Metastatic castration-resistant prostate cancer: targeting the mechanisms of resistance to abiraterone acetate and enzalutamide

References

• Massard C, Fizazi K. Targeting continued androgen receptor signaling in prostate cancer. Clin Cancer Res 2011;17:3876-83
   PubMed Web of Science ®Google Scholar
• Garraway LA, Sellers WR. Lineage dependency and lineage-survival oncogenes in human cancer. Nat Rev Cancer 2006;6:593-602
   PubMed Web of Science ®Google Scholar
• Fizazi K, Scher HI, Molina A, et al. Abiraterone acetate for treatment of metastatic castration-resistant prostate cancer: final overall survival analysis of the COU-AA-301 randomised, double-blind, placebo-controlled phase 3 study. Lancet Oncol 2012;13:983-92
   PubMed Web of Science ®Google Scholar
• Ryan CJ, Smith MR, de Bono JS, et al. Abiraterone in metastatic prostate cancer without previous chemotherapy. N Engl J Med 2013;368:138-48
   PubMed Web of Science ®Google Scholar
• Ryan CJ, Smith MR, Fizazi K, et al. Abiraterone acetate plus prednisone versus placebo plus prednisone in chemotherapy-naive men with metastatic castration-resistant prostate cancer (COU-AA-302): final overall survival analysis of a randomised, double-blind, placebo-controlled phase 3 study. Lancet Oncol 2015;16:152-60
   PubMed Web of Science ®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
• Beer TM, 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
• Logothetis CJ, Gallick GE, Maity SN, et al. Molecular classification of prostate cancer progression: foundation for marker-driven treatment of prostate cancer. Cancer Discov 2013;3:849-61
   PubMed Web of Science ®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. Cancer Res 2008;68:4447-54
   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
• Chang KH, Li R, Kuri B, et al. A gain-of-function mutation in DHT synthesis in castration-resistant prostate cancer. Cell 2013;154:1074-84
   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 in bone. J Clin Oncol 2012;30:637-43
   PubMed Web of Science ®Google Scholar
• Donovan MJ, Osman I, Khan FM, et al. Androgen receptor expression is associated with prostate cancer-specific survival in castrate patients with metastatic disease. BJU Int 2010;105:462-7
   PubMed Web of Science ®Google Scholar
• Waltering KK, Urbanucci A, Visakorpi T. Androgen receptor (AR) aberrations in castration-resistant prostate cancer. Mol Cell Endocrinol 2012;360:38-43
   PubMed Web of Science ®Google Scholar
• Grasso CS, Wu YM, Robinson DR, et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 2012;487:239-43
   PubMed Web of Science ®Google Scholar
• Taplin ME, Bubley GJ, Ko YJ, et al. Selection for androgen receptor mutations in prostate cancers treated with androgen antagonist. Cancer Res 1999;59:2511-15
   PubMed Web of Science ®Google Scholar
• Taplin ME, Rajeshkumar B, Halabi S, et al. Androgen receptor mutations in androgen-independent prostate cancer: Cancer and Leukemia Group B Study 9663. J Clin Oncol 2003;21:2673-8
   PubMed Web of Science ®Google Scholar
• Gottlieb B, Beitel LK, Wu JH, Trifiro M. The androgen receptor gene mutations database (ARDB): 2004 update. Hum Mutat 2004;23:527-33
   PubMed Web of Science ®Google Scholar
• Zong Y, Goldstein AS. Adaptation or selection–mechanisms of castration-resistant prostate cancer. Nat Rev Urol 2013;10:90-8
   PubMed Web of Science ®Google Scholar
• Joseph JD, Lu N, Qian 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
• 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
• Clegg NJ, Wongvipat J, Joseph JD, et al. ARN-509: a novel antiandrogen for prostate cancer treatment. Cancer Res 2012;72:1494-503
   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
• Claessens F, Helsen C, Prekovic S, et al. Emerging mechanisms of enzalutamide resistance in prostate cancer. Nat Rev Urol 2014;11:712-16
   PubMed Web of Science ®Google Scholar
• Andersen RJ, Mawji NR, Wang J, et al. Regression of castrate-recurrent prostate cancer by a small-molecule inhibitor of the amino-terminus domain of the androgen receptor. Cancer Cell 2010;17:535-46
   PubMed Web of Science ®Google Scholar
• Dehm SM, Schmidt LJ, Heemers HV, et al. Splicing of a novel androgen receptor exon generates a constitutively active androgen receptor that mediates prostate cancer therapy resistance. Cancer Res 2008;68:5469-77
   PubMed Web of Science ®Google Scholar
• Sun S, Sprenger CC, Vessella RL, et al. Castration resistance in human prostate cancer is conferred by a frequently occurring androgen receptor splice variant. J Clin Invest 2010;120:2715-30
   PubMed Web of Science ®Google Scholar
• Yu Z, Chen S, Sowalsky AG, et al. Rapid induction of androgen receptor splice variants by androgen deprivation in prostate cancer. Clin Cancer Res 2014;20:1590-600
   PubMed Web of Science ®Google Scholar
• Zhang X, Morrissey C, Sun S, et al. Androgen receptor variants occur frequently in castration resistant prostate cancer metastases. PLoS One 2011;6:e27970
   PubMed Web of Science ®Google Scholar
• Bitting RL, Schaeffer D, Somarelli JA, et al. The role of epithelial plasticity in prostate cancer dissemination and treatment resistance. Cancer Metastasis Rev 2014;33:441-68
   PubMed Web of Science ®Google Scholar
• Cottard F, Asmane I, Erdmann E, et al. Constitutively active androgen receptor variants upregulate expression of mesenchymal markers in prostate cancer cells. PLoS One 2013;8:e63466
   Google Scholar
• Hornberg E, Ylitalo EB, Crnalic S, et al. Expression of androgen receptor splice variants in prostate cancer bone metastases is associated with castration-resistance and short survival. PLoS One 2011;6:e19059
   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
• Cao B, Qi Y, Zhang G, et al. Androgen receptor splice variants activating the full-length receptor in mediating resistance to androgen-directed therapy. Oncotarget 2014;5:1646-56
   PubMed Web of Science ®Google Scholar
• Taplin ME. Drug insight: role of the androgen receptor in the development and progression of prostate cancer. Nat Clin Pract Oncol 2007;4:236-44
   PubMedGoogle 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
• Watson PA, Chen YF, Balbas MD, et al. Constitutively active androgen receptor splice variants expressed in castration-resistant prostate cancer require full-length androgen receptor. Proc Natl Acad Sci USA 2010;107:16759-65
   PubMed Web of Science ®Google Scholar
• Antonarakis ES, Lu C, Chen Y, et al. AR splice variant 7 (AR-V7) and response to taxanes in men with metastatic castration-resistant prostate cancer (mCRPC). 2015 ASCO Meeting Abstracts 2015;33:138
   Google Scholar
• Nelson PS. Targeting the androgen receptor in prostate cancer–a resilient foe. N Engl J Med 2014;371:1067-9
   PubMed Web of Science ®Google Scholar
• Ravindranathan P, Lee TK, Yang L, et al. Peptidomimetic targeting of critical androgen receptor-coregulator interactions in prostate cancer. Nat Commun 2013;4:1923
   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
• Sahu B, Laakso M, Ovaska K, et al. Dual role of FoxA1 in androgen receptor binding to chromatin, androgen signalling and prostate cancer. EMBO J 2011;30:3962-76
   PubMed Web of Science ®Google Scholar
• Yan TZ, Jin FS, Xie LP, Li LC. Relationship between glucocorticoid receptor signal pathway and androgen-independent prostate cancer. Urol Int 2008;81:228-33
   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
• Davies P, Rushmere NK. Association of glucocorticoid receptors with prostate nuclear sites for androgen receptors and with androgen response elements. J Mol Endocrinol 1990;5:117-27
   PubMed Web of Science ®Google Scholar
• Scher HI, Fizazi K, Saad F, et al. Impact of on-study corticosteroid use on efficacy and safety in the phase III AFFIRM study of enzalutamide (ENZA), an androgen receptor inhibitor. ASCO Meeting Abstracts 2013;31:6
   Google Scholar
• Montgomery RB, Molina A, Li J, et al. Effect of corticosteroid (CS) use at baseline (CUB) on overall survival (OS) in patients (pts) receiving abiraterone acetate (AA): results from a randomized study (COU-AA-301) in metastatic castration-resistant prostate cancer (mCRPC) post-docetaxel (D). J Clin Oncol 2013;31
   Google Scholar
• Mulholland DJ, Jiao J, Wu H. Hormone refractory prostate cancer: Lessons learned from the PTEN prostate cancer model. Adv Exp Med Biol 2008;617:87-95
   PubMed Web of Science ®Google Scholar
• Mulholland DJ, Tran LM, Li Y, et al. Cell autonomous role of PTEN in regulating castration-resistant prostate cancer growth. Cancer Cell 2011;19:792-804
   PubMed Web of Science ®Google Scholar
• Thomas C, Lamoureux F, Crafter C, et al. Synergistic targeting of PI3K/AKT pathway and androgen receptor axis significantly delays castration-resistant prostate cancer progression in vivo. Mol Cancer Ther 2013;12:2342-55
   PubMed Web of Science ®Google Scholar
• Signoretti S, Montironi R, Manola J, et al. Her-2-neu expression and progression toward androgen independence in human prostate cancer. J Natl Cancer Inst 2000;92:1918-25
   PubMed Web of Science ®Google Scholar
• Yeh S, Lin HK, Kang HY, et al. From HER2/Neu signal cascade to androgen receptor and its coactivators: a novel pathway by induction of androgen target genes through MAP kinase in prostate cancer cells. Proc Natl Acad Sci USA 1999;96:5458-63
   PubMed Web of Science ®Google Scholar
• Wen Y, Hu MC, Makino K, et al. HER-2/neu promotes androgen-independent survival and growth of prostate cancer cells through the Akt pathway. Cancer Res 2000;60:6841-5
   PubMed Web of Science ®Google Scholar
• McDonnell TJ, Troncoso P, Brisbay SM, et al. Expression of the protooncogene bcl-2 in the prostate and its association with emergence of androgen-independent prostate cancer. Cancer Res 1992;52:6940-4
   PubMed Web of Science ®Google Scholar
• Debes JD, Tindall DJ. Mechanisms of androgen-refractory prostate cancer. N Engl J Med 2004;351:1488-90
   PubMed Web of Science ®Google Scholar
• Ammirante M, Luo JL, Grivennikov S, et al. B-cell-derived lymphotoxin promotes castration-resistant prostate cancer. Nature 2010;464:302-5
   PubMed Web of Science ®Google Scholar
• Jennbacken K, Tesan T, Wang W, et al. N-cadherin increases after androgen deprivation and is associated with metastasis in prostate cancer. Endocr Relat Cancer 2010;17:469-79
   PubMed Web of Science ®Google Scholar
• Wang L, Hsu CL, Chang C. Androgen receptor corepressors: an overview. Prostate 2005;63:117-30
   PubMed Web of Science ®Google Scholar
• Gregory CW, Fei X, Ponguta LA, et al. Epidermal growth factor increases coactivation of the androgen receptor in recurrent prostate cancer. J Biol Chem 2004;279:7119-30
   PubMed Web of Science ®Google Scholar
• Heemers HV, Tindall DJ. Androgen receptor (AR) coregulators: a diversity of functions converging on and regulating the AR transcriptional complex. Endocr Rev 2007;28:778-808
   PubMed Web of Science ®Google Scholar
• Gioeli D, Paschal BM. Post-translational modification of the androgen receptor. Mol Cell Endocrinol 2012;352:70-8
   PubMed Web of Science ®Google Scholar
• Kumar A, White TA, MacKenzie AP, et al. Exome sequencing identifies a spectrum of mutation frequencies in advanced and lethal prostate cancers. Proc Natl Acad Sci USA 2011;108:17087-92
   PubMed Web of Science ®Google Scholar
• TOPARP: A phase II trial of olaparib in patients with advanced castration resistant prostate cancer. Available from: https://clinicaltrials.gov/ct2/show/NCT01682772
   Google Scholar
• Efstathiou TM, Tsavachidou D, Karlou HM, et al. MDV3100 effects on androgen receptor (AR) signaling and bone marrow testosterone concentration modulation: a preliminary report. J Clin Oncol 2011;29
   PubMed Web of Science ®Google Scholar
• Cai C, Chen S, Ng P, et al. Intratumoral de novo steroid synthesis activates androgen receptor in castration-resistant prostate cancer and is upregulated by treatment with CYP17A1 inhibitors. Cancer Res 2011;71:6503-13
   PubMed Web of Science ®Google Scholar
• Schrader AJ, Boegemann M, Ohlmann CH, et al. Enzalutamide in castration-resistant prostate cancer patients progressing after docetaxel and abiraterone. Eur Urol 2014;65:30-6
   PubMed Web of Science ®Google Scholar
• Loriot Y, Bianchini D, Ileana E, et al. Antitumour activity of abiraterone acetate against metastatic castration-resistant prostate cancer progressing after docetaxel and enzalutamide (MDV3100). Ann Oncol 2013;24:1807-12
   PubMed Web of Science ®Google Scholar
• Noonan KL, North 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
• Caffo O, De Giorgi U, Fratino L, et al. Clinical outcomes of castration-resistant prostate cancer treatments administered as third or fourth line following failure of docetaxel and other second-line treatment: results of an Italian multicentre study. Eur Urol 2014
   Web of Science ®Google Scholar
• van Soest RJ, de Morrèe ES, Moll JM, et al. Cross-resistance between taxanes and new hormonal agents abiraterone and enzalutamide may affect drug sequence choices in metastatic castration-resistant prostate cancer. Eur J Cancer 2013;49:3821-30
   PubMed Web of Science ®Google Scholar
• Loriot Y, Fizazi K. Towards random sequencing or precision medicine in castration-resistant prostate cancer? Eur Urol 2014;65:37-8
   PubMed Web of Science ®Google Scholar
• Antonarakis ES, Eisenberger MA. Phase III trials with docetaxel-based combinations for metastatic castration-resistant prostate cancer: time to learn from past experiences. J Clin Oncol 2013;31:1709-12
   PubMed Web of Science ®Google Scholar
• Glickman MS, Sawyers CL. Converting cancer therapies into cures: lessons from infectious diseases. Cell 2012;148:1089-98
   PubMed Web of Science ®Google Scholar
• Sadar MD, Williams DE, Mawji NR, et al. Sintokamides A to E, chlorinated peptides from the sponge Dysidea sp. that inhibit transactivation of the N-terminus of the androgen receptor in prostate cancer cells. Org Lett 2008;10:4947-50
   PubMed Web of Science ®Google Scholar
• Myung JK, 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
• Thompson TC. Grappling with the androgen receptor: a new approach for treating advanced prostate cancer. Cancer Cell 2010;17:525-6
   PubMed Web of Science ®Google Scholar
• Sadar MD. Small molecule inhibitors targeting the ‘Achilles’ heel’ of androgen receptor activity. Cancer Res 2011;71:1208-13
   PubMed Web of Science ®Google Scholar
• Liu C, Lou W, Zhu Y, et al. Niclosamide inhibits androgen receptor variants expression and overcomes enzalutamide resistance in castration-resistant prostate cancer. Clin Cancer Res 2014;20:3198-210
   PubMed Web of Science ®Google Scholar
• Rathkopf DE, Morris MJ, Fox JJ, et al. Phase I study of ARN-509, a novel antiandrogen, in the treatment of castration-resistant prostate cancer. J Clin Oncol 2013;31:3525-30
   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
• Nakka M, Agoulnik IU, Weigel NL. Targeted disruption of the p160 coactivator interface of androgen receptor (AR) selectively inhibits AR activity in both androgen-dependent and castration-resistant AR-expressing prostate cancer cells. Int J Biochem Cell Biol 2013;45:763-72
   PubMed Web of Science ®Google Scholar
• Bohrer LR, Liu P, Zhong J, et al. FOXO1 binds to the TAU5 motif and inhibits constitutively active androgen receptor splice variants. Prostate 2013;73:1017-27
   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
• Centenera MM, Gillis JL, Hanson AR, et al. Evidence for efficacy of new Hsp90 inhibitors revealed by ex vivo culture of human prostate tumors. Clin Cancer Res 2012;18:3562-70
   PubMed Web of Science ®Google Scholar
• A Service of the U.S. National Institutes of Health, Clinicaltrials.gov. Available from: https://www.clinicaltrials.gov/
   Google Scholar
• A study to determine safety and tolerability of enzalutamide (mdv3100) in combination with abiraterone acetate in bone metastatic castration-resistant prostate cancer patients. Available from: https://clinicaltrials.gov/ct2/show/NCT01650194
   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
• A 2 part, phase 2 trial of galeterone in the treatment of castration resistant prostate cancer (ARMOR2). Available from: https://clinicaltrials.gov/ct2/show/NCT01709734
   Google Scholar
• Safety, tolerability, pharmacokinetics, and preliminary anti-tumor activity of ascending doses of arn 509 in combination with abiraterone acetate. Available from: https://clinicaltrials.gov/ct2/show/NCT01792687
   Google Scholar
• Safety, pharmacokinetic and proof-of-concept study of arn-509 in castration-resistant prostate cancer (CRPC). Available from: https://clinicaltrials.gov/ct2/show/NCT01171898
   Google Scholar
• A study of hsp90 inhibitor at13387 alone or in combination with abiraterone acetate. Available from: https://clinicaltrials.gov/ct2/show/NCT01685268
   Google Scholar
• BKM120 in Metastatic castration-resistant prostate cancer. Available from: https://clinicaltrials.gov/ct2/show/NCT01385293
   Google Scholar
• Phase Ib of abiraterone acetate plus bez235 or bkm120 in castration-resistant prostate cancer (CRPC) patients. Available from: https://clinicaltrials.gov/ct2/show/NCT01634061
   Google Scholar
• Ph II study to evaluate olaparib with abiraterone in treating metastatic castration resistant prostate cancer. Available from: https://clinicaltrials.gov/ct2/show/NCT01972217
   Google Scholar