« Back Urologic Oncology: Seminars and Original Investigations

Article in Press

The ubiquitin-proteasome system in prostate cancer and its transition to castration resistance

Received 22 December 2009 ,Revised 16 March 2010 ,Accepted 18 March 2010. Published online 28 June 2010 Corrected Proof

References 

  1. Delongchamps NB, Singh A, Haas GP. The role of prevalence in the diagnosis of prostate cancer. Cancer Control. 2006;13:158–168
  2. Sakr WA, Grignon DJ, Crissman JD, et al. High grade prostatic intraepithelial neoplasia (HGPIN) and prostatic adenocarcinoma between the ages of 20 and 69: An autopsy study of 249 cases. In Vivo. 1994;8:439–444
  3. Loblaw DA, Virgo KS, Nam R, et al. Initial hormonal management of androgen-sensitive metastatic, recurrent, or progressive prostate cancer: 2007 update of an American Society of Clinical Oncology practice guideline. J Clin Oncol. 2007;25:1596–1605
  4. de Leval J, Boca P, Yousef E, et al. Intermittent versus continuous total androgen blockade in the treatment of patients with advanced hormone-naive prostate cancer: Results of a prospective randomized multicenter trial. Clin Prostate Cancer. 2002;1:163–171
  5. Patterson SG, Balducci L, Pow-Sang JM. Controversies surrounding androgen deprivation for prostate cancer. Cancer Control. 2002;9:315–325
  6. Horwich A, Huddart RA, Gadd J, et al. A pilot study of intermittent androgen deprivation in advanced prostate cancer. Br J Urol. 1998;81:96–99
  7. Feldman BJ, Feldman D. The development of androgen-independent prostate cancer. Nat Rev Cancer. 2001;1:34–45
  8. Yeh S, Lin H-K, Kang H-Y, 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;96:5458–5463
  9. Nazareth LV, Weigel NL. Activation of the human androgen receptor through a protein kinase A signaling pathway. J Biol Chem. 1996;271:19900–19907
  10. Marcelli M, Ittmann M, Mariani S, et al. Androgen receptor mutations in prostate cancer. Cancer Res. 2000;60:944–949
  11. Koivisto P, Kononen J, Palmberg C, et al. Androgen receptor gene amplification: A possible molecular mechanism of androgen deprivation therapy failure in prostate cancer. Cancer Res. 1997;57:314–319
  12. Wen Y, Hu MC-T, Makino K, et al. HER-2/neu promotes androgen-independent survival and growth of prostate cancer cells through the akt pathway. Cancer Res. 2000;60:6841–6845
  13. Mani A, Gelmann EP. The ubiquitin-proteasome pathway and its role in cancer. J Clin Oncol. 2005;23:4776–4789
  14. Almond JB, Cohen GM. The proteasome: A novel target for cancer chemotherapy. Leukemia. 2002;16:433–443
  15. Voutsadakis IA. Pathogenesis of colorectal carcinoma and therapeutic implications: The roles of the ubiquitin-proteasome system and Cox-2. J Cell Mol Med. 2007;11:252–285
  16. Wolf DH, Hilt W. The proteasome: A proteolytic nanomachine of cell regulation and waste disposal. Biochim Biophys Acta. 2004;1695:19–31
  17. Rechsteiner M. The 26S Proteasome. In:  Mayer RJ,  Ciechanover A,  Rechsteiner M editor. Protein degradation. Weinheim: Wiley-VCH Verlag; 2005;p. 220–47
  18. Vodermaier HC. APC/C and SCF: Controlling each other and the cell cycle. Curr Biol. 2004;14:R787–R796
  19. Hershko A. Mechanisms and regulation of the degradation of cyclin B. Phil Trans R Soc London B. 1999;354:1571–1576
  20. Sun X-M, Butterworth M, MacFarlane M, et al. Caspase activation inhibits proteasome function during apoptosis. Mol Cell. 2004;14:81–93
  21. Adrain C, Creagh EM, Cullen SP, et al. Caspase-dependent inactivation of proteasome function during programmed cell death in drosophila and man. J Biol Chem. 2004;279:36923–36930
  22. Friedman J, Xue D. To live or die by the sword: The regulation of apoptosis by the proteasome. Dev Cell. 2004;7:460–461
  23. Li B, Dou QP. Bax degradation by the ubiquitin/proteasome-dependent pathway: Involvement in tumor survival and progression. Proc Natl Acad Sci USA. 2000;97:3850–3855
  24. Zoubeidi A, Zardan A, Beraldi E, et al. Cooperative interactions between androgen receptor (AR) and heat-shock protein 27 facilitate AR transcriptional activity. Cancer Res. 2007;67:10455–10465
  25. Buchanan G, Ricciardelli C, Harris JM, et al. Control of androgen receptor signaling in prostate cancer by the cochaperone small glutamine-rich tetratricopeptide repeat containing protein α. Cancer Res. 2007;67:10087–10096
  26. Yong W, Yang Z, Periyasamy S, et al. Essential role for co-chaperone Fkbp52 but not Fkbp51 in androgen receptor-mediated signaling and physiology. J Biol Chem. 2007;282:5026–5036
  27. Hassan S, Biswas MHU, Zhang C, et al. Heat shock protein 27 mediates repression of androgen receptor function by protein kinase D1 in prostate cancer cells. Oncogene. 2009;28:4386–4396
  28. Nelson PS, Clegg N, Arnold H, et al. The program of androgen-responsive genes in neoplastic prostate epithelium. Proc Natl Acad Sci USA. 2002;99:11890–11895
  29. Huang W, Shostak Y, Tarr P, et al. Cooperative assembly of androgen receptor into a nucleoprotein complex that regulates the prostate-specific antigen enhancer. J Biol Chem. 1999;274:25756–25768
  30. Claessens F, Denayer S, Van Tilborgh N, et al. Diverse roles of androgen receptor (AR) domains in AR-mediated signaling. Nuclear Receptor Signaling. 2008;6:e008
  31. Moore SM, Nelson PS. Gene expression profiling of the human prostate androgen response program. J Androl. 2002;23:163–169
  32. Holzbeierlein J, Lal P, LaTulippe E, et al. Gene expression analysis of human prostate carcinoma during hormonal therapy identifies androgen-responsive genes and mechanisms of therapy resistance. Am J Pathol. 2004;164:217–227
  33. Chandra S, Shao J, Li JX, et al. A common motif targets Huntingtin and the androgen receptor to the proteasome. J Biol Chem. 2008;283:23950–23955
  34. Jaworski T. Degradation and beyond: Control of androgen receptor activity by the proteasome system. Cell Mol Biol Lett. 2006;11:109–131
  35. Voutsadakis IA. PPARγ and colorectal carcinogenesis. J Cancer Res Clin Oncol. 2007;133:917–928
  36. Kinyamu HK, Chen J, Archer TK. Linking the ubiquitin-proteasome pathway to chromatin remodeling/modification by nuclear receptors. J Mol Endocrinol. 2005;34:281–297
  37. Kinyamu HK, Jefferson WN, Archer TK. Intersection of nuclear receptors and the proteasome on the epigenetic landscape. Environ Mol Mutagen. 2008;49:83–95
  38. Rochette-Egly C. Dynamic combinatorial networks in nuclear receptor-mediated transcription. J Biol Chem. 2005;280:32565–32568
  39. Lonard DM, Lanz RB, O'Malley BW. Nuclear receptor co-regulators and human disease. Endocr Rev. 2007;28:575–587
  40. Chen P-H, Tsao Y-P, Wang C-C, et al. Nuclear receptor interaction protein, a coactivator of androgen receptors (AR), is regulated by AR and Sp1 to feed forward and activate its own gene expression through AR protein stability. Nucleic Acids Res. 2008;36:51–66
  41. Jenster G, Spencer TE, Burcin MM, et al. Steroid receptor induction of gene transcription: A two-step model. Proc Natl Acad Sci USA. 1997;94:7879–7884
  42. Zhang Y. Transcriptional regulation by histone ubiquitination and de-ubiquitination. Genes Dev. 2003;17:2733–2740
  43. Dover J, Schneider J, Tawiah-Boateng MA, et al. Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J Biol Chem. 2002;277:28368–28371
  44. Sun ZW, Allis CD. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature. 2002;418:104–108
  45. Laribee RN, Fuchs SM, Strahl BD. H2B ubiquitination in transcriptional control: A FACT-finding mission. Genes Dev. 2007;21:737–743
  46. Ezhkova E, Tansey WP. Proteasomal ATPases link ubiquitylation of histone H2B to methylation of histone H3. Mol Cell. 2004;13:435–442
  47. Logan IR, Gaughan L, McCracken SRC, et al. Human PIRH2 enhances androgen receptor signaling through inhibition of histone deacetylase 1 and is overexpressed in prostate cancer. Mol Cell Biol. 2006;26:6502–6510
  48. Boeger H, Bushnell DA, Davis R, et al. Structural basis of eukaryotic gene transcription. FEBS Lett. 2005;579:899–903
  49. Boeger H, Griesenbeck J, Strattan JS, et al. Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Mol Cell. 2004;14:667–673
  50. Perissi V, Scafoglio C, Zhang J, et al. TBL1 and TBLR1 phosphorylation on regulated gene promoters overcomes dual CtBP and NCoR/SMRT transcriptional repression checkpoints. Mol Cell. 2008;29:755–766
  51. Gaughan L, Logan IR, Neal DE, et al. Regulation of androgen receptor and histone deacetylase 1 by mdm2-mediated ubiquitylation. Nucleic Acids Res. 2005;33:13–26
  52. Ramamoorthy S, Nawaz Z. E6-associated protein (E6-AP) is a dual function coactivator of steroid hormone receptors. Nuclear Receptor Signaling. 2008;6:e006
  53. Vijayvargia R, May MS, Fondell JD. A co-regulatory role for the mediator complex in prostate cancer cell proliferation and gene expression. Cancer Res. 2007;67:4034–4041
  54. Conaway RC, Brower CS, Conaway JW. Emerging roles of ubiquitin in transcriptional regulation. Science. 2002;296:1254–1258
  55. Burgdorf S, Leister P, Scheidtmann KH. TSG101 interacts with apoptosis-antagonizing transcription factor and enhances androgen receptor-mediated transcription by promoting its mono-ubiquitination. J Biol Chem. 2004;279:17524–17534
  56. Kang Z, Pirskanen A, Jänne OA, et al. Involvement of proteasome in the dynamic assembly of the androgen receptor transcription complex. J Biol Chem. 2002;277:48366–48371
  57. Tyagi RK, Lavrovsky Y, Ahn SC, et al. Dynamics of intracellular movement and nucleocytoplasmic recycling of the ligand-activated androgen receptor in living cells. Mol Endocrinol. 2000;14:1162–1174
  58. Page ST, Lin DW, Mostaghel EA, et al. Persistent intraprostatic androgen concentrations after medical castration in healthy men. J Clin Endocrinol Metab. 2006;91:3850–3856
  59. Moehler JL, Gregory CW, Ford OH, et al. The androgen axis in recurrent prostate cancer. Clin Cancer Res. 2004;10:440–448
  60. Harris WP, Mostaghel EA, Nelson PS, et al. Androgen deprivation therapy: Progress in understanding mechanisms of resistance and optimizing androgen depletion. Nat Clin Pract Urol. 2009;6:76–85
  61. Pienta KJ, Bradley D. Mechanisms underlying the development of androgen-independent prostate cancer. Clin Cancer Res. 2006;12:1665–1671
  62. Balk SP, Knudsen KE. AR, the cell cycle, and prostate cancer. Nuclear Receptor Signaling. 2008;6:e001
  63. Chen CD, Welsbie DS, Tran C, et al. Molecular determinants of resistance to antiandrogen therapy. Nat Med. 2004;10:33–39
  64. Gregory CW, He B, Johnson RT, et al. A mechanism for androgen receptor-mediated prostate cancer recurrence after androgen deprivation therapy. Cancer Res. 2001;61:4315–4319
  65. Shah RB, Mehra R, Chinnaiyan AM, et al. Androgen-independent prostate cancer is a heterogeneous group of diseases: Lessons from a rapid autopsy program. Cancer Res. 2004;64:9209–9216
  66. Gregory CW, Johnson RT, Mohler JL, et al. Androgen receptor stabilization in recurrent prostate cancer is associated with hypersensitivity to low androgen. Cancer Res. 2001;61:2892–2898
  67. Nanus DM. Of peptides and peptidases: The role of cell surface peptidases in cancer. Clin Cancer Res. 2003;9:6307–6309
  68. Sumitomo M, Shen R, Nanus DM. Involvement of neutral endopeptidase in neoplastic progression. Biochim Biophys Acta. 2005;1751:52–59
  69. Pinet F. À quoi sert le système endothéline?. Med Sci. 2004;20:339–345
  70. Papandreou CN, Usmani B, Geng Y, et al. Neutral endopeptidase 24.11 loss in metastatic human prostate cancer contributes to androgen-independent progression. Nat Med. 1998;4:50–57
  71. Osman I, Dai J, Mikhail M, et al. Loss of neutral endopeptidase and activation of protein kinase B (Akt) is associated with prostate cancer progression. Cancer. 2006;107:2628–2636
  72. Shen R, Dai J, Sumitomo M, et al. Identification and characterization of two androgen response regions in the human neutral endopeptidase gene. Mol Cell Endocrinol. 2000;170:131–142
  73. Shen R, Sumitomo M, Dai J, et al. Androgen-induced growth inhibition of androgen receptor expressing androgen-independent prostate cancer cells is mediated by increased levels of neutral endopeptidase. Endocrinol. 2000;141:1699–1704
  74. Levine L, Lucci JA, Pazdrak B, et al. Bombesin stimulates nuclear factor κB activation and expression of proangiogenic factors in prostate cancer cells. Cancer Res. 2003;63:3495–3502
  75. Sumitomo M, Shen R, Walburg M, et al. Neutral endopeptidase inhibits prostate cancer cell migration by blocking focal adhesion kinase signaling. J Clin Invest. 2000;106:1399–1407
  76. Sumitomo M, Iwase A, Zheng R, et al. Synergy in tumor suppression by direct interaction of neutral endopeptidase with PTEN. Cancer Cell. 2004;5:67–78
  77. Sumitomo M, Asano T, Asakuma J, et al. Chemosensitization of androgen-independent prostate cancer with neutral endopeptidase. Clin Cancer Res. 2004;10:260–266
  78. Patrikidou A, Voutsadakis IA, Karagiannaki A, et al. Inverse relationship between NEP expression, proteasomal activity and NF-κB activation in androgen-dependent and independent prostate cancer, with evidence of existence of a neuropeptide-inducible link. Proceedings of the ASCO Genitourinary Cancers Symposium, San Francisco, CA, February, 2008. p.134 [Abstract 78].
  79. Srivastava J, Procyk KJ, Iturrioz X, et al. Phosphorylation is required for PMA- and cell-cycle-induced degradation of protein kinase Cδ. Biochem J. 2002;368:349–355
  80. Adachi M, Katsumura KR, Fujii K, et al. Proteasome-dependent decrease in Akt by growth factors in vascular smooth muscle cells. FEBS Lett. 2003;554:77–80
  81. Dai J, Shen R, Sumitomo M, et al. Synergistic activation of the androgen receptor by bombesin and low-dose androgen. Clin Cancer Res. 2002;8:2399–2405
  82. Osman I, Yee H, Taneja SS, et al. Neutral endopeptidase protein expression and prognosis in localized prostate cancer. Clin Cancer Res. 2004;10:4096–4100
  83. Santer FR, Bacher N, Moser B, et al. Nuclear insulin-like growth factor binding protein-3 induces apoptosis and is targeted to ubiquitin/proteasome-dependent proteolysis. Cancer Res. 2006;66:3024–3033
  84. Gur G, Rubin C, Katz M, et al. LRIG1 restricts growth factor signaling by enhancing receptor ubiquitylation and degradation. EMBO J. 2004;23:3270–3281
  85. Moro L, Arbini AA, Marra E, et al. Up-regulation of Skp2 after prostate cancer cell adhesion to basement membranes results in BRCA2 degradation and cell proliferation. J Biol Chem. 2006;281:22100–22107
  86. Carano AC, Pagano M. Role of the F-Box protein Skp2 in adhesion-dependent cell cycle progression. J Cell Biol. 2001;153:1381–1389
  87. Friedberg EC. How nucleotide excision repair protects against cancer. Nat Rev Cancer. 2001;1:22–33
  88. Huang H, Regan KM, Wang F, et al. Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc Natl Acad Sci USA. 2005;102:1649–1654
  89. Yang G, Ayala G, De Marzo A, et al. Elevated Skp2 protein expression in human prostate cancer: Association with loss of the cyclin-dependent kinase inhibitor p27 and PTEN and with reduced recurrence-free survival. Clin Cancer Res. 2002;8:3419–3426
  90. Shim E-H, Johnson L, Noh H-L, et al. Expression of the F-Box protein SKP2 induces hyperplasia, dysplasia, and low-grade carcinoma in the mouse prostate. Cancer Res. 2003;63:1583–1588
  91. Hsu T, Trojanowska M, Watson DK. Ets proteins in biological control and cancer. J Cell Biochem. 2004;91:896–903
  92. Oettgen P. Regulation of vascular inflammation and remodeling by ETS factors. Circ Res. 2006;99:1159–1166
  93. Tomlins SA, Rhodes DR, Perner S, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 2005;310:644–648
  94. Mehra R, Tomlins SA, Shen R, et al. Comprehensive assessment of TMPRSS2 and ETS family gene aberrations in clinically localized prostate cancer. Mod Pathol. 2007;20:538–544
  95. Massie CE, Adryan B, Barbosa-Morais NL, et al. New androgen receptor genomic targets show an interaction with the ETS1 transcription factor. EMBO Rep. 2007;8:871–878
  96. Ilyas M. Wnt signaling and the mechanistic basis of tumor development. J Pathol. 2005;205:130–144
  97. Yang F, Li X, Sharma M, et al. Linking β-catenin to androgen-signaling pathway. J Biol Chem. 2002;277:11336–11344
  98. Schweizer L, Rizzo CA, Spires TE, et al. The androgen receptor can signal through Wnt/β-catenin in prostate cancer cells as an adaptation mechanism to castration levels of androgens. BMC Cell Biol. 2008;9:4
  99. Zoubeidi A, Chi K, Gleave M. Targeting the cytoprotective chaperone, clusterin, for treatment of advanced cancer. Clin Cancer Res. 2010;16:1088–1093
  100. Rocchi P, So A, Kojima S, et al. Heat shock protein 27 increases after androgen ablation and plays a cytoprotective role in hormone-refractory prostate cancer. Cancer Res. 2004;64:6595–6602
  101. Miyake H, Nelson C, Rennie PS, et al. Testosterone-repressed prostate message-2 is an antiapoptotic gene involved in progression to androgen independence in prostate cancer. Cancer Res. 2000;60:170–176
  102. Parcellier A, Schmitt E, Gurbuxani S, et al. HSP27 is a ubiquitin-binding protein involved in I-κB proteasomal degradation. Mol Cell Biol. 2003;23:5790–5802
  103. Zoubeidi A, Ettinger S, Beraldi E, et al. Clusterin facilitates COMMD1 and I-κB degradation to enhance NF-κB activity in prostate cancer cells. Mol Cancer Res. 2010;8:119–130
  104. Papandreou CN, Logothetis CJ. Bortezomib as a potential treatment for prostate cancer. Cancer Res. 2004;64:5036–5043
  105. Richardson PG, Hideshima T, Anderson KC. Bortezomib (PS-341): A novel, first-in-class proteasome inhibitor for the treatment of multiple myeloma and other cancers. Cancer Control. 2003;10:361–369
  106. Ikezoe T, Yang Y, Saito T, et al. Proteasome inhibitor PS-341 down-regulates prostate-specific antigen (PSA) and induces growth arrest and apoptosis of androgen-dependent human prostate cancer LNCaP cells. Cancer Sci. 2004;95:271–275
  107. Thorpe PA, Christian PA, Schwarze SR. Proteasome inhibition blocks caspase-8 degradation and sensitizes prostate cancer cells to death receptor-mediated apoptosis. Prostate. 2008;68:200–209
  108. Lin H-K, Altuwaijri S, Lin W-J, et al. Proteasome activity is required for androgen receptor transcriptional activity via regulation of androgen receptor nuclear translocation and interaction with co-regulators in prostate cancer cells. J Biol Chem. 2002;277:36570–36576
  109. Vu H-Y, Juvekar A, Ghosh C, et al. Proteasome inhibitors induce apoptosis of prostate cancer cells by inducing nuclear translocation of IκBα. Arch Biochem Biophys. 2008;475:156–163
  110. Huang Y-T, Pan S-L, Guh J-H, et al. YC-1 suppresses constitutive nuclear factor-κB activation and induces apoptosis in human prostate cancer cells. Mol Cancer Ther. 2005;4:1628–1635
  111. Li W, Zhang X, Olumi AF. MG-132 sensitizes TRAIL-resistant prostate cancer cells by activating c-Fos/c-Jun heterodimers and repressing c-FLIP(L). Cancer Res. 2007;67:2247–2255
  112. Lashinger LM, Zhu K, Williams SA, et al. Bortezomib abolishes tumor necrosis factor-related apoptosis-inducing ligand resistance via a p21-dependent mechanism in human bladder and prostate cancer cells. Cancer Res. 2005;65:4902–4908
  113. Nikrad M, Johnson T, Puthalalath H, et al. The proteasome inhibitor bortezomib sensitizes cells to killing by death receptor ligand TRAIL via BH3-only proteins Bik and Bim. Mol Cancer Ther. 2005;4:443–449
  114. Kandasamy K, Kraft AS. Proteasome inhibitor PS-341 (VELCADE) induces stabilization of the TRAIL receptor DR5 mRNA through the 3′-untranslated region. Mol Cancer Ther. 2008;7:1091–1100
  115. Yoshida T, Shiraishi T, Nakata S, et al. Proteasome inhibitor MG132 induces death receptor 5 through CCAAT/enhancer-binding protein homologous protein. Cancer Res. 2005;65:5662–5667
  116. Williams S, Pettaway C, Song R, et al. Differential effects of the proteasome inhibitor bortezomib on apoptosis and angiogenesis in human prostate tumor xenografts. Mol Cancer Ther. 2003;2:835–843
  117. Papandreou CN, Daliani DD, Nix D, et al. Phase I trial of the proteasome inhibitor bortezomib in patients with advanced solid tumors with observations in androgen-independent prostate cancer. J Clin Oncol. 2004;22:2108–2121
  118. Dreicer R, Petrylak D, Agus D, et al. Phase I/II study of bortezomib plus docetaxel in patients with advanced androgen-independent prostate cancer. Clin Cancer Res. 2007;13:1208–1215
  119. Meluch AA, Spigel DS, Greco FA, et al. Weekly docetaxel and bortezomib in the treatment of patients with advanced hormone refractory prostate cancer (HRPC): A Minnie Pearl Cancer Research Network Phase II trial. J Clin Oncol. 2005;23:436s;[Abstract 4735].
  120. Siefker-Radtke AO, Poulter V, Mathew P, et al. Preliminary evidence of efficacy and tolerance for weekly intravenous bortezomib plus mitoxantrone in patients with advanced androgen-independent prostate cancer (AIPCa). J Clin Oncol. 2005;23:394s;[Abstract 4567].
  121. Woodham C, Birch L, Prins GS. Neonatal estrogen down-regulates prostatic androgen receptor through a proteasome-mediated protein degradation pathway. Endocrinol. 2003;144:4841–4850
  122. Sakamoto KM, Kim KB, Verma R, et al. Development of Protacs to target cancer-promoting proteins for ubiquitination and degradation. Mol Cell Proteomics. 2003;2:1350–1358

PII: S1078-1439(10)00069-4

doi: 10.1016/j.urolonc.2010.03.013

« Back Urologic Oncology: Seminars and Original Investigations

Article in Press

Article Tools

* Image Usage & Resolution