Androgen Receptor Gene Expression in Prostate Cancer Is Directly Suppressed by the Androgen Receptor Through Recruitment of Lysine-Specific Demethylase 1

Cancer Cell

Volumn 20, Issue 4, 2011, Pages 457-471

  Cai, Changmeng ^a   He, Housheng Hansen ^a,b   Chen, Sen ^a   Coleman, Ilsa ^c   Wang, Hongyun ^a   Fang, Zi ^a   Chen, Shaoyong ^a   Nelson, Peter S ^c   Liu, X Shirley ^b   Brown, Myles ^a   Balk, Steven P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; HISTONE H3; HISTONE H3K4ME1,2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LSD1; UNCLASSIFIED DRUG;

ANDROGEN DEPRIVATION THERAPY; ANDROGEN RECEPTOR BINDING SITE; ANDROGEN SYNTHESIS; ARTICLE; BINDING SITE; CASTRATION RESISTANT PROSTATE CANCER; CELL PROLIFERATION; CONTROLLED STUDY; DEMETHYLATION; DNA SYNTHESIS; ENHANCER REGION; GENE EXPRESSION; GENE REPRESSION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; INTRON; LIPOGENESIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RECEPTOR BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; TUMOR XENOGRAFT;

EID: 80054761058     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2011.09.001     Document Type: Article

References (38)

1. Bauman D.R., Steckelbroeck S., Williams M.V., Peehl D.M., Penning T.M. Identification of the major oxidative 3alpha-hydroxysteroid dehydrogenase in human prostate that converts 5alpha-androstane-3alpha,17beta-diol to 5alpha-dihydrotestosterone: a potential therapeutic target for androgen-dependent disease. Mol. Endocrinol. 2006, 20:444-458.
2. Blok L.J., Themmen A.P., Peters A.H., Trapman J., Baarends W.M., Hoogerbrugge J.W., Grootegoed J.A. Transcriptional regulation of androgen receptor gene expression in Sertoli cells and other cell types. Mol. Cell. Endocrinol. 1992, 88:153-164.
3. Cai C., Wang H., Xu Y., Chen S., Balk S.P. Reactivation of androgen receptor-regulated TMPRSS2:ERG gene expression in castration-resistant prostate cancer. Cancer Res. 2009, 69:6027-6032.
4. 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.
5. Cheng S., Brzostek S., Lee S.R., Hollenberg A.N., Balk S.P. Inhibition of the dihydrotestosterone-activated androgen receptor by nuclear receptor corepressor. Mol. Endocrinol. 2002, 16:1492-1501.
6. Garcia-Bassets I., Kwon Y.S., Telese F., Prefontaine G.G., Hutt K.R., Cheng C.S., Ju B.G., Ohgi K.A., Wang J., Escoubet-Lozach L., et al. Histone methylation-dependent mechanisms impose ligand dependency for gene activation by nuclear receptors. Cell 2007, 128:505-518.
7. Gregory C.W., Johnson R.T., Mohler J.L., French F.S., Wilson E.M. Androgen receptor stabilization in recurrent prostate cancer is associated with hypersensitivity to low androgen. Cancer Res. 2001, 61:2892-2898.
8. Holzbeierlein J., Lal P., LaTulippe E., Smith A., Satagopan J., Zhang L., Ryan C., Smith S., Scher H., Scardino P., et al. Gene expression analysis of human prostate carcinoma during hormonal therapy identifies androgen-responsive genes and mechanisms of therapy resistance. Am. J. Pathol. 2004, 164:217-227.
9. Kemppainen J.A., Lane M.V., Sar M., Wilson E.M. Androgen receptor phosphorylation, turnover, nuclear transport, and transcriptional activation: specificity for steroids and antihormones. J. Biol. Chem. 1992, 267:968-974.
10. Korenchuk S., Lehr J.E., McLean L., Lee Y.G., Whitney S., Vessella R., Lin D.L., Pienta K.J. VCaP, a cell-based model system of human prostate cancer. In Vivo 2001, 15:163-168.
11. Krongrad A., Wilson C.M., Wilson J.D., Allman D.R., McPhaul M.J. Androgen increases androgen receptor protein while decreasing receptor mRNA in LNCaP cells. Mol. Cell. Endocrinol. 1991, 76:79-88.
12. Kumar M.V., Jones E.A., Grossmann M.E., Blexrud M.D., Tindall D.J. Identification and characterization of a suppressor element in the 5'-flanking region of the mouse androgen receptor gene. Nucleic Acids Res. 1994, 22:3693-3698.
13. Loberg R.D., St John L.N., Day L.L., Neeley C.K., Pienta K.J. Development of the VCaP androgen-independent model of prostate cancer. Urol. Oncol. 2006, 24:161-168.
14. 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.
15. Metzger E., Wissmann M., Yin N., Müller J.M., Schneider R., Peters A.H., Günther T., Buettner R., Schüle R. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 2005, 437:436-439.
16. Metzger E., Yin N., Wissmann M., Kunowska N., Fischer K., Friedrichs N., Patnaik D., Higgins J.M., Potier N., Scheidtmann K.H., et al. Phosphorylation of histone H3 at threonine 11 establishes a novel chromatin mark for transcriptional regulation. Nat. Cell Biol. 2008, 10:53-60.
17. Metzger E., Imhof A., Patel D., Kahl P., Hoffmeyer K., Friedrichs N., Müller J.M., Greschik H., Kirfel J., Ji S., et al. Phosphorylation of histone H3T6 by PKCbeta(I) controls demethylation at histone H3K4. Nature 2010, 464:792-796.
18. Morris M.J., Huang D., Kelly W.K., Slovin S.F., Stephenson R.D., Eicher C., Delacruz A., Curley T., Schwartz L.H., Scher H.I. Phase 1 trial of high-dose exogenous testosterone in patients with castration-resistant metastatic prostate cancer. Eur. Urol. 2009, 56:237-244.
19. Perillo B., Ombra M.N., Bertoni A., Cuozzo C., Sacchetti S., Sasso A., Chiariotti L., Malorni A., Abbondanza C., Avvedimento E.V. DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression. Science 2008, 319:202-206.
20. Quarmby V.E., Yarbrough W.G., Lubahn D.B., French F.S., Wilson E.M. Autologous down-regulation of androgen receptor messenger ribonucleic acid. Mol. Endocrinol. 1990, 4:22-28.
21. Ruizeveld de Winter J.A., Janssen P.J., Sleddens H.M., Verleun-Mooijman M.C., Trapman J., Brinkmann A.O., Santerse A.B., Schröder F.H., van der Kwast T.H. Androgen receptor status in localized and locally progressive hormone refractory human prostate cancer. Am. J. Pathol. 1994, 144:735-746.
22. Shan L.X., Rodriguez M.C., Jänne O.A. Regulation of androgen receptor protein and mRNA concentrations by androgens in rat ventral prostate and seminal vesicles and in human hepatoma cells. Mol. Endocrinol. 1990, 4:1636-1646.
23. 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.
24. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., Casero R.A., Shi Y. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119:941-953.
25. Shi Y.J., Matson C., Lan F., Iwase S., Baba T., Shi Y. Regulation of LSD1 histone demethylase activity by its associated factors. Mol. Cell. 2005, 19:857-864.
26. Stanbrough M., Bubley G.J., Ross K., Golub T.R., Rubin M.A., Penning T.M., Febbo P.G., Balk S.P. Increased expression of genes converting adrenal androgens to testosterone in androgen-independent prostate cancer. Cancer Res. 2006, 66:2815-2825.
27. Taplin M.E., Bubley G.J., Shuster T.D., Frantz M.E., Spooner A.E., Ogata G.K., Keer H.N., Balk S.P. Mutation of the androgen-receptor gene in metastatic androgen-independent prostate cancer. N. Engl. J. Med. 1995, 332:1393-1398.
28. Umekita Y., Hiipakka R.A., Kokontis J.M., Liao S. Human prostate tumor growth in athymic mice: inhibition by androgens and stimulation by finasteride. Proc. Natl. Acad. Sci. USA 1996, 93:11802-11807.
29. Visakorpi T., Hyytinen E., Koivisto P., Tanner M., Keinänen R., Palmberg C., Palotie A., Tammela T., Isola J., Kallioniemi O.P. In vivo amplification of the androgen receptor gene and progression of human prostate cancer. Nat. Genet. 1995, 9:401-406.
30. Wang L.G., Johnson E.M., Kinoshita Y., Babb J.S., Buckley M.T., Liebes L.F., Melamed J., Liu X.M., Kurek R., Ossowski L., Ferrari A.C. Androgen receptor overexpression in prostate cancer linked to Pur alpha loss from a novel repressor complex. Cancer Res. 2008, 68:2678-2688.
31. Wang L.G., Ossowski L., Ferrari A.C. Androgen receptor level controlled by a suppressor complex lost in an androgen-independent prostate cancer cell line. Oncogene 2004, 23:5175-5184.
32. Wang Q., Li W., Liu X.S., Carroll J.S., Jänne O.A., Keeton E.K., Chinnaiyan A.M., Pienta K.J., Brown M. A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol. Cell 2007, 27:380-392.
33. 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.
34. Wissmann M., Yin N., Müller J.M., Greschik H., Fodor B.D., Jenuwein T., Vogler C., Schneider R., Günther T., Buettner R., et al. Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptor-dependent gene expression. Nat. Cell Biol. 2007, 9:347-353.
35. Xu Y., Chen S.Y., Ross K.N., Balk S.P. Androgens induce prostate cancer cell proliferation through mammalian target of rapamycin activation and post-transcriptional increases in cyclin D proteins. Cancer Res. 2006, 66:7783-7792.
36. Yeap B.B., Voon D.C., Vivian J.P., McCulloch R.K., Thomson A.M., Giles K.M., Czyzyk-Krzeska M.F., Furneaux H., Wilce M.C., Wilce J.A., Leedman P.J. Novel binding of HuR and poly(C)-binding protein to a conserved UC-rich motif within the 3'-untranslated region of the androgen receptor messenger RNA. J. Biol. Chem. 2002, 277:27183-27192.
37. 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.
38. Yuan X., Balk S.P. Mechanisms mediating androgen receptor reactivation after castration. Urol. Oncol. 2009, 27:36-41.