Understanding the mechanisms of androgen deprivation resistance in prostate cancer at the molecular level

European Urology

Volumn 67, Issue 3, 2015, Pages 470-479

  Karantanos, Theodoros ^a   Evans, Christopher P ^b   Tombal, Bertrand ^c   Thompson, Timothy C ^a   Montironi, Rodolfo ^d   Isaacs, William B ^e  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

^d UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^e DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

Alternative signaling; Androgen receptor; Castration resistant prostate cancer; Novel antiandrogens

Indexed keywords

4 [7 [6 CYANO 5 (TRIFLUOROMETHYL) 3 PYRIDINYL] 8 OXO 6 THIOXO 5,7 DIAZASPIRO[3.4]OCTAN 5 YL] 2 FLUORO N METHYLBENZAMIDE; ABIRATERONE; ANDROGEN; ANDROGEN RECEPTOR; ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS; ENZALUTAMIDE; GLUCOCORTICOID RECEPTOR; ANDROSTANE DERIVATIVE; ANTIANDROGEN; AR PROTEIN, HUMAN; ARN-509; PHENYLTHIOHYDANTOIN; THIOHYDANTOIN DERIVATIVE;

ANDROGEN DEPRIVATION THERAPY; ANDROGEN SYNTHESIS; ARTICLE; CANCER GROWTH; CANCER PATIENT; CANCER RESISTANCE; CANCER SURVIVAL; CARCINOGENESIS; CASTRATION RESISTANT PROSTATE CANCER; DRUG TARGETING; GENE AMPLIFICATION; GENE MUTATION; GENETIC VARIABILITY; GENOME ANALYSIS; HOST SELECTION; HOST SUSCEPTIBILITY; HUMAN; MALE; MEDLINE; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; QUALITY OF LIFE; SIGNAL TRANSDUCTION; SYSTEMIC THERAPY; TUMOR MICROENVIRONMENT; ANALOGS AND DERIVATIVES; ANIMAL; CELL PROLIFERATION; DISEASE COURSE; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT;

ANDROGEN ANTAGONISTS; ANDROSTENES; ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; CELL PROLIFERATION; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; PHENYLTHIOHYDANTOIN; PROSTATIC NEOPLASMS, CASTRATION-RESISTANT; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION; THIOHYDANTOINS;

EID: 84922121997     PISSN: 03022838     EISSN: 18737560     Source Type: Journal    
DOI: 10.1016/j.eururo.2014.09.049     Document Type: Article

References (96)

1. R. Siegel, D. Naishadham, and A. Jemal Cancer statistics, 2013 CA Cancer J Clin 63 2013 11 30
2. J. Sturge, M.P. Caley, and J. Waxman Bone metastasis in prostate cancer: emerging therapeutic strategies Nat Rev Clin Oncol 8 2011 357 368
3. J.N. Wu, K.M. Fish, C.P. Evans, R.W. Devere White, and M.A. Dall'era No improvement noted in overall or cause-specific survival for men presenting with metastatic prostate cancer over a 20-year period Cancer 120 2014 818 823
4. W.P. Harris, E.A. Mostaghel, P.S. Nelson, and B. Montgomery Androgen deprivation therapy: progress in understanding mechanisms of resistance and optimizing androgen depletion Nat Clin Pract Urol 6 2009 76 85
5. I.F. Tannock, R. de Wit, and W.R. Berry Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer N Engl J Med 351 2004 1502 1512
6. J.S. de Bono, S. Oudard, M. Ozguroglu, S. Hansen, and J.P. Machiels Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial Lancet 376 2010 1147 1154
7. P.G. Kluetz, W. Pierce, and V.E. Maher Radium Ra 223 dichloride injection: U.S. Food and Drug Administration drug approval summary Clin Cancer Res 20 2014 9 14
8. J.S. de Bono, C.J. Logothetis, and A. Molina Abiraterone and increased survival in metastatic prostate cancer N Engl J Med 364 2011 1995 2005
9. C.J. Ryan, M.R. Smith, and J.S. de Bono Abiraterone in metastatic prostate cancer without previous chemotherapy N Engl J Med 368 2013 138 148
10. C. Tran, S. Ouk, and N.J. Clegg Development of a second-generation antiandrogen for treatment of advanced prostate cancer Science 324 2009 787 790
11. H.I. Scher, K. Fizazi, and F. Saad Increased survival with enzalutamide in prostate cancer after chemotherapy N Engl J Med 367 2012 1187 1197
12. T.M. Beer, A.J. Armstrong, and C. Sternberg Enzalutamide in men with chemotherapy-naive metastatic prostate cancer (mCRPC): results of phase III PREVAIL study [abstract LBA1] J Clin Oncol 32 Suppl 4 2014
13. N.J. Clegg, J. Wongvipat, and J.D. Joseph ARN-509: a novel antiandrogen for prostate cancer treatment Cancer Res 72 2012 1494 1503
14. D.E. Rathkopf, M.J. Morris, and J.J. Fox Phase I study of ARN-509, a novel antiandrogen, in the treatment of castration-resistant prostate cancer J Clin Oncol 31 2013 3525 3530
15. P.J. Toren, and M.E. Gleave Evolving landscape and novel treatments in metastatic castrate-resistant prostate cancer Asian J Androl 15 2013 342 349
16. C.J. Logothetis, G.E. Gallick, and S.N. Maity Molecular classification of prostate cancer progression: foundation for marker-driven treatment of prostate cancer Cancer Discov 3 2013 849 861
17. R.B. Montgomery, E.A. Mostaghel, R. Vessella, and D.L. Hess Maintenance of intratumoral androgens in metastatic prostate cancer: a mechanism for castration-resistant tumor growth Cancer Res 68 2008 4447 4454
18. K.H. Chang, R. Li, and M. Papari-Zareei Dihydrotestosterone synthesis bypasses testosterone to drive castration-resistant prostate cancer Proc Natl Acad Sci U S A 108 2011 13728 13733
19. K.H. Chang, R. Li, and B. Kuri A gain-of-function mutation in DHT synthesis in castration-resistant prostate cancer Cell 154 2013 1074 1084
20. E. Efstathiou, M. Titus, and D. Tsavachidou Effects of abiraterone acetate on androgen signaling in castrate-resistant prostate cancer in bone J Clin Oncol 30 2012 637 643
21. T. Saloniemi, H. Jokela, L. Strauss, P. Pakarinen, and M. Poutanen The diversity of sex steroid action: novel functions of hydroxysteroid (17beta) dehydrogenases as revealed by genetically modified mouse models J Endocrinol 212 2012 27 40
22. F. Ishizaki, T. Nishiyama, and T. Kawasaki Androgen deprivation promotes intratumoral synthesis of dihydrotestosterone from androgen metabolites in prostate cancer Sci Rep 3 2013 1528
23. P.R. Dillard, M.F. Lin, and S.A. Khan Androgen-independent prostate cancer cells acquire the complete steroidogenic potential of synthesizing testosterone from cholesterol Mol Cell Endocrinol 295 2008 115 120
24. B.H. Lee, M.G. Taylor, P. Robinet, and J.D. Smith Dysregulation of cholesterol homeostasis in human prostate cancer through loss of ABCA1 Cancer Res 73 2013 1211 1218
25. E.A. Mostaghel, B.T. Marck, S.R. Plymate, and R.L. Vessella Resistance to CYP17A1 inhibition with abiraterone in castration-resistant prostate cancer: induction of steroidogenesis and androgen receptor splice variants Clin Cancer Res 17 2011 5913 5925
26. Z. Culig, A. Hobisch, and M.V. Cronauer Mutant androgen receptor detected in an advanced-stage prostatic carcinoma is activated by adrenal androgens and progesterone Mol Endocrinol 7 1993 1541 1550
27. R. De Wit, K. Fizazi, V. Jinga, E. Efstathiou, P. Fong, and M. Wirth Results from a phase 3, randomized, double-blind, multicenter, placebo-controlled trial of orteronel (TAK-700) plus prednisone in patients with metastatic castration-resistant prostate cancer (mCRPC) that has progressed during or following docetaxel-based therapy (ELM-PC 5 trial) Clin Adv Hematol Oncol 12 2014 6 7
28. J. Holzbeierlein, P. Lal, and E. LaTulippe Gene expression analysis of human prostate carcinoma during hormonal therapy identifies androgen-responsive genes and mechanisms of therapy resistance Am J Pathol 16 2004 217 227
29. M.E. Taplin, B. Rajeshkumar, S. Halabi, C.P. Werner, and B.A. Woda Androgen receptor mutations in androgen-independent prostate cancer: Cancer and Leukemia Group B study 9663 J Clin Oncol 21 2003 2673 2678
30. M.E. Taplin, G.J. Bubley, and T.D. Shuster Mutation of the androgen-receptor gene in metastatic androgen-independent prostate cancer N Engl J Med 332 1995 1393 1398
31. B.S. Taylor, N. Schultz, and H. Hieronymus Integrative genomic profiling of human prostate cancer Cancer Cell 18 2010 11 22
32. C.E. Barbieri, S.C. Baca, and M.S. Lawrence Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer Nat Genet 44 2012 685 689
33. C.S. Grasso, Y.M. Wu, and D.R. Robinson The mutational landscape of lethal castration resistant prostate cancer Nature 487 2012 239 243
34. M.E. Taplin, G.J. Bubley, and Y.J. Ko Selection for androgen receptor mutations in prostate cancers treated with androgen antagonist Cancer Res 59 1999 2511 2515
35. Z. Culig, A. Hobisch, and M.V. Cronauer Mutant androgen receptor detected in an advanced-stage prostatic carcinoma is activated by adrenal androgens and progesterone Mol Endocrinol 7 1993 1541 1550
36. K. Steketee, L. Timmerman, A.C. Ziel-van der Made, P. Doesburg, A.O. Brinkmann, and J. Trapman Broadened ligand responsiveness of androgen receptor mutants obtained by random amino acid substitution of H874 and mutation hot spot T877 in prostate cancer Int J Cancer 100 2002 309 317
37. Z. Culig, J. Hoffmann, and M. Erdel Switch from antagonist to agonist of the androgen receptor bicalutamide is associated with prostate tumour progression in a new model system Br J Cancer 81 1999 242 251
38. J. Duff, and I.M. McEwan Mutation of histidine 874 in the androgen receptor ligand-binding domain leads to promiscuous ligand activation and altered p160 coactivator interactions Mol Endocrinol 19 2005 2943 2954
39. M.P. Steinkamp, O.A. O'Mahony, and M. Brogley Treatment-dependent androgen receptor mutations in prostate cancer exploit multiple mechanisms to evade therapy Cancer Res 69 2009 4434 4442
40. M. Korpal, J.M. Korn, X. Gao, and D.P. Rakiec An F876L mutation in androgen receptor confers genetic and phenotypic resistance to MDV3100 Cancer Discov 3 2013 1030 1043
41. J.D. Joseph, N. Lu, J. Qian, J. Sensintaffar, and G. Shao A clinically relevant androgen receptor mutation confers resistance to second-generation antiandrogens enzalutamide and ARN-509 Cancer Discov 3 2013 1020 1029
42. W.G. Nelson, and S. Yegnasubramanian Resistance emerges to second-generation antiandrogens in prostate cancer Cancer Discov 3 2013 971 974
43. C.G. Tepper, D.L. Boucher, and P.E. Ryan Characterization of a novel androgen receptor mutation in a relapsed CWR22 prostate cancer xenograft and cell line Cancer Res 62 2002 6606 6614
44. S.J. Libertini, C.G. Tepper, V. Rodriguez, D.M. Asmuth, H.J. Kung, and M. Mudryj Evidence for calpain-mediated androgen receptor cleavage as a mechanism for androgen independence Cancer Res 67 2007 9001 9005
45. Z. Guo, X. Yang, and F. Sun A novel androgen receptor splice variant is up-regulated during prostate cancer progression and promotes androgen depletion-resistant growth Cancer Res 69 2009 2305 2313
46. S.M. Dehm, L.J. Schmidt, H.V. Heemers, R.L. Vessella, and D.J. Tindall Splicing of a novel androgen receptor exon generates a constitutively active androgen receptor that mediates prostate cancer therapy resistance Cancer Res 68 2008 5469 5477
47. R. Hu, T.A. Dunn, and S. Wei Ligand-independent androgen receptor variants derived from splicing of cryptic exons signify hormone-refractory prostate cancer Cancer Res 69 2009 16 22
48. R. Hu, W.B. Isaacs, and J. Luo A snapshot of the expression signature of androgen receptor splicing variants and their distinctive transcriptional activities Prostate 71 2011 1656 1667
49. P.A. Watson, Y.F. Chen, and M.D. Balbas Constitutively active androgen receptor splice variants expressed in castration-resistant prostate cancer require full-length androgen receptor Proc Natl Acad Sci U S A 107 2010 16759 16765
50. S. Sun, C.C. Sprenger, and R.L. Vessella Castration resistance in human prostate cancer is conferred by a frequently occurring androgen receptor splice variant J Clin Invest 120 2010 2715 2730
51. E. Hörnberg, E.B. Ylitalo, and S. Crnalic Expression of androgen receptor splice variants in prostate cancer bone metastases is associated with castration-resistance and short survival PLoS ONE 6 2011 e19059
52. R. Hu, C. Lu, and E.A. Mostaghel Distinct transcriptional programs mediated by the ligand-dependent full-length androgen receptor and its splice variants in castration-resistant prostate cancer Cancer Res 72 2012 3457 3462
53. Y. Li, S.C. Chan, L.J. Brand, T.H. Hwang, K.A. Silverstein, and S.M. Dehm Androgen receptor splice variants mediate enzalutamide resistance in castration-resistant prostate cancer cell lines Cancer Res 73 2012 483 489
54. N. Nadiminty, R. Tummala, and C. Liu NF-κB2/p52 induces resistance to enzalutamide in prostate cancer: role of androgen receptor and its variants Mol Cancer Ther 12 2013 1629 1637
55. C. Liu, W. Lou, and Y. Zhu Niclosamide inhibits androgen receptor variants expression and overcomes enzalutamide resistance in castration resistant prostate cancer Clin Cancer Res 20 2014 3198 3210
56. E.S. Antonarakis, C. Lu, and H. Wang AR-V7 and resistance to enzalutamide and abiraterone in prostate cancer N Engl J Med 371 2014 1028 1038
57. M.D. Sadar Small molecule inhibitors targeting the "Achilles' heel" of androgen receptor activity Cancer Res 71 2011 1208 1213
58. Efstathiou E, Titus M, Wen AS, SanMiguel A, Hoang A, De Haas-Amatsaleh A, et al. The effects of enzalutamide (ENZA) in combination with abiraterone acetate (AA) in patients with bone metastatic castration resistant prostate cancer (mCRPC). Presented at: European Cancer Congress 2013; 27 September-1 October 2013; Amsterdam, The Netherlands. Abstract 2854.
59. Z. Guo, B. Dai, and T. Jiang Regulation of androgen receptor activity by tyrosine phosphorylation Cancer Cell 10 2006 309 319
60. T. Ueda, N.R. Mawji, N. Bruchovsky, and M.D. Sadar 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 2002 38087 38094
61. I.U. Agoulnik, A. Vaid, and W.E. Bingman III Role of SRC-1 in the promotion of prostate cancer cell growth and tumor progression Cancer Res 65 2005 7959 7967
62. S. Feng, Q. Tang, M. Sun, J.Y. Chun, C.P. Evans, and A.C. Gao Interleukin-6 increases prostate cancer cells resistance to bicalutamide via TIF2 Mol Cancer Ther 8 2009 665 671
63. I.U. Agoulnik, A. Vaid, and M. Nakka 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 2006 10594 10602
64. Z. Culig, A. Hobisch, and M.V. Cronauer Androgen receptor activation in prostatic tumor cell lines by insulin-like growth factor-I, keratinocyte growth factor, and epidermal growth factor Cancer Res 54 1994 5474 5478
65. I.K. Mellinghoff, I. Vivanco, A. Kwon, C. Tran, J. Wongvipat, and C.L. Sawyers HER2/neu kinase-dependent modulation of androgen receptor function through effects on DNA binding and stability Cancer Cell 6 2004 517 527
66. L. Chen, B.A. Mooso, and M.K. Jathal Dual EGFR/HER2 inhibition sensitizes prostate cancer cells to androgen withdrawal by suppressing ErbB3 Clin Cancer Res 17 2011 6218 6228
67. B.S. Carver, C. Chapinski, and J. Wongvipat Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer Cancer Cell 19 2011 575 586
68. B.S. Taylor, N. Schultz, and H. Hieronymus Integrative genomic profiling of human prostate cancer Cancer Cell 18 2010 11 22
69. J. Zhong, L. Ding, and L.R. Bohrer P300 acetyltransferase regulates androgen receptor degradation and PTEN-deficient prostate tumorigenesis Cancer Res 74 2014 1870 1880
70. J.D. Debes, L.J. Schmidt, H. Huang, and D.J. Tindall p300 mediates androgen-independent transactivation of the androgen receptor by interleukin 6 Cancer Res 62 2002 5632 5636
71. R. Venkitaraman, K. Thomas, R.A. Huddart, A. Horwich, D.P. Dearnaley, and C.C. Parker Efficacy of low-dose dexamethasone in castration-refractory prostate cancer BJU Int 101 2008 440 443
72. A. Yemelyanov, J. Czwornog, and D. Chebotaev Tumor suppressor activity of glucocorticoid receptor in the prostate Oncogene 26 2007 1885 1896
73. B. Sahu, M. Laakso, and P. Pihlajamaa FoxA1 specifies unique androgen and glucocorticoid receptor binding events in prostate cancer cells Cancer Res 73 2013 1570 1580
74. V.K. Arora, E. Schenkein, and R. Murali Glucocorticoid receptor confers resistance to antiandrogens by bypassing androgen receptor blockade Cell 155 2013 1309 1322
75. P. Davies, and N.K. Rushmere Association of glucocorticoid receptors with prostate nuclear sites for androgen receptors and with androgen response elements J Mol Endocrinol 5 1990 117 127
76. C. Cai, H.H. He, and S. Chen Androgen receptor gene expression in prostate cancer is directly suppressed by the androgen receptor through recruitment of lysine-specific demethylase 1 Cancer Cell 20 2011 457 471
77. D.J. Mulholland, L.M. Tran, Y. Li, H. Cai, A. Morim, and S. Wang Cell autonomous role of PTEN in regulating castration-resistant prostate cancer growth Cancer Cell 19 2011 792 804
78. H.K. Lin, L. Wang, Y.C. Hu, S. Altuwaijri, and C. Chang Phosphorylation-dependent ubiquitylation and degradation of androgen receptor by Akt require Mdm2 E3 ligase EMBO J 21 2002 4037 4048
79. M. Nakabayashi, L. Werner, and K.D. Courtney Phase II trial of RAD001 and bicalutamide for castration-resistant prostate cancer BJU Int 110 2012 1729 1735
80. T. Muranen, L.M. Selfors, and D.T. Worster Inhibition of PI3K/mTOR leads to adaptive resistance in matrix-attached cancer cells Cancer Cell 21 2012 227 239
81. S. Varambally, S.M. Dhanasekaran, and M. Zhou The polycomb group protein EZH2 is involved in progression of prostate cancer Nature 419 2002 624 629
82. L.R. Bohrer, S. Chen, T.C. Hallstrom, and H. Huang Androgens suppress EZH2 expression via retinoblastoma (RB) and p130-dependent pathways: a potential mechanism of androgen-refractory progression of prostate cancer Endocrinology 151 2010 5136 5145
83. K. Xu, Z.J. Wu, and A.C. Groner EZH2 oncogenic activity in castration-resistant prostate cancer cells is Polycomb-independent Science 338 2012 1465 1469
84. J. Abdulghani, L. Gu, and A. Dagvadorj Stat3 promotes metastatic progression of prostate cancer Am J Pathol 172 2008 1717 1728
85. A. Schroeder, A. Herrmann, and G. Cherryholmes Loss of androgen receptor expression promotes a stem-like cell phenotype in prostate cancer through STAT3 signaling Cancer Res 74 2014 1227 1237
86. C. Liu, Y. Zhu, W. Lou, Y. Cui, C.P. Evans, and A.C. Gao Inhibition of constitutively active Stat3 reverses enzalutamide resistance in LNCaP derivative prostate cancer cells Prostate 74 2014 201 209
87. B.S. Knudsen, and M. Edlund Prostate cancer and the met hepatocyte growth factor receptor Adv Cancer Res 91 2004 31 67
88. S. Kasai, K. Sugimura, K. Matsumoto, N. Nishi, T. Kishimoto, and T. Nakamura Hepatocyte growth factor is a paracrine regulator of rat prostate epithelial growth Biochem Biophys Res Commun 228 1996 646 652
89. P.A. Humphrey, X. Zhu, and R. Zarnegar Hepatocyte growth factor and its receptor (c-MET) in prostatic carcinoma Am J Pathol 147 1995 386 396
90. Y. Loriot, A. Zoubeidi, and M.E. Gleave Targeted therapies in metastatic castration-resistant prostate cancer: beyond the androgen receptor Urol Clin North Am 39 2012 517 531
91. M. Verras, J. Lee, and H. Xue The androgen receptor negatively regulates the expression of c-Met: implications for a novel mechanism of PCa progression Cancer Res 67 2007 967 975
92. T. Liu, D.E. Mendes, and C.E. Berkman From AR to c-Met: androgen deprivation leads to a signaling pathway switch in prostate cancer cells Int J Oncol 43 2013 1125 1130
93. D.C. Smith, M.R. Smith, and C. Sweeney Cabozantinib in patients with advanced prostate cancer: results of a phase II randomized discontinuation trial J Clin Oncol 31 2013 412 419
94. L. Li, W. Chang, and G. Yang Targeting poly(ADP-ribose) polymerase and the c-Myb-regulated DNA damage response pathway in castration-resistant prostate cancer Sci Signal 7 2014 ra47
95. G. Stenman, M.K. Andersson, and Y. Andrén New tricks from an old oncogene: gene fusion and copy number alterations of MYB in human cancer Cell Cycle 9 2010 2986 2995
96. J. Edwards, N.S. Krishna, K.M. Grigor, and J.M. Bartlett Androgen receptor gene amplification and protein expression in hormone refractory prostate cancer Br J Cancer 89 2003 552 556