38087–38094
66. Dobrovolna J, Chinenov Y, Kennedy MA, Liu B, Rogatsky I (2012) Glucocorticoid-dependent phosphorylation of the transcriptional coregulator GRIP1. Mol Cell Biol 32:730–739
67. Lopez GN, Turck CW, Schaufele F, Stallcup MR, Kushner PJ (2001) Growth factors signal to steroid receptors through mitogen-activated protein kinase regulation of p160 coactivator activity. J Biol Chem 276:22177–22182
68. Gregory CW, Fei X, Ponguta LA, He B, Bill HM, French FS, Wilson EM (2004) Epidermal growth factor increases coactivation of the androgen receptor in recurrent prostate cancer. J Biol Chem 279:7119–7130
69. Frigo DE, Basu A, Nierth-Simpson EN, Weldon CB, Dugan CM, Elliott S, Collins-Burow BM, Salvo VA, Zhu Y, Melnik LI, Lopez GN, Kushner PJ, Curiel TJ, Rowan BG, McLachlan JA, Burow ME (2006) p38 mitogen-activated protein kinase stimulates estrogen-mediated transcription and proliferation through the phosphorylation and potentiation of the p160 coactivator glucocorticoid receptor-interacting protein 1. Mol Endocrinol 20:971–983
70. Rodriguez AL, Tamrazi A, Collins ML, Katzenellenbogen JA (2004) Design, synthesis, and in vitro biological evaluation of small molecule inhibitors of estrogen receptor alpha coactivator binding. J Med Chem 47:600–611
71. Williams AB, Weiser PT, Hanson RN, Gunther JR, Katzenellenbogen JA (2009) Synthesis of biphenyl proteomimetics as estrogen receptor-alpha coactivator binding inhibitors. Org Lett 11:5370–5373
72. Mettu NB, Stanley TB, Dwyer MA, Jansen MS, Allen JE, Hall JM, McDonnell DP (2007) The nuclear receptor-coactivator interaction surface as a target for peptide antagonists of the peroxisome proliferator-activated receptors. Mol Endocrinol 21:2361–2377
73. Wang Y, Lonard DM, Yu Y, Chow DC, Palzkill TG, O’Malley BW (2011) Small molecule inhibition of the steroid receptor coactivators, SRC-3 and SRC-1. Mol Endocrinol 25:2041–2053
74. Wang Y, Lonard DM, Yu Y, Chow DC, Palzkill TG, Wang J, Qi R, Matzuk AJ, Song X, Madoux F, Hodder P, Chase P, Griffin PR, Zhou S, Liao L, Xu J, O’Malley BW (2014) Bufalin is a potent small-molecule inhibitor of the steroid receptor coactivators SRC-3 and SRC-1. Cancer Res 74:1506–1517
75. Yan F, Yu Y, Chow DC, Palzkill T, Madoux F, Hodder P, Chase P, Griffin PR, O’Malley BW, Lonard DM (2014) Identification of verrucarin a as a potent and selective steroid receptor coactivator-3 small molecule inhibitor. PLoS One 9:e95243
76. Song X, Zhang C, Zhao M, Chen H, Liu X, Chen J, Lonard DM, Qin L, Xu J, Wang X, Li F, O’Malley BW, Wang J (2015) Steroid receptor coactivator-3 (SRC-3/AIB1) as a novel therapeutic target in triple negative breast cancer and its inhibition with a phospho-bufalin prodrug. PLoS One 10:e0140011
77. Wang L, Yu Y, Chow DC, Yan F, Hsu CC, Stossi F, Mancini MA, Palzkill T, Liao L, Zhou S, Xu J, Lonard DM, O’Malley BW (2015) Characterization of a steroid receptor coactivator small molecule stimulator that overstimulates cancer cells and leads to cell stress and death. Cancer Cell 28:240–252