Targeting neuroendocrine prostate cancer: Molecular and clinical perspectives

Frontiers in Oncology

Volumn 5, Issue FEB, 2015, Pages

  Vlachostergios, Panagiotis J ^a   Papandreou, Christos N ^b  

^a LUTHERAN MEDICAL CENTER   (United States)

^b UNIVERSITY OF THESSALY   (Greece)

Author keywords

Androgen independent; Castration resistant; Neuroendocrine prostate cancer; Small cell prostate carcinoma; Targeted therapy

Indexed keywords

ANDROGEN RECEPTOR; AURORA KINASE INHIBITOR; BIOLOGICAL MARKER; BONE MORPHOGENETIC PROTEIN 6; CARCINOEMBRYONIC ANTIGEN; CD56 ANTIGEN; CHROMOGRANIN; FOCAL ADHESION KINASE; GELATINASE B; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 6; LACTATE DEHYDROGENASE; MESSENGER RNA; NEURON RESTRICTIVE SILENCER FACTOR; OSTEOCLAST DIFFERENTIATION FACTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PIGMENT EPITHELIUM DERIVED FACTOR; PROSTATE SPECIFIC ANTIGEN; PROTEIN P53; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; RETINOBLASTOMA BINDING PROTEIN 1; STAT3 PROTEIN; STEM CELL FACTOR; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG;

ANDROGEN DEPRIVATION THERAPY; CANCER MORPHOLOGY; CANCER RESISTANCE; DOWN REGULATION; ENDOCRINE TUMOR; EPIGENETIC REPRESSION; GENE MUTATION; HUMAN; MITOSIS; MOLECULARLY TARGETED THERAPY; NONHUMAN; NUCLEAR REPROGRAMMING; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROSTATE CANCER; REVIEW; TUMOR DIFFERENTIATION; TUMOR MICROENVIRONMENT; TUMOR SUPPRESSOR GENE;

EID: 84923225609     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2015.00006     Document Type: Review

References (75)

1. Papandreou CN, Daliani DD, Thall PF, Tu SM, Wang X, Reyes A, et al. Results of a phase II study with doxorubicin, etoposide, and cisplatin in patients with fully characterized small-cell carcinoma of the prostate. J Clin Oncol (2002) 20:3072-80. doi:10.1200/JCO.2002.12.065
2. Epstein JI, Amin MB, Beltran H, Lotan TL, Mosquera JM, Reuter VE, et al. Proposed morphologic classification of prostate cancer with neuroendocrine differentiation. Am J Surg Pathol (2014) 38:756-67. doi:10.1097/PAS.0000000000000208
3. Culine S, El Demery M, Lamy PJ, Iborra F, Avancès C, Pinguet F. Docetaxel and cisplatin in patients with metastatic androgen independent prostate cancer and circulating neuroendocrine markers. J Urol (2007) 178:844. doi:10.1016/j.juro.2007.05.044
4. Aparicio AM, Harzstark AL, Corn PG, Wen S, Araujo JC, Tu SM, et al. Platinum-based chemotherapy for variant castrate-resistant prostate cancer. Clin Cancer Res (2013) 19:3621-30. doi:10.1158/1078-0432.CCR-12-3791
5. Kani K, Malihi PD, Jiang Y, Wang H, Wang Y, Ruderman DL, et al. Anterior gradient 2 (AGR2): blood-based biomarker elevated in metastatic prostate cancer associated with the neuroendocrine phenotype. Prostate (2013) 73:306-15. doi:10.1002/pros.22569
6. Rapa I, Volante M, Migliore C, Farsetti A, Berruti A, Vittorio Scagliotti G, et al. Human ASH-1 promotes neuroendocrine differentiation in androgen deprivation conditions and interferes with androgen responsiveness in prostate cancer cells. Prostate (2013) 73:1241-9. doi:10.1002/pros.22679
7. Surcel CI, van Oort IM, Sooriakumaran P, Briganti A, De Visschere PJ, Fütterer JJ, et al. Prognostic effect of neuroendocrine differentiation in prostate cancer: a critical review. Urol Oncol (2014). doi:10.1016/j.urolonc.2014.08.007
8. Logothetis CJ, Gallick GE, Maity SN, Kim J, Aparicio A, Efstathiou E, et al. Molecular classification of prostate cancer progression: foundation for marker-driven treatment of prostate cancer. Cancer Discov (2013) 3:849-61. doi:10.1158/2159-8290.CD-12-0460
9. Terry S, Beltran H. The many faces of neuroendocrine differentiation in prostate cancer progression. Front Oncol (2014) 4:60. doi:10.3389/fonc.2014.00060
10. Chen H, Sun Y, Wu C, Magyar CE, Li X, Cheng L, et al. Pathogenesis of prostatic small cell carcinoma involves the inactivation of the P53 pathway. Endocr Relat Cancer (2012) 19:321-31. doi:10.1530/ERC-11-0368
11. Li Z, Chen CJ, Wang JK, Hsia E, Li W, Squires J, et al. Neuroendocrine differentiation of prostate cancer. Asian J Androl (2013) 15:328-32. doi:10.1038/aja.2013.7
12. Tan HL, Sood A, Rahimi HA, Wang W, Gupta N, Hicks J, et al. Rb loss is characteristic of prostatic small cell neuroendocrine carcinoma. Clin Cancer Res (2014) 20:890-903. doi:10.1158/1078-0432.CCR-13-1982
13. Lens SM, Voest EE, Medema RH. Shared and separate functions of polo-like kinases and aurora kinases in cancer. Nat Rev Cancer (2010) 10:825-41. doi:10.1038/nrc2964
14. Deeraksa A, Pan J, Sha Y, Liu XD, Eissa NT, Lin SH, et al. Plk1 is upregulated in androgen-insensitive prostate cancer cells and its inhibition leads to necroptosis. Oncogene (2013) 32:2973-83. doi:10.1038/onc.2012.309
15. Mosquera JM, Beltran H, Park K, MacDonald TY, Robinson BD, Tagawa ST, et al. Concurrent AURKA and MYCN gene amplifications are harbingers of lethal treatment-related neuroendocrine prostate cancer. Neoplasia (2013) 15:1-10. doi:10.1593/neo.121550
16. Otto T, Horn S, Brockmann M, Eilers U, Schüttrumpf L, Popov N, et al. Stabilization of N-Myc is a critical function of Aurora A in human neuroblastoma. Cancer Cell (2009) 15:67-78. doi:10.1016/j.ccr.2008.12.005
17. Wang J, Kim J, Roh M, Franco OE, Hayward SW, Wills ML, et al. Pim1 kinase synergizes with c-MYC to induce advanced prostate carcinoma. Oncogene (2010) 29:2477-87. doi:10.1038/onc.2010.10
18. Tzelepi V, Zhang J, Lu JF, Kleb B, Wu G, Wan X, et al. Modeling a lethal prostate cancer variant with small-cell carcinoma features. Clin Cancer Res (2012) 18:666-77. doi:10.1158/1078-0432.CCR-11-1867
19. Lapuk AV, Wu C, Wyatt AW, McPherson A, McConeghy BJ, Brahmbhatt S, et al. From sequence to molecular pathology, and a mechanism driving the neuroendocrine phenotype in prostate cancer. J Pathol (2012) 227:286-97. doi:10.1002/path.4047
20. Svensson C, Ceder J, Iglesias-Gato D, Chuan YC, Pang ST, Bjartell A, et al. REST mediates androgen receptor actions on gene repression and predicts early recurrence of prostate cancer. Nucleic Acids Res (2014) 42:999-1015. doi:10.1093/nar/gkt921
21. Terry S, Maillé P, Baaddi H, Kheuang L, Soyeux P, Nicolaiew N, et al. Cross modulation between the androgen receptor axis and protocadherin-PC in mediating neuroendocrine transdifferentiation and therapeutic resistance of prostate cancer. Neoplasia (2013) 15:761-72. doi:10.1593/neo.122070
22. Yang X, Chen MW, Terry S, Vacherot F, Chopin DK, Bemis DL, et al. A human- and male-specific protocadherin that acts through the wnt signaling pathway to induce neuroendocrine transdifferentiation of prostate cancer cells. Cancer Res (2005) 65:5263-71. doi:10.1158/0008-5472.CAN-05-0162
23. Chang PC, Wang TY, Chang YT, Chu CY, Lee CL, Hsu HW, et al. Autophagy pathway is required for IL-6 induced neuroendocrine differentiation and chemoresistance of prostate cancer LNCaP cells. PLoS One (2014) 9:e88556. doi:10.1371/journal.pone.0088556
24. Asangani IA, Dommeti VL, Wang X, Malik R, Cieslik M, Yang R, et al. Therapeutic targeting of BET bromodomain proteins in castration-resistant prostate cancer. Nature (2014) 510:278-82. doi:10.1038/nature13229
25. Wee ZN, Li Z, Lee PL, Lee ST, Lim YP, Yu Q. EZH2-mediated inactivation of IFN-γ-JAK-STAT1 signaling is an effective therapeutic target in MYC-driven prostate cancer. Cell Rep (2014) 8:204-16. doi:10.1016/j.celrep.2014.05.045
26. Lee SO, Chun JY, Nadiminty N, Lou W, Gao AC. Interleukin-6 undergoes transition from growth inhibitor associated with neuroendocrine differentiation to stimulator accompanied by androgen receptor activation during LNCaP prostate cancer cell progression. Prostate (2007) 67:764-73. doi:10.1002/pros.20553
27. Smith ND, Schulze-Hoepfner FT, Veliceasa D, Filleur S, Shareef S, Huang L, et al. Pigment epithelium-derived factor and interleukin-6 control prostate neuroendocrine differentiation via feed-forward mechanism. J Urol (2008) 179:2427-34. doi:10.1016/j.juro.2008.01.081
28. Jin RJ, Lho Y, Connelly L, Wang Y, Yu X, Saint Jean L, et al. The nuclear factor-kappaB pathway controls the progression of prostate cancer to androgen-independent growth. Cancer Res (2008) 68:6762-9. doi:10.1158/0008-5472.CAN-08-0107
29. Tawadros T, Alonso F, Jichlinski P, Clarke N, Calandra T, Haefliger JA, et al. Release of macrophage migration inhibitory factor by neuroendocrine-differentiated LNCaP cells sustains the proliferation and survival of prostate cancer cells. Endocr Relat Cancer (2013) 20:137-49. doi:10.1530/ERC-12-0286
30. Slack-Davis JK, Hershey ED, Theodorescu D, Frierson HF, Parsons JT. Differential requirement for focal adhesion kinase signaling in cancer progression in the transgenic adenocarcinoma of mouse prostate model. Mol Cancer Ther (2009) 8:2470-7. doi:10.1158/1535-7163.MCT-09-0262
31. Qi J, Nakayama K, Cardiff RD, Borowsky AD, Kaul K, Williams R, et al. Siah2-dependent concerted activity of HIF and FoxA2 regulates formation of neuroendocrine phenotype and neuroendocrine prostate tumors. Cancer Cell (2010) 18:23-38. doi:10.1016/j.ccr.2010.05.024
32. Danza G, Di Serio C, Rosati F, Lonetto G, Sturli N, Kacer D, et al. Notch signaling modulates hypoxia-induced neuroendocrine differentiation of human prostate cancer cells. Mol Cancer Res (2012) 10:230-8. doi:10.1158/1541-7786.MCR-11-0296
33. Pittoni P, Tripodo C, Piconese S, Mauri G, Parenza M, Rigoni A, et al. Mast cell targeting hampers prostate adenocarcinoma development but promotes the occurrence of highly malignant neuroendocrine cancers. Cancer Res (2011) 71:5987-97. doi:10.1158/0008-5472.CAN-11-1637
34. Pittoni P, Colombo MP. The dark side of mast cell-targeted therapy in prostate cancer. Cancer Res (2012) 72:831-5. doi:10.1158/0008-5472.CAN-11-3110
35. McKeithen D, Graham T, Chung LW, Odero-Marah V. Snail transcription factor regulates neuroendocrine differentiation in LNCaP prostate cancer cells. Prostate (2010) 70:982-92. doi:10.1002/pros.21132
36. Smith BN, Odero-Marah VA. The role of Snail in prostate cancer. Cell Adh Migr (2012) 6:433-41. doi:10.4161/cam.21687
37. Berenguer C, Boudouresque F, Dussert C, Daniel L, Muracciole X, Grino M, et al. Adrenomedullin, an autocrine/paracrine factor induced by androgen withdrawal, stimulates 'neuroendocrine phenotype' in LNCaP prostate tumor cells. Oncogene (2008) 27:506-18. doi:10.1038/sj.onc.1210656
38. Vlaeminck-Guillem V, Gillet G, Rimokh R. SRC: marker or actor in prostate cancer aggressiveness. Front Oncol (2014) 4:222. doi:10.3389/fonc.2014.00222
39. Salah Z, Maoz M, Pizov G, Bar-Shavit R. Transcriptional regulation of human protease-activated receptor 1: a role for the early growth response-1 protein in prostate cancer. Cancer Res (2007) 67:9835-43. doi:10.1158/0008-5472.CAN-07-1886
40. DaSilva J, Gioeli D, Weber MJ, Parsons SJ. The neuroendocrine-derived peptide parathyroid hormone-related protein promotes prostate cancer cell growth by stabilizing the androgen receptor. Cancer Res (2009) 69:7402-11. doi:10.1158/0008-5472.CAN-08-4687
41. Lee GT, Kwon SJ, Lee JH, Jeon SS, Jang KT, Choi HY, et al. Macrophages induce neuroendocrine differentiation of prostate cancer cells via BMP6-IL6 loop. Prostate (2011) 71:1525-37. doi:10.1002/pros.21369
42. Chu GC, Zhau HE, Wang R, Rogatko A, Feng X, Zayzafoon M, et al. RANK- and c-Met-mediated signal network promotes prostate cancer metastatic colonization. Endocr Relat Cancer (2014) 21:311-26. doi:10.1530/ERC-13-0548
43. Hashimoto K, Masumori N, Tanaka T, Maeda T, Kobayashi K, Kitamura H, et al. Zoledronic acid but not somatostatin analogs exerts anti-tumor effects in a model of murine prostatic neuroendocrine carcinoma of the development of castration-resistant prostate cancer. Prostate (2013) 73:500-11. doi:10.1002/pros.22590
44. Choi SY, Gout PW, Collins CC, Wang Y. Epithelial immune cell-like transition (EIT): a proposed transdifferentiation process underlying immune-suppressive activity of epithelial cancers. Differentiation (2012) 83:293-8. doi:10.1016/j.diff.2012.02.005
45. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med (2010) 363:411-22. doi:10.1056/NEJMoa1001294
46. Meulenbeld HJ, Bleuse JP, Vinci EM, Raymond E, Vitali G, Santoro A, et al. Randomized phase II study of danusertib in patients with metastatic castration-resistant prostate cancer after docetaxel failure. BJU Int (2013) 111:44-52. doi:10.1111/j.1464-410X.2012.11404.x
47. Aparicio A, Logothetis CJ, Maity SN. Understanding the lethal variant of prostate cancer: power of examining extremes. Cancer Discov (2011) 1:466-8. doi:10.1158/2159-8290.CD-11-0259
48. Beltran H, Rubin MA. New strategies in prostate cancer: translating genomics into the clinic. Clin Cancer Res (2013) 19:517-23. doi:10.1158/1078-0432.CCR-12-1452
49. Yu EY, Wilding G, Posadas E, Gross M, Culine S, Massard C, et al. Phase II study of dasatinib in patients with metastatic castration-resistant prostate cancer. Clin Cancer Res (2009) 15:7421-8. doi:10.1158/1078-0432.CCR-09-1691
50. Araujo JC, Trudel GC, Saad F, Armstrong AJ, Yu EY, Bellmunt J, et al. Docetaxel and dasatinib or placebo in men with metastatic castration-resistant prostate cancer (READY): a randomised, double-blind phase 3 trial. Lancet Oncol (2013) 14:1307-16. doi:10.1016/S1470-2045(13)70479-0
51. Schöffski P, Blay JY, De Greve J, Brain E, Machiels JP, Soria JC, et al. Multicentric parallel phase II trial of the polo-like kinase 1 inhibitor BI 2536 in patients with advanced head and neck cancer, breast cancer, ovarian cancer, soft tissue sarcoma and melanoma. The first protocol of the European Organization for Research and Treatment of Cancer (EORTC) Network of Core Institutes (NOCI). Eur J Cancer (2010) 46:2206-15. doi:10.1016/j.ejca.2010.03.039
52. Schöffski P, Awada A, Dumez H, Gil T, Bartholomeus S, Wolter P, et al. A phase I, dose-escalation study of the novel Polo-like kinase inhibitor volasertib (BI 6727) in patients with advanced solid tumours. Eur J Cancer (2012) 48:179-86. doi:10.1016/j.ejca.2011.11.001
53. Beltran H, Tomlins S, Aparicio A, Arora V, Rickman D, Ayala G, et al. Aggressive variants of castration-resistant prostate cancer. Clin Cancer Res (2014) 20:2846-50. doi:10.1158/1078-0432.CCR-13-3309
54. Smith DC, Smith MR, Sweeney C, Elfiky AA, Logothetis C, Corn PG, et al. Cabozantinib in patients with advanced prostate cancer: results of a phase II randomized discontinuation trial. J Clin Oncol (2013) 31:412-9. doi:10.1200/JCO.2012.45.0494
55. Available from: http://www.exelixis.com/investors-media/press-releases
56. Molife LR, Yan L, Vitfell-Rasmussen J, Zernhelt AM, Sullivan DM, Cassier PA, et al. Phase 1 trial of the oral AKT inhibitor MK-2206 plus carboplatin/paclitaxel, docetaxel, or erlotinib in patients with advanced solid tumors. J Hematol Oncol (2014) 7:1. doi:10.1186/1756-8722-7-1
57. Carducci MA, Saad F, Abrahamsson PA, Dearneley DP, Schulman CC, North SA, et al. A phase 3 randomized controlled trial of the efficacy and safety of atrasentan in men with metastatic hormone-refractory prostate cancer. Cancer (2007) 110:1959-66. doi:10.1002/cncr.22996
58. Nelson JB, Love W, Chin JL, Saad F, Schulman CC, Sleep DJ, et al. Phase 3, randomized, controlled trial of atrasentan in patients with nonmetastatic, hormone-refractory prostate cancer. Cancer (2008) 113:2478-87. doi:10.1002/cncr.23864
59. Quinn DI, Tangen CM, Hussain M, Lara PN Jr, Goldkorn A, Moinpour CM, et al. Docetaxel and atrasentan versus docetaxel and placebo for men with advanced castration-resistant prostate cancer (SWOG S0421): a randomised phase 3 trial. Lancet Oncol (2013) 14:893-900. doi:10.1016/S1470-2045(13)70294-8
60. Nelson JB, Fizazi K, Miller K, Higano C, Moul JW, Akaza H, et al. Phase 3, randomized, placebo-controlled study of zibotentan (ZD4054) in patients with castration-resistant prostate cancer metastatic to bone. Cancer (2012) 118:5709-18. doi:10.1002/cncr.27674
61. Fizazi KS, Higano CS, Nelson JB, Gleave M, Miller K, Morris T, et al. Phase III, randomized, placebo-controlled study of docetaxel in combination with zibotentan in patients with metastatic castration-resistant prostate cancer. J Clin Oncol (2013) 31:1740-7. doi:10.1200/JCO.2012.46.4149
62. Wang S, Sun W, Zhao Y, McEachern D, Meaux I, Barrière C, et al. SAR405838: an optimized inhibitor of MDM2-p53 interaction that induces complete and durable tumor regression. Cancer Res (2014) 74:5855-65. doi:10.1158/0008-5472.CAN-14-0799
63. Zhao J, Zhang Z, Liao Y, Du W. Mutation of the retinoblastoma tumor suppressor gene sensitizes cancers to mitotic inhibitor induced cell death. Am J Cancer Res (2014) 4:42-52.
64. Kim J, Roh M, Abdulkadir SA. Pim1 promotes human prostate cancer cell tumorigenicity and c-MYC transcriptional activity. BMC Cancer (2010) 10:248. doi:10.1186/1471-2407-10-248
65. Holder S, Zemskova M, Zhang C, Tabrizizad M, Bremer R, Neidigh JW, et al. Characterization of a potent and selective small-molecule inhibitor of the PIM1 kinase. Mol Cancer Ther (2007) 6:163-72. doi:10.1158/1535-7163.MCT-06-0397
66. Kroon P, Berry PA, Stower MJ, Rodrigues G, Mann VM, Simms M, et al. JAK-STAT blockade inhibits tumor initiation and clonogenic recovery of prostate cancer stem-like cells. Cancer Res (2013) 73:5288-98. doi:10.1158/0008-5472.CAN-13-0874
67. Meyer-Siegler KL, Iczkowski KA, Leng L, Bucala R, Vera PL. Inhibition of macrophage migration inhibitory factor or its receptor (CD74) attenuates growth and invasion of DU-145 prostate cancer cells. J Immunol (2006) 177:8730-9. doi:10.4049/jimmunol.177.12.8730
68. Lee BY, Hochgräfe F, Lin HM, Castillo L, Wu J, Raftery MJ, et al. Phosphoproteomic profiling identifies focal adhesion kinase as a mediator of docetaxel resistance in castrate-resistant prostate cancer. Mol Cancer Ther (2014) 13:190-201. doi:10.1158/1535-7163.MCT-13-0225-T
69. Lin AM, Rini BI, Derynck MK, Weinberg V, Park M, Ryan CJ, et al. A phase I trial of docetaxel/estramustine/imatinib in patients with hormone-refractory prostate cancer. Clin Genitourin Cancer (2007) 5:323-8. doi:10.3816/CGC.2007.n.011
70. Bajaj GK, Zhang Z, Garrett-Mayer E, Drew R, Sinibaldi V, Pili R, et al. Phase II study of imatinib mesylate in patients with prostate cancer with evidence of biochemical relapse after definitive radical retropubic prostatectomy or radiotherapy. Urology (2007) 69:526-31. doi:10.1016/j.urology.2006.12.006
71. Lin AM, Rini BI, Weinberg V, Fong K, Ryan CJ, Rosenberg JE, et al. A phase II trial of imatinib mesylate in patients with biochemical relapse of prostate cancer after definitive local therapy. BJU Int (2006) 98:763-9. doi:10.1111/j.1464-410X.2006.06396.x
72. Michaelson MD, Oudard S, Ou YC, Sengeløv L, Saad F, Houede N, 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. doi:10.1200/JCO.2012.48.5268
73. Safarinejad MR. Safety and efficacy of sorafenib in patients with castrate resistant prostate cancer: a phase II study. Urol Oncol (2010) 28:21-7. doi:10.1016/j.urolonc.2008.06.003
74. Soria JC, Massard C, Magné N, Bader T, Mansfield CD, Blay JY, et al. Phase 1 dose-escalation study of oral tyrosine kinase inhibitor masitinib in advanced and/or metastatic solid cancers. Eur J Cancer (2009) 45:2333-41. doi:10.1016/j.ejca.2009.05.010
75. Baritaki S, Yeung K, Palladino M, Berenson J, Bonavida B. Pivotal roles of Snail inhibition and RKIP induction by the proteasome inhibitor NPI-0052 in tumor cell chemoimmunosensitization. Cancer Res (2009) 69:8376-85. doi:10.1158/0008-5472.CAN-09-1069