STAT3 and STAT5A are potential therapeutic targets in castration-resistant prostate cancer

Oncotarget

Volumn 8, Issue 49, 2017, Pages 85997-86010

  Mohanty, Sambit K ^a   Yagiz, Kader ^a   Pradhan, Dinesh ^b   Luthringer, Daniel J ^a   Amin, Mahul B ^c   Alkan, Serhan ^a   Cinar, Bekir ^d,e  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^d CLARK ATLANTA UNIVERSITY   (United States)

^e EMORY UNIVERSITY   (United States)

Author keywords

Castration resistance; Pimozide; Prostate cancer; STAT3; STAT5A

Indexed keywords

MESSENGER RNA; PIMOZIDE; STAT3 PROTEIN; STAT5A PROTEIN;

22RV1 CELL LINE; ADULT; AGED; ANDROGEN DEPRIVATION THERAPY; APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER RESISTANCE; CASTRATION RESISTANT PROSTATE CANCER; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GLEASON SCORE; HUMAN; HUMAN CELL; HUMAN TISSUE; JAK-STAT SIGNALING; LNCAP C4-2 CELL LINE; LNCAP CELL LINE; MALE; METASTASIS; MIDDLE AGED; PC-3 [HUMAN PROSTATE CARCINOMA] CELL LINE; PROSTATE HYPERTROPHY; PROTEIN EXPRESSION; STAT3 GENE; STAT5A GENE; VERY ELDERLY;

EID: 85031504172     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.20844     Document Type: Article

References (65)

1. Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2017. CA Cancer J Clin. 2017; 67:7-30
2. Zhou Y, Bolton EC, Jones JO. Androgens and androgen receptor signaling in prostate tumorigenesis. J Mol Endocrinol. 2015; 54:R15-29
3. Wang D, Tindall DJ. Androgen action during prostate carcinogenesis. Methods Mol Biol. 2011; 776:25-44
4. Saylor PJ. Prostate cancer: The androgen receptor remains front and centre. Nat Rev Clin Oncol. 2013; 10:126-128
5. Feldman BJ, Feldman D. The development of androgenindependent prostate cancer. Nat Rev Cancer. 2001; 1:34-45
6. Cancer Genome Atlas Research Network. The Molecular Taxonomy of Primary Prostate Cancer. Cell. 2015; 163:1011-1025
7. Yuan X, Cai C, Chen S, Chen S, Yu Z, Balk SP. Androgen receptor functions in castration-resistant prostate cancer and mechanisms of resistance to new agents targeting the androgen axis. Oncogene. 2014; 33:2815-2825
8. Yin L, Hu Q. CYP17 inhibitors abiraterone, C17,20-lyase inhibitors and multi-targeting agents. Nat Rev Urol. 2014; 11:32-42
9. Watson PA, Arora VK, Sawyers CL. Emerging mechanisms of resistance to androgen receptor inhibitors in prostate cancer. Nat Rev Cancer. 2015; 15:701-711
10. Lorente D, Mateo J, Zafeiriou Z, Smith AD, Sandhu S, Ferraldeschi R, de Bono JS. Switching and withdrawing hormonal agents for castration-resistant prostate cancer. Nat Rev Urol. 2015; 12:37-47
11. Harris WP, Mostaghel EA, Nelson PS, Montgomery B. Androgen deprivation therapy: progress in understanding mechanisms of resistance and optimizing androgen depletion. Nat Clin Pract Urol. 2009; 6:76-85
12. Ciccarese C, Santoni M, Brunelli M, Buti S, Modena A, Nabissi M, Artibani W, Martignoni G, Montironi R, Tortora G, Massari F. AR-V7 and prostate cancer: The watershed for treatment selection? Cancer Treat Rev. 2016; 43:27-35
13. Antonarakis ES, Lu C, Wang H, Luber B, Nakazawa M, Roeser JC, Chen Y, Mohammad TA, Chen Y, Fedor HL, Lotan TL, Zheng Q, De Marzo AM, et al. AR-V7 and resistance to enzalutamide and abiraterone in prostate cancer. N Engl J Med. 2014; 371:1028-1038
14. Katzenwadel A, Wolf P. Androgen deprivation of prostate cancer: Leading to a therapeutic dead end. Cancer Lett. 2015; 367:12-17
15. Beltran H, Tomlins S, Aparicio A, Arora V, Rickman D, Ayala G, Huang J, True L, Gleave ME, Soule H, Logothetis C, Rubin MA. Aggressive variants of castration-resistant prostate cancer. Clin Cancer Res. 2014; 20:2846-2850
16. Attard G, Reid AH, Olmos D, de Bono JS. Antitumor activity with CYP17 blockade indicates that castration-resistant prostate cancer frequently remains hormone driven. Cancer Res. 2009; 69:4937-4940
17. Ardiani A, Farsaci B, Rogers CJ, Protter A, Guo Z, King TH, Apelian D, Hodge JW. Combination therapy with a secondgeneration androgen receptor antagonist and a metastasis vaccine improves survival in a spontaneous prostate cancer model. Clin Cancer Res. 2013; 19:6205-6218
18. Alva A, Hussain M. Intermittent androgen deprivation therapy in advanced prostate cancer. Curr Treat Options Oncol. 2014; 15:127-136
19. Wagner KU, Schmidt JW. The two faces of Janus kinases and their respective STATs in mammary gland development and cancer. J Carcinog. 2011; 10:32
20. Zhang X, Blaskovich MA, Forinash KD, Sebti SM. Withacnistin inhibits recruitment of STAT3 and STAT5 to growth factor and cytokine receptors and induces regression of breast tumours. Br J Cancer. 2014; 111:894-902
21. Valgeirsdottir S, Paukku K, Silvennoinen O, Heldin CH, Claesson-Welsh L. Activation of Stat5 by platelet-derived growth factor (PDGF) is dependent on phosphorylation sites in PDGF beta-receptor juxtamembrane and kinase insert domains. Oncogene. 1998; 16:505-515
22. Sato K, Nagao T, Iwasaki T, Nishihira Y, Fukami Y. Srcdependent phosphorylation of the EGF receptor Tyr-845 mediates Stat-p21waf1 pathway in A431 cells. Genes Cells. 2003; 8:995-1003
23. Runge DM, Runge D, Foth H, Strom SC, Michalopoulos GK. STAT 1alpha/1beta, STAT 3 and STAT 5: expression and association with c-MET and EGF-receptor in longterm cultures of human hepatocytes. Biochem Biophys Res Commun. 1999; 265:376-381
24. Neilson LM, Zhu J, Xie J, Malabarba MG, Sakamoto K, Wagner KU, Kirken RA, Rui H. Coactivation of janus tyrosine kinase (Jak)1 positively modulates prolactin-Jak2 signaling in breast cancer: recruitment of ERK and signal transducer and activator of transcription (Stat)3 and enhancement of Akt and Stat5a/b pathways. Mol Endocrinol. 2007; 21:2218-2232
25. Kirken RA, Erwin RA, Wang L, Wang Y, Rui H, Farrar WL. Functional uncoupling of the Janus kinase 3-Stat5 pathway in malignant growth of human T cell leukemia virus type 1-transformed human T cells. J Immunol. 2000; 165:5097-5104
26. Katsha A, Arras J, Soutto M, Belkhiri A, El-Rifai W. AURKA regulates JAK2-STAT3 activity in human gastric and esophageal cancers. Mol Oncol. 2014; 8:1419-1428
27. Frost RA, Nystrom GJ, Lang CH. Regulation of IGF-I mRNA and signal transducers and activators of transcription-3 and-5 (Stat-3 and-5) by GH in C2C12 myoblasts. Endocrinology. 2002; 143:492-503
28. Chang M, Kanwar N, Feng E, Siu A, Liu X, Ma D, Jongstra J. PIM kinase inhibitors downregulate STAT3(Tyr705) phosphorylation. Mol Cancer Ther. 2010; 9:2478-2487
29. Gu L, Dagvadorj A, Lutz J, Leiby B, Bonuccelli G, Lisanti MP, Addya S, Fortina P, Dasgupta A, Hyslop T, Bubendorf L, Nevalainen MT. Transcription factor Stat3 stimulates metastatic behavior of human prostate cancer cells in vivo, whereas Stat5b has a preferential role in the promotion of prostate cancer cell viability and tumor growth. Am J Pathol. 2010; 176:1959-1972
30. Cocchiola R, Romaniello D, Grillo C, Altieri F, Liberti M, Magliocca FM, Chichiarelli S, Marrocco I, Borgoni G, Perugia G, Eufemi M. Analysis of STAT3 post-translational modifications (PTMs) in human prostate cancer with different Gleason Score. Oncotarget. 2017; 8:42560-70. https://doi.org/10.18632/oncotarget.17245
31. Don-Doncow N, Marginean F, Coleman I, Nelson PS, Ehrnstrom R, Krzyzanowska A, Morrissey C, Hellsten R, Bjartell A. Expression of STAT3 in Prostate Cancer Metastases. Eur Urol. 2017; 71:313-316
32. Gu L, Liao Z, Hoang DT, Dagvadorj A, Gupta S, Blackmon S, Ellsworth E, Talati P, Leiby B, Zinda M, Lallas CD, Trabulsi EJ, McCue P, et al. Pharmacologic inhibition of Jak2-Stat5 signaling By Jak2 inhibitor AZD1480 potently suppresses growth of both primary and castrate-resistant prostate cancer. Clin Cancer Res. 2013; 19:5658-5674
33. Haddad BR, Gu L, Mirtti T, Dagvadorj A, Vogiatzi P, Hoang DT, Bajaj R, Leiby B, Ellsworth E, Blackmon S, Ruiz C, Curtis M, Fortina P, et al. STAT5A/B gene locus undergoes amplification during human prostate cancer progression. Am J Pathol. 2013; 182:2264-2275
34. Han G, Yu JY, Chen YD, Cao XL, Zhu J, Wang W, Wang XX, Zhang X, Yan JQ, Gao JP. The usefulness of phosphorylated-signal transduction and activators of transcription 3 in detecting prostate cancer from negative biopsies. Eur J Surg Oncol. 2012; 38:367-373
35. Ni Z, Lou W, Lee SO, Dhir R, DeMiguel F, Grandis JR, Gao AC. Selective activation of members of the signal transducers and activators of transcription family in prostate carcinoma. J Urol. 2002; 167:1859-1862
36. Singh N, Hussain S, Bharadwaj M, Kakkar N, Singh SK, Sobti RC. Overexpression of signal transducer and activator of transcription (STAT-3 and STAT-5) transcription factors and alteration of suppressor of cytokine signaling (SOCS-1) protein in prostate cancer. J Recept Signal Transduct Res. 2012; 32:321-327
37. Singh RP, Raina K, Deep G, Chan D, Agarwal R. Silibinin suppresses growth of human prostate carcinoma PC-3 orthotopic xenograft via activation of extracellular signalregulated kinase 1/2 and inhibition of signal transducers and activators of transcription signaling. Clin Cancer Res. 2009; 15:613-621
38. Tam L, McGlynn LM, Traynor P, Mukherjee R, Bartlett JM, Edwards J. Expression levels of the JAK/STAT pathway in the transition from hormone-sensitive to hormone-refractory prostate cancer. Br J Cancer. 2007; 97:378-383
39. Nelson EA, Walker SR, Weisberg E, Bar-Natan M, Barrett R, Gashin LB, Terrell S, Klitgaard JL, Santo L, Addorio MR, Ebert BL, Griffin JD, Frank DA. The STAT5 inhibitor pimozide decreases survival of chronic myelogenous leukemia cells resistant to kinase inhibitors. Blood. 2011; 117:3421-3429
40. Epstein JI, Amin MB, Beltran H, Lotan TL, Mosquera JM, Reuter VE, Robinson BD, Troncoso P, Rubin MA. Proposed morphologic classification of prostate cancer with neuroendocrine differentiation. Am J Surg Pathol. 2014; 38:756-767
41. Mohanty SK, Smith SC, Chang E, Luthringer DJ, Gown AM, Aron M, Amin MB. Evaluation of contemporary prostate and urothelial lineage biomarkers in a consecutive cohort of poorly differentiated bladder neck carcinomas. Am J Clin Pathol. 2014; 142:173-183
42. Ylitalo EB, Thysell E, Jernberg E, Lundholm M, Crnalic S, Egevad L, Stattin P, Widmark A, Bergh A, Wikstrom P. Subgroups of Castration-resistant Prostate Cancer Bone Metastases Defined Through an Inverse Relationship Between Androgen Receptor Activity and Immune Response. Eur Urol. 2017; 71:776-787
43. Horoszewicz JS, Leong SS, Kawinski E, Karr JP, Rosenthal H, Chu TM, Mirand EA, Murphy GP. LNCaP model of human prostatic carcinoma. Cancer Res. 1983; 43:1809-1818
44. Thalmann GN, Anezinis PE, Chang SM, Zhau HE, Kim EE, Hopwood VL, Pathak S, von Eschenbach AC, Chung LW. Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer. Cancer Res. 1994; 54:2577-2581
45. Kaighn ME, Narayan KS, Ohnuki Y, Lechner JF, Jones LW. Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol. 1979; 17:16-23
46. Sramkoski RM, Pretlow TG 2nd, Giaconia JM, Pretlow TP, Schwartz S, Sy MS, Marengo SR, Rhim JS, Zhang D, Jacobberger JW. A new human prostate carcinoma cell line, 22Rv1. In Vitro Cell Dev Biol Anim. 1999; 35:403-409
47. Beltran H, Prandi D, Mosquera JM, Benelli M, Puca L, Cyrta J, Marotz C, Giannopoulou E, Chakravarthi BV, Varambally S, Tomlins SA, Nanus DM, Tagawa ST, et al. Divergent clonal evolution of castrationresistant neuroendocrine prostate cancer. Nat Med. 2016; 22:298-305
48. Stephenson AJ, Bolla M, Briganti A, Cozzarini C, Moul JW, Roach M 3rd, van Poppel H, Zietman A. Postoperative radiation therapy for pathologically advanced prostate cancer after radical prostatectomy. Eur Urol. 2012; 61:443-451
49. Warde P, Mason M, Ding K, Kirkbride P, Brundage M, Cowan R, Gospodarowicz M, Sanders K, Kostashuk E, Swanson G, Barber J, Hiltz A, Parmar MK, et al, and NCIC CTG PR.3/MRC UK PR07 investigators. Combined androgen deprivation therapy and radiation therapy for locally advanced prostate cancer: a randomised, phase 3 trial. Lancet. 2011; 378:2104-2111
50. Ferraldeschi R, Welti J, Luo J, Attard G, de Bono JS. Targeting the androgen receptor pathway in castrationresistant prostate cancer: progresses and prospects. Oncogene. 2015; 34:1745-1757
51. Smith DC, Smith MR, Sweeney C, Elfiky AA, Logothetis C, Corn PG, Vogelzang NJ, Small EJ, Harzstark AL, Gordon MS, Vaishampayan UN, Haas NB, Spira AI, et al. Cabozantinib in patients with advanced prostate cancer: results of a phase II randomized discontinuation trial. J Clin Oncol. 2013; 31:412-419
52. Quinn DI, Tangen CM, Hussain M, Lara PN Jr, Goldkorn A, Moinpour CM, Garzotto MG, Mack PC, Carducci MA, Monk JP, Twardowski PW, Van Veldhuizen PJ, Agarwal N, et al. Docetaxel and atrasentan versus docetaxel and placebo for men with advanced castration-resistant prostate cancer (SWOG S0421): a randomised phase 3 trial. Lancet Oncol. 2013; 14:893-900
53. Clarke RA, Allen BJ. Next-generation therapy for residual prostate cancer. Immunotherapy. 2013; 5:1235-1241
54. Santer FR, Erb HH, McNeill RV. Therapy escape mechanisms in the malignant prostate. Semin Cancer Biol. 2015; 35:133-144
55. Robinson D, Van Allen EM, Wu YM, Schultz N, Lonigro RJ, Mosquera JM, Montgomery B, Taplin ME, Pritchard CC, Attard G, Beltran H, Abida W, Bradley RK, et al. Integrative clinical genomics of advanced prostate cancer. Cell. 2015; 161:1215-1228
56. Kroon P, Berry PA, Stower MJ, Rodrigues G, Mann VM, Simms M, Bhasin D, Chettiar S, Li C, Li PK, Maitland NJ, Collins AT. JAK-STAT blockade inhibits tumor initiation and clonogenic recovery of prostate cancer stem-like cells. Cancer Res. 2013; 73:5288-5298
57. Kwon EM, Holt SK, Fu R, Kolb S, Williams G, Stanford JL, Ostrander EA. Androgen metabolism and JAK/STAT pathway genes and prostate cancer risk. Cancer Epidemiol. 2012; 36:347-353
58. Gu L, Vogiatzi P, Puhr M, Dagvadorj A, Lutz J, Ryder A, Addya S, Fortina P, Cooper C, Leiby B, Dasgupta A, Hyslop T, Bubendorf L, et al. Stat5 promotes metastatic behavior of human prostate cancer cells in vitro and in vivo. Endocr Relat Cancer. 2010; 17:481-493
59. Borcherding DC, Tong W, Hugo ER, Barnard DF, Fox S, LaSance K, Shaughnessy E, Ben-Jonathan N. Expression and therapeutic targeting of dopamine receptor-1 (D1R) in breast cancer. Oncogene. 2016; 35:3103-3113
60. Hussein N, Amawi H, Karthikeyan C, Hall FS, Mittal R, Trivedi P, Ashby CR Jr, Tiwari AK. The dopamine D3 receptor antagonists PG01037, NGB2904, SB277011A, and U99194 reverse ABCG2 transporter-mediated drug resistance in cancer cell lines. Cancer Lett. 2017; 396:167-180
61. Jandaghi P, Najafabadi HS, Bauer AS, Papadakis AI, Fassan M, Hall A, Monast A, von Knebel Doeberitz M, Neoptolemos JP, Costello E, Greenhalf W, Scarpa A, Sipos B, et al. Expression of DRD2 Is Increased in Human Pancreatic Ductal Adenocarcinoma and Inhibitors Slow Tumor Growth in Mice. Gastroenterology. 2016; 151:1218-1231
62. Roy S, Lu K, Nayak MK, Bhuniya A, Ghosh T, Kundu S, Ghosh S, Baral R, Dasgupta PS, Basu S. Activation of D2 Dopamine Receptors in CD133+ve Cancer Stem Cells in Non-small Cell Lung Carcinoma Inhibits Proliferation, Clonogenic Ability, and Invasiveness of These Cells. J Biol Chem. 2017; 292:435-445
63. Sachlos E, Risueño RM, Laronde S, Shapovalova Z, Lee JH, Russell J, Malig M, McNicol JD, Fiebig-Comyn A, Graham M, Levadoux-Martin M, Lee JB, Giacomelli AO, et al. Identification of drugs including a dopamine receptor antagonist that selectively target cancer stem cells. Cell. 2012; 149:1284-1297
64. Cinar B, Collak FK, Lopez D, Akgul S, Mukhopadhyay NK, Kilicarslan M, Gioeli DG, Freeman MR. MST1 is a multifunctional caspase-independent inhibitor of androgenic signaling. Cancer Res. 2011; 71:4303-4313
65. Kuser-Abali G, Alptekin A, Lewis M, Garraway IP, Cinar B. YAP1 and AR interactions contribute to the switch from androgen-dependent to castration-resistant growth in prostate cancer. Nat Commun. 2015; 6:8126