Molecular classifi cation of prostate cancer progression: Foundation for marker-driven treatment of prostate cancer

Cancer Discovery

Volumn 3, Issue 8, 2013, Pages 849-861

  Logothetis, Christopher J ^a   Gallick, Gary E ^a   Maity, Sankar N ^a   Kim, Jeri ^a   Aparicio, Ana ^a   Efstathiou, Eleni ^a   Lin, Sue Hwa ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABIRATERONE; ANDROSTANOLONE; ANTINEOPLASTIC AGENT; CABOZANTINIB; DANUSERTIB; DUTASTERIDE; FINASTERIDE; MVD 3100; PROSTATE SPECIFIC ANTIGEN; PROTEIN P53; UNCLASSIFIED DRUG; ANDROGEN RECEPTOR; AR PROTEIN, HUMAN; TUMOR MARKER;

ADENOCARCINOMA; CANCER CHEMOTHERAPY; CANCER CLASSIFICATION; CANCER GROWTH; CANCER SURVIVAL; CASTRATION RESISTANT PROSTATE CANCER; CELL INVASION; CELL PROLIFERATION; CELL SURVIVAL; CIRCULATING TUMOR CELL; CLINICAL TRIAL (TOPIC); DRUG EFFICACY; HUMAN; METASTASIS; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; PROSTATE CANCER; REVIEW; TUMOR MICROENVIRONMENT; CLASSIFICATION; DISEASE COURSE; DRUG DEVELOPMENT; GENETICS; MALE; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PATHOPHYSIOLOGY; PROSTATE TUMOR; TREATMENT OUTCOME; PROSTATIC NEOPLASMS;

ANTINEOPLASTIC AGENTS; DISEASE PROGRESSION; DRUG DISCOVERY; HUMANS; MALE; MOLECULAR TARGETED THERAPY; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL; TUMOR MICROENVIRONMENT;

EID: 84881505886     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-12-0460     Document Type: Review

References (96)

1. Gleason DF. Classifi cation of prostatic carcinomas. Cancer Chemother Rep 1966; 50: 125-8.
2. Gleason DF, Mellinger GT. Prediction of prognosis for prostatic adenocarcinoma by combined histological grading and clinical staging. J Urol 1974; 111: 58-64.
3. Ryan CJ, Smith A, Lal P, Satagopan J, Reuter V, Scardino P, et al. Persistent prostate-specifi c antigen expression after neoadjuvant androgen depletion: an early predictor of relapse or incomplete androgen suppression. Urology 2006; 68: 834-9.
4. McKenney JK, Simko J, Bonham M, True LD, Troyer D, Hawley S, et al. The potential impact of reproducibility of Gleason grading in men with early stage prostate cancer managed by active surveillance: a multi-institutional study. J Urol 2011; 186: 465-9.
5. Gravis G, Fizazi K, Joly F, Oudard S, Priou F, Esterni B, et al. Androgendeprivation therapy alone or with docetaxel in non-castrate metastatic prostate cancer (GETUG-AFU 15): a randomised, open-label, phase 3 trial. Lancet Oncol 2013; 14: 149-58.
6. Efstathiou E, Abrahams NA, Tibbs RF, Wang X, Pettaway CA, Pisters LL, et al. Morphologic characterization of preoperatively treated prostate cancer: toward a post-therapy histologic classifi cation. Eur Urol 2010; 57: 1030-8.
7. Efstathiou E, Logothetis CJ. A new therapy paradigm for prostate cancer founded on clinical observations. Clin Cancer Res 2010; 16: 1100-7.
8. Millikan RE, Wen S, Pagliaro LC, Brown MA, Moomey B, Do KA, et al. Phase III trial of androgen ablation with or without three cycles of systemic chemotherapy for advanced prostate cancer. J Clin Oncol 2008; 26: 5936-42.
9. Loberg RD, Gayed BA, Olson KB, Pienta KJ. A paradigm for the treatment of prostate cancer bone metastases based on an understanding of tumor cell-microenvironment interactions. J Cell Biochem 2005; 96: 439-46.
10. Logothetis CJ, Lin SH. Osteoblasts in prostate cancer metastasis to bone. Nat Rev Cancer 2005; 5: 21-8.
11. Attard G, Richards J, de Bono JS. New strategies in metastatic prostate cancer: targeting the androgen receptor signaling pathway. Clin Cancer Res 2011; 17: 1649-57.
12. de Bono JS, Logothetis CJ, Molina A, Fizazi K, North S, Chu L, et al. Abiraterone and increased survival in metastatic prostate cancer. N Engl J Med 2011; 364: 1995-2005.
13. Wang Q, Li W, Zhang Y, Yuan X, Xu K, Yu J, et al. Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 2009; 138: 245-56.
14. Efstathiou E, Titus M, Tsavachidou D, Tzelepi V, Wen S, Hoang A, et al. Effects of abiraterone acetate on androgen signaling in castrate-resistant prostate cancer in bone. J Clin Oncol 2012; 30: 637-43.
15. Mostaghel EA, Marck BT, Plymate SR, Vessella RL, Balk S, Matsumoto AM, 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.
16. Grasso CS, Wu YM, Robinson DR, Cao X, Dhanasekaran SM, Khan AP, et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 2012; 487: 239-43.
17. Aparicio A, Den RB, Knudsen KE. Time to stratify? The retinoblastoma protein in castrate-resistant prostate cancer. Nat Rev Urol 2011; 8: 562-8.
18. Udayakumar T, Shareef MM, Diaz DA, Ahmed MM, Pollack A. The E2F1/Rb and p53/MDM2 pathways in DNA repair and apoptosis: understanding the crosstalk to develop novel strategies for prostate cancer radiotherapy. Semin Radiat Oncol 2010; 20: 258-66.
19. 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.
20. Lotan TL, Gurel B, Sutcliffe S, Esopi D, Liu W, Xu J, et al. PTEN protein loss by immunostaining: analytic validation and prognostic indicator for a high risk surgical cohort of prostate cancer patients. Clin Cancer Res 2011; 17: 6563-73.
21. Verras M, Lee J, Xue H, Li TH, 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: 967-75.
22. Yu J, Akishita M, Eto M, Koizumi H, Hashimoto R, Ogawa S, et al. Src kinase-mediates androgen receptor-dependent non-genomic activation of signaling cascade leading to endothelial nitric oxide synthase. Biochem Biophys Res Commun 2012; 424: 538-43.
23. Liu Y, Karaca M, Zhang Z, Gioeli D, Earp HS, Whang YE. Dasatinib inhibits site-specifi c tyrosine phosphorylation of androgen receptor by Ack1 and Src kinases. Oncogene 2010; 29: 3208-16.
24. Gioeli D, Ficarro SB, Kwiek JJ, Aaronson D, Hancock M, Catling AD, et al. Androgen receptor phosphorylation. Regulation and identifi cation of the phosphorylation sites. J Biol Chem 2002; 277: 29304-14.
25. Ponguta LA, Gregory CW, French FS, Wilson EM. Site-specifi c androgen receptor serine phosphorylation linked to epidermal growth factor-dependent growth of castration-recurrent prostate cancer. J Biol Chem 2008; 283: 20989-1001.
26. Nilsson S, Strang P, Aksnes AK, Franzen L, Olivier P, Pecking A, et al. A randomized, dose-response, multicenter phase II study of radium-223 chloride for the palliation of painful bone metastases in patients with castration-resistant prostate cancer. Eur J Cancer 2012; 48: 678-86.
27. Shelley MD, Mason MD. Radium-223 for men with hormone-refractory prostate cancer and bone metastases. Lancet Oncol 2007; 8: 564-5.
28. Tu SM, Millikan RE, Mengistu B, Delpassand ES, Amato RJ, Pagliaro LC, et al. Bone-targeted therapy for advanced androgen-independent carcinoma of the prostate: a randomised phase II trial. Lancet 2001; 357: 336-41.
29. Russell DW, Wilson JD. Steroid 5 alpha-reductase: two genes/two enzymes. Annu Rev Biochem 1994; 63: 25-61.
30. Sharifi N. The 5alpha-androstanedione pathway to dihydrotestosterone in castration-resistant prostate cancer. J Invest Med 2012; 60: 504-7.
31. Thompson IM, Goodman PJ, Tangen CM, Lucia MS, Miller GJ, Ford LG, et al. The infl uence of fi nasteride on the development of prostate cancer. N Engl J Med 2003; 349: 215-24.
32. Andriole GL, Bostwick DG, Brawley OW, Gomella LG, Marberger M, Montorsi F, et al. Effect of dutasteride on the risk of prostate cancer. N Engl J Med 2010; 362: 1192-202.
33. Fleshner NE, Lucia MS, Egerdie B, Aaron L, Eure G, Nandy I, et al. Dutasteride in localised prostate cancer management: the REDEEM randomised, double-blind, placebo-controlled trial. Lancet 2012; 379: 1103-11.
34. Roehrborn CG, Andriole GL, Wilson TH, Castro R, Rittmaster RS. Effect of dutasteride on prostate biopsy rates and the diagnosis of prostate cancer in men with lower urinary tract symptoms and enlarged prostates in the Combination of Avodart and Tamsulosin trial. Eur Urol 2011; 59: 244-9.
35. Lin TM, Chang C. Cloning and characterization of TDD5, an androgen target gene that is differentially repressed by testosterone and dihydrotestosterone. Proc Natl Acad Sci U S A 1997; 94: 4988-93.
36. Dadras SS, Cai X, Abasolo I, Wang Z. Inhibition of 5alpha-reductase in rat prostate reveals differential regulation of androgen-response gene expression by testosterone and dihydrotestosterone. Gene Expr 2001; 9: 183-94.
37. Li J, Ding Z, Wang Z, Lu JF, Maity SN, Navone NM, et al. Androgen regulation of 5alpha-reductase isoenzymes in prostate cancer: implications for prostate cancer prevention. PLoS ONE 2011; 6: e28840.
38. Mitsiades N, Sung CC, Schultz N, Danila DC, He B, Eedunuri VK, et al. Distinct patterns of dysregulated expression of enzymes involved in androgen synthesis and metabolism in metastatic prostate cancer tumors. Cancer Res 2012; 72: 6142-52.
39. Mostaghel EA, Geng L, Holcomb I, Coleman IM, Lucas J, True LD, et al. Variability in the androgen response of prostate epithelium to 5alpha-reductase inhibition: implications for prostate cancer chemoprevention. Cancer Res 2010; 70: 1286-95.
40. Kim J, Amos CI, Logothetis C. 5alpha-Reductase inhibitors for prostatecancer prevention. N Engl J Med 2011; 365: 2340.
41. Shen MM, Abate-Shen C. Molecular genetics of prostate cancer: new prospects for old challenges. Genes Dev 2010; 24: 1967-2000.
42. Gallick GE, Corn PG, Zurita AJ, Lin SH. Small-molecule protein tyrosine kinase inhibitors for the treatment of metastatic prostate cancer. Future Med Chem 2012; 4: 107-19.
43. Deocampo ND, Huang H, Tindall DJ. The role of PTEN in the progression and survival of prostate cancer. Minerva Endocrinol 2003; 28: 145-53.
44. Zhu ML, Kyprianou N. Role of androgens and the androgen receptor in epithelial-mesenchymal transition and invasion of prostate cancer cells. FASEB J 2010; 24: 769-77.
45. Jennbacken K, Tesan T, Wang W, Gustavsson H, Damber JE, Welen K. N-cadherin increases after androgen deprivation and is associated with metastasis in prostate cancer. Endocr Relat Cancer 2010; 17: 469-79.
46. Lee YC, Cheng CJ, Huang M, Bilen MA, Ye X, Navone NM, et al. Androgen depletion up-regulates cadherin-11 expression in prostate cancer. J Pathol 2010; 221: 68-76.
47. Taplin ME, Balk SP. Androgen receptor: a key molecule in the progression of prostate cancer to hormone independence. J Cell Biochem 2004; 91: 483-90.
48. Scher HI, Fizazi K, Saad F, Taplin ME, Sternberg CN, Miller K, et al. Increased survival with enzalutamide in prostate cancer after chemotherapy. N Engl J Med 2012; 367: 1187-97.
49. Zhao XY, Malloy PJ, Krishnan AV, Swami S, Navone NM, Peehl DM, et al. Glucocorticoids can promote androgen-independent growth of prostate cancer cells through a mutated androgen receptor. Nat Med 2000; 6: 703-6.
50. Andersen RJ, Mawji NR, Wang J, Wang G, Haile S, Myung JK, 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.
51. Hu R, Dunn TA, Wei S, Isharwal S, Veltri RW, Humphreys E, et al. Ligand-independent androgen receptor variants derived from splicing of cryptic exons signify hormone-refractory prostate cancer. Cancer Res 2009; 69: 16-22.
52. Hu R, Lu C, Mostaghel EA, Yegnasubramanian S, Gurel M, Tannahill C, et al. Distinct transcriptional programs mediated by the liganddependent full-length androgen receptor and its splice variants in castration-resistant prostate cancer. Cancer Res 2012; 72: 3457-62.
53. Sun S, Sprenger CC, Vessella RL, Haugk K, Soriano K, Mostaghel EA, 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.
54. Cai C, He HH, Chen S, Coleman I, Wang H, Fang Z, et al. Androgen receptor gene expression in prostate cancer is directly suppressed by the androgen receptor through recruitment of lysine-specifi c demethylase 1. Cancer Cell 2011; 20: 457-71.
55. Tanaka H, Kono E, Tran CP, Miyazaki H, Yamashiro J, Shimomura T, et al. Monoclonal antibody targeting of N-cadherin inhibits prostate cancer growth, metastasis and castration resistance. Nat Med 2010; 16: 1414-20.
56. Smith DC, Smith MR, Sweeney C, Elfi ky 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.
57. Cai H, Babic I, Wei X, Huang J, Witte ON. Invasive prostate carcinoma driven by c-Src and androgen receptor synergy. Cancer Res 2011; 71: 862-72.
58. Gleave M, Hsieh JT, Gao CA, von Eschenbach AC, Chung LW. Acceleration of human prostate cancer growth in vivo by factors produced by prostate and bone fi broblasts. Cancer Res 1991; 51: 3753-61.
59. Wu TT, Sikes RA, Cui Q, Thalmann GN, Kao C, Murphy CF, et al. Establishing human prostate cancer cell xenografts in bone: induction of osteoblastic reaction by prostate-specifi c antigen-producing tumors in athymic and SCID/bg mice using LNCaP and lineagederived metastatic sublines. Int J Cancer 1998; 77: 887-94.
60. Thalmann GN, Sikes RA, Wu TT, Degeorges A, Chang SM, Ozen M, et al. LNCaP progression model of human prostate cancer: androgenindependence and osseous metastasis. Prostate 2000; 44: 91-103.
61. Lee YC, Cheng CJ, Bilen MA, Lu JF, Satcher RL, Yu-Lee LY, et al. BMP4 promotes prostate tumor growth in bone through osteogenesis. Cancer Res 2011; 71: 5194-203.
62. Dai J, Keller J, Zhang J, Lu Y, Yao Z, Keller ET. Bone morphogenetic protein-6 promotes osteoblastic prostate cancer bone metastases through a dual mechanism. Cancer Res 2005; 65: 8274-85.
63. Dai J, Kitagawa Y, Zhang J, Yao Z, Mizokami A, Cheng S, et al. Vascular endothelial growth factor contributes to the prostate cancerinduced osteoblast differentiation mediated by bone morphogenetic protein. Cancer Res 2004; 64: 994-9.
64. Kitagawa Y, Dai J, Zhang J, Keller JM, Nor J, Yao Z, et al. Vascular endothelial growth factor contributes to prostate cancer-mediated osteoblastic activity. Cancer Res 2005; 65: 10921-9.
65. Li ZG, Mathew P, Yang J, Starbuck MW, Zurita AJ, Liu J, et al. Androgen receptor-negative human prostate cancer cells induce osteogenesis in mice through FGF9-mediated mechanisms. J Clin Invest 2008; 118: 2697-710.
66. Chen N, Ye XC, Chu K, Navone NM, Sage EH, Yu-Lee LY, e t al. A secreted isoform of ErbB3 promotes osteonectin expression in bone and enhances the invasiveness of prostate cancer cells. Cancer Res 2007; 67: 6544-8.
67. Jacob K, Webber M, Benayahu D, Kleinman HK. Osteonectin promotes prostate cancer cell migration and invasion: a possible mechanism for metastasis to bone. Cancer Res 1999; 59: 4453-7.
68. Chen G, Sircar K, Aprikian A, Potti A, Goltzman D, Rabbani SA. Expression of RANKL/RANK/OPG in primary and metastatic human prostate cancer as markers of disease stage and functional regulation. Cancer 2006; 107: 289-98.
69. Jung K, Lein M, Stephan C, Von Hosslin K, Semjonow A, Sinha P, et al. Comparison of 10 serum bone turnover markers in prostate carcinoma patients with bone metastatic spread: diagnostic and prognostic implications. Int J Cancer 2004; 111: 783-91.
70. Saad F, Lipton A. Bone-marker levels in patients with prostate cancer: potential correlations with outcomes. Curr Opin Support Palliat Care 2010; 4: 127-34.
71. Oreffo RO, Mundy GR, Seyedin SM, Bonewald LF. Activation of the bone-derived latent TGF beta complex by isolated osteoclasts. Biochem Biophys Res Commun 1989; 158: 817-23.
72. Abrahamsson PA. Neuroendocrine differentiation in prostatic carcinoma. Prostate 1999; 39: 135-48.
73. Clegg N, Ferguson C, True LD, Arnold H, Moorman A, Quinn JE, et al. Molecular characterization of prostatic small-cell neuroendocrine carcinoma. Prostate 2003; 55: 55-64.
74. Tetu B, Ro JY, Ayala AG, Johnson DE, Logothetis CJ, Ordonez NG. Small cell carcinoma of the prostate. Part I. A clinicopathologic study of 20 cases. Cancer 1987; 59: 1803-9.
75. Humphrey PA. Histological variants of prostatic carcinoma and their signifi cance. Histopathology 2012; 60: 59-74.
76. Aparicio A, Tzelepi V, Araujo JC, Guo CC, Liang S, Troncoso P, et al. Neuroendocrine prostate cancer xenografts with large-cell and small-cell features derived from a single patient's tumor: morphological, immunohistochemical, and gene expression profi les. Prostate 2011; 71: 846-56.
77. Guo CC, Wang Y, Xiao L, Troncoso P, Czerniak BA. The relationship of TMPRSS2-ERG gene fusion between primary and metastatic prostate cancers. Hum Pathol 2012; 43: 644-9.
78. Mosquera JM, Mehra R, Regan MM, Perner S, Genega EM, Bueti G, et al. Prevalence of TMPRSS2-ERG fusion prostate cancer among men undergoing prostate biopsy in the United States. Clin Cancer Res 2009; 15: 4706-11.
79. Aparicio A, Logothetis CJ, Maity SN. Understanding the lethal variant of prostate cancer: power of examining extremes. Cancer Discov 2011; 1: 466-8.
80. Beltran H, Rickman DS, Park K, Chae SS, Sboner A, MacDonald TY, et al. Molecular characterization of neuroendocrine prostate cancer and identifi cation of new drug targets. Cancer Discov 2011; 1: 487-95.
81. Qin J, Liu X, Laffin B, Chen X, Choy G, Jeter CR, et al. The PSA(-/lo) prostate cancer cell population harbors self-renewing long-term tumor-propagating cells that resist castration. Cell Stem Cell 2012; 10: 556-69.
82. Deeraksa A, Pan J, Sha Y, Liu XD, Eissa NT, Lin SH, e t al. Plk1 is upregulated in androgen-insensitive prostate cancer cells and its inhibition leads to necroptosis. Oncogene. 2012 Aug 13. [Epub ahead of print]
83. Mosquera JM, Beltran H, Park K, Macdonald TY, Robinson BD, Tagawa ST, et al. Concurrent AURKA and MYCN gene amplifi cations are harbingers of lethal treatment-related neuroendocrine prostate cancer. Neoplasia 2013; 15: 1-10.
84. Otto T, Horn S, Brockmann M, Eilers U, Schuttrumpf 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.
85. 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.
86. Weichert W, Schmidt M, Gekeler V, Denkert C, Stephan C, Jung K, et al. Polo-like kinase 1 is overexpressed in prostate cancer and linked to higher tumor grades. Prostate 2004; 60: 240-5.
87. Liu XS, Song B, Elzey BD, Ratliff TL, Konieczny SF, Cheng L, et al. Polo-like kinase 1 facilitates loss of Pten tumor suppressorinduced prostate cancer formation. J Biol Chem 2011; 286: 35795-800.
88. Wang W, Epstein JI. Small cell carcinoma of the prostate. A morphologic and immunohistochemical study of 95 cases. Am J Surg Pathol 2008; 32: 65-71.
89. 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.
90. Reagan-Shaw S, Ahmad N. Polo-like kinase (Plk) 1 as a target for prostate cancer management. IUBMB Life 2005; 57: 677-82.
91. Luo J, Liu X. Polo-like kinase 1, on the rise from cell cycle regulation to prostate cancer development. Protein Cell 2012; 3: 182-97.
92. Eckerdt F, Yuan J, Strebhardt K. Polo-like kinases and oncogenesis. Oncogene 2005; 24: 267-76.
93. Schoffski 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 fi rst protocol of the European Organization for Research and Treatment of Cancer (EORTC) Network Of Core Institutes (NOCI). Eur J Cancer 2010; 46: 2206-15.
94. Schoffski 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.
95. Beltran H, Rubin MA. New strategies in prostate cancer: translating genomics into the clinic. Clin Cancer Res 2013; 19: 517-23.
96. Sowalsky AG, Ye H, Bubley GJ, Balk SP. Clonal progression of prostate cancers from Gleason grade 3 to grade 4. Cancer Res 2013; 73: 1050-5.