Androgen pathway resistance in prostate cancer and therapeutic implications

Bibliography

• Surveillance, Epidemiology, and End Results (SEER) Program Populations (1969-2012) (www.seer.cancer.gov/popdata; National Cancer Institute, DCCPS, Surveillance Research Program, Surveillance Systems Branch, released March 2014
   Google Scholar
• Beer MT, Armstrong AJ, Rathkopf DE, et al. Enzalutamide in metastatic prostate cancer before chemotherapy. N Engl J Med 2014;371:424-33
   PubMed Web of Science ®Google Scholar
• Sweeney C, Chen Y-H, Carducci MA, et al. Impact on overall survival (OS) with chemohormonal therapy versus hormonal therapy for hormone-sensitive newly metastatic prostate cancer (mPrCa): An ECOG-led phase III randomized trial. J Clin Oncol 2014;32:5s
   PubMed Web of Science ®Google Scholar
• Roy AK, Tyagi RK, Song CS, et al. Androgen Receptor: Structural Domains and Functional Dynamics after Ligand-Receptor Interaction. Ann N Y Acad Sci 2001;949:44-57
   PubMed Web of Science ®Google Scholar
• Darshan MS, Loftus MS, Thadani-Mulero M, et al. Taxane-Induced Blockade to Nuclear Accumulation of the Androgen Receptor Predicts Clinical Responses in Metastatic Prostate Cancer. Cancer Res 2011;71:6019-29
   PubMed Web of Science ®Google Scholar
• Edwards J, Krishna NS, Mukherjee R, et al. Amplification of the androgen receptor may not explain the development of androgen-independent prostate cancer. BJU Int 2001;88:633-7
   PubMed Web of Science ®Google Scholar
• Linja MJ, Savinainen KJ, Saramaki OR, et al. Amplification and overexpression of androgen receptor gene in hormone-refractory prostate cancer. Cancer Res 2001;61:3550-5
   PubMed Web of Science ®Google Scholar
• Haffner MC, Aryee MJ, Toubaji A, et al. Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements. Nat Genet 2010;42:668-75
   PubMed Web of Science ®Google Scholar
• Haffner MC, De Marzo AM, Meeker AK, et al. Transcription-induced DNA double strand breaks: both oncogenic force and potential therapeutic target? Clin Cancer Res 2011;17:3858-64
   PubMed Web of Science ®Google Scholar
• Schweizer MT, Antonarakis ES, Wang H, et al. Effect of bipolar androgen therapy for asymptomatic men with castration-resistant prostate cancer: Results from a pilot clinical study. Sci Transl Med 2015;7:269ra2
   PubMed Web of Science ®Google Scholar
• RE-sensitizing with supraphysiologic testosterone to overcome resistance to abiraterone and enzalutamide (The RESTORE Study). Available from: https://clinicaltrials.gov/ct2/show/NCT02090114
   Google Scholar
• Testosterone Revival Abolishes Negative Symptoms, Fosters Objective Response and Modulates Enzalutamide Resistance (TRANSFORMER). Available from: https://clinicaltrials.gov/ct2/show/NCT02286921
   Google Scholar
• Montgomery RB, Mostaghel EA, Vessella R, et al. Maintenance of intratumoral androgens in metastatic prostate cancer: A mechanism for castration-resistant tumor growth. Can Res 2008;68:4447-54
   PubMed Web of Science ®Google Scholar
• Mohler JL, Gregory CW, Ford OH, et al. The androgen axis in recurrent prostate cancer. Clin Can Res 2004;10:440-8
   PubMed Web of Science ®Google Scholar
• Knuuttila M, Yatkin E, Kallio J, et al. Castration induces up-regulation of intratumoral androgen biosynthesis and androgen receptor expression in an orthotopic VCaP human prostate cancer xenograft model. Am J Pathol 2014;184:2163-73
   PubMed Web of Science ®Google Scholar
• Locke JA, Guns ES, Lubik AA, et al. Androgen levels increase by intratumoral de novo steroidogenesis during progression of castration-resistant prostate cancer. Can Res 2008;68:6407-15
   PubMed Web of Science ®Google Scholar
• Beer TM, Armstrong AJ, Rathkopf DE, et al. Enzalutamide in metastatic prostate cancer before chemotherapy. N Eng J Med 2014;37:424-33
   Google Scholar
• Ryan CJ, Smith MR, de Bono JS, et al. Abiraterone in metastatic prostate cancer without previous chemotherapy. N Engl J Med 2013;10:138-48
   Google Scholar
• Scher HI, Fizazi K, Saad F, et al. Increased survival with enzalutamide in prostate cancer after chemotherapy. N Engl J Med 2012;367:1187-97
   PubMed Web of Science ®Google Scholar
• de Bono JS, Logothetis CJ, Molina A, et al. Abiraterone and increased survival in metastatic prostate cancer. N Engl J Med 2011;364:1995-2005
   PubMed Web of Science ®Google Scholar
• Efstathiou E, Titus M, Tsavachidou D, et al. Effects of Abiraterone Acetate on Androgen Signaling in Castrate-Resistant Prostate Cancer. JCO 2011;6:637-43
   Google Scholar
• Efstathiou E, Titus M, Wen S, et al. Molecular characterization of enzalutamide-treated bone metastatic castration-resistant prostate cancer. Eur Urol 2015;1:53-60
   Google Scholar
• Antonarakis ES. Predicting treatment response in castration-resistant prostate cancer: could androgen receptor variant-7 hold the key? Expert Rev Anticancer Ther 2014;15:143-5
   PubMed Web of Science ®Google Scholar
• Nadiminty N, Tummala R, Liu C, et al. NF-κB2/p52 induces resistance to enzalutamide in prostate cancer: role of androgen receptor and its variants. Mol Cancer Ther 2013;12:1629-37
   PubMed Web of Science ®Google Scholar
• Mostaghel EA, Marck BT, Plymate SR, et al. Resistance to CYP17A1 inhibition with abiraterone in castration-resistant prostate cancer: induction of steroidogenesis and androgen receptor splice variants. Clin Cancer Res 2011;17:5913-25
   PubMed Web of Science ®Google Scholar
• Hu R, Lu C, Mostaghel EA, et al. Distinct transcriptional programs mediated by the ligand-dependent full-length androgen receptor and its splice variants in castration-resistant prostate cancer. Cancer Res 2012;72:3457-62
   PubMed Web of Science ®Google Scholar
• Li Y, Chan SC, Brand LJ, et al. Androgen receptor splice variants mediate enzalutamide resistance in castration-resistant prostate cancer cell lines. Cancer Res 2013;73:483-9
   PubMed Web of Science ®Google Scholar
• Antonarakis ES, Lu C, Wang H, et al. AR-V7 and resistance to enzalutamide and abiraterone in prostate cancer. N Engl J Med 2014;371:1028-38
   PubMed Web of Science ®Google Scholar
• Development of circulating molecular predictors of chemotherapy and novel hormonal therapy benefit in men with metastatic castration resistant prostate cancer (mCRPC). Available from: https://clinicaltrials.gov/ct2/show/NCT02269982
   Google Scholar
• Antonarakis ES, Lu C, Luber B, et al. Androgen receptor splice variant 7 and efficacy of taxane chemotherapy in patients with metastatic castration-resistant prostate cancer. JAMA Oncology 2015;10.1001/jamaoncol.2015.1341
   PubMed Web of Science ®Google Scholar
• Thadani-Mulero M, Portella L, Sun S, et al. Androgen receptor splice variants determine taxane sensitivity in prostate cancer. Can Res 2014;74:2270-82
   PubMed Web of Science ®Google Scholar
• Mediwala SN, Sun H, Szafran AT, et al. The activity of the androgen receptor variant AR-V7 is regulated by FOXO1 in a PTEN-PI3K-AKT-dependent way. Prostate 2013;73:267-77
   PubMed Web of Science ®Google Scholar
• Koochekpour S. Androgen receptor signaling and mutations in prostate cancer. Asian J Androl 2010;12(5):639-57
   PubMed Web of Science ®Google Scholar
• McEwan IJ, Hay CW. The impact of point mutations in the human androgen receptor: classification of mutations on the basis of transcriptional activity. PLoS One 2012;7(3):e32514
   PubMed Web of Science ®Google Scholar
• Gottliet B, Beitel LK, Nadarajah A, et al. The Androgen receptor gene mutations database: 2012. Hum Mut 2012;33:887-94
   PubMed Web of Science ®Google Scholar
• Korpal M, Korn JM, Gao X, et al. An F876L Mutation in Androgen Receptor Confers Genetic and Phenotypic Resistance to MDV3100 (Enzalutamide). Cancer Discov 2013;3:1030-43
   PubMed Web of Science ®Google Scholar
• Balbas MD, Evans MJ, Hosfield DJ, et al. Overcoming mutation-based resistance to antiandrogens with rational drug design. Elife 2013;2:e00499
   PubMed Web of Science ®Google Scholar
• Joseph JD, Qian J, Sensintaffar J, et al. A clinically relevant androgen receptor mutation confers resistance to second-generation antiandrogens enzalutamide and ARN-509. Cancer Discov 2013;3:1020-9
   PubMed Web of Science ®Google Scholar
• Azad AA, Volik SV, Wyatt AW, et al. Androgen receptor gene aberrations in circulating cell-free DNA: biomarkers of therapeutic resistance in castration-resistant prostate cancer. Clin Can Res 2015;21(10):2315-24
   PubMed Web of Science ®Google Scholar
• Chen EJ, Sowalsky AG, Gao S, et al. Abiraterone treatment in castration-resistant prostate cancer selects for progesterone responsive mutant androgen receptors. Clin Cancer Res 2015;21:1273-80
   PubMed Web of Science ®Google Scholar
• Joyce R, Fenton MA, Rode P, et al. High dose bicalutamide for androgen independent prostate cancer: effect of prior hormonal therapy. J Urol 1998;159:149-53
   PubMed Web of Science ®Google Scholar
• Arora VK, Schenkein E, Murali R, et al. Glucocorticoid Receptor confers resistance to antiandrogens by bypassing androgen receptor blockade. Cell 2013;155:1309-22
   PubMed Web of Science ®Google Scholar
• Richards J, Lim AC, Hay CW, et al. Interactions of abiraterone, eplerenone, and prednisolone with wild-type and mutant androgen receptor: a rationale for increasing abiraterone exposure or combining with MDV3100. Cancer Res 2012;72:2176-82
   PubMed Web of Science ®Google Scholar
• Carreira S, Romanel A, Goodall J, et al. Tumor clone dynamics in lethal prostate cancer. Sci Transl Med 2014;6:254ra125
   PubMed Web of Science ®Google Scholar
• Enzalutamide with or without abiraterone and prednisone in treating patients with castration-resistant metastatic prostate cancer. Available from: https://clinicaltrials.gov/ct2/show/NCT01949337
   Google Scholar
• Taylor BS, Schultz N, Hieronymus H, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010;18:11-22
   PubMed Web of Science ®Google Scholar
• Kinkade CW, Castillio-Martin M, Puzio-Kuter A, et al. Targeting AKT/mTOR and ERK MAPK signaling inhibits hormone-refractory prostate cancer in a preclinical mouse model. J Clin Invest 2008;118:3051-64
   PubMed Web of Science ®Google Scholar
• Zhang W, Zhu J, Efferson CL, et al. Inhibition of tumor growth progression by antiandrogens and mTOR inhibitor in a PTEN-deficient mouse model of prostate cancer. Cancer Res 2009;69:7466-72
   PubMed Web of Science ®Google Scholar
• Carver BS, Chapinski C, Wongvipat J, et al. Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer. Cancer Cell 2011;19:575-86
   PubMed Web of Science ®Google Scholar
• Kruczek K, Ratterman M, Tolzien K, et al. A phase II study evaluating the toxicity and efficacy of single-agent temsirolimus in chemotherapy-naïve castration-resistant prostate cancer. Br J Cancer 2013;109:1711-16
   PubMed Web of Science ®Google Scholar
• Chee KG, Longmate J, Quinn DI, et al. The AKT inhibitor perifosine in biochemically recurrent prostate cancer: a phase II California/Pittsburgh cancer consortium trial. Clin Genitourin Cancer 2007;5:433-7
   PubMed Web of Science ®Google Scholar
• Armstrong AJ, Shen T, Halabi S, et al. A phase II trial of temsirolimus in men with castration-resistant metastatic prostate cancer. Clin Genitourin Cancer 2013;11:397-406
   PubMed Web of Science ®Google Scholar
• Stefanou D, Batistatou A, Kamina S, et al. Expression of vascular endothelial growth factor (VEGF) and association with microvessel density in benign prostatic hyperplasia and prostate cancer. In Vivo 2004;18(2):155-60
   PubMed Web of Science ®Google Scholar
• Weidner N, Carroll PR, Flax J, et al. Tumor angiogenesis correlates with metastasis in invasive prostate carcinoma. Am J Pathol 1993;143:401-9
   PubMed Web of Science ®Google Scholar
• Park HS, Hong SK, Oh MM, et al. Synergistic Antitumor effect of NVP-BEZ235 and sunitinib on docetaxel resistant human castration-resistant prostate cancer cells. Anticancer Res 2014;34:3457-68
   PubMed Web of Science ®Google Scholar
• Michaelson MD, Oudard S, Ou YC, et al. Randomized, placebo controlled, phase III trial of sunitinib plus prednisone versus prednisone alone in progressive, metastatic castration-resistant prostate cancer. J Clin Oncol 2014;32:76-82
   PubMed Web of Science ®Google Scholar
• Meulenbeld HJ, de Bono J, Tagawa ST, et al. Tolerability, safety and pharmacokinetics of ridaforolimus in combination with bicalutamide in patients with asymptomatic, metastatic castration-resistant prostate cancer (CRPC). Cancer Chemother Pharmacol 2013;72:909-16
   PubMed Web of Science ®Google Scholar
• Amato RJ, Wilding G, Bubley G, et al. Safety and preliminary efficacy analysis of the mTOR inhibitor ridaforolimus in patients with taxane-treated, castration-resistant prostate cancer. Clin Genitourin Cancer 2012;10:232-8
   PubMed Web of Science ®Google Scholar
• Templeton AJ, Dutoit V, Cathomas R, et al. Phase 2 trial of single-agent everolimus in chemotherapy-naive patients with castration-resistant prostate cancer (SAKK 08/08). Eur Urol 2013;64:150-8
   PubMed Web of Science ®Google Scholar
• Coffey K, Robson CN. Regulation of the androgen receptor by post-translational modifications. J Endocrinol 2012;215:221-37
   PubMed Web of Science ®Google Scholar
• Meulenbeld HJ, Bleuse JP, Vinci EM, et al. Randomized phase II study of danusertib in patients with metastatic castration-resistant prostate cancer after docetaxel failure. BJU Int 2013;111(1):44-52
   PubMed Web of Science ®Google Scholar
• Beltran H, Rickman DS, Park K, et al. Molecular characterization of neuroendocrine prostate cancer and identification of new drug targets. Cancer Discov 2011;1:487-95
   PubMed Web of Science ®Google Scholar
• A Phase II Trial of MLN8237 in patients with metastatic castrate resistant and neuroendocrine prostate cancer. Available from: https://clinicaltrials.gov/ct2/show/NCT01799278
   Google Scholar
• Alisertib, abiraterone acetate and prednisone in treating patients with hormone-resistant prostate cancer. Available from: https://clinicaltrials.gov/ct2/show/NCT01848067
   Google Scholar
• Heemers HV, Sebo TJ, Debes JD, et al. Androgen deprivation increases p300 expression in prostate cancer cells. Cancer Res 2007;67:3422-30
   PubMed Web of Science ®Google Scholar
• Santer FR, Hoschele PP, Oh SJ, et al. Inhibition of the acetyltransferases p300 and CBP reveals a targetable function for p300 in the survival and invasion pathways of prostate cancer cell lines. Mol Cancer Ther 2011;10:1644-55
   PubMed Web of Science ®Google Scholar
• Qin J, Lee HJ, Wu SP, et al. Androgen deprivation-induced NCoA2 promotes metastatic and castration-resistant prostate cancer. J Clin Invest 2014;124:5013-26
   PubMed Web of Science ®Google Scholar
• Obinata D, Takayama K, Urano T, et al. Oct1 regulates cell growth of LNCaP cells and is a prognostic factor for prostate cancer. Int J Cancer 2012;130:1021-8
   PubMed Web of Science ®Google Scholar
• Aggarwal R, Halabi S, Kelly WK, et al. The effect of prior androgen synthesis inhibition on outcomes of subsequent therapy with docetaxel in patients with metastatic castrate-resistant prostate cancer: results from a retrospective analysis of a randomized phase 3 clinical trial (CALGB 90401) (Alliance). Cancer 2013;119:3636-43
   PubMed Web of Science ®Google Scholar
• Mezynski J, Pezaro C, Bianchini D, et al. Antitumour activity of docetaxel following treatment with the CYP17A1 inhibitor abiraterone: clinical evidence for cross-resistance? Ann Oncol 2012;23:2943-7
   PubMed Web of Science ®Google Scholar
• Schweizer MT, Zhou XC, Wang H, et al. The Influence of Prior Abiraterone Treatment on the Clinical Activity of Docetaxel in Men with Metastatic Castration-resistant Prostate Cancer. Eur Urol 2014;66:646-52
   PubMed Web of Science ®Google Scholar
• Badrising S, van der Noort V, van Oort IM, et al. Clinical activity and tolerability of enzalutamide (MDV3100) in patients with metastatic, castration-resistant prostate cancer who progress after docetaxel and abiraterone treatment. Cancer 2014;120:968-75
   PubMed Web of Science ®Google Scholar
• Schrader AJ, Boegemann M, Ohlmann C-H, et al. Enzalutamide in Castration-resistant prostate cancer patients progressing after docetaxel and abiraterone. Europ Urol 2014;65:30-6
   PubMed Web of Science ®Google Scholar
• Zafeiriou Z, Ferraldeshi R, Omlin AG, et al. Sequencing of docetaxel and abiraterone acetate for metastatic castration-resistant prostate cancer (mCRPC). Ann Oncol 2014;25(Suppl 4):6360
   Google Scholar
• Noonan KL, Sorth S, Bitting RL, et al. Clinical activity of abiraterone acetate in patients with metastatic castration-resistant prostate cancer progressing after enzalutamide. Ann Oncol 2013;24:1802-7
   PubMed Web of Science ®Google Scholar
• Azad AA, Eigl BJ, Murray N, et al. Efficacy of Enzalutamide Following Abiraterone Acetate in Chemotherapy-naive Metastatic Castration-resistant Prostate Cancer Patients. Eur Urol 2015;67:23-9
   PubMed Web of Science ®Google Scholar
• Suzman DL, Luber B, Schweizer MT, et al. Clinical activity of enzalutamide versus docetaxel in men with castration-resistant prostate cancer progressing after abiraterone. Prostate 2014;74:1278-85
   PubMed Web of Science ®Google Scholar
• Cabazitaxel versus the switch to alternative AR targeted therapy enzalutamide or abiraterone in metastatic castration-resistant prostate cancer (mCRPC) primary resistant patients to abiraterone or Enz (PRIMCAB). Available from: https://clinicaltrials.gov/ct2/show/NCT02379390
   Google Scholar
• Kwon ED, Drake CG, Scher HI, et al. Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicenter, randomized, double-blind, phase 3 trial. Lancet Oncol 2014;15:700-12
   PubMed Web of Science ®Google Scholar
• Phase 3 study of immunotherapy to treat advanced prostate cancer. Available from: https://clinicaltrials.gov/ct2/show/NCT01057810
   Google Scholar
• Pembrolizumab in treating patients with metastatic castration resistant prostate cancer previously treated with enzalutamide. Available from: https://clinicaltrials.gov/ct2/show/NCT02312557
   Google Scholar
• Combining ipilimumab with abiraterone acetate plus prednisone in chemotherapy and immunotherapy-naïve patients with progressive metastatic castration-resistant prostate cancer. Available from: https://clinicaltrials.gov/ct2/show/NCT01688492
   Google Scholar
• Phase III study of DCVAC added to standard chemotherapy for men with metastatic castration resistant prostate cancer. Available from: https://clinicaltrials.gov/ct2/show/NCT02111577
   Google Scholar
• CYT107 with or without vaccine therapy in treating patients with metastatic hormone-resistant prostate cancer. Available from: https://clinicaltrials.gov/ct2/show/NCT01881867
   Google Scholar
• PROSTVAC®-VF/TRICOM™ vaccine for the treatment of metastatic prostate cancer after failing hormone therapy. Available from: https://clinicaltrials.gov/ct2/show/NCT00078585
   Google Scholar
• A Phase IB Trial With OTX015, a small molecule inhibitor of the bromodomain and extra-terminal (BET) proteins, in patients with selected advanced solid tumors. Available from: https://clinicaltrials.gov/ct2/show/NCT02259114
   Google Scholar
• Wuyce A, Degenhardt Y, Bai Y, et al. Inhibition of BET bromodomain proteins as a therapeutic approach in prostate cancer. Oncotarget 2013;4:2419-29
   PubMedGoogle Scholar
• Asangani IA, Dommeti VL, Wang X, et al. Therapeutic targeting of BET bromodomain proteins in castration-resistant prostate cancer. Nature 2014;510:278-82
   PubMed Web of Science ®Google Scholar
• Vasaitis T, Belosay A, Schayowitz A, et al. Androgen receptor inactivation contributes to antitumor efficacy of 17{alpha}-hydroxylase/17,20-lyase inhibitor 3beta-hydroxy-17-(1H-benzimidazole-1-yl)androsta-5,16-diene in prostate cancer. Mol Cancer Ther 2008;7:2348-57
   PubMed Web of Science ®Google Scholar
• Purushottamachar P, Godbole AM, Gediya LK, et al. Systematic structure modifications of multitarget prostate cancer drug candidate galeterone to produce novel androgen receptor down-regulating agents as an approach to treatment of advanced prostate cancer. J Med Chem 2013;56:48880-98
   Web of Science ®Google Scholar
• kwegyir-Afful AK, Ramalingam S, Purushottamachar P, et al. Clinical candidate galeterone (VN/124-1 or TOK-001) induces the degradation of full-length and splice variant androgen receptors in human prostate cancer cell lines via PI3K-Akt-Mdm2 pathway: implications for prostate cancer therapy. Cancer Res 2013;73(8 Suppl):1322
   Web of Science ®Google Scholar
• Taplin ME, Chi KN, Chu F, et al. Galeterone in 4 patient populations of men with CRPC: Results from ARMOR2. Annals of Oncology 2014;25(suppl_4):iv255-79
   Google Scholar
• Roberts J, Dhillon R, Dransfield D, et al. Androgen Receptor Modulation Optimized for Response in Splice Variant (ARMOR3-SV): Randomized, open-label, multicenter, controlled study of galeterone versus enzalutamide (enz) in men expressing AR-V7 splice variant (SV), metastatic castrate resistant prostate cancer (mCRPC). J Clin Oncol 2015;33(Suppl 7); abstr 259
   PubMed Web of Science ®Google Scholar
• Myung J-K, Banuelos CA, Fernandez JG, et al. An androgen receptor N-terminal domain antagonist for treating prostate cancer. J Clin Invest 2013;123:2948-60
   PubMed Web of Science ®Google Scholar
• Martin SK, Banuelos CA, Sadar MD, et al. N-terminal targeting of androgen receptor variant enhances response of castration resistant prostate cancer to taxane chemotherapy. Mol Oncol 2015;9:628-39
   Web of Science ®Google Scholar
• Montgomery RB, Antonarkis ES, Hussain M, et al. A phase 1/2 open-label study of safety and antitumor activity of EPI-506, a novel AR N-terminal domain inhibitor, in men with metastatic castration-resistant prostate cancer (mCRPC) with progression after enzalutamide or abiraterone. J Clin Oncol 2015;33(Suppl); abstr TPS5072
   Google Scholar