Androgen receptor-mediated gene repression

Molecular and Cellular Endocrinology

Volumn 352, Issue 1-2, 2012, Pages 46-56

  Grosse, Andreas ^a   Bartsch, Sophie ^a   Baniahmad, Aria ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Gene repression; Nuclear hormone receptor; Prostate cancer; Therapy; Transcription factor

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; CASPASE 2; CYCLIN D1; GLUCURONOSYLTRANSFERASE; GONADOTROPIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MASPIN; MATRIX METALLOPROTEINASE; SCATTER FACTOR RECEPTOR; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR ERM; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SP1; TRANSFORMING GROWTH FACTOR BETA; UDP GLUCURONOSYLTRANSFERASE 2 B15; UNCLASSIFIED DRUG; UVOMORULIN;

CELL NUCLEUS; CHRM1 GENE; CHROMATIN CONDENSATION; COMPLEX FORMATION; DNA BINDING; DOWN REGULATION; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCATION; GENE PRODUCT; GENE REPRESSION; GENE SILENCING; GENE TARGETING; GENOMICS; HORMONE SYNTHESIS; HUMAN; KIAA1217 GENE; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WBSCR28 GENE;

CHROMATIN; DNA; GENE EXPRESSION REGULATION; HUMANS; MALE; RECEPTORS, ANDROGEN;

EID: 84856525070     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.06.032     Document Type: Review

References (97)

1. Aarnisalo P., Palvimo J.J., Jänne O.A. CREB-binding protein in androgen receptor-mediated signaling. Proc. Natl. Acad. Sci. USA 1998, 95:2122-2127.
2. Aarnisalo P., Santti H., Poukka H., Palvimo J.J., Jänne O.A. Transcription activating and repressing functions of the androgen receptor are differentially influenced by mutations in the deoxyribonucleic acid-binding domain. Endocrinology 1999, 140:3097-3105.
3. Agoulnik I.U., Weigel N.L. Coactivator selective regulation of androgen receptor activity. Steroids 2009, 74:669-674.
4. Baniwal S.K., Khalid O., Sir D., Buchanan G., Coetzee G.A., Frenkel B. Repression of Runx2 by androgen receptor (AR) in osteoblasts and prostate cancer cells: AR binds Runx2 and abrogates its recruitment to DNA. Mol. Endocrinol. 2009, 23:1203-1214.
5. Bao B.Y., Chuang B.F., Wang Q., Sartor O., Balk S.P., Brown M., Kantoff P.W., Lee G.S. Androgen receptor mediates the expression of UDP-glucuronosyltransferase 2 B15 and B17 genes. Prostate 2008, 68:839-848.
6. Battaglia S., Maguire O., Campbell M.J. Transcription factor co-repressors in cancer biology: roles and targeting. Int. J. Cancer 2010, 126:2511-2519.
7. Behrens J., Mareel M.M., Van Roy F.M., Birchmeier W. Dissecting tumor cell invasion: epithelial cells acquire invasive properties after the loss of uvomorulin-mediated cell-cell adhesion. J. Cell Biol. 1989, 108:2435-2447.
8. Birchmeier C., Birchmeier W., Gherardi E., Vande Woude G.F. Met, metastasis, motility and more. Nat. Rev. Mol. Cell. Biol. 2003, 4:915-925.
9. Bohrer L.R., Chen S., Hallstrom T.C., Huang H. Androgens suppress EZH2 expression via retinoblastoma (RB) and p130-dependent pathways: a potential mechanism of androgen-refractory progression of prostate cancer. Endocrinology 2010, 151:5136-5145.
10. Bolton E.C., So A.Y., Chaivorapol C., Haqq C.M., Li H., Yamamoto K.R. Cell- and gene-specific regulation of primary target genes by the androgen receptor. Genes Dev. 2007, 21:2005-2017.
11. Bonaccorsi L., Muratori M., Carloni V., Marchiani S., Formigli L., Forti G., Baldi E. The androgen receptor associates with the epidermal growth factor receptor in androgen-sensitive prostate cancer cells. Steroids 2004, 69:549-552.
12. Bonaccorsi L., Muratori M., Marchiani S., Forti G., Baldi E. The androgen receptor and prostate cancer invasion. Mol. Cell. Endocrinol. 2006, 246:157-162.
13. Bonaccorsi L., Nosi D., Quercioli F., Formigli L., Zecchi S., Maggi M., Forti G., Baldi E. Prostate cancer: a model of integration of genomic and non-genomic effects of the androgen receptor in cell lines model. Steroids 2008, 73:1030-1037.
14. Bottaro D.P., Rubin J.S., Faletto D.L., Chan A.M., Kmiecik T.E., Vande Woude G.F., Aaronson S.A. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 1991, 251:802-804.
15. Carver B.S., Chapinski C., Wongvipat J., Hieronymus H., Chen Y., Chandarlapaty S., Arora V.K., Le C., Koutcher J., Scher H., Scardino P.T., Rosen N., Sawyers C.L. Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer. Cancer Cell 2011, 19:575-586.
16. Cato A.C., Peterziel H. The androgen receptor as mediator of gene expression and signal transduction pathways. TEM 1998, 9:150-154.
17. Chipuk J.E., Cornelius S.C., Pultz N.J., Jorgensen J.S., Bonham M.J., Kim S.J., Danielpour D. The androgen receptor represses transforming growth factor-beta signaling through interaction with Smad3. J. Biol. Chem. 2002, 277:1240-1248.
18. Chouinard S., Barbier O., Bélanger A. UDP-glucuronosyltransferase 2B15 (UGT2B15) and UGT2B17 enzymes are major determinants of the androgen response in prostate cancer LNCaP cells. J. Biol. Chem. 2007, 282:33466-33474.
19. Claessens F., Verrijdt G., Schoenmakers E., Haelens A., Peeters B., Verhoeven G., Rombauts W. Selective DNA binding by the androgen receptor as a mechanism for hormone-specific gene regulation. J. Steroid Biochem. Mol. Biol. 2001, 76:23-30.
20. Clay C.M., Keri R.A., Finicle A.B., Heckert L.L., Hamernik D.L., Marschke K.M., Wilson E.M., French F.S., Nilson J.H. Transcriptional repression of the glycoprotein hormone alpha subunit gene by androgen may involve direct binding of androgen receptor to the proximal promoter. J. Biol. Chem. 1993, 268:13556-13564.
21. Culig Z., Hobisch A., Hittmair A., Peterziel H., Cato A.C., Bartsch G., Klocker H. Expression, structure, and function of androgen receptor in advanced prostatic carcinoma. Prostate 1998, 35:63-70.
22. Curtin D., Jenkins S., Farmer N., Anderson A.C., Haisenleder D.J., Rissman E., Wilson E.M., Shupnik M.A. Androgen suppression of GnRH-stimulated rat LHbeta gene transcription occurs through Sp1 sites in the distal GnRH-responsive promoter region. Mol. Endocrinol. 2001, 15:1906-1917.
23. Degterev A., Boyce M., Yuan J. A decade of caspases. Oncogene 2003, 22:8543-8567.
24. Denayer S., Helsen C., Thorrez L., Haelens A., Claessens F. The rules of DNA recognition by the androgen receptor. Mol. Endocrinol. 2010, 24:898-913.
25. Dotzlaw H., Moehren U., Mink S., Cato A.C., Iñiguez Lluhí J.A., Baniahmad A. The amino terminus of the human AR is target for corepressor action and antihormone agonism. Mol. Endocrinol. 2002, 16:661-673.
26. Dotzlaw H., Papaioannou M., Moehren U., Claessens F., Baniahmad A. Agonist-antagonist induced coactivator and corepressor interplay on the human androgen receptor. Mol. Cell. Endocrinol. 2003, 213:79-85.
27. Ducrest A.L., Szutorisz H., Lingner J., Nabholz M. Regulation of the human telomerase reverse transcriptase gene. Oncogene 2002, 21:541-552.
28. Gatson J.W., Kaur P., Singh M. Dihydrotestosterone differentially modulates the mitogen-activated protein kinase and the phosphoinositide 3-kinase/Akt pathways through the nuclear and novel membrane androgen receptor in C6 cells. Endocrinology 2006, 147:2028-2034.
29. Gelman E.P. Molecular biology of the androgen receptor. J. Clin. Oncol. 2002, 20:3001-3015.
30. Guo C., Armbruster B.N., Price D.T., Counter C.M. In vivo regulation of hTERT expression and telomerase activity by androgen. J. Urol. 2003, 170:615-618.
31. Harley C.B., Villeponteau B. Telomeres and telomerase in aging and cancer. Curr. Opin. Genet. Dev. 1995, 5:249-255.
32. He M.L., Jiang A.L., Zhang P.J., Hu X.Y., Liu Z.F., Yuan H.Q., Zhang J.Y. Identification of androgen-responsive element ARE and Sp1 element in the maspin promoter. Chin. J. Physiol. 2005, 48:160-166.
33. Heckert L.L., Wilson E.M., Nilson J.H. Transcriptional repression of the alpha-subunit gene by androgen receptor occurs independently of DNA binding but requires the DNA-binding and ligand-binding domains of the receptor. Mol. Endocrinol. 1997, 11:1497-1506.
34. Heemers H.V., Tindall D.J. Androgen receptor (AR) coregulators: a diversity of functions converging on and regulating the AR transcriptional complex. Endocr. Rev. 2007, 28:778-808.
35. Heinlein C.A., Chang C. The roles of androgen receptors and androgen-binding proteins in nongenomic androgen actions. Mol. Endocrinol. 2002, 16:2181-2187.
36. Hodgson M.C., Shen H.C., Hollenberg A.N., Balk S.P. Structural basis for nuclear receptor corepressor recruitment by antagonist-liganded androgen receptor. Mol. Cancer Ther. 2008, 7:3187-3194.
37. Holter E., Kotaja N., Mäkela S., Strauss L., Kietz S., Jänne O.A., Gustafsson J.A., Palvimo J.J., Treuter E. Inhibition of androgen receptor (AR) function by the reproductive orphan nuclear receptor DAX-1. Mol. Endocrinol. 2002, 16:515-528.
38. Horoszewicz J.S., Leong S.S., Kawinski E., Karr J.P., Rosenthal H., Chu T.M., Mirand E.A., Murphy G.P. LNCaP model of human prostatic carcinoma. Cancer Res. 1983, 43:1809-1818.
39. Huang H., Zegarra-Moro O.L., Benson D., Tindall D.J. Androgens repress Bcl-2 expression via activation of the retinoblastoma (RB) protein in prostate cancer cells. Oncogene 2004, 23:2161-2176.
40. Itoh S., ten Dijke P. Negative regulation of TGF-beta receptor/Smad signal transduction. Curr. Opin. Cell. Biol. 2007, 19:176-184.
41. Jariwala U., Prescott J., Jia L., Barski A., Pregizer S., Cogan J.P., Arasheben A., Tilley W.D., Scher H.I., Gerald W.L., Buchanan G., Coetzee G.A., Frenkel B. Identification of novel androgen receptor target genes in prostate cancer. Mol. Cancer 2007, 6:39.
42. 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.
43. Jiang, J., Pan, Y., Regan, K.M., Wu, C., Zhang, X., Tindall, D.J., Huang, H., 2011. Androgens repress expression of the f-box protein Skp2 via p107 dependent and independent mechanisms in LNCaP prostate cancer cells. Prostate. [Epub ahead of print].
44. Jorgensen J.S., Nilson J.H. AR suppresses transcription of the LHbeta subunit by interacting with steroidogenic factor-1. Mol. Endocrinol. 2001, 15:1505-1516.
45. Jorgensen J.S., Nilson J.H. AR suppresses transcription of the alpha glycoprotein hormone subunit gene through protein-protein interactions with cJun and activation transcription factor 2. Mol. Endocrinol. 2001, 15:1496-1504.
46. Kaighn M.E., Narayan K.S., Ohnuki Y., Lechner J.F., Jones L.W. Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest. Urol. 1979, 17:16-23.
47. Kallio P.J., Poukka H., Moilanen A., Jänne O.A., Palvimo J.J. Androgen receptor-mediated transcriptional regulation in the absence of direct interaction with a specific DNA element. Mol. Endocrinol. 1995, 9:1017-1028.
48. Kousteni S., Bellido T., Plotkin L.I., O'Brien C.A., Bodenner D.L., Han L., Han K., DiGregorio G.B., Katzenellenbogen J.A., Katzenellenbogen B.S., Roberson P.K., Weinstein R.S., Jilka R.L., Manolagas S.C. Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 2001, 104:719-730.
49. Lamb L.E., Knudsen B.S., Miranti C.K. E-cadherin-mediated survival of androgen-receptor-expressing secretory prostate epithelial cells derived from a stratified in vitro differentiation model. J. Cell Sci. 2010, 123:266-276.
50. Lanzino M., Sisci D., Morelli C., Garofalo C., Catalano S., Casaburi I., Capparelli C., Giordano C., Giordano F., Maggiolini M., Andò S. Inhibition of cyclin D1 expression by androgen receptor in breast cancer cells - identification of a novel androgen response element. Nucleic Acids Res. 2010, 38:5351-5365.
51. Lin B., Wang J., Hong X., Yan X., Hwang D., Cho J.-H., Yi D., Utleg A.G., Fang X., Schones D.E., Zhao K., Omenn G.S., Hood L. Integrated expression profiling and ChIP-seq analyses of the growth inhibition response program of the androgen receptor. PLoS One 2009, 4:e6589.
52. Liu M.M., Albanese C., Anderson C.M., Hilty K., Webb P., Uht R.M., Price R.H.Jr., Pestell R.G., Kushner P.J. Opposing action of estrogen receptors alpha and beta on cyclin D1 gene expression. J. Biol. Chem. 2002, 277:24353-24360.
53. Liu Y.N., Liu Y., Lee H.J., Hsu Y.H., Chen J.H. Activated androgen receptor down-regulates E-cadherin gene expression and promotes tumor metastasis. Mol. Cell. Biol. 2008, 28:7096-7108.
54. Martikainen P., Kyprianou N., Isaacs J.T. Effect of transforming growth factor-beta 1 on proliferation and death of rat prostatic cells. Endocrinology 1990, 127:2963-2968.
55. Messie 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.
56. Migliaccio A., Castoria G., Di Domenico M., de Falco A., Bilancio A., Lombardi M., Barone M.V., Ametrano D., Zannini M.S., Abbondanza C., Auricchio F. Steroid-induced androgen receptor-oestradiol receptor beta-Src complex triggers prostate cancer cell proliferation. EMBO J. 2000, 19:5406-5417.
57. Moehren U., Eckey M., Baniahmad A. Gene repression by nuclear hormone receptors. Essays Biochem. 2004, 40:89-104.
58. Moehren U., Papaioannou M., Reeb C.A., Hong W., Baniahmad A. Alien interacts with the human androgen receptor and inhibits prostate cancer cell growth. Mol. Endocrinol. 2007, 21:1039-1048.
59. Moehren U., Papaioannou M., Reeb C.A., Grasselli A., Nanni S., Asim M., Roell D., Prade I., Farsetti A., Baniahmad A. Wild-type but not mutant androgen receptor inhibits expression of the hTERT telomerase subunit: a novel role of AR mutation for prostate cancer development. FASEB J. 2008, 22:1258-1267.
60. Musgrove E.A., Hamilton J.A., Lee C.S., Sweeney K.J., Watts C.K., Sutherland R.L. Growth factor, steroid, and steroid antagonist regulation of cyclin gene expression associated with changes in T-47D human breast cancer cell cycle progression. Mol. Cell. Biol. 1993, 13:3577-3587.
61. Nelius T., Filleur S., Yemelyanov A., Budunova I., Shroff E., Mirochnik Y., Aurora A., Veliceasa D., Xiao W., Wang Z., Volpert O.V. Androgen receptor targets NFkappaB and TSP1 to suppress prostate tumor growth in vivo. Int. J. Cancer 2007, 121:999-1008.
62. Nelson P.S., Clegg N., Arnold H., Ferguson C., Bonham M., White J., Hood L., Lin B. The program of androgen-responsive genes in neoplastic prostate epithelium. PNAS 2002, 99:11890-11895.
63. Ngan S., Stronach E.A., Photiou A., Waxman J., Ali S., Buluwela L. Microarray coupled to quantitative RT-PCR analysis of androgen-regulated genes in human LNCaP prostate cancer cells. Oncogene 2009, 28:2051-2063.
64. Nicolás Díaz-Chico B., Germán Rodríguez F., González A., Ramírez R., Bilbao C., Cabrera de León A., Aguirre Jaime A., Chirino R., Navarro D., Díaz-Chico J.C. Androgens and androgen receptors in breast cancer. J. Steroid Biochem. Mol. Biol. 2007, 105:1-15.
65. Niu Y., Chang T.-M., Yeh S., Ma W.-L., Wang Y.Z., Chang C. Differential androgen receptor signals in different cells explain why androgen-deprivation therapy of prostate cancer fails. Oncogene 2010, 29:3593-3604.
66. Palvimo J.J., Reinikainen P., Ikonen T., Kallio P.J., Moilanen A., Jänne O.A. Mutual transcriptional interference between RelA and androgen receptor. J. Biol. Chem. 1996, 271:24151-24156.
67. Papadopoulou N., Charalampopoulos I., Anagnostopoulou V., Konstantinidis G., Föller M., Gravanis A., Alevizopoulos K., Lang F., Stournaras C. Membrane androgen receptor activation triggers down-regulation of PI-3K/Akt/NF-kappaB activity and induces apoptotic responses via Bad, FasL and caspase-3 in DU145 prostate cancer cells. Mol. Cancer 2008, 7:88.
68. Papaioannou M., Schleich S., Prade I., Degen S., Roell D., Schubert U., Tanner T., Claessens F., Matusch R., Baniahmad A. The natural compound atraric acid is an antagonist of the human androgen receptor inhibiting cellular invasiveness and prostate cancer cell growth. J. Cell. Mol. Med. 2009, 13:2210-2223.
69. Peterziel H., Mink S., Schonert A., Becker M., Klocker H., Cato A.C. Rapid signalling by androgen receptor in prostate cancer cells. Oncogene 1999, 18:6322-6329.
70. Poole J.C., Andrews L.G., Tollefsbol T.O. Activity, function, and gene regulation of the catalytic subunit of telomerase (hTERT). Gene 2001, 16:1-12.
71. Pratap J., Lian J.B., Javed A., Barnes G.L., van Wijnen A.J., Stein J.L., Stein G.S. Regulatory roles of Runx2 in metastatic tumor and cancer cell interactions with bone. Cancer Metastasis Rev. 2006, 25:589-600.
72. Prescott J., Jariwala U., Jia L., Cogan J.P., Barski A., Pregizer S., Shen H.C., Arasheben A., Neilson J.J., Frenkel B., Coetzee G.A. Androgen receptor-mediated repression of novel target genes. Prostate 2007, 67:1371-1383.
73. Qi W., Gao S., Wang Z. Transcriptional regulation of the TGF-beta1 promoter by androgen receptor. Biochem. J. 2008, 416:453-462.
74. Roche P.J., Hoare S.A., Parker M.G. A consensus DNA-binding site for the androgen receptor. Mol. Endocrinol. 1992, 6:2229-2235.
75. Rokhlin O.W., Taghiyev A.F., Guseva N.V., Glover R.A., Chumakov P.M., Kravchenko J.E., Cohen M.B. Androgen regulates apoptosis induced by TNFR family ligands via multiple signaling pathways in LNCaP. Oncogene 2005, 24:6773-6784.
76. Shakil T., Hoque A.N., Husain M., Belsham D.D. Differential regulation of gonadotropin-releasing hormone secretion and gene expression by androgen: membrane versus nuclear receptor activation. Mol. Endocrinol. 2002, 16:2592-2602.
77. Schipper J.H., Frixen U.H., Behrens J., Unger A., Jahnke K., Birchmeier W. E-cadherin expression in squamous cell carcinomas of head and neck: inverse correlation with rumor dedifferentiation and lymph node metastasis. Cancer Res. 1991, 51:6328-6337.
78. Schneikert J., Peterziel H., Defossez P.A., Klocker H., Launoit Y., Cato A.C. Androgen receptor-Ets protein interaction is a novel mechanism for steroid hormone-mediated down-modulation of matrix metalloproteinase expression. J. Biol. Chem. 1996, 271:23907-23913.
79. Sheng S., Carey J., Seftor E.A., Dias L., Hendrix M.J., Sager R. Maspin acts at the cell membrane to inhibit invasion and motility of mammary and prostatic cancer cells. Proc. Natl. Acad. Sci. USA 1996, 93:11669-11674.
80. Shi H.Y., Zhang W., Liang R., Abraham S., Kittrell F.S., Medina D., Zhang M. Blocking tumor growth, invasion, and metastasis by maspin in a syngeneic breast cancer model. Cancer Res. 2001, 61:6945-6951.
81. Soda H., Raymond E., Sharma S., Lawrence R., Davidson K., Oka M., Kohno S., Izbicka E., Von Hoff D.D. Effects of androgens on telomerase activity in normal and malignant prostate cells in vitro. Prostate 2000, 43:161-168.
82. Song K., Wang H., Krebs T.L., Kim S.J., Danielpour D. Androgenic control of transforming growth factor-beta signaling in prostate epithelial cells through transcriptional suppression of transforming growth factor-beta receptor II. Cancer Res. 2008, 68:8173-8182.
83. Song K., Wang H., Krebs T.L., Wang B., Kelley T.J., Danielpour D. DHT selectively reverses Smad3-mediated/TGF-beta-induced responses through transcriptional downregulation of Smad3 in prostate epithelial cells. Mol. Endocrinol. 2010, 24:2019-2029.
84. Tang B., de Castro K., Barnes H.E., Parks W.T., Stewart L., Böttinger E.P., Danielpour D., Wakefield L.M. Loss of responsiveness to transforming growth factor beta induces malignant transformation of nontumorigenic rat prostate epithelial cells. Cancer Res. 1999, 59:4834-4842.
85. Takayama K., Kaneshiro K., Tsutsumi S., Horie-Inoue K., Ikeda K., Urano T., Ijichi N., Ouchi Y., Shirahige K., Aburatani H., Inoue S. Identification of novel androgen response genes in prostate cancer cells by coupling chromatin immunoprecipitation and genomic microarray analysis. Oncogene 2007, 26:4453-4463.
86. Talbert P.B., Henikoff S. Spreading of silent chromatin: inaction at a distance. Nat. Rev. Genet. 2006, 7:793-803.
87. van der Deen M., Akech J., Wang T., FitzGerald T.J., Altieri D.C., Languino L.R., Lian J.B., van Wijnen A.J., Stein J.L., Stein G.S. The cancer-related Runx2 protein enhances cell growth and responses to androgen and TGFbeta in prostate cancer cells. J. Cell. Biochem. 2010, 109:828-837.
88. Veldscholte J., Ris-Stalpers C., Kuiper G.G., Jenster G., Berrevoets C., Claassen E., van Rooij H.C., Trapman J., Brinkmann A.O., Mulder E. A mutation in the ligand binding domain of the androgen receptor of human LNCaP cells affects steroid binding characteristics and response to anti-androgens. Biochem. Biophys. Res. Commun. 1990, 173:534-540.
89. Verras M., Lee J., Xue H., Li T.H., Wang Y., Sun Z. The androgen receptor negatively regulates the expression of c-Met: implications for a novel mechanism of prostate cancer progression. Cancer Res. 2007, 67:967-975.
90. 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.
91. Yuan X., Lu M.L., Li T., Balk S.P. SRY interacts with and negatively regulates androgen receptor transcriptional activity. J. Biol. Chem. 2001, 276:46647-46654.
92. Yan J., Brown T.R. Cell proliferation and expression of cell cycle regulatory proteins that control the G1/S transition are age dependent and lobe specific in the Brown Norway rat model of prostatic hyperplasia. Endocrinology 2008, 149:193-207.
93. Zaidi S.K., Pande S., Pratap J., Gaur T., Grigoriu S., Ali S.A., Stein J.L., Lian J.B., van Wijnen A.J., Stein G.S. Runx2 deficiency and defective subnuclear targeting bypass senescence to promote immortalization and tumorigenic potential. Proc. Natl. Acad. Sci. USA 2007, 104:19861-19866.
94. Zhang M., Magit D., Sager R. Expression of maspin in prostate cells is regulated by a positive ets element and a negative hormonal responsive element site recognized by androgen receptor. Proc. Natl. Acad. Sci. USA 1997, 94:5673-5678.
95. Zhang M., Maass N., Magit D., Sager R. Transactivation through Ets and Ap1 transcription sites determines the expression of the tumor-suppressing gene maspin. Cell Growth Differ. 1997, 8:179-186.
96. Zhu M.L., Kyprianou N. Role of androgens and the androgen receptor in epithelial-mesenchymal transition and invasion of prostate cancer cells. FASEB J. 2010, 24:769-777.
97. Zou Z., Zhang W., Young D., Gleave M.G., Rennie P., Connell T., Connelly R., Moul J., Srivastava S., Sesterhenn I. Maspin expression profile in human prostate cancer (CaP) and in vitro induction of Maspin expression by androgen ablation. Clin. Cancer Res. 2002, 8:1172-1177.