Finding the place of histone deacetylase inhibitors in prostate cancer therapy

Expert Review of Clinical Pharmacology

Volumn 2, Issue 6, 2009, Pages 619-630

  Marrocco Tallarigo, Deborah L ^a   Centenera, Margaret M ^a   Scher, Howard I ^b   Tilley, Wayne D ^a   Butler, Lisa M ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Androgen signaling; Clinical trials; Combination therapies; Histone deacetylase inhibitors; Prostate cancer

Indexed keywords

4 [N (2 HYDROXYETHYL) N [2 (3 INDOLYL)ETHYL]AMINOMETHYL]CINNAMOHYDROXAMIC ACID; 4 N ACETYLDINALINE; AMIDOHYDROLASE INHIBITOR; ANDROGEN RECEPTOR; BELINOSTAT; BICALUTAMIDE; BUTYRIC ACID; CG 1521; DOCETAXEL; GEMCITABINE; HEAT SHOCK PROTEIN 90; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; N (2 AMINOPHENYL) 4 (3 PYRIDINYLMETHOXYCARBONYLAMINOMETHYL)BENZAMIDE; N (2 AMINOPHENYL) 4 [4 (3 PYRIDINYL) 2 PYRIMIDINYLAMINOMETHYL]BENZAMIDE; PANOBINOSTAT; ROMIDEPSIN; SB 379872A; SB 429201; SEMAXANIB; SK 7041; SK 7068; TRAPOXIN; TRICHOSTATIN A; TUBACIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; UNINDEXED DRUG; VALPROIC ACID; VASCULOTROPIN; VORINOSTAT;

ACETYLATION; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; CANCER CELL; CANCER RADIOTHERAPY; CARDIOTOXICITY; CLINICAL TRIAL; DRUG MECHANISM; DRUG POTENTIATION; DRUG TARGETING; ENZYME INHIBITION; FATIGUE; HUMAN; NAUSEA AND VOMITING; NEUROLOGIC DISEASE; NONHUMAN; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN TARGETING; REVIEW;

EID: 70549095136     PISSN: 17512433     EISSN: None     Source Type: Journal    
DOI: 10.1586/ecp.09.44     Document Type: Review

References (120)

1. Jemal A, Siegel R, Ward E et al. Cancer statistics, 2008. CA Cancer J. Clin. 58(2), 71-96 (2008).
2. Han M, Partin A, Pound C, Epstein J, Walsh P. Long-term biochemical disease-free and cancer-specific survival following anatomic radical retropubic prostatectomy. The 15-year Johns Hopkins experience. Urol. Clin. North Am. 28(3), 555-565 (2001). (Pubitemid 32916759)
3. Scher HI, Halabi S, Tannock I et al. Design and end points of clinical trials for patients with progressive prostate cancer and castrate levels of testosterone: recommendations of the Prostate Cancer Clinical Trials Working Group. J. Clin. Oncol. 26(7), 1148-1159 (2008).
4. Petrylak DP, Tangen CM, Hussain MH et al. Docetaxel and estramustine compared with mitoxantrone and prednisone for advanced refractory prostate cancer. N. Engl. J. Med. 351(15), 1513-1520 (2004).
5. Tannock IF, de Wit R, Berry WR et al. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N. Engl. J. Med. 351(15), 1502-1512 (2004).
6. Attard G, Reid AHM, A'Hern R et al. Selective inhibition of CYP17 with abiraterone acetate is highly active in the treatment of castration-resistant prostate cancer. J. Clin. Oncol. 27(23), 3742-3748 (2009).
7. Tran C, Ouk S, Clegg NJ et al. Development of a second-generation antiandrogen for treatment of advanced prostate cancer. Science 324(5928), 787-790 (2009).
8. Marks PA, Breslow R. Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat. Biotechnol. 25(1), 84-90 (2007). •• Contemporary overview of the preclinical and clinical development of vorinostat, the first histone deacetylase inhibitor (HDACI) to be approved by the US FDA for use in cancer treatment. (Pubitemid 46087907)
9. Gleave ME, Sato N, Sadar M et al. Butyrate analogue, isobutyramide, inhibits tumor growth and time to androgen-independent progression in the human prostate LNCaP tumor model. J. Cell. Biochem. 69(3), 271-281 (1998). • First demonstration of tumor suppressive activity of a nonspecific HDACI in prostate cancer cells. (Pubitemid 28227704)
10. Butler LM, Agus DB, Scher HI et al. Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses the growth of prostate cancer cells in vitro and in vivo. Cancer Res. 60(18), 5165-5170. (2000). • A specific HDACI, vorinostat, was shown to have strong antiproliferative activity in prostate cancer cells in culture and tumor suppressive activity in vivo, leading to subsequent assessment of vorinostat in clinical prostate cancer.
11. Butler LM, Webb Y, Agus DB et al. Inhibition of transformed cell growth and induction of cellular differentiation by pyroxamide, an inhibitor of histone deacetylase. Clin. Cancer Res. 7(4), 962-970 (2001). (Pubitemid 32708735)
12. Camphausen K, Scott T, Sproull M, Tofilon PJ. Enhancement of xenograft tumor radiosensitivity by the histone deacetylase inhibitor MS-275 and correlation with histone hyperacetylation. Clin. Cancer Res. 10(18 Pt 1), 6066-6071 (2004). (Pubitemid 39302609)
13. Kuefer R, Hofer MD, Altug V et al. Sodium butyrate and tributyrin induce in vivo growth inhibition and apoptosis in human prostate cancer. Br. J. Cancer 90(2), 535-541 (2004). (Pubitemid 38258278)
14. Thelen P, Schweyer S, Hemmerlein B et al. Expressional changes after histone deacetylase inhibition by valproic acid in LNCaP human prostate cancer cells. Int. J. Oncol. 24(1), 25-31 (2004).
15. Fronsdal K, Saatcioglu F. Histone deacetylase inhibitors differentially mediate apoptosis in prostate cancer cells. Prostate 62(3), 299-306 (2005). (Pubitemid 40129069)
16. Roy S, Packman K, Jeffrey R, Tenniswood M. Histone deacetylase inhibitors differentially stabilize acetylated p53 and induce cell cycle arrest or apoptosis in prostate cancer cells. Cell Death Differ. 12(5), 482-491 (2005). (Pubitemid 40662846)
17. Glaser KB. HDAC inhibitors: clinical update and mechanism-based potential. Biochem. Pharmacol. 74(5), 659-671 (2007). • Comprehensive overview of clinical development of HDACIs.
18. Agalioti T, Chen G, Thanos D. Deciphering the transcriptional histone acetylation code for a human gene. Cell 111(3), 381-392 (2002). (Pubitemid 35341391)
19. Polevoda B, Sherman F. The diversity of acetylated proteins. Genome Biol. 3(5), reviews0006.1-reviews0006.6 (2002).
20. Richards EJ, Elgin SC. Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108(4), 489-500 (2002).
21. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 10(1), 32-42 (2009). • Provides a contemporary picture of our current understanding of HDAC structure and function.
22. Villagra A, Cheng F, Wang HW et al. The histone deacetylase HDAC11 regulates the expression of interleukin 10 and immune tolerance. Nat. Immunol. 10(1), 92-100 (2009).
23. Glozak MA, Seto E. Acetylation/ deacetylation modulates the stability of DNA replication licensing factor CDt1. J. Biol. Chem. 284(17), 11446-11453 (2009).
24. Finnin M, Donigian J, Cohen A et al. Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature 401(6749), 188-193 (1999). • Elucidated the crystal structure of an HDAC bound to its inhibitors, and provided critical insight into the mechanism of interaction between HDACIs and HDACs, thus paving the way for rational design of new-generation inhibitors. (Pubitemid 29436325)
25. Somoza JR, Skene RJ, Katz BA et al. Structural snapshots of human HDAC8 provide insights into the class I histone deacetylases. Structure 12(7), 1325-1334 (2004).
26. Vannini A, Volpari C, Filocamo G et al. Crystal structure of a eukaryotic zinc-dependent histone deacetylase, human HDAC8, complexed with a hydroxamic acid inhibitor. Proc. Natl Acad. Sci. USA 101(42), 15064-15069 (2004). (Pubitemid 39391719)
27. Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl Acad. Sci. USA 100(8), 4389-4394 (2003).
28. Hu E, Dul E, Sung C-M et al. Identification of novel isoform-selective inhibitors within class I histone deacetylases. J. Pharmacol. Exp. Ther. 307(2), 720-728 (2003). (Pubitemid 37310689)
29. Halkidou K, Gaughan L, Cook S et al. Upregulation and nuclear recruitment of HDAC1 in hormone refractory prostate cancer. Prostate 59(2), 177-189 (2004). (Pubitemid 38481229)
30. Waltregny D, North B, Van Mellaert F et al. Screening of histone deacetylases (HDAC) expression in human prostate cancer reveals distinct class I HDAC profiles between epithelial and stromal cells. Eur. J. Histochem. 48(3), 273-290 (2004).
31. Nakagawa M, Oda Y, Eguchi T et al. Expression profile of class I histone deacetylases in human cancer tissues. Oncol. Rep. 18(4), 769-774 (2007).
32. Weichert W, Roske A, Gekeler V et al. Histone deacetylases 1, 2 and 3 are highly expressed in prostate cancer and HDAC2 expression is associated with shorter PSA relapse time after radical prostatectomy. Br. J. Cancer 98(3), 604-610 (2008). (Pubitemid 351214528)
33. Halkidou K, Cook S, Leung HY, Neal DE, Robson CN. Nuclear accumulation of histone deacetylase 4 (HDAC4) coincides with the loss of androgen sensitivity in hormone refractory cancer of the prostate. Eur. Urol. 45(3), 382-389 (2004). (Pubitemid 38221414)
34. Patra SK, Patra A, Dahiya R. Histone deacetylase and DNA methyltransferase in human prostate cancer. Biochem. Biophys. Res. Commun. 287(3), 705-713 (2001). (Pubitemid 32912772)
35. Huffman DM, Grizzle WE, Bamman MM et al. SIRT1 Is Significantly Elevated in Mouse and Human Prostate Cancer. Cancer Res. 67(14), 6612-6618 (2007).
36. Jung-Hynes B, Nihal M, Zhong W, Ahmad N. Role of Sirtuin Histone Deacetylase SIRT1 in prostate cancer: a target for prostate cancer management via its inhibition? J. Biol. Chem. 284(6), 3823-3832 (2009).
37. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 403(6765), 41-45 (2000).
38. Kouzarides T. Chromatin modifications and their function. Cell 128(4), 693-705 (2007). • Comprehensive overview of the nature and functional consequences of posttranslational chromatin modifications.
39. Shahbazian MD, Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76(75-100 (2007).
40. Seligson DB, Horvath S, Shi T et al. Global histone modification patterns predict risk of prostate cancer recurrence. Nature 435(7046), 1262-1266 (2005). • First evidence that alterations in certain histone modifications can predict the clinical behavior of human prostate tumors. (Pubitemid 40943093)
41. Mohamed MA, Greif PA, Diamond J et al. Epigenetic events, remodelling enzymes and their relationship to chromatin organization in prostatic intraepithelial neoplasia and prostatic adenocarcinoma. BJU Int. 99(4), 908-915 (2007). (Pubitemid 46439577)
42. Gregoretti IV, Lee YM, Goodson HV. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J. Mol. Biol. 338(1), 17-31 (2004).
43. Glozak MA, Sengupta N, Zhang X, Seto E. Acetylation and deacetylation of non-histone proteins. Gene 363, 15-23 (2005).
44. Fuino L, Bali P, Wittmann S et al. Histone deacetylase inhibitor LAQ824 down-regulates Her-2 and sensitizes human breast cancer cells to trastuzumab, taxotere, gemcitabine, and epothilone B. Mol. Cancer Ther. 2(10), 971-984 (2003).
45. Nimmanapalli R, Fuino L, Bali P et al. Histone deacetylase inhibitor LAQ824 both lowers expression and promotes proteasomal degradation of Bcr-Abl and induces apoptosis of imatinib mesylate-sensitive or -refractory chronic myelogenous leukemia-blast crisis cells. Cancer Res. 63(16), 5126-5135 (2003). (Pubitemid 37022654)
46. Bali P, Pranpat M, Bradner J et al. Inhibition of histone deacetylase 6 acetylates and disrupts the chaperone function of heat shock protein 90: a novel basis for antileukemia activity of histone deacetylase inhibitors. J. Biol. Chem. 280(29), 26729-26734 (2005). (Pubitemid 41040705)
47. Chen L, Meng S, Wang H et al. Chemical ablation of androgen receptor in prostate cancer cells by the histone deacetylase inhibitor LAQ824. Mol. Cancer Ther. 4(9), 1311-1319 (2005).
48. Bali P, Pranpat M, Swaby R et al. Activity of suberoylanilide hydroxamic acid against human breast cancer cells with amplification of her-2. Clin. Cancer Res. 11(17), 6382-6389 (2005). (Pubitemid 41262970)
49. Yu X, Guo ZS, Marcu MG et al. Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. J. Natl Cancer Inst. 94(7), 504-513 (2002). (Pubitemid 34411289)
50. Kovacs JJ, Murphy PJM, Gaillard S et al. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell 18(5), 601-607 (2005). •• Demonstration of acetylation of the molecular chaperone heat-shock protein 90, which is now one of the best-characterized modifications of a non-histone protein, providing a post-transcriptional mechanism by which HDACIs may alter cellular signaling pathways in cancer cells. (Pubitemid 40726236)
51. Murphy PJ, Morishima Y, Kovacs JJ, Yao TP, Pratt WB. Regulation of the dynamics of hsp90 action on the glucocorticoid receptor by acetylation/ deacetylation of the chaperone. J. Biol. Chem. 280(40), 33792-33799 (2005). (Pubitemid 41443098)
52. George P, Bali P, Annavarapu S et al. Combination of the histone deacetylase inhibitor LBH589 and the hsp90 inhibitor 17-AAG is highly active against human CML-BC cells and AML cells with activating mutation of FLT-3. Blood. 105(4), 1768-1776 (2005). (Pubitemid 40223701)
53. Rahmani M, Yu C, Dai Y et al. Coadministration of the heat shock protein 90 antagonist 17-allylamino- 17-demethoxygeldanamycin with suberoylanilide hydroxamic acid or sodium butyrate synergistically induces apoptosis in human leukemia cells. Cancer Res. 63(23), 8420-8427 (2003). (Pubitemid 37549498)
54. Popov VM, Wang C, Shirley LA et al. The functional significance of nuclear receptor acetylation. Steroids 72(2), 221-230 (2007). (Pubitemid 46273505)
55. Fu M, Wang C, Reutens AT et al. p300 and p300/cAMP-response element-binding protein-associated factor acetylate the androgen receptor at sites governing hormone-dependent transactivation. J. Biol. Chem. 275(27), 20853-20860 (2000). • Acetylation of the androgen receptor, another non-histone protein and a key mediator of prostate cancer cell growth and survival, is shown to enhance its DNA-binding and transactivation activity. (Pubitemid 30457679)
56. Fu M, Wang C, Wang J et al. Androgen receptor acetylation governs trans activation and MEKK1-induced apoptosis without affecting in vitro sumoylation and trans-repression function. Mol. Cell. Biol. 22(10), 3373-3388 (2002). (Pubitemid 34453978)
57. Gaughan L, Logan IR, Cook S, Neal DE, Robson CN. Tip60 and histone deacetylase 1 regulate androgen receptor activity through changes to the acetylation status of the receptor. J. Biol. Chem. 277(29), 25904-25913 (2002). (Pubitemid 34967070)
58. Gaughan L, Logan IR, Neal DE, Robson CN. Regulation of androgen receptor and histone deacetylase 1 by Mdm2-mediated ubiquitylation. Nucleic Acids Res. 33(1), 13-26 (2005). (Pubitemid 40276925)
59. Thomas M, Dadgar N, Aphale A et al. Androgen receptor acetylation site mutations cause trafficking defects, misfolding, and aggregation similar to expanded glutamine tracts. J. Biol. Chem. 279(9), 8389-8395 (2004). (Pubitemid 38294731)
60. Fu M, Rao M, Wang C et al. Acetylation of androgen receptor enhances coactivator binding and promotes prostate cancer cell growth. Mol. Cell. Biol. 23(23), 8563-8575 (2003). (Pubitemid 37433362)
61. Melchior SW, Brown LG, Figg WD et al. Effects of phenylbutyrate on proliferation and apoptosis in human prostate cancer cells in vitro and in vivo. Int. J. Oncol. 14(3), 501-508 (1999).
62. Qian DZ, Wang X, Kachhap SK et al. The histone deacetylase inhibitor NVP-LAQ824 inhibits angiogenesis and has a greater antitumor effect in combination with the vascular endothelial growth factor receptor tyrosine kinase inhibitor PTK787/ZK222584. Cancer Res. 64(18), 6626-6634 (2004). (Pubitemid 39297923)
63. Chinnaiyan P, Vallabhaneni G, Armstrong E, Huang SM, Harari PM. Modulation of radiation response by histone deacetylase inhibition. Int. J. Radiat. Oncol. Biol. Phys. 62(1), 223-229 (2005). (Pubitemid 40591946)
64. Gediya LK, Chopra P, Purushottamachar P, Maheshwari N, Njar VC. A new simple and high-yield synthesis of suberoylanilide hydroxamic acid and its inhibitory effect alone or in combination with retinoids on proliferation of human prostate cancer cells. J. Med. Chem. 48(15), 5047-5051 (2005). (Pubitemid 41033145)
65. Kulp SK, Chen CS, Wang DS, Chen CY. Antitumor effects of a novel phenylbutyrate-based histone deacetylase inhibitor, (S)-HDAC-42, in prostate cancer. Clin. Cancer Res. 12(17), 5199-5206 (2006).
66. Rokhlin OW, Glover RB, Guseva NV et al. Mechanisms of cell death induced by histone deacetylase inhibitors in androgen receptor-positive prostate cancer cells. Mol. Cancer Res. 4(2), 113-123 (2006).
67. Xia Q, Sung J, Chowdhury W et al. Chronic administration of valproic acid inhibits prostate cancer cell growth in vitro and in vivo. Cancer Res. 66(14), 7237-7244 (2006). (Pubitemid 44197704)
68. Xu W, Ngo L, Perez G, Dokmanovic M, Marks PA. Intrinsic apoptotic and thioredoxin pathways in human prostate cancer cell response to histone deacetylase inhibitor. Proc. Natl Acad. Sci. USA 103(42), 15540-15545 (2006). (Pubitemid 44625628)
69. Lai MT, Yang CC, Lin TY, Tsai FJ, Chen WC. Depsipeptide (FK228) inhibits growth of human prostate cancer cells. Urol. Oncol. 26(2), 182-189 (2008).
70. Qian X, Ara G, Mills E et al. Activity of the histone deacetylase inhibitor belinostat (PXD101) in preclinical models of prostate cancer. Int. J. Cancer 122(6), 1400-1410 (2008). (Pubitemid 351287242)
71. Sargeant AM, Rengel RC, Kulp SK et al. OSU-HDAC42, a histone deacetylase inhibitor, blocks prostate tumor progression in the transgenic adenocarcinoma of the mouse prostate model. Cancer Res. 68(10), 3999-4009 (2008).
72. Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 26(37), 5541-5552 (2007).
73. Sonnemann J, Hartwig M, Plath A et al. Histone deacetylase inhibitors require caspase activity to induce apoptosis in lung and prostate carcinoma cells. Cancer Lett. 232(2), 148-160 (2006). (Pubitemid 43170964)
74. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat. Rev. Drug Discov. 5(9), 769-784 (2006). •• Detailed review of the molecular events in cells that occur in response to HDACIs, and the potential mechanisms underlying their antiproliferative effects in cancer cells.
75. Valentini A, Biancolella M, Amati F et al. Valproic acid induces neuroendocrine differentiation and UGT2B7 up-regulation in human prostate carcinoma cell line. Drug Metab. Dispos. 35(6), 968-972 (2007). (Pubitemid 46798607)
76. Frigo DE, McDonnell DP. Differential effects of prostate cancer therapeutics on neuroendocrine transdifferentiation. Mol. Cancer Ther. 7(3), 659-669 (2008). • Intriguing study that raises the possibility that HDACIs may cause prostate cancer cells to differentiate into a neuroendocrine phenotype.
77. Marrocco DL, Tilley WD, Bianco-Miotto T et al. Suberoylanilide hydroxamic acid (vorinostat) represses androgen receptor expression and acts synergistically with an androgen receptor antagonist to inhibit prostate cancer cell proliferation. Mol. Cancer Ther. 6(1), 51-60 (2007). • First study to demonstrate that combining an androgen receptor (AR) antagonist with HDACIs synergistically induces prostate cancer cell death, and that AR is targeted by an HDACI. (Pubitemid 46209918)
78. Roy S, Jeffrey R, Tenniswood M. Array-based analysis of the effects of trichostatin A and CG-1521 on cell cycle and cell death in LNCaP prostate cancer cells. Mol. Cancer Ther. 7(7), 1931-1939 (2008).
79. Welsbie DS, Xu J, Chen Y et al. Histone deacetylases are required for androgen receptor function in hormone-sensitive and castrate-resistant prostate cancer. Cancer Res. 69(3), 958-966 (2009). • This study determined that the mechanism by which HDACIs downregulate AR activity in prostate cancer cells was primarily via reduced transcription of the AR gene, and by suppression of AR transcriptional activity.
80. Wang LG, Ossowski L, Ferrari AC. Androgen receptor level controlled by a suppressor complex lost in an androgen-independent prostate cancer cell line. Oncogene 23(30), 5175-5184 (2004). (Pubitemid 38980350)
81. Goh M, Chen F, Paulsen MT et al. Phenylbutyrate attenuates the expression of Bcl-X(L), DNA-PK, caveolin-1, and VEGF in prostate cancer cells. Neoplasia 3(4), 331-338 (2001). (Pubitemid 32801883)
82. Sasakawa Y, Naoe Y, Noto T et al. Antitumor efficacy of FK228, a novel histone deacetylase inhibitor, depends on the effect on expression of angiogenesis factors. Biochem. Pharmacol. 66(6), 897-906 (2003). (Pubitemid 37083586)
83. Butler LM, Zhou X, Xu WS et al. The histone deacetylase inhibitor SAHA arrests cancer cell growth, up-regulates thioredoxin-binding protein-2, and down-regulates thioredoxin. Proc. Natl Acad. Sci. USA 99(18), 11700-11705. (2002). (Pubitemid 34994462)
84. Roy S, Tenniswood M. Site specific acetylation of p53 directs selective transcription complex assembly. J. Biol. Chem. 282(7), 4765-4771 (2007). (Pubitemid 47100922)
85. Butler LM, Agus DB, Scher HI et al. Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses the growth of prostate cancer cells in vitro and in vivo. Cancer Res. 60(18), 5165-5170 (2000).
86. Bjorkman M, Iljin K, Halonen P et al. Defining the molecular action of HDAC inhibitors and synergism with androgen deprivation in ERG-positive prostate cancer. Int. J. Cancer 123(12), 2774-2781 (2008). • Extended the studies of Marrocco et al to demonstrate that synergism between AR antagonists and HDACIs is most prominent in prostate cancer cells with TMPRSS2-ERG gene fusions.
87. Karagiannis TC, El-Osta A. Modulation of cellular radiation responses by histone deacetylase inhibitors. Oncogene 25(28), 3885-3893 (2006). (Pubitemid 43990743)
88. Basch EM, Somerfield MR, Beer TM et al. American Society of Clinical Oncology endorsement of the Cancer Care Ontario Practice Guideline on nonhormonal therapy for men with metastatic hormone-refractory (castration-resistant) prostate cancer. J. Clin. Oncol. 25(33), 5313-5318 (2007).
89. Kanzaki M, Kakinuma H, Kumazawa T et al. Low concentrations of the histone deacetylase inhibitor, depsipeptide, enhance the effects of gemcitabine and docetaxel in hormone refractory prostate cancer cells. Oncol. Rep. 17(4), 761-767 (2007).
90. Zhang Z, Stanfield J, Frenkel E, Kabbani W, Hsieh JT. Enhanced therapeutic effect on androgen-independent prostate cancer by depsipeptide (FK228), a histone deacetylase inhibitor, in combination with docetaxel. Urology 70(2), 396-401 (2007). (Pubitemid 47362245)
91. Chen CS, Wang YC, Yang HC et al. Histone deacetylase inhibitors sensitize prostate cancer cells to agents that produce DNA double-strand breaks by targeting Ku70 acetylation. Cancer Res. 67(11), 5318-5327 (2007).
92. Borgstrom P, Bourdon MA, Hillan KJ, Sriramarao P, Ferrara N. Neutralizing anti-vascular endothelial growth factor antibody completely inhibits angiogenesis and growth of human prostate carcinoma micro tumors in vivo. Prostate 35(1), 1-10 (1998). (Pubitemid 28158631)
93. Melnyk O, Zimmerman M, Kim KJ, Shuman M. Neutralizing anti-vascular endothelial growth factor antibody inhibits further growth of established prostate cancer and metastases in a pre-clinical model. J. Urol. 161(3), 960-963 (1999). (Pubitemid 29422416)
94. Takei Y, Kadomatsu K, Yuzawa Y, Matsuo S, Muramatsu T. A small interfering RNA targeting vascular endothelial growth factor as cancer therapeutics. Cancer Res. 64(10), 3365-3370 (2004). (Pubitemid 38657905)
95. Fox WD, Higgins B, Maiese KM et al. Antibody to vascular endothelial growth factor slows growth of an androgen-independent xenograft model of prostate cancer. Clin. Cancer Res. 8(10), 3226-3231 (2002). (Pubitemid 35155035)
96. Verheul H, Pinedo H. Vascular endothelial growth factor and its inhibitors. Drugs Today (Barc.) 39(Suppl. C), 81-93 (2003). (Pubitemid 37509403)
97. Nakamura K, Yamamoto A, Kamishohara M et al. KRN633: a selective inhibitor of vascular endothelial growth factor receptor-2 tyrosine kinase that suppresses tumor angiogenesis and growth. Mol. Cancer Ther. 3(12), 1639-1649 (2004). (Pubitemid 40136720)
98. Nicholson B, Gulding K, Conaway M, Wedge SR, Theodorescu D. Combination antiangiogenic and androgen deprivation therapy for prostate cancer: a promising therapeutic approach. Clin. Cancer Res. 10(24), 8728-8734 (2004). (Pubitemid 40053442)
99. Stadler WM, Cao D, Vogelzang NJ et al. A randomized Phase II trial of the antiangiogenic agent SU5416 in hormone-refractory prostate cancer. Clin. Cancer Res. 10(10), 3365-3370 (2004). (Pubitemid 38685441)
100. Ellis L, Hammers H, Pili R. Targeting tumor angiogenesis with histone deacetylase inhibitors. Cancer Lett. 280(2), 145-153 (2009).
101. Kimberley FC, Screaton GR. Following a TRAIL: update on a ligand and its five receptors. Cell Res. 14(5), 359-372 (2004).
102. Yagita H, Takeda K, Hayakawa Y, Smyth MJ, Okumura K. TRAIL and its receptors as targets for cancer therapy. Cancer Sci. 95(10), 777-783 (2004). (Pubitemid 39545582)
103. Norris JS, Hyer ML, Voelkel-Johnson C et al. The use of Fas Ligand, TRAIL and Bax in gene therapy of prostate cancer. Curr. Gene Ther. 1(1), 123-136 (2001).
104. Taghiyev AF, Guseva NV, Sturm MT, Rokhlin OW, Cohen MB. Trichostatin A (TSA) sensitizes the human prostatic cancer cell line DU145 to death receptor ligands treatment. Cancer Biol. Ther. 4(4), 382-390 (2005).
105. Vanoosten RL, Moore JM, Ludwig AT, Griffith TS. Depsipeptide (FR901228) enhances the cytotoxic activity of TRAIL by redistributing TRAIL receptor to membrane lipid rafts. Mol. Ther. 11(4), 542-552 (2005).
106. Lakshmikanthan V, Kaddour-Djebbar I, Lewis RW, Kumar MV. SAHA-sensitized prostate cancer cells to TNFα-related apoptosis-inducing ligand (TRAIL): mechanisms leading to synergistic apoptosis. Int. J. Cancer 119(1), 221-228 (2006).
107. VanOosten RL, Earel JK Jr, Griffith TS. Histone deacetylase inhibitors enhance Ad5-TRAIL killing of TRAIL-resistant prostate tumor cells through increased caspase-2 activity. Apoptosis 12(3), 561-571 (2007).
108. Huggins C SRHC. Studies on prostatic cancer. II. The effect of castration on advanced carcinoma of the prostate gland. Arch. Surg. 43, 209-228 (1941).
109. Mohler JL. A role for the androgenre-ceptor in clinically localized and advanced prostate cancer. Best Pract. Res. Clin. Endocrinol. Metab. 22(2), 357-372 (2008).
110. Mehra R, Tomlins SA, Shen R et al. Comprehensive assessment of TMPRSS2 and ETS family gene aberrations in clinically localized prostate cancer. Mod. Pathol. 20(5), 538-544 (2007). (Pubitemid 46631996)
111. Bradley DA, Dunn R, Rathkopf D et al. Vorinistat in hormone refractory prostate cancer (HRPC): trial results and IL-6 analysis. Program and Abstracts of the American Society of Clinical Oncology Genitourinary Cancers Symposium. San Francisco, CA, USA, 14-16 February 2008 (Absract 211).
112. Sharma S, Symanowski J, Wong B et al. A Phase II clinical trial of oral valproic acid in patients with castration-resistant prostate cancers using an intensive biomarker sampling strategy. Transl. Oncol. 1(3), 141-147 (2008). • First published study on the clinical use of an HDACI, valproic acid, in prostate cancer.
113. Molife LR, Attard G, Fong PC et al. Phase II, two-stage, single-arm trial of the histone deacetylase inhibitor (HDACi) romidepsin in metastatic castrationresistant prostate cancer (CRPC). Ann. Oncol. (2009) (Epub ahead of print).
114. Shah MH, Binkley P, Chan K et al. Cardiotoxicity of histone deacetylase inhibitor depsipeptide in patients with metastatic neuroendocrine tumors. Clin. Cancer Res. 12(13), 3997-4003 (2006). (Pubitemid 44078086)
115. Molife R, Patterson S, Riggs C et al. Phase II study of FK228 in patients with hormone refractory prostate cancer (HRPC). J. Clin. Oncol. (Meeting Abstracts) 24, 14554 (2006).
116. Piekarz RL, Frye AR, Wright JJ et al. Cardiac studies in patients treated with depsipeptide, FK228, in a Phase II trial for T-cell lymphoma. Clin. Cancer Res. 12(12), 3762-3773 (2006).
117. A Phase I Study of LBH589 (Panobinostat) in Combination With External Beam Radiotherapy for the Treatment of Prostate Cancer, Esophageal Cancer and Head and Neck Cancer (NCT00670553) www.clinicaltrials.gov/ct2/show/NCT006 70553?term=NCT00670553&rank=1
118. Androgen Deprivation Therapy and Vorinostat Followed by Radical Prostatectomy in Treating Patients With Localized Prostate Cancer (NCT00589472) www.clinicaltrials.gov/ct2/show/NCT005 89472?term=NCT00589472&rank=1
119. Safety and Efficacy Studies of Panobinostat and Bicalutamide in Patients With Recurrent Prostate Cancer After Castration (NCT00878436) www.clinicaltrials.gov/ct2/show/NCT008 78436?term=NCT00878436&rank=1
120. A dose finding study with I.V. panobinostat (LBH589), docetaxel, and prednisone in patients with hormone refractory prostate cancer (NCT00663832) www.clinicaltrials.gov/ct2/ results?term=NCT00663832