New paradigms in microtubule-mediated endocrine signaling in prostate cancer

Molecular Cancer Therapeutics

Volumn 12, Issue 5, 2013, Pages 555-566

  Mistry, Sucharita J ^a   Oh, William K ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHOXYESTRADIOL; ABIRATERONE ACETATE; ANDROGEN RECEPTOR; ANTINEOPLASTIC AGENT; CABAZITAXEL; CISPLATIN; DOCETAXEL; ENZALUTAMIDE; ESTRAMUSTINE; FOSFESTROL; MICROTUBULE TARGETING AGENT; MITOXANTRONE; PREDNISONE; STATHMIN; TAU PROTEIN; UNCLASSIFIED DRUG;

ANDROGEN DEPRIVATION THERAPY; CANCER COMBINATION CHEMOTHERAPY; CANCER SURVIVAL; CARCINOGENESIS; CASTRATION RESISTANT PROSTATE CANCER; CELL DIVISION; CELL PROLIFERATION; CHEMOSENSITIVITY; DRUG EFFICACY; DRUG RECEPTOR BINDING; DRUG SAFETY; ESTROGEN THERAPY; HUMAN; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; INTRACELLULAR SIGNALING; MICROTUBULE; MITOSIS; MULTIPLE CYCLE TREATMENT; NEUTROPENIA; NONHUMAN; OVERALL SURVIVAL; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; QUALITY OF LIFE; REVIEW; SURVIVAL RATE; SURVIVAL TIME;

ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC AGENTS, HORMONAL; ESTROGENS; HUMANS; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION; SPINDLE APPARATUS; TUBULIN MODULATORS;

EID: 84877638660     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-12-0871     Document Type: Review

References (75)

1. Jemal A, Seigel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010;60:277-300.
2. Debes JD, Tindall DJ. Mechanisms of androgen-refractory prostate cancer. N Engl J Med 2004;351:1488-90.
3. Chen CD, Welsbie DS, Tran C, Baek SH, Chen R, Vessella R, et al. Molecular determinants of resistance to antiandrogen therapy. Nat Med 2004;10:33-9.
4. Oh WK, Kantoff PW. Management of hormone refractory prostate cancer: current standards and future prospects. J Urol 1998;160: 1220-9.
5. Desai A, Mitchison TJ. Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 1997;13:83-117.
6. Mistry SJ, Atweh GF. Role of stathmin in the regulation of the mitotic spindle: potential applications in cancer therapy. Mt Sinai J Med 2002;69:299-304.
7. Berges RR, Vukanovic J, Epstein JI, CarMichel M, Cisek L, Johnson DE, et al. Implication of cell kinetic changes during the progression of human prostatic cancer. Clin Cancer Res 1995;1:473-80.
8. Carbonaro M, O'Brate A, Giannakakou P. Microtubule disruption targets HIF-1alpha mRNA to cytoplasmic P-bodies for translational repression. J Cell Biol 2011;192:83-99.
9. Giannakakou P, Nakano M, Nicolaou KC, O'Brate A, Yu J, Blagosklonny MV, et al. Enhanced microtubule-dependent trafficking and p53 nuclear accumulation by suppression of microtubule dynamics. Proc Natl Acad Sci U S A 2002;99:10855-60.
10. Schurko B, Oh WK. Docetaxel chemotherapy remains the standard of care in castration-resistant prostate cancer. Nat Clin Pract Oncol 2008;5:506-7.
11. Petrylak DP, Tangen CM, Hussain MH, Lara PN Jr, Jones JA, Taplin ME, et al. Docetaxel and estramustine compared with mitoxantrone and prednisone for advanced refractory prostate cancer. N Engl J Med 2004;351:1513-20.
12. Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, et al. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med 2004;351:1502-12.
13. Berthold DR, Pond GR, Soban F, de Wit R, Eisenberger M, Tannock IF. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer: updated survival in the TAX 327 study. J Clin Oncol 2008;26:242-5.
14. Morris MJ, Hammers HJ, Sweeney C, Bloma M, Aksnes AK, O'Bryan-Tear G, et al. A phase 1/11a study of the safety and efficacy of radium-223 chloride (Ra-223) with docetaxel for castration resistant prostate cancer (CRPC) patients with bone metastases. J Clin Oncol 30, 2012 (suppl; abstr TPS4694).
15. Galsky MD, Dritselis A, Kirkpatrick P, Oh WK. Cabazitaxel. Nat Rev Drug Discov 2010;9:677-8.
16. Bradshaw DM, Arceci RJ. Clinical relevance of transmembrane drug efflux as a mechanism of multidrug resistance. J Clin Oncol 1998;16:3674-90.
17. Mita AC, Denis LJ, Rowinsky EK, Debono JS, Goetz AD, Ochoa L, et al. Phase I and pharmacokinetic study of XRP6258 (RPR 116258A), a novel taxane, administered as a 1-hour infusion every 3 weeks in patients with advanced solid tumors. Clin Cancer Res 2009;15: 723-30.
18. de Bono JS, Oudard S, Ozguroglu M, Hansen S, Machiels JP, Kocak I, et al. Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial. Lancet 2010;376:1147-54.
19. Lockhart AC, Sundaram S, Sarantopoulos J, Mita MM, Lane AR, Moseley JL, et al. Phase 1 trial of cabazitaxel plus cisplatin in patients with advanced solid tumors. J Clin Oncol 30, 2012 (suppl 5; abstr 162).
20. Galsky MD, Small EJ, Oh WK, Chen I, Smith DC, Colevas AD, et al. Multi-institutional randomized phase II trial of the epothilone B analog ixabepilone (BMS-247550) with or without estramustine phosphate in patients with progressive castrate metastatic prostate cancer. J Clin Oncol 2005;23:1439-46.
21. Hussain A, DiPaola RS, Baron AD, Higano CS, Tchekmedyian NS, Johri AR. Phase II trial of weekly patupilone in patients with castrationresistant prostate cancer. Ann Oncol 2009;20:492-97.
22. Feldman BJ, Feldman D. The development of androgen-independent prostate cancer. Nat Rev Cancer 2001;1:34-45.
23. Attard G, de Bono JS. Prostate cancer: PSA as an intermediate end point in clinical trials. Nat Rev Urol 2009;6:473-5.
24. Sun S, Sprenger CT, Vessella RL, Haugk K, Soraino K, Mostaghel E, 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.
25. Mostaghel EA, Marck BT, Plymate S, Vessella R, 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.
26. 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.
27. Kuroda K, Liu H, KIm S, Guo M, Navarro V, Bander NH. Docetaxel down-regulates the expression of androgen receptor and prostatespecific antigen but not prostate-specific membrane antigen in prostate cancer cell lines: implications for PSA surrogacy. Prostate 2009;69:1579-85.
28. Gan L, Chen S, Wang Y, Watahiki A, Bohrer L, Sun Z, et al. Inhibition of the androgen receptor as a novel mechanism of taxol chemotherapy in prostate cancer. Cancer Res 2009;69:8386-94.
29. Bertram J, Peacock JW, Fazli L, Mui AL, Chung SW, Cox ME, et al. Loss of PTEN is associated with progression to androgen independence. Prostate 2006;66:895-902.
30. Zhu ML, Horbinski CM, Garzotto M, Qian DZ, Beer TM, Kyprianou N. Tubulin-targeting chemotherapy impairs androgen receptor activity in prostate cancer. Cancer Res 2010;70:7992-8002.
31. Darshan MS, Loftus MS, Thadani-Mulero M, Levy BP, Escuin D, Zhou XK, et al. Taxane-induced blockade to nuclear accumulation of the androgen receptor predicts clinical responses in metastatic prostate cancer. Cancer Res 2011;71:6019-29.
32. Thadani-Mulero M, Nanus DM, Giannakakou P. Androgen receptor on the move: boarding the microtubule expressway to the nucleus. Cancer Res 2012;72:4611-5.
33. Attard G, Belldegrun AS, de Bono JS. Selective blockade of androgenic steroid synthesis by novel lyase inhibitors as a therapeutic strategy for treating metastatic prostate cancer. BJU Int 2005;96: 1241-6.
34. Tran C, Ouk S, Clegg NJ, Chen Y, Watson PA, Arora V, et al. Development of a second-generation antiandrogen for treatment of advanced prostate cancer. Science 2009;324:787-90.
35. Attard G, Reid AH, Yap TA, Raynaud F, Dowsett M, Settatree S, et al. 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 2008;26:4563-71.
36. Danila DC, Morris MJ, de Bono JS, Ryan CJ, Denmeade SR, Smith MR, et al. Phase II multicenter study of abiraterone acetate plus prednisone therapy in patients with docetaxel-treated castration-resistant prostate cancer. J Clin Oncol 2010;28:1496-501.
37. 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.
38. Mezynski J, Bianchini PD, Sandu ZS, Hunt TJ, Baikady SB, Maier SG, et al. Antitumour activity of docetaxel following treatment with the CYP17A1 inhibitor abiraterone: clinical evidence for cross-resistance? Ann Oncol 2012;23:2943-7.
39. 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.
40. Oh WK. The evolving role of estrogen therapy in prostate cancer. Clin Prostate Cancer 2002;1:81-9.
41. Huggins C, Hodges CV. Studies on prostatic cancer: I. The effect of castration, of estrogen and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate 1941. J Urol 2002;168: 9-12.
42. Flocks RH, Marberger H, Begley BJ, Prendergast LJ. Prostatic carcinoma: treatment of advanced cases with intravenous diethylstilbestrol diphosphate. J Urol 1955;74:549-51.
43. Sharp DC, Parry JM. Diethylstilboestrol: the binding and effects of diethylstilboestrol upon the polymerisation and depolymerisation of purified microtubule protein in vitro. Carcinogenesis 1985; 6:865-71.
44. Robertson CN, Roberson KM, Padilla GM, O'Brien ET, Cook JM, Kim CS, et al. Induction of apoptosis by diethylstilbestrol in hormone-insensitive prostate cancer cells. J Natl Cancer Inst 1996;88: 908-17.
45. de Voogt HJ, Smith PH, Pavone-Macaluso M, de Pauw M, Suciu S. Cardiovascular side effects of diethylstilbestrol, cyproterone acetate, medroxyprogesterone acetate and estramustine phosphate used for the treatment of advanced prostatic cancer: results from European Organization for Research on Treatment of Cancer trials 30761 and 30762. J Urol 1986;135:303-7.
46. Dahllof B, Bilstrom A, Cabral F, Hartley-Asp B. Estramustine depolymerizes microtubules by binding to tubulin. Cancer Res 1993;53: 4573-81.
47. Hudes GR, Greenberg R, Krigel RL, Fox S, Scher R, Litwin S, et al. Phase II study of estramustine and vinblastine, two microtubule inhibitors, in hormone-refractory prostate cancer. J Clin Oncol 1992;10: 1754-61.
48. Caffo O, Sava T, Comploj E, Fariello A, Zustovich F, Segati R, et al. Docetaxel, with or without estramustine phosphate, as first-line chemotherapy for hormone-refractory prostate cancer: results of a multicentre, randomized phase II trial. BJU Int 2008;102:1080-5.
49. Caffo O, Sava T, Comploj E, Fariello A, Zustovich F, Segati R, et al. Impact of docetaxel-based chemotherapy on quality of life of patients with castration-resistant prostate cancer: results from a prospective phase II randomized trial. BJU Int 2011;108:1825-32.
50. Fizazi K, Lesaunier F, Delva R, Gravis G, Rolland F, Priou F. A phase III trial of docetaxel-estramustine in high-risk localised prostate cancer: a planned analysis of response, toxicity and quality of life in the GETUG 12. trial. Eur J Cancer 2012;48:209-17.
51. Fotsis T, Zhang Y, Pepper MS, Adlercreutz H, Montesano R, Nawroth PP, et al. The endogenous oestrogen metabolite 2-methoxyoestradiol inhibits angiogenesis and suppresses tumour growth. Nature 1994;368:237-9.
52. Qadan LR, Perez-Stable CM, Anderson C, D'lppolito G, Herron A, Howard GA, et al. 2-Methoxyestradiol induces G2/M arrest and apoptosis in prostate cancer. Biochem Biophys Res Commun 2001;285: 1259-66.
53. Tevaarwerk AJ, Holen KD, Alberti DB, Sidor C, Arnott J, Quon C, et al. Phase I trial of 2-methoxyestradiol Nano Crystal dispersion in advanced solid malignancies. Clin Cancer Res 2009;15:1460-5.
54. Harrison MR, Hahn NM, Pili R, Oh WK, Hammers H, Sweeney C, et al. A phase II study of 2-methoxyestradiol (2ME2) Nano Crystal(R) dispersion (NCD) in patients with taxane-refractory, metastatic castrate-resistant prostate cancer (CRPC). Invest New Drugs 2011; 29:1465-74.
55. Mistry SJ, Atweh GF. Stathmin inhibition enhances okadaic acidinduced mitotic arrest: a potential role for stathmin in mitotic exit. J Biol Chem 2001;276:31209-15.
56. Marklund U, Larsson N, Gradin HM, Brattsand G, Gullberg M. Oncoprotein 18 is a phosphorylation-responsive regulator of microtubule dynamics. EMBO J 1996;15:5290-8.
57. Luo XN, Mookerjee B, Ferrari A, Mistry S, Atweh GF. Regulation of phosphoprotein p18 in leukemic cells. Cell cycle regulated phosphorylation by p34cdc2 kinase. J Biol Chem 1994;269:10312-8.
58. Belmont LD, Mitchison TJ. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell 1996;84:623-31.
59. Friedrich B, Gronberg H, Landstrom M, Gullberg M, Bergh A. Differentiation-stage specific expression of oncoprotein 18 in human and rat prostatic adenocarcinoma. Prostate 1995;27:102-9.
60. Tradonsky A, Rubin T, Beck R, Ring B, Seitz R, Mair S. A search for reliable molecular markers of prognosis in prostate cancer: a study of 240 cases. Am J Clin Pathol 2012;137:918-30.
61. Mistry SJ, Bank A, Atweh GF. Targeting stathmin in prostate cancer. Mol Cancer Ther 2005;4:1821-9.
62. Mistry SJ, Atweh GF. Therapeutic interactions between stathmin inhibition and chemotherapeutic agents in prostate cancer. Mol Cancer Ther 2006;5:3248-57.
63. Howell B, Deacon H, Cassimeris L. Decreasing oncoprotein 18/stathmin levels reduces microtubule catastrophes and increases microtubule polymer in vivo. J Cell Sci 1999;112:3713-22.
64. Parness J, Horwitz SB. Taxol binds to polymerized tubulin in vitro. J Biol Chem 1981;91:479-87.
65. Lock RB. Inhibition of p34cdc2 kinase activation, p34cdc2 tyrosine dephosphorylation, and mitotic progression in Chinese hamster ovary cells exposed to etoposide. Cancer Res 1992;52:1817-22.
66. Drechsel DN, Hyman AA, Cobb MH, Kirschner MW. Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 1992;3:1141-54.
67. Billingsley ML, Kincaid RL. Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration. Biochem J 1997;323: 577-91.
68. Sangrajrang S, Denoulet P, Millot G, Tatloud R, Podgorniak MP, Tew KD. Estramustine resistance correlates with tau over-expression in human prostatic carcinoma cells. Int J Cancer 1998;77:626-31.
69. Wagner P, Wang B, Clark E, Lee H, Rouzier R, Pusztai L. Microtubule associated protein (MAP)-Tau: a novel mediator of paclitaxel sensitivity in vitro and in vivo. Cell Cycle 2005;4:1149-52.
70. Mimori K, Sadanaga N, Yoshikawa Y, Ishikawa K, Hashimoto M, Tanaka F, et al. Reduced tau expression in gastric cancer can identify candidates for successful Paclitaxel treatment. Br J Cancer 2006; 94:1894-7.
71. Rouzier R, Rajan R, Wagner P, Hess KR, Gold DL, Stec J, et al. Microtubule-associated protein tau: a marker of paclitaxel sensitivity in breast cancer. Proc Natl Acad Sci U S A 2005;102: 8315-20.
72. Andre F, Hatzis C, Anderson K, Sotiriou C, Mazaouni C, Mejia J, et al. Microtubule-associated protein-tau is a bifunctional predictor of endocrine sensitivity and chemotherapy resistance in estrogen receptor-positive breast cancer. Clin Cancer Res 2007;13: 2061-7.
73. Golouh R, Cufer T, Sadikov A, Nussdorfer P, Usher PA, Brunner N, et al. The prognostic value of Stathmin-1, S100A2, and SYK proteins in ERpositive primary breast cancer patients treated with adjuvant tamoxifen monotherapy: an immunohistochemical study. Breast Cancer Res Treat 2008;110:317-26.
74. Drury SC, Detre S, Leary A, Salter J, Reis-Filho J, Barbahina V, et al. Changes in breast cancer biomarkers in the IGF1R/PI3K pathway in recurrent breast cancer after tamoxifen treatment. Endocr Relat Cancer 2011;18:565-77.
75. Baquero MT, Hanna JA, Neumeister V, Cheng H, Molinaro AM, Harris LN, et al. Stathmin expression and its relationship to microtubule-associated protein tau and outcome in breast cancer. Cancer 2012; 118:4660-9.