The Androgen Receptor Induces a Distinct Transcriptional Program in Castration-Resistant Prostate Cancer in Man

Cancer Cell

Volumn 23, Issue 1, 2013, Pages 35-47

  Sharma, Naomi L ^a,b,f   Massie, Charlie E ^a   Ramos Montoya, Antonio ^a   Zecchini, Vincent ^a   Scott, Helen E ^a   Lamb, Alastair D ^a,b   MacArthur, Stewart ^a   Stark, Rory ^a   Warren, Anne Y ^b   Mills, Ian G ^a,d,e   Neal, David E ^a,b,c  

^a Cambridge Research Institute   (United Kingdom)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d OSLO UNIVERSITY HOSPITAL   (Norway)

^e UNIVERSITY OF OSLO   (Norway)

^f UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR;

ARTICLE; BINDING SITE; CASTRATION RESISTANT PROSTATE CANCER; CONTROLLED STUDY; GENE MAPPING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

EID: 84872391385     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2012.11.010     Document Type: Article

References (46)

1. Attar R.M., Jure-Kunkel M., Balog A., Cvijic M.E., Dell-John J., Rizzo C.A., Schweizer L., Spires T.E., Platero J.S., Obermeier M., et al. Discovery of BMS-641988, a novel and potent inhibitor of androgen receptor signaling for the treatment of prostate cancer. Cancer Res. 2009, 69:6522-6530.
2. Attard G., Reid A.H., Yap T.A., Raynaud F., Dowsett M., Settatree S., Barrett M., Parker C., Martins V., Folkerd E., et al. Phase I clinical trial of a selective inhibitor of CYP17, abiraterone acetate, confirms that castration-resistant prostate cancer commonly remains hormone driven. J. Clin. Oncol. 2008, 26:4563-4571.
3. Badis G., Berger M.F., Philippakis A.A., Talukder S., Gehrke A.R., Jaeger S.A., Chan E.T., Metzler G., Vedenko A., Chen X., et al. Diversity and complexity in DNA recognition by transcription factors. Science 2009, 324:1720-1723.
4. Bernard D., Pourtier-Manzanedo A., Gil J., Beach D.H. Myc confers androgen-independent prostate cancer cell growth. J. Clin. Invest. 2003, 112:1724-1731.
5. Best C.J., Gillespie J.W., Yi Y., Chandramouli G.V., Perlmutter M.A., Gathright Y., Erickson H.S., Georgevich L., Tangrea M.A., Duray P.H., et al. Molecular alterations in primary prostate cancer after androgen ablation therapy. Clin. Cancer Res. 2005, 11:6823-6834.
6. Blankenberg D., Taylor J., Schenck I., He J., Zhang Y., Ghent M., Veeraraghavan N., Albert I., Miller W., Makova K.D., et al. A framework for collaborative analysis of ENCODE data: making large-scale analyses biologist-friendly. Genome Res. 2007, 17:960-964.
7. Chen C.D., Welsbie D.S., Tran C., Baek S.H., Chen R., Vessella R., Rosenfeld M.G., Sawyers C.L. Molecular determinants of resistance to antiandrogen therapy. Nat. Med. 2004, 10:33-39.
8. Consortium E.P. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 2011, 9:e1001046. ENCODE Project Consortium.
9. Eisen M.B., Spellman P.T., Brown P.O., Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 1998, 95:14863-14868.
10. Ellwood-Yen K., Graeber T.G., Wongvipat J., Iruela-Arispe M.L., Zhang J., Matusik R., Thomas G.V., Sawyers C.L. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell 2003, 4:223-238.
11. Gao N., Zhang J., Rao M.A., Case T.C., Mirosevich J., Wang Y., Jin R., Gupta A., Rennie P.S., Matusik R.J. The role of hepatocyte nuclear factor-3 alpha (Forkhead Box A1) and androgen receptor in transcriptional regulation of prostatic genes. Mol. Endocrinol. 2003, 17:1484-1507.
12. Gao P., Tchernyshyov I., Chang T.C., Lee Y.S., Kita K., Ochi T., Zeller K.I., De Marzo A.M., Van Eyk J.E., Mendell J.T., Dang C.V. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 2009, 458:762-765.
13. Glinsky G.V., Glinskii A.B., Stephenson A.J., Hoffman R.M., Gerald W.L. Gene expression profiling predicts clinical outcome of prostate cancer. J. Clin. Invest. 2004, 113:913-923.
14. Hedvat M., Huszar D., Herrmann A., Gozgit J.M., Schroeder A., Sheehy A., Buettner R., Proia D., Kowolik C.M., Xin H., et al. The JAK2 inhibitor AZD1480 potently blocks Stat3 signaling and oncogenesis in solid tumors. Cancer Cell 2009, 16:487-497.
15. Hurtado A., Holmes K.A., Geistlinger T.R., Hutcheson I.R., Nicholson R.I., Brown M., Jiang J., Howat W.J., Ali S., Carroll J.S. Regulation of ERBB2 by oestrogen receptor-PAX2 determines response to tamoxifen. Nature 2008, 456:663-666.
16. Ji X., Li W., Song J., Wei L., Liu X.S. CEAS: cis-regulatory element annotation system. Nucleic Acids Res. 2006, 34(Web Server issue):W551-W554.
17. Jia L., Berman B.P., Jariwala U., Yan X., Cogan J.P., Walters A., Chen T., Buchanan G., Frenkel B., Coetzee G.A. Genomic androgen receptor-occupied regions with different functions, defined by histone acetylation, coregulators and transcriptional capacity. PLoS ONE 2008, 3:e3645.
18. Lupien M., Eeckhoute J., Meyer C.A., Wang Q., Zhang Y., Li W., Carroll J.S., Liu X.S., Brown M. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 2008, 132:958-970.
19. Massie C.E., Adryan B., Barbosa-Morais N.L., Lynch A.G., Tran M.G., Neal D.E., Mills I.G. New androgen receptor genomic targets show an interaction with the ETS1 transcription factor. EMBO Rep. 2007, 8:871-878.
20. Massie C.E., Lynch A., Ramos-Montoya A., Boren J., Stark R., Fazli L., Warren A., Scott H., Madhu B., Sharma N., et al. The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J. 2011, 30:2719-2733.
21. McLean C.Y., Bristor D., Hiller M., Clarke S.L., Schaar B.T., Lowe C.B., Wenger A.M., Bejerano G. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 2010, 28:495-501.
22. Mendiratta P., Mostaghel E., Guinney J., Tewari A.K., Porrello A., Barry W.T., Nelson P.S., Febbo P.G. Genomic strategy for targeting therapy in castration-resistant prostate cancer. J. Clin. Oncol. 2009, 27:2022-2029.
23. Mootha V.K., Lindgren C.M., Eriksson K.F., Subramanian A., Sihag S., Lehar J., Puigserver P., Carlsson E., Ridderstråle M., Laurila E., et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 2003, 34:267-273.
24. Mostaghel E.A., Page S.T., Lin D.W., Fazli L., Coleman I.M., True L.D., Knudsen B., Hess D.L., Nelson C.C., Matsumoto A.M., et al. Intraprostatic androgens and androgen-regulated gene expression persist after testosterone suppression: therapeutic implications for castration-resistant prostate cancer. Cancer Res. 2007, 67:5033-5041.
25. Palomero T., Lim W.K., Odom D.T., Sulis M.L., Real P.J., Margolin A., Barnes K.C., O'Neil J., Neuberg D., Weng A.P., et al. NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth. Proc. Natl. Acad. Sci. USA 2006, 103:18261-18266.
26. Roche P.J., Hoare S.A., Parker M.G. A consensus DNA-binding site for the androgen receptor. Mol. Endocrinol. 1992, 6:2229-2235.
27. Schmidt D., Stark R., Wilson M.D., Brown G.D., Odom D.T. Genome-scale validation of deep-sequencing libraries. PLoS ONE 2008, 3:e3713.
28. Sharma A., Yeow W.S., Ertel A., Coleman I., Clegg N., Thangavel C., Morrissey C., Zhang X., Comstock C.E., Witkiewicz A.K., et al. The retinoblastoma tumor suppressor controls androgen signaling and human prostate cancer progression. J. Clin. Invest. 2010, 120:4478-4492.
29. Shu G., Zeng B., Chen Y.P., Smith O.H. Performance assessment of kernel density clustering for gene expression profile data. Comp. Funct. Genomics 2003, 4:287-299.
30. Snoek R., Cheng H., Margiotti K., Wafa L.A., Wong C.A., Wong E.C., Fazli L., Nelson C.C., Gleave M.E., Rennie P.S. In vivo knockdown of the androgen receptor results in growth inhibition and regression of well-established, castration-resistant prostate tumors. Clin. Cancer Res. 2009, 15:39-47.
31. Stoecklin E., Wissler M., Moriggl R., Groner B. Specific DNA binding of Stat5, but not of glucocorticoid receptor, is required for their functional cooperation in the regulation of gene transcription. Mol. Cell. Biol. 1997, 17:6708-6716.
32. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102:15545-15550.
33. Tam L., McGlynn L.M., Traynor P., Mukherjee R., Bartlett J.M., Edwards J. Expression levels of the JAK/STAT pathway in the transition from hormone-sensitive to hormone-refractory prostate cancer. Br. J. Cancer 2007, 97:378-383.
34. Taylor B.S., Schultz N., Hieronymus H., Gopalan A., Xiao Y., Carver B.S., Arora V.K., Kaushik P., Cerami E., Reva B., et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010, 18:11-22.
35. Taylor J., Schenck I., Blankenberg D., Nekrutenko A. Using galaxy to perform large-scale interactive data analyses. Curr. Protoc. Bioinformatics 2007, (Suppl 38). 10.5.1-10.5.47.
36. Terada N., Shimizu Y., Kamba T., Inoue T., Maeno A., Kobayashi T., Nakamura E., Kamoto T., Kanaji T., Maruyama T., et al. Identification of EP4 as a potential target for the treatment of castration-resistant prostate cancer using a novel xenograft model. Cancer Res. 2010, 70:1606-1615.
37. Tomlins S.A., Mehra R., Rhodes D.R., Cao X., Wang L., Dhanasekaran S.M., Kalyana-Sundaram S., Wei J.T., Rubin M.A., Pienta K.J., et al. Integrative molecular concept modeling of prostate cancer progression. Nat. Genet. 2007, 39:41-51.
38. Tran C., Ouk S., Clegg N.J., Chen Y., Watson P.A., Arora V., Wongvipat J., Smith-Jones P.M., Yoo D., Kwon A., et al. Development of a second-generation antiandrogen for treatment of advanced prostate cancer. Science 2009, 324:787-790.
39. Varambally S., Yu J., Laxman B., Rhodes D.R., Mehra R., Tomlins S.A., Shah R.B., Chandran U., Monzon F.A., Becich M.J., et al. Integrative genomic and proteomic analysis of prostate cancer reveals signatures of metastatic progression. Cancer Cell 2005, 8:393-406.
40. Venables W.N., Ripley B.D. Modern Applied Statistics with S 2002, Springer, New York. Fourth Edition.
41. Wang D., Garcia-Bassets I., Benner C., Li W., Su X., Zhou Y., Qiu J., Liu W., Kaikkonen M.U., Ohgi K.A., et al. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 2011, 474:390-394.
42. Wang Q., Li W., Zhang Y., Yuan X., Xu K., Yu J., Chen Z., Beroukhim R., Wang H., Lupien M., et al. Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 2009, 138:245-256.
43. Wei C.L., Wu Q., Vega V.B., Chiu K.P., Ng P., Zhang T., Shahab A., Yong H.C., Fu Y., Weng Z., et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 2006, 124:207-219.
44. Wilson M.D., Barbosa-Morais N.L., Schmidt D., Conboy C.M., Vanes L., Tybulewicz V.L., Fisher E.M., Tavaré S., Odom D.T. Species-specific transcription in mice carrying human chromosome 21. Science 2008, 322:434-438.
45. Yu J., Yu J., Mani R.S., Cao Q., Brenner C.J., Cao X., Wang X., Wu L., Li J., Hu M., et al. An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 2010, 17:443-454.
46. Yu Y.P., Landsittel D., Jing L., Nelson J., Ren B., Liu L., McDonald C., Thomas R., Dhir R., Finkelstein S., et al. Gene expression alterations in prostate cancer predicting tumor aggression and preceding development of malignancy. J. Clin. Oncol. 2004, 22:2790-2799.