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Expert Review of Endocrinology & Metabolism Volume 8, 2013 - Issue 4
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Review

Emerging therapeutics targeting castration-resistant prostate cancer: the AR-mageddon of tumor epithelial–mesenchymal transition

Lauren N Hendrix Division of Urology, University of Kentucky College of Medicine, Lexington, KY, USA; Division of Urology, University of Kentucky College of Medicine, Lexington, KY, USA
,
David A Hamilton Jr Division of Urology, University of Kentucky College of Medicine, Lexington, KY, USA; Division of Urology, University of Kentucky College of Medicine, Lexington, KY, USA
&
Natasha Kyprianou Division of Urology, University of Kentucky College of Medicine, Lexington, KY, USA. [email protected]; Department of Molecular and Cellular Biochemistry, University of Kentucky College of Medicine, Lexington, KY, USA; Department of Pathology, University of Kentucky College of Medicine, Lexington, KY, USA
Pages 403-416 | Published online: 10 Jan 2014

References

  • Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA. Cancer J. Clin. 62(1), 10–29 (2012).
  • 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. 167(2 Pt 2), 948–951; discussion 952 (2002).
  • Mostaghel EA, Montgomery B, Nelson PS. Castration-resistant prostate cancer: targeting androgen metabolic pathways in recurrent disease. Urol. Oncol. 27(3), 251–257 (2009).
  • Tannock IF, de Wit R, Berry WR et al.; TAX 327 Investigators. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N. Engl. J. Med. 351(15), 1502–1512 (2004).
  • 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).
  • de Bono JS, Oudard S, Ozguroglu M et al.; TROPIC Investigators. Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial. Lancet 376(9747), 1147–1154 (2010).
  • Garcia JA, Dreicer R. Immunotherapy in castration-resistant prostate cancer: integrating sipuleucel-T into our current treatment paradigm. Oncology (Williston Park, N.Y.) 25(3), 242–249 (2011).
  • Sakamoto S, McCann RO, Dhir R, Kyprianou N. Talin1 promotes tumor invasion and metastasis via focal adhesion signaling and anoikis resistance. Cancer Res. 70(5), 1885–1895 (2010).
  • Mahon KL, Henshall SM, Sutherland RL, Horvath LG. Pathways of chemotherapy resistance in castration-resistant prostate cancer. Endocr. Relat. Cancer 18(4), R103–R123 (2011).
  • Gelmann EP. Molecular biology of the androgen receptor. J. Clin. Oncol. 20(13), 3001–3015 (2002).
  • Azzouni F, Mohler J. Biology of castration-recurrent prostate cancer. Urol. Clin. North Am. 39(4), 435–452 (2012).
  • Heemers HV, Tindall DJ. Androgen receptor (AR) coregulators: a diversity of functions converging on and regulating the AR transcriptional complex. Endocr. Rev. 28(7), 778–808 (2007).
  • Gottlieb B, Beitel LK, Wu JH, Trifiro M. The androgen receptor gene mutations database (ARDB): 2004 update. Hum. Mutat. 23(6), 527–533 (2004).
  • 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. 64(24), 9209–9216 (2004).
  • Niu Y, Chang TM, Yeh S, Ma WL, Wang YZ, Chang C. Differential androgen receptor signals in different cells explain why androgen-deprivation therapy of prostate cancer fails. Oncogene 29(25), 3593–3604 (2010).
  • Mulholland DJ, Tran LM, Li Y et al. Cell autonomous role of PTEN in regulating castration-resistant prostate cancer growth. Cancer Cell 19(6), 792–804 (2011).
  • Carver BS, Chapinski C, Wongvipat J et al. Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer. Cancer Cell 19(5), 575–586 (2011).
  • Kim JJ, Keizman D, Denmeade SR, Antonarakis ES. The unfolding treatment landscape for men with castration-resistant prostate cancer. Clin. Investig. (Lond.) 1(11), 1533–1544 (2011).
  • Friedlander T, Roy R, Tomlins S et al. Common structural and epigenetic changes in the genome of castrate-resistant prostate cancer. Cancer Res. 68, 4447–4454 (2008).
  • Lu W, Xie Y, Ma Y, Matusik RJ, Chen Z. ARF represses androgen receptor transactivation in prostate cancer. Mol. Endocrinol. 27(4), 635–648 (2013).
  • Friedlander TW, Ryan CJ. Targeting the androgen receptor. Urol. Clin. North Am. 39(4), 453–464 (2012).
  • Small EJ, Halabi S, Dawson NA et al. Antiandrogen withdrawal alone or in combination with ketoconazole in androgen-independent prostate cancer patients: a Phase III trial (CALGB 9583). J. Clin. Oncol. 22(6), 1025–1033 (2004).
  • Katagiri M, Kagawa N, Waterman MR. The role of cytochrome b5 in the biosynthesis of androgens by human P450c17. Arch. Biochem. Biophys. 317(2), 343–347 (1995).
  • Keizman D, Huang P, Carducci MA, Eisenberger MA. Contemporary experience with ketoconazole in patients with metastatic castration-resistant prostate cancer: clinical factors associated with PSA response and disease progression. Prostate 72(4), 461–467 (2012).
  • Attard G, Reid AH, Yap TA 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. 26(28), 4563–4571 (2008).
  • Schweizer MT, Antonarakis ES. Abiraterone and other novel androgen-directed strategies for the treatment of prostate cancer: a new era of hormonal therapies is born. Ther. Adv. Urol. 4(4), 167–178 (2012).
  • de Bono JS, Logothetis CJ, Molina A et al.; COU-AA-301 Investigators. Abiraterone and increased survival in metastatic prostate cancer. N. Engl. J. Med. 364(21), 1995–2005 (2011).
  • Ryan CJ, Smith MR, de Bono JS et al. Interim analysis results of COU-AA-302, a randomized, Phase III study of abiraterone acetate in chemotherapy-naïve patients with metastatic castration-resistant prostate cancer. J. Clin. Oncol. 30(Suppl.), Abstract LBA4518 (2012).
  • Cai H, Babic I, Wei X, Huang J, Witte ON. Invasive prostate carcinoma driven by c-Src and androgen receptor synergy. Cancer Res. 71(3), 862–872 (2011).
  • Attard G, Reid A, Olmos D, de Bono JS. Antitumor activity with CYP17 blockade indicates that castration-resistant prostate cancer frequently remains hormone driven. Cancer Res. 69(12), 4937–4940 (2009).
  • Agus D, Stadler W, Shevrin L et al. Safety, efficacy, and pharmacodynamics of the investigational agent TAK-700 in metastatic castration-resistant prostate cancer: updated data from a Phase I/II study. J. Clin. Oncol. 29(Suppl.), Abstract 4531 (2011).
  • Vasaitis T, Belosay A, Schayowitz A et al. Androgen receptor inactivation contributes to antitumor efficacy of 17{α}-hydroxylase/17,20-lyase inhibitor 3β-hydroxy-17-(1H-benzimidazole-1-yl)androsta-5,16-diene in prostate cancer. Mol. Cancer Ther. 7(8), 2348–2357 (2008).
  • Vasaitis TS, Bruno RD, Njar VC. CYP17 inhibitors for prostate cancer therapy. J. Steroid Biochem. Mol. Biol. 125(1–2), 23–31 (2011).
  • Taplin M, Chu Franklin F, Morrison JP et al. ARMOR1: safety of galeterone (TOK-001) in a Phase I clinical trial in chemotherapy-naïve patients with castration-resistant prostate cancer (CRPC). Cancer Res. 72(8)(Suppl. 1), Abstract CT-07 (2012).
  • Chen CD, Welsbie DS, Tran C et al. Molecular determinants of resistance to antiandrogen therapy. Nat. Med. 10(1), 33–39 (2004).
  • Scher HI, Beer TM, Higano CS et al.; Prostate Cancer Foundation/Department of Defense Prostate Cancer Clinical Trials Consortium. Antitumour activity of MDV3100 in castration-resistant prostate cancer: a Phase 1–2 study. Lancet 375(9724), 1437–1446 (2010).
  • 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).
  • Scher HI, Fizazi K, Saad F et al.; for the AFFIRM Investigators. Effect of MDV3100, an androgen receptor signaling inhibitor, on overall survival in patients with prostate cancer post docetaxel: results from the Phase III AFFIRM Study. J. Clin. Oncol. 30(Suppl. 5), Abstract LBA1 (2012).
  • de Bono JS, Fizazi K, Saad F et al.; for the AFFIRM Investigators. Primary, secondary, and quality-of-life endpoints from the Phase III AFFIRM study. J. Clin. Oncol. 30(Suppl.), Abstract 4519 (2012).
  • Clegg NJ, Wongvipat J, Joseph JD et al. ARN-509: a novel antiandrogen for prostate cancer treatment. Cancer Res. 72(6), 1494–1503 (2012).
  • Foster WR, Car BD, Shi H et al. Drug safety is a barrier to the discovery and development of new androgen receptor antagonists. Prostate 71(5), 480–488 (2011).
  • Rathkopf D, Danila D, Morris M et al. Phase I/II safety and pharmacokinetic (PK) study of ARN-509 in patients with metastatic castration-resistant prostate cancer (mCRPC): Phase I results of a Prostate Cancer Clinical Trials Consortium Study. J. Clin. Oncol. 30(Suppl. 5), Abstract 43 (2012).
  • Schiewer MJ, Goodwin JF, Han S et al. Dual roles of PARP-1 promote cancer growth and progression. Cancer Discov. 2(12), 1134–1149 (2012).
  • Zhang Y, Castaneda S, Dumble M et al. Reduced expression of the androgen receptor by third generation of antisense shows antitumor activity in models of prostate cancer. Mol. Cancer Ther. 10(12), 2309–2319 (2011).
  • Loddick SA, Bradbury R, Broadbent N et al. Preclinical profile of AZD3514: A small molecule-targeting androgen receptor function with a novel mechanism of action and the potential to treat castration-resistant prostate cancer. Cancer Res. 72(8 Suppl. 1), Abstract 3848 (2012).
  • Andersen RJ, Mawji NR, Wang J et al. Regression of castrate-recurrent prostate cancer by a small-molecule inhibitor of the amino-terminus domain of the androgen receptor. Cancer Cell 17(6), 535–546 (2010).
  • Ischia J, Saad F, Gleave M. The promise of heat shock protein inhibitors in the treatment of castration resistant prostate cancer. Curr. Opin. Urol. 23(3), 194–200 (2013).
  • Catelli MG, Binart N, Jung-Testas I et al. The common 90-kd protein component of non-transformed ‘8S’ steroid receptors is a heat-shock protein. EMBO J. 4(12), 3131–3135 (1985).
  • Hayashi N, Peacock JW, Beraldi E, Zoubeidi A, Gleave ME, Ong CJ. Hsp27 silencing coordinately inhibits proliferation and promotes Fas-induced apoptosis by regulating the PEA-15 molecular switch. Cell Death Differ. 19(6), 990–1002 (2012).
  • Chi KN, Yu EY, Ellard S et al. OGX-427 in castration resistant prostate cancer patients. Presented at: 37th ESMO Congress. Vienna, Austria, ix297, 28 September–2 October 2012.
  • Shiota M, Zoubeidi A, Kumano M et al. Clusterin is a critical downstream mediator of stress-induced YB-1 transactivation in prostate cancer. Mol. Cancer Res. 9(12), 1755–1766 (2011).
  • Saad F, Hotte S, North S et al.; Canadian Uro-Oncology Group. 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(17), 5765–5773 (2011).
  • Lamoureux F, Thomas C, Yin MJ et al. A novel HSP90 inhibitor delays castrate-resistant prostate cancer without altering serum PSA levels and inhibits osteoclastogenesis. Clin. Cancer Res. 17(8), 2301–2313 (2011).
  • Heath EI, Hillman DW, Vaishampayan U et al. A Phase II trial of 17-allylamino-17-demethoxygeldanamycin in patients with hormone-refractory metastatic prostate cancer. Clin. Cancer Res. 14(23), 7940–7946 (2008).
  • Michelotti GA, Price DT, Schwinn DA. α 1-adrenergic receptor regulation: basic science and clinical implications. Pharmacol. Ther. 88(3), 281–309 (2000).
  • Desiniotis A, Kyprianou N. Advances in the design and synthesis of prazosin derivatives over the last ten years. Expert Opin. Ther. Targets 15(12), 1405–1418 (2011).
  • Arends MJ, Wyllie AH. Apoptosis: mechanisms and roles in pathology. Int. Rev. Exp. Pathol. 32, 223–254 (1991).
  • Kyprianou N. Induction of apoptosis by α1-adrenoceptor antagonists in benign prostatic hyperplasia and prostate cancer. Prostate Cancer Prostatic Dis. 3(S1), S24–S25 (2000).
  • Isaacs JT. Apoptosis: translating theory to therapy for prostate cancer. J. Natl. Cancer Inst. 92(17), 1367–1369 (2000).
  • Siu FM, Ma DL, Cheung YW et al. Proteomic and transcriptomic study on the action of a cytotoxic saponin (Polyphyllin D): induction of endoplasmic reticulum stress and mitochondria-mediated apoptotic pathways. Proteomics 8(15), 3105–3117 (2008).
  • Kyprianou N, Litvak JP, Borkowski A, Alexander R, Jacobs SC. Induction of prostate apoptosis by doxazosin in benign prostatic hyperplasia. J. Urol. 159(6), 1810–1815 (1998).
  • Brogden RN, Heel RC, Speight TM, Avery GS. Prazosin: a review of its pharmacological properties and therapeutic efficacy in hypertension. Drugs 14(3), 163–197 (1977).
  • Kyprianou N, Benning CM. Suppression of human prostate cancer cell growth by α1-adrenoceptor antagonists doxazosin and terazosin via induction of apoptosis. Cancer Res. 60(16), 4550–4555 (2000).
  • Yang G, Timme TL, Park SH, Wu X, Wyllie MG, Thompson TC. Transforming growth factor beta 1 transduced mouse prostate reconstitutions: II. Induction of apoptosis by doxazosin. Prostate 33(3), 157–163 (1997).
  • Kyprianou N, Chon J, Benning CM. Effects of α(1)-adrenoceptor (α(1)-AR) antagonists on cell proliferation and apoptosis in the prostate: therapeutic implications in prostatic disease. Prostate Suppl. 9, 42–46 (2000).
  • Kyprianou N, Isaacs JT. Expression of transforming growth factor-beta in the rat ventral prostate during castration-induced programmed cell death. Mol. Endocrinol. 3(10), 1515–1522 (1989).
  • Kim IY, Ahn HJ, Zelner DJ et al. Loss of expression of transforming growth factor beta type I and type II receptors correlates with tumor grade in human prostate cancer tissues. Clin. Cancer Res. 2(8), 1255–1261 (1996).
  • Wrana JL, Attisano L, Wieser R, Ventura F, Massagué J. Mechanism of activation of the TGF-beta receptor. Nature 370(6488), 341–347 (1994).
  • Kyprianou N. Doxazosin and terazosin suppress prostate growth by inducing apoptosis: clinical significance. J. Urol. 169(4), 1520–1525 (2003).
  • Noble AJ, Chess-Williams R, Couldwell C et al. The effects of tamsulosin, a high affinity antagonist at functional α 1A- and α 1D-adrenoceptor subtypes. Br. J. Pharmacol. 120(2), 231–238 (1997).
  • Tahmatzopoulos A, Kyprianou N. Apoptotic impact of α1-blockers on prostate cancer growth: a myth or an inviting reality? Prostate 59(1), 91–100 (2004).
  • Pan SL, Guh JH, Huang YW, Chern JW, Chou JY, Teng CM. Identification of apoptotic and antiangiogenic activities of terazosin in human prostate cancer and endothelial cells. J. Urol. 169(2), 724–729 (2003).
  • Partin JV, Anglin IE, Kyprianou N. Quinazoline-based α 1-adrenoceptor antagonists induce prostate cancer cell apoptosis via TGF-beta signalling and I kappa B α induction. Br. J. Cancer 88(10), 1615–1621 (2003).
  • Fernando MA, Heaney AP. α1-adrenergic receptor antagonists: novel therapy for pituitary adenomas. Mol. Endocrinol. 19(12), 3085–3096 (2005).
  • Garrison JB, Shaw YJ, Chen CS, Kyprianou N. Novel quinazoline-based compounds impair prostate tumorigenesis by targeting tumor vascularity. Cancer Res. 67(23), 11344–11352 (2007).
  • Sakamoto S, Schwarze S, Kyprianou N. Anoikis disruption of focal adhesion–Akt signaling impairs renal cell carcinoma. Eur. Urol. 59(5), 734–744 (2011).
  • Giardinà D, Martarelli D, Sagratini G et al. Doxazosin-related α1-adrenoceptor antagonists with prostate antitumor activity. J. Med. Chem. 52(15), 4951–4954 (2009).
  • Guo Y, Kyprianou N. Restoration of transforming growth factor beta signaling pathway in human prostate cancer cells suppresses tumorigenicity via induction of caspase-1-mediated apoptosis. Cancer Res. 59(6), 1366–1371 (1999).
  • Mendelsohn J, Baselga J. The EGF receptor family as targets for cancer therapy. Oncogene 19(56), 6550–6565 (2000).
  • Wheeler DL, Dunn EF, Harari PM. Understanding resistance to EGFR inhibitors-impact on future treatment strategies. Nat. Rev. Clin. Oncol. 7(9), 493–507 (2010).
  • Canil CM, Moore MJ, Winquist E et al. Randomized Phase II study of two doses of gefitinib in hormone-refractory prostate cancer: a trial of the National Cancer Institute of Canada-Clinical Trials Group. J. Clin. Oncol. 23(3), 455–460 (2005).
  • Small EJ, Fontana J, Tannir N et al. A Phase II trial of gefitinib in patients with non-metastatic hormone-refractory prostate cancer. BJU Int. 100(4), 765–769 (2007).
  • Joensuu G, Joensuu T, Nupponen N et al. A Phase II trial of gefitinib in patients with rising PSA following radical prostatectomy or radiotherapy. Acta Oncol. 51(1), 130–133 (2012).
  • Curigliano G, Pelosi G, De Pas T et al. Absence of epidermal growth factor receptor gene mutations in patients with hormone refractory prostate cancer not responding to gefitinib. Prostate 67(6), 603–604 (2007).
  • Carrión-Salip D, Panosa C, Menendez JA et al. Androgen-independent prostate cancer cells circumvent EGFR inhibition by overexpression of alternative HER receptors and ligands. Int. J. Oncol. 41(3), 1128–1138 (2012).
  • Nabhan C, Lestingi TM, Galvez A et al. Erlotinib has moderate single-agent activity in chemotherapy-naïve castration-resistant prostate cancer: final results of a Phase II trial. Urology 74(3), 665–671 (2009).
  • Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 139(5), 871–890 (2009).
  • Matuszak EA, Kyprianou N. Androgen regulation of epithelial-mesenchymal transition in prostate tumorigenesis. Expert Rev. Endocrinol. Metab. 6(3), 469–482 (2011).
  • Xu J, Lamouille S, Derynck R. TGF-beta-induced epithelial to mesenchymal transition. Cell Res. 19(2), 156–172 (2009).
  • Zavadil J, Böttinger EP. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 24(37), 5764–5774 (2005).
  • Bhowmick NA, Ghiassi M, Bakin A et al. Transforming growth factor-β1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol. Biol. Cell 12(1), 27–36 (2001).
  • Bakin AV, Tomlinson AK, Bhowmick NA, Moses HL, Arteaga CL. Phosphatidylinositol 3-kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition and cell migration. J. Biol. Chem. 275(47), 36803–36810 (2000).
  • Lee YI, Kwon YJ, Joo CK. Integrin-linked kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition. Biochem. Biophys. Res. Commun. 316(4), 997–1001 (2004).
  • Lo HW, Hsu SC, Xia W et al. Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res. 67(19), 9066–9076 (2007).
  • Graham TR, Zhau HE, Odero-Marah VA et al. Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithelial-to-mesenchymal transition in human prostate cancer cells. Cancer Res. 68(7), 2479–2488 (2008).
  • Acevedo VD, Gangula RD, Freeman KW et al. Inducible FGFR-1 activation leads to irreversible prostate adenocarcinoma and an epithelial-to-mesenchymal transition. Cancer Cell 12(6), 559–571 (2007).
  • Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119(6), 1420–1428 (2009).
  • Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer 9(4), 265–273 (2009).
  • Kalluri R. EMT: when epithelial cells decide to become mesenchymal-like cells. J. Clin. Invest. 119(6), 1417–1419 (2009).
  • Zhu ML, Kyprianou N. Role of androgens and the androgen receptor in epithelial-mesenchymal transition and invasion of prostate cancer cells. FASEB J. 24(3), 769–777 (2010).
  • Sirotnak FM, She Y, Khokhar NZ, Hayes P, Gerald W, Scher HI. Microarray analysis of prostate cancer progression to reduced androgen dependence: studies in unique models contrasts early and late molecular events. Mol. Carcinog. 41(3), 150–163 (2004).
  • Yakes FM, Chen J, Tan J et al. Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth. Mol. Cancer Ther. 10(12), 2298–2308 (2011).
  • Smith DC, Smith MR, Sweeney C et al. Cabozantinib in patients with advanced prostate cancer: results of a Phase II randomized discontinuation trial. J. Clin. Oncol. 31(4), 412–419 (2013).
  • Wu K, Zeng J, Li L et al. Silibinin reverses epithelial-to-mesenchymal transition in metastatic prostate cancer cells by targeting transcription factors. Oncol. Reports 23, 1545–1552 (2010).
  • Flaig TW, Glodé M, Gustafson D et al. A study of high-dose oral silybin-phytosome followed by prostatectomy in patients with localized prostate cancer. Prostate 70(8), 848–855 (2010).
  • Harris AM, Warner BW, Wilson JM et al. Effect of α1-adrenoceptor antagonist exposure on prostate cancer incidence: an observational cohort study. J. Urol. 178(5), 2176–2180 (2007).
  • Armstrong AJ, Eisenberger MA, Halabi S et al. Biomarkers in the management and treatment of men with metastatic castration-resistant prostate cancer. Eur. Urol. 61(3), 549–559 (2012).

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