Reconstruction of nuclear receptor network reveals that NR2E3 is a novel upstream regulator of ESR1 in breast cancer

EMBO Molecular Medicine

Volumn 4, Issue 1, 2012, Pages 52-67

  Park, Yun Yong ^a   Kim, Kyounghyun ^b   Kim, Sang Bae ^a   Hennessy, Bryan T ^a,b   Kim, Soo Mi ^a   Park, Eun Sung ^a   Lim, Jae Yun ^a   Li, Jane ^a   Lu, Yiling ^a   Gonzalez Angulo, Ana Maria ^a   Jeong, Woojin ^a,c   Mills, Gordon B ^a   Safe, Stephen ^b,d   Lee, Ju Seog ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^c Ewha Womans University   (South Korea)

^d TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Breast cancer; Genomics; Microarray; NR2E3; Nuclear receptor

Indexed keywords

CELL NUCLEUS RECEPTOR; CELL NUCLEUS RECEPTOR 2E3; CELL NUCLEUS RECEPTOR ESR1; ESTROGEN RECEPTOR; TAMOXIFEN; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CANCER RECURRENCE; CANCER SURVIVAL; CELL ACTIVITY; CONTROLLED STUDY; DISEASE FREE SURVIVAL; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS, HORMONAL; BIOLOGICAL MARKERS; BREAST NEOPLASMS; CELL LINE, TUMOR; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; ORPHAN NUCLEAR RECEPTORS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, ESTROGEN; RNA INTERFERENCE; RNA, SMALL INTERFERING; TAMOXIFEN;

EID: 84855228591     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201100187     Document Type: Article

References (63)

1. Ali S, Coombes RC (2002) Endocrine-responsive breast cancer and strategies for combating resistance. Nat Rev Cancer 2: 101-112.
2. Amundson SA, Do KT, Vinikoor LC, Lee RA, Koch-Paiz CA, Ahn J, Reimers M, Chen Y, Scudiero DA, Weinstein JN, et al (2008) Integrating global gene expression and radiation survival parameters across the 60 cell lines of the National Cancer Institute Anticancer Drug Screen. Cancer Res 68: 415-424.
3. Ban R, Nishida T, Urano T (2011) Mitotic kinase Aurora-B is regulated by SUMO-2/3 conjugation/deconjugation during mitosis. Genes Cells 16: 652-669.
4. Bookout AL, Jeong Y, Downes M, Yu RT, Evans RM, Mangelsdorf DJ (2006) Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 126: 789-799.
5. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR, et al (2005) Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122: 33-43.
6. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J, Brodsky AS, Keeton EK, Fertuck KC, Hall GF, et al (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38: 1289-1297.
7. Chen J, Rattner A, Nathans J (2005) The rod photoreceptor-specific nuclear receptor Nr2e3 represses transcription of multiple cone-specific genes. J Neurosci 25: 118-129.
8. Chung CD, Liao J, Liu B, Rao X, Jay P, Berta P, Shuai K (1997) Specific inhibition of Stat3 signal transduction by PIAS3. Science 278: 1803-1805.
9. Cosman F, Lindsay R (1999) Selective estrogen receptor modulators: clinical spectrum. Endocr Rev 20: 418-434.
10. Daidone MG, Coradini D, Martelli G, Veneroni S (2003) Primary breast cancer in elderly women: biological profile and relation with clinical outcome. Crit Rev Oncol Hematol 45: 313-325.
11. deGraffenried LA, Hilsenbeck SG, Fuqua SA (2002) Sp1 is essential for estrogen receptor alpha gene transcription. J Steroid Biochem Mol Biol 82: 7-18.
12. Early Breast Cancer Trialists' Collaborative Group (EBCTCG) (2005) Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 365: 1687-1717.
13. Eeckhoute J, Keeton EK, Lupien M, Krum SA, Carroll JS, Brown M (2007) Positive cross-regulatory loop ties GATA-3 to estrogen receptor alpha expression in breast cancer. Cancer Res 67: 6477-6483.
14. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868.
15. Fisher B, Redmond C, Fisher ER, Caplan R (1988) Relative worth of estrogen or progesterone receptor and pathologic characteristics of differentiation as indicators of prognosis in node negative breast cancer patients: findings from National Surgical Adjuvant Breast and Bowel Project Protocol B-06. J Clin Oncol 6: 1076-1087.
16. Gronemeyer H, Gustafsson JA, Laudet V (2004) Principles for modulation of the nuclear receptor superfamily. Nat Rev Drug Discov 3: 950-964.
17. Hegele RA (2005) Retinoid X receptor heterodimers in the metabolic syndrome. N Engl J Med 353: 2088.
18. Hilsenbeck SG, Ravdin PM, de Moor CA, Chamness GC, Osborne CK, Clark GM (1998) Time-dependence of hazard ratios for prognostic factors in primary breast cancer. Breast Cancer Res Treat 52: 227-237.
19. Hosey AM, Gorski JJ, Murray MM, Quinn JE, Chung WY, Stewart GE, James CR, Farragher SM, Mulligan JM, Scott AN, et al (2007) Molecular basis for estrogen receptor alpha deficiency in BRCA1-linked breast cancer. J Natl Cancer Inst 99: 1683-1694.
20. Hsu YC, Yuan S, Chen HY, Yu SL, Liu CH, Hsu PY, Wu G, Lin CH, Chang GC, Li KC, et al (2009) A four-gene signature from NCI-60 cell line for survival prediction in non-small cell lung cancer. Clin Cancer Res 15: 7309-7315.
21. Hu Z, Fan C, Oh DS, Marron JS, He X, Qaqish BF, Livasy C, Carey LA, Reynolds E, Dressler L, et al (2006) The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genomics 7: 96.
22. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15.
23. Iwasaki K, Hailemariam K, Tsuji Y (2007) PIAS3 interacts with ATF1 and regulates the human ferritin H gene through an antioxidant-responsive element. J Biol Chem 282: 22335-22343.
24. Jimenez-Lara AM, Heine MJ, Gronemeyer H (2002) PIAS3 (protein inhibitor of activated STAT-3) modulates the transcriptional activation mediated by the nuclear receptor coactivator TIF2. FEBS Lett 526: 142-146.
25. Junicho A, Matsuda T, Yamamoto T, Kishi H, Korkmaz K, Saatcioglu F, Fuse H, Muraguchi A (2000) Protein inhibitor of activated STAT3 regulates androgen receptor signaling in prostate carcinoma cells. Biochem Biophys Res Commun 278: 9-13.
26. Kanavos P (2006) The rising burden of cancer in the developing world. Ann Oncol 17: viii15-viii23.
27. Kobayashi M, Takezawa S, Hara K, Yu RT, Umesono Y, Agata K, Taniwaki M, Yasuda K, Umesono K (1999) Identification of a photoreceptor cell-specific nuclear receptor. Proc Natl Acad Sci USA 96: 4814-4819.
28. Krum SA, Miranda-Carboni GA, Lupien M, Eeckhoute J, Carroll JS, Brown M (2008) Unique ERalpha cistromes control cell type-specific gene regulation. Mol Endocrinol 22: 2393-2406.
29. Lee JS, Chu IS, Mikaelyan A, Calvisi DF, Heo J, Reddy JK, Thorgeirsson SS (2004) Application of comparative functional genomics to identify best-fit mouse models to study human cancer. Nat Genet 36: 1306-1311.
30. Lee JS, Heo J, Libbrecht L, Chu IS, Kaposi-Novak P, Calvisi DF, Mikaelyan A, Roberts LR, Demetris AJ, Sun Z, et al (2006) A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 12: 410-416.
31. Li X, Wong J, Tsai SY, Tsai MJ, O'Malley BW (2003) Progesterone and glucocorticoid receptors recruit distinct coactivator complexes and promote distinct patterns of local chromatin modification. Mol Cell Biol 23: 3763-3773.
32. Loi S (2008) Molecular analysis of hormone receptor positive (luminal) breast cancers: What have we learnt? Eur J Cancer 44: 2813-2818.
33. Loi S, Haibe-Kains B, Desmedt C, Lallemand F, Tutt AM, Gillet C, Ellis P, Harris A, Bergh J, Foekens JA, et al (2007) Definition of clinically distinct molecular subtypes in estrogen receptor-positive breast carcinomas through genomic grade. J Clin Oncol 25: 1239-1246.
34. Loi S, Haibe-Kains B, Desmedt C, Wirapati P, Lallemand F, Tutt AM, Gillet C, Ellis P, Ryder K, Reid JF, et al (2008) Predicting prognosis using molecular profiling in estrogen receptor-positive breast cancer treated with tamoxifen. BMC Genomics 9: 239.
35. McKenna NJ, Cooney AJ, DeMayo FJ, Downes M, Glass CK, Lanz RB, Lazar MA, Mangelsdorf DJ, Moore DD, Qin J, et al (2009) Minireview: evolution of NURSA, the nuclear receptor signaling atlas. Mol Endocrinol 23: 740-746.
36. Monks A, Scudiero D, Skehan P, Shoemaker R, Paull K, Vistica D, Hose C, Langley J, Cronise P, Vaigro-Wolff A, et al (1991) Feasibility of a high-flux anticancer drug screen using a diverse panel of cultured human tumor cell lines. J Natl Cancer Inst 83: 757-766.
37. Oh DS, Troester MA, Usary J, Hu Z, He X, Fan C, Wu J, Carey LA, Perou CM (2006) Estrogen-regulated genes predict survival in hormone receptor-positive breast cancers. J Clin Oncol 24: 1656-1664.
38. Onishi A, Peng GH, Hsu C, Alexis U, Chen S, Blackshaw S (2009) Pias3-dependent SUMOylation directs rod photoreceptor development. Neuron 61: 234-246.
39. Park YY, Ahn SW, Kim HJ, Kim JM, Lee IK, Kang H, Choi HS (2005) An autoregulatory loop controlling orphan nuclear receptor DAX-1 gene expression by orphan nuclear receptor ERRgamma. Nucleic Acids Res 33: 6756-6768.
40. Park ES, Rabinovsky R, Carey M, Hennessy BT, Agarwal R, Liu W, Ju Z, Deng W, Lu Y, Woo HG, et al (2010) Davies MA Integrative analysis of proteomic signatures, mutations, and drug responsiveness in the NCI 60 cancer cell line set. Mol Cancer Ther 9: 257-267.
41. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, Davies S, Fauron C, He X, Hu Z, et al (2009) Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 27: 1160-1167.
42. Peng G, Yim EK, Dai H, Jackson AP, Burgt I, Pan MR, Hu R, Li K, Lin SY (2009) BRIT1/MCPH1 links chromatin remodelling to DNA damage response. Nat Cell Biol 11: 865-872.
43. Potti A, Dressman HK, Bild A, Riedel RF, Chan G, Sayer R, Cragun J, Cottrill H, Kelley MJ, Petersen R, et al (2006) Genomic signatures to guide the use of chemotherapeutics. Nat Med 12: 1294-1300.
44. Reinhold WC, Mergny JL, Liu H, Ryan M, Pfister TD, Kinders R, Parchment R, Doroshow J, Weinstein JN, Pommier Y, et al (2010) Pommier Y Exon array analyses across the NCI-60 reveal potential regulation of TOP1 by transcription pausing at guanosine quartets in the first intron. Cancer Res 70: 2191-2203.
45. Safe S, Kim K (2004) Nuclear receptor-mediated transactivation through interaction with Sp proteins. Prog Nucleic Acid Res Mol Biol 77: 1-36.
46. Sakaguchi K, Koshiyama A, Iwabata K (2007) Meiosis and small ubiquitin-related modifier (SUMO)-conjugating enzyme, Ubc9. FEBS J 274: 3519-3531.
47. Scherf U, Ross DT, Waltham M, Smith LH, Lee JK, Tanabe L, Kohn KW, Reinhold WC, Myers TG, Andrews DT, et al (2000) A gene expression database for the molecular pharmacology of cancer. Nat Genet 24: 236-244.
48. Schorderet DF, Escher P (2009) NR2E3 mutations in enhanced S-cone sensitivity syndrome (ESCS), Goldmann-Favre syndrome (GFS), clumped pigmentary retinal degeneration (CPRD), and retinitis pigmentosa (RP). Hum Mutat 30: 1475-1485.
49. Shirley SH, Rundhaug JE, Tian J, Cullinan-Ammann N, Lambertz I, Conti CJ, Fuchs-Young R (2009) Transcriptional regulation of estrogen receptor-alpha by p53 in human breast cancer cells. Cancer Res 69: 3405-3414.
50. Shoemaker RH (2006) The NCI60 human tumour cell line anticancer drug screen. Nat Rev Cancer 6: 813-823.
51. Simon R, Lam A, Li MC, Ngan M, Menenzes S, Zhao Y (2007) Analysis of gene expression data using BRB-array tools. Cancer Inform 3: 11-17.
52. Stemke-Hale K, Gonzalez-Angulo AM, Lluch A, Neve RM, Kuo WL, Davies M, Carey M, Hu Z, Guan Y, Sahin A, et al (2008) An integrative genomic and proteomic analysis of PIK3CA, PTEN, and AKT mutations in breast cancer. Cancer Res 68: 6084-6091.
53. Sundar SN, Marconett CN, Doan VB, Willoughby JA, Sr Firestone GL (2008) Artemisinin selectively decreases functional levels of estrogen receptor-alpha and ablates estrogen-induced proliferation in human breast cancer cells. Carcinogenesis 29: 2252-2258.
54. Takezawa S, Yokoyama A, Okada M, Fujiki R, Iriyama A, Yanagi Y, Ito H, Takada I, Kishimoto M, Miyajima A, et al (2007) A cell cycle-dependent co-repressor mediates photoreceptor cell-specific nuclear receptor function. EMBO J 26: 764-774.
55. Tomlins SA, Rhodes DR, Yu J, Varambally S, Mehra R, Perner S, Demichelis F, Helgeson BE, Laxman B, Morris DS, et al (2008) The role of SPINK1 in ETS rearrangement-negative prostate cancers. Cancer Cell 13: 519-528.
56. van de Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, Voskuil DW, Schreiber GJ, Peterse JL, Roberts C, Marton MJ, et al (2002) A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 347: 1999-2009.
57. Wang YP, Li KB (2009) Correlation of expression profiles between microRNAs and mRNA targets using NCI-60 data. BMC Genomics 10: 218.
58. Wang Q, Li W, Zhang Y, Yuan X, Xu K, Yu J, Chen Z, Beroukhim R, Wang H, Lupien M et al (2009) Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 138: 245-256.
59. Wright GW, Simon RM (2003) A random variance model for detection of differential gene expression in small microarray experiments. Bioinformatics 19: 2448-2455.
60. 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.
61. Yang X, Downes M, Yu RT, Bookout AL, He W, Straume M, Mangelsdorf DJ, Evans RM (2006) Nuclear receptor expression links the circadian clock to metabolism. Cell 126: 801-810.
62. Zhang S, Li X, Burghardt R, Smith R, III, Safe SH (2005) Role of estrogen receptor (ER) alpha in insulin-like growth factor (IGF)-I-induced responses in MCF-7 breast cancer cells. J Mol Endocrinol 35: 433-447.
63. 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.