Overcoming docetaxel resistance in prostate cancer: A perspective review

Therapeutic Advances in Medical Oncology

Volumn 4, Issue 6, 2012, Pages 329-340

  Hwang, Clara ^a  

^a HENRY FORD HOSPITAL   (United States)

Author keywords

abiraterone; Alpharadin; cabazitaxel; docetaxel; MDV3100; prostate cancer; TAK 700; taxane resistance; tubulin

Indexed keywords

ABIRATERONE; ALPHA TUBULIN; BETA TUBULIN; CABAZITAXEL; CABOZANTINIB; CUSTIRSEN; DOCETAXEL; ENZALUTAMIDE; ESTRAMUSTINE; HYDROCORTISONE; IXABEPILONE; MITOXANTRONE; ORTERONEL; PREDNISONE; RADIUM CHLORIDE RA 223;

CANCER PAIN; CANCER PALLIATIVE THERAPY; CANCER SURVIVAL; CASTRATION RESISTANT PROSTATE CANCER; CYTOTOXICITY; DISEASE COURSE; DRUG BINDING; DRUG EFFICACY; DRUG INDICATION; DRUG MECHANISM; DRUG RESPONSE; DRUG TOLERABILITY; DRUG WITHDRAWAL; HUMAN; METASTATIC CASTRATION RESISTANT PROSTATE CANCER; MONOTHERAPY; MULTIDRUG RESISTANCE; MULTIPLE CYCLE TREATMENT; OVERALL SURVIVAL; PAIN ASSESSMENT; PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REVIEW; SURVIVAL RATE; SURVIVAL TIME; TREATMENT DURATION;

EID: 84871858375     PISSN: 17588340     EISSN: 17588359     Source Type: Journal    
DOI: 10.1177/1758834012449685     Document Type: Article

References (83)

1. Agus D.B. Stadler W.M. Shevrin D.H. Hart L. MacVicar G.R. Hamid O. et al. (2011) Safety, efficacy, and pharmacodynamics of the investigational agent TAK-700 in metastatic castration-resistant prostate cancer (mCRPC): updated data from a phase I / II study. ASCO Meeting Abstracts 29(15 Suppl.): 4531.
2. Attard G. Cooper C.S. de Bono J.S. (2009) Steroid hormone receptors in prostate cancer: a hard habit to break? Cancer Cell 16: 458–462
3. Attard G. Reid A.H. Yap T.A. Raynaud F. Dowsett M. Settatree S. et al. (2008) Phase I clinical trial of a selective inhibitor of CYP17, abiraterone acetate, confirms that castration-resistant prostate cancer commonly remains hormone driven. J Clin Oncol 26: 4563–4571.
4. Attard G. Richards J. de Bono J.S. (2011) New strategies in metastatic prostate cancer: targeting the androgen receptor signaling pathway. Clin Cancer Res 17: 1649–1657.
5. Beer T.M. Lalani A.S. Lee S. Mori M. Eilers K.M. Curd J.G. et al. (2008) C-reactive protein as a prognostic marker for men with androgen-independent prostate cancer: results from the ASCENT trial. Cancer 112: 2377–2383.
6. Berrieman H.K. Lind M.J. Cawkwell L. (2004) Do beta-tubulin mutations have a role in resistance to chemotherapy? Lancet Oncol 5: 158–164.
7. Berry W. Dakhil S. Modiano M. Gregurich M. Asmar L. (2002) Phase III study of mitoxantrone plus low dose prednisone versus low dose prednisone alone in patients with asymptomatic hormone refractory prostate cancer. J Urol 168: 2439–2443.
8. Berthold D.R. Pond G.R. Soban F. de Wit R. Eisenberger M. Tannock I.F. (2008) Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer: updated survival in the TAX 327 study. J Clin Oncol 26: 242–245.
9. Bhangal G. Halford S. Wang J. Roylance R. Shah R. Waxman J. (2000) Expression of the multidrug resistance gene in human prostate cancer. Urol Oncol 5: 118–121.
10. Cai C. Omwancha J. Hsieh C.L. Shemshedini L. (2007) Androgen induces expression of the multidrug resistance protein gene MRP 4 in prostate cancer cells. Prostate Cancer Prostatic Dis 10: 39–45.
11. Chen Z.S. Lee K. Walther S. Raftogianis R.B. Kuwano M. Zeng H. et al. (2002) Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP 4 is a component of the methotrexate efflux system. Cancer Res 62: 3144–3150.
12. Chi K.N. Hotte S.J. Yu E.Y. Tu D. Eigl B.J. Tannock I. et al. (2010) Randomized phase II study of docetaxel and prednisone with or without OGX-011 in patients with metastatic castration-resistant prostate cancer. J Clin Oncol 28: 4247–4254.
13. Cortes J.E. Pazdur R. (1995) Docetaxel. J Clin Oncol 13: 2643–2655.
14. Dahllof B. Billstrom A. Cabral F. Hartley-Asp B. (1993) Estramustine depolymerizes microtubules by binding to tubulin. Cancer Res 53: 4573–4581.
15. David-Beabes G.L. Overman M.J. Petrofski J.A. Campbell P.A. de Marzo A.M. Nelson W.G. (2000) Doxorubicin-resistant variants of human prostate cancer cell lines DU-145, PC-3, PPC-1, and TSU-PR1: characterization of biochemical determinants of antineoplastic drug sensitivity. Int J Oncol 17: 1077–1086.
16. de Bono J.S. Logothetis C.J. Molina A. Fizazi K. North S. Chu L. et al. (2011) Abiraterone and increased survival in metastatic prostate cancer. N Engl J Med 364: 1995–2005.
17. de Bono J.S. Oudard S. Ozguroglu M. Hansen S. Machiels J.P. Kocak I. et al. (2010) Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial. Lancet 376: 1147–1154.
18. de Marzo A.M. Platz E.A. Sutcliffe S. Xu J. Gronberg H. Drake C.G. et al. (2007) Inflammation in prostate carcinogenesis. Nat Rev Cancer 7: 256–269.
19. Ding X.W. Wu J.H. Jiang C.P. (2010) ABCG2: a potential marker of stem cells and novel target in stem cell and cancer therapy. Life Sci 86: 631–637.
20. Domingo-Domenech J. Oliva C. Rovira A. Codony-Servat J. Bosch M. Filella X. et al. (2006) Interleukin 6, a nuclear factor-kappaB target, predicts resistance to docetaxel in hormone-independent prostate cancer and nuclear factor-kappaB inhibition by PS-1145 enhances docetaxel antitumor activity. Clin Cancer Res 12: 5578–5586.
21. Dumontet C. Jordan M.A. Lee F.F. (2009) Ixabepilone: targeting betaIII-tubulin expression in taxane-resistant malignancies. Mol Cancer Ther 8: 17–25.
22. Eisenberger M.A. Simon R. O'Dwyer P.J. Wittes R.E. Friedman M.A. (1985) A reevaluation of nonhormonal cytotoxic chemotherapy in the treatment of prostatic carcinoma. J Clin Oncol 3: 827–841.
23. Faulds D. Balfour J.A. Chrisp P. Langtry H.D. (1991) Mitoxantrone. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic potential in the chemotherapy of cancer. Drugs 41: 400–449.
24. Fojo A.T. Ueda K. Slamon D.J. Poplack D.G. Gottesman M.M. Pastan I. (1987) Expression of a multidrug-resistance gene in human tumors and tissues. Proc Natl Acad Sci U S A 84: 265–269.
25. Galletti E. Magnani M. Renzulli M.L. Botta M. (2007) Paclitaxel and docetaxel resistance: molecular mechanisms and development of new generation taxanes. ChemMedChem 2: 920–942.
26. Gardner E.R. Ahlers C.M. Shukla S. Sissung T.M. Ockers S.B. Price D.K. et al. (2008) Association of the ABCG 2 C421A polymorphism with prostate cancer risk and survival. BJU Int 102: 1694–1699.
27. Gordon M.S. Vogelzang N.J. Schoffski P. Daud A. Spira A.I. O'Keeffe B.A. et al. (2011) Activity of cabozantinib (XL184) in soft tissue and bone: Results of a phase II randomized discontinuation trial (RDT) in patients (pts) with advanced solid tumors. ASCO Meeting Abstracts 29(15 Suppl.): 3010.
28. Ho L.L. Kench J.G. Handelsman D.J. Scheffer G.L. Stricker P.D. Grygiel J.G. et al. (2008) Androgen regulation of multidrug resistance-associated protein 4 (MRP4/ABCC4) in prostate cancer. Prostate 68: 1421–1429.
29. Holzbeierlein J. Lal P. LaTulippe E. Smith A. Satagopan J. Zhang L. et al. (2004) Gene expression analysis of human prostate carcinoma during hormonal therapy identifies androgen-responsive genes and mechanisms of therapy resistance. Am J Pathol 164: 217–227.
30. Homma S. Komohara Y. Harada M. Saya H. Todo S. Itoh K. et al. (2007) Differential levels of human leukocyte antigen-class I, multidrug-resistance 1 and androgen receptor expressions in untreated prostate cancer cells: the robustness of prostate cancer. Oncol Rep 18: 343–346.
31. Hussain M. Smith M.R. Sweeney C. Corn P.G. Elfiky A. Gordon M.S. et al. (2011) Cabozantinib (XL184) in metastatic castration-resistant prostate cancer (mCRPC): results from a phase II randomized discontinuation trial. ASCO Meeting Abstracts 29(15 Suppl.): 4516.
32. Ignatoski K.M. Friedman J. Escara-Wilke J. Zhang X. Daignault S. Dunn R.L. et al. (2009) Change in markers of bone metabolism with chemotherapy for advanced prostate cancer: interleukin-6 response is a potential early indicator of response to therapy. J Interferon Cytokine Res 29: 105–112.
33. Jemal A. Siegel R. Xu J. Ward E. (2010) Cancer statistics, 2010. CA Cancer J Clin 60: 277–300.
34. Kantoff P.W. Halabi S. Conaway M. Picus J. Kirshner J. Hars V. et al. (1999) Hydrocortisone with or without mitoxantrone in men with hormone-refractory prostate cancer: results of the Cancer and Leukemia Group B 9182 study. J Clin Oncol 17: 2506–2513.
35. Kawai K. Sakurai M. Sakai T. Misaki M. Kusano I. Shiraishi T. et al. (2000) Demonstration of MDR 1 P-glycoprotein isoform expression in benign and malignant human prostate cells by isoform-specific monoclonal antibodies. Cancer Lett 150: 147–153.
36. Laing N. Dahllof B. Hartley-Asp B. Ranganathan S. Tew K.D. (1997) Interaction of estramustine with tubulin isotypes. Biochemistry 36: 871–878.
37. Lee J.J. Swain S.M. (2005) Development of novel chemotherapeutic agents to evade the mechanisms of multidrug resistance (MDR). Semin Oncol 32(6 Suppl. 7): S22–S26.
38. Lee K. Belinsky M.G. Bell D.W. Testa J.R. Kruh G.D. (1998) Isolation of MOAT-B, a widely expressed multidrug resistance-associated protein / canalicular multispecific organic anion transporter-related transporter. Cancer Res 58: 2741–2747.
39. Lee K. Klein-Szanto A.J. Kruh G.D. (2000) Analysis of the MRP 4 drug resistance profile in transfected NIH3T3 cells. J Natl Cancer Inst 92: 1934–1940.
40. Leggas M. Adachi M. Scheffer G.L. Sun D. Wielinga P. Du G. et al. (2004) Mrp 4 confers resistance to topotecan and protects the brain from chemotherapy. Mol Cell Biol 24: 7612–7621.
41. Lubiniecki G.M. Berlin J.A. Weinstein R.B. Vaughn D.J. (2004) Thromboembolic events with estramustine phosphate-based chemotherapy in patients with hormone-refractory prostate carcinoma: results of a meta-analysis. Cancer 101: 2755–2759.
42. Machiels J.P. Mazzeo F. Clausse M. Filleul B. Marcelis L. Honhon B. et al. (2008) Prospective randomized study comparing docetaxel, estramustine, and prednisone with docetaxel and prednisone in metastatic hormone-refractory prostate cancer. J Clin Oncol 26: 5261–5268.
43. Maher J.M. Cheng X. Tanaka Y. Scheffer G.L. Klaassen C.D. (2006) Hormonal regulation of renal multidrug resistance-associated proteins 3 and 4 (Mrp3 and Mrp4) in mice. Biochem Pharmacol 71: 1470–1478.
44. Mathew G. Timm E.A. Jr Sotomayor P. Godoy A. Montecinos V.P. Smith G.J. et al. (2009) ABCG2-mediated DyeCycle Violet efflux defined side population in benign and malignant prostate. Cell Cycle 8: 1053–1061.
45. Miyake H. Chi K.N. Gleave M.E. (2000 a) Antisense TRPM-2 oligodeoxynucleotides chemosensitize human androgen-independent PC-3 prostate cancer cells both in vitro and in vivo. Clin Cancer Res 6: 1655–1663.
46. Miyake H. Hara I. Kamidono S. Gleave M.E. Eto H. (2003) Resistance to cytotoxic chemotherapy-induced apoptosis in human prostate cancer cells is associated with intracellular clusterin expression. Oncol Rep 10: 469–473.
47. Miyake H. Nelson C. Rennie P.S. Gleave M.E. (2000 b) Acquisition of chemoresistant phenotype by overexpression of the antiapoptotic gene testosterone-repressed prostate message-2 in prostate cancer xenograft models. Cancer Res 60: 2547–2554.
48. Miyake H. Nelson C. Rennie P.S. Gleave M.E. (2000 c) Testosterone-repressed prostate message-2 is an antiapoptotic gene involved in progression to androgen independence in prostate cancer. Cancer Res 60: 170–176.
49. Montgomery R.B. Mostaghel E.A. Vessella R. Hess D.L. Kalhorn T.F. Higano C.S. et al. (2008) Maintenance of intratumoral androgens in metastatic prostate cancer: a mechanism for castration-resistant tumor growth. Cancer Res 68: 4447–4454.
50. Nilsson S. Franzen L. Parker C. Tyrrell C. Blom R. Tennvall J. et al. (2007) Bone-targeted radium-223 in symptomatic, hormone-refractory prostate cancer: a randomised, multicentre, placebo-controlled phase II study. Lancet Oncol 8: 587–594.
51. Nitiss J.L. (2009) Targeting DNA topoisomerase II in cancer chemotherapy. Nat Rev Cancer 9: 338–350.
52. Panda D. Miller H.P. Islam K. Wilson L. (1997) Stabilization of microtubule dynamics by estramustine by binding to a novel site in tubulin: a possible mechanistic basis for its antitumor action. Proc Natl Acad Sci U S A 94: 10560–10564.
53. Parker C. Heidreich D. O'Sullivan J.M. Fossa S.D. Chodacki A. Demkow T. et al. (2011) Overall survival benefit of radium-223 chloride (AlpharadinTM) in the treatment of patients with symptomatic bone metastases in castration resistant prostate cancer (CRPC): a phase III randomised trial (ALSYMPCA). Eur J Cancer 47(Suppl. 2): LBA1.
54. Petrylak D.P. Tangen C.M. Hussain M.H. Lara P.N. Jr. Jones J.A. Taplin M.E. et al. (2004) Docetaxel and estramustine compared with mitoxantrone and prednisone for advanced refractory prostate cancer. N Engl J Med 351: 1513–1520.
55. Ploussard G. Terry S. Maille P. Allory Y. Sirab N. Kheuang L. et al. (2010) Class III beta-tubulin expression predicts prostate tumor aggressiveness and patient response to docetaxel-based chemotherapy. Cancer Res 70: 9253–9264.
56. Rosenberg J.E. Weinberg V.K. Kelly W.K. Michaelson D. Hussain M.H. Wilding G. et al. (2007) Activity of second-line chemotherapy in docetaxel-refractory hormone-refractory prostate cancer patients: randomized phase 2 study of ixabepilone or mitoxantrone and prednisone. Cancer 110: 556–563.
57. Saad F. Hotte S. North S. Eigl B. Chi K. Czaykowski P. et al. (2011) Randomized phase II trial of custirsen (OGX-011) in combination with docetaxel or mitoxantrone as second-line therapy in patients with metastatic castrate-resistant prostate cancer progressing after first-line docetaxel: CUOG Trial P-06c. Clin Cancer Res 17: 5765–5773.
58. Sanchez C. Mendoza P. Contreras H.R. Vergara J. McCubrey J.A. Huidobro C. et al. (2009) Expression of multidrug resistance proteins in prostate cancer is related with cell sensitivity to chemotherapeutic drugs. Prostate 69: 1448–1459.
59. Scher H.I. Beer T.M. Higano C.S. Anand A., Taplin M.E. Efstathiou E. et al. (2010) Antitumour activity of MDV 3100 in castration-resistant prostate cancer: a phase 1–2 study. Lancet 375: 1437–1446.
60. Scher H.I. Fizazi K. Saad F. Taplin M.E. Sternberg C.N. Miller K. et al. (2012) Effect of MDV3100, an androgen receptor signaling inhibitor (ARSI), on overall survival in patients with prostate cancer postdocetaxel: results from the phase III AFFIRM study. J Clin Oncol 30(5 Suppl.): LBA1.
61. Scher H.I., Halabi S. Tannock I. Morris M. Sternberg C.N. Carducci M.A. et al. (2008) 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: 1148–1159.
62. Scher H.I. Sawyers C.L. (2005) Biology of progressive, castration-resistant prostate cancer: directed therapies targeting the androgen-receptor signaling axis. J Clin Oncol 23: 8253–8261.
63. Seruga B. Ocana A. Tannock I.F. (2011) Drug resistance in metastatic castration-resistant prostate cancer. Nat Rev Clin Oncol 8: 12–23.
64. Seve P. Dumontet C. (2008) Is class III beta-tubulin a predictive factor in patients receiving tubulin-binding agents? Lancet Oncol 9: 168–175.
65. Sissung T.M. Baum C.E. Deeken J. Price D.K. Aragon-Ching J. Steinberg S.M. et al. (2008) ABCB 1 genetic variation influences the toxicity and clinical outcome of patients with androgen-independent prostate cancer treated with docetaxel. Clin Cancer Res 14: 4543-4549.
66. Sowery R.D. Hadaschik B.A. So A.I. Zoubeidi A. Fazli L. Hurtado-Coll A. et al. (2008) Clusterin knockdown using the antisense oligonucleotide OGX-011 re-sensitizes docetaxel-refractory prostate cancer PC-3 cells to chemotherapy. BJU Int 102: 389–397.
67. Stanbrough M. Bubley G.J. Ross K. Golub T.R. Rubin M.A. Penning T.M. et al. (2006) Increased expression of genes converting adrenal androgens to testosterone in androgen-independent prostate cancer. Cancer Res 66: 2815–2825.
68. Stearns M.E. Tew K.D. (1985) Antimicrotubule effects of estramustine, an antiprostatic tumor drug. Cancer Res 45: 3891–3897.
69. Sullivan G.F. Amenta P.S. Villanueva J.D. Alvarez C.J. Yang J.M. Hait W.N. (1998) The expression of drug resistance gene products during the progression of human prostate cancer. Clin Cancer Res 4: 1393–1403.
70. Tannock I.F. de Wit R. Berry W.R. Horti J. Pluzanska A. Chi K.N. et al. (2004) Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med 351: 1502–1512.
71. Tannock I.F. Osoba D. Stockler M.R. Ernst D.S. Neville A.J. Moore M.J. et al. (1996) Chemotherapy with mitoxantrone plus prednisone or prednisone alone for symptomatic hormone-resistant prostate cancer: a Canadian randomized trial with palliative end points. J Clin Oncol 14: 1756–1764.
72. Tew K.D. Erickson L.C. White G. Wang A.L. Schein P.S. Hartley-Asp B. (1983) Cytotoxicity of estramustine, a steroid-nitrogen mustard derivative, through non-DNA targets. Mol Pharmacol 24: 324–328.
73. Tian Q. Zhang J. Tan T.M. Chan E. Duan W. Chan S.Y. et al. (2005) Human multidrug resistance associated protein 4 confers resistance to campto thecins. Pharm Res 22: 1837–1853.
74. Tran C. Ouk S. Clegg N.J. Chen Y. Watson P.A. Arora V. et al. (2009) Development of a second-generation antiandrogen for treatment of advanced prostate cancer. Science 324: 787–790.
75. van Brussel J.P. Jan van Steenbrugge G. van Krimpen C. Bogdanowicz J.F. van der Kwast T.H. Schroder F.H. et al. (2001) Expression of multidrug resistance related proteins and proliferative activity is increased in advanced clinical prostate cancer. J Urol 165: 130–135.
76. van Brussel J.P. van Steenbrugge G.J. Romijn J.C. Schroder F.H. Mickisch G.H. (1999) Chemosensitivity of prostate cancer cell lines and expression of multidrug resistance-related proteins. Eur J Cancer 35: 664–671.
77. Vasiliou V. Vasiliou K. Nebert D.W. (2009) Human ATP-binding cassette (ABC) transporter family. Hum Genomics 3: 281–290.
78. Xie Y. Xu K. Linn D.E. Yang X. Guo Z. Shimelis H. et al. (2008) The 44-kDa Pim-1 kinase phosphorylates BCRP/ABCG2 and thereby promotes its multimerization and drug-resistant activity in human prostate cancer cells. J Biol Chem 283: 3349–3356.
79. Yagoda A. Petrylak D. (1993) Cytotoxic chemotherapy for advanced hormone-resistant prostate cancer. Cancer 71(3 Suppl.): 1098–1109.
80. Yamaoka M. Hara T. Kusaka M. (2010) Overcoming persistent dependency on androgen signaling after progression to castration-resistant prostate cancer. Clin Cancer Res 16: 4319–4324.
81. Zalcberg J. Hu X.F. Slater A. Parisot J. El-Osta S. Kantharidis P. et al. (2000) MRP 1 not MDR 1 gene expression is the predominant mechanism of acquired multidrug resistance in two prostate carcinoma cell lines. Prostate Cancer Prostatic Dis 3: 66–75.
82. Zellweger T. Kiyama S. Chi K. Miyake H. Adomat H. Skov K. et al. (2003) Overexpression of the cytoprotective protein clusterin decreases radiosensitivity in the human LNCaP prostate tumour model. BJU Int 92: 463–469.
83. Zhao L. Lee B.Y. Brown D.A. Molloy M.P. Marx G.M. Pavlakis N. et al. (2009) Identification of candidate biomarkers of therapeutic response to docetaxel by proteomic profiling. Cancer Res 69: 7696–7703.