Targeting ribosomal S6 kinases/Y-box binding protein-1 signaling improves cellular sensitivity to taxane in prostate cancer

Prostate

Volumn 74, Issue 8, 2014, Pages 829-838

  Shiota, Masaki ^a   Itsumi, Momoe ^a   Yokomizo, Akira ^a   Takeuchi, Ario ^a   Imada, Kenjiro ^a   Kashiwagi, Eiji ^a   Inokuchi, Junichi ^a   Tatsugami, Katsunori ^a   Uchiumi, Takeshi ^a   Naito, Seiji ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

prostate cancer; RSK; taxane; YB 1

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PACLITAXEL; PROTEIN KINASE INHIBITOR; RAF PROTEIN; S6 KINASE; SL 0101; SMALL INTERFERING RNA; TAXANE DERIVATIVE; UNCLASSIFIED DRUG; Y BOX BINDING PROTEIN 1;

ARTICLE; CONTROLLED STUDY; CYTOTOXICITY ASSAY; DRUG TARGETING; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

PROSTATE CANCER; RSK; TAXANE; YB-1;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; BRIDGED COMPOUNDS; CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; DRUG RESISTANCE, NEOPLASM; GENE KNOCKDOWN TECHNIQUES; HUMANS; MALE; PACLITAXEL; PROSTATIC NEOPLASMS; RIBOSOMAL PROTEIN S6 KINASES; SIGNAL TRANSDUCTION; TAXOIDS; Y-BOX-BINDING PROTEIN 1;

EID: 84899587018     PISSN: 02704137     EISSN: 10970045     Source Type: Journal    
DOI: 10.1002/pros.22799     Document Type: Article

References (49)

1. Sharifi N, Gulley JL, Dahut WL,. An update on androgen deprivation therapy for prostate cancer. Endocr Relat Cancer 2010; 17: R305-R315.
2. Sadar MD,. Small molecule inhibitors targeting the "achilles' heel" of androgen receptor activity. Cancer Res 2011; 71: 1208-1213.
3. Shiota M, Yokomizo A, Naito S,. Pro-survival and anti-apoptotic properties of androgen receptor signaling by oxidative stress promote treatment resistance in prostate cancer. Endocr Relat Cancer 2012; 19: R245-R253.
4. Tannock IF, de Wit R, Berry WR, Horti J, Pluzanska A, Chi KN, Oudard S, Théodore C, James ND, Turesson I, Rosenthal MA, Eisenberger MA, TAX 327 Investigators. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N Engl J Med 2004; 351: 1502-1512.
5. Petrylak DP, Tangen CM, Hussain MH, Lara PN Jr, Jones JA, Taplin ME, Burch PA, Berry D, Moinpour C, Kohli M, Benson MC, Small EJ, Raghavan D, Crawford ED,. Docetaxel and estramustine compared with mitoxantrone and prednisone for advanced refractory prostate cancer. N Engl J Med 2004; 351: 1513-1520.
6. de Bono JS, Oudard S, Ozguroglu M, Hansen S, Machiels JP, Kocak I, Gravis G, Bodrogi I, Mackenzie MJ, Shen L, Roessner M, Gupta S, Sartor AO, TROPIC Investigators. Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: A randomised open-label trial. Lancet 2010; 376: 1147-1154.
7. Fujimoto N, Shiota M, Kubo T, Matsumoto T,. Novel therapeutic strategies following docetaxel-based chemotherapy in castration-resistant prostate cancer. Expert Rev Clin Pharmacol 2010; 3: 785-795.
8. Shiota M, Yokomizo A, Fujimoto N, Kuruma H, Naito S,. Castration-resistant prostate cancer: Novel therapeutics pre- or post- taxane administration. Curr Cancer Drug Targets 2013; 13: 444-459.
9. Kohno K, Izumi H, Uchiumi T, Ashizuka M, Kuwano M,. The pleiotropic functions of the Y-box-binding protein, YB-1. Bioessays 2003; 25: 691-698.
10. Kuwano M, Oda Y, Izumi H, Yang SJ, Uchiumi T, Iwamoto Y, Toi M, Fujii T, Yamana H, Kinoshita H, Kamura T, Tsuneyoshi M, Yasumoto K, Kohno K,. The role of nuclear Y-box binding protein 1 as a global marker in drug resistance. Mol Cancer Ther 2004; 3: 1485-1492.
11. Imada K, Shiota M, Kohashi K, Kuroiwa K, Song Y, Sugimoto M, Naito S, Oda Y,. Mutual regulation between Raf/MEK/ERK signaling and Y-box-binding protein-1 promotes prostate cancer progression. Clin Cancer Res 2013; 19: 4638-4650.
12. Giménez-Bonafé P, Fedoruk MN, Whitmore TG, Akbari M, Ralph JL, Ettinger S, Gleave ME, Nelson CC,. YB-1 is upregulated during prostate cancer tumor progression and increases P-glycoprotein activity. Prostate 2004; 59: 337-349.
13. Shiota M, Song Y, Takeuchi A, Yokomizo A, Kashiwagi E, Kuroiwa K, Tatsugami K, Uchiumi T, Oda Y, Naito S,. Antioxidant therapy alleviates oxidative stress by androgen deprivation and prevents conversion from androgen dependent to castration resistant prostate cancer. J Urol 2012; 187: 707-714.
14. Koike K, Uchiumi T, Ohga T, Toh S, Wada M, Kohno K, Kuwano M,. Nuclear translocation of the Y-box binding protein by ultraviolet irradiation. FEBS Lett 1997; 417: 390-394.
15. Fujita T, Ito K, Izumi H, Kimura M, Sano M, Nakagomi H, Maeno K, Hama Y, Shingu K, Tsuchiya S, Kohno K, Fujimori M,. Increased nuclear localization of transcription factor Y-box binding protein 1 accompanied by up-regulation of P-glycoprotein in breast cancer pretreated with paclitaxel. Clin Cancer Res 2005; 11: 8837-8844.
16. Shiota M, Zoubeidi A, Kumano M, Beraldi E, Naito S, Nelson CC, Sorensen PH, Gleave ME,. Clusterin is a critical downstream mediator of stress-induced YB-1 transactivation in prostate cancer. Mol Cancer Res 2011; 9: 1755-1766.
17. Cohen SB, Ma W, Valova VA, Algie M, Harfoot R, Woolley AG, Robinson PJ, Braithwaite AW,. Genotoxic stress-induced nuclear localization of oncoprotein YB-1 in the absence of proteolytic processing. Oncogene 2010; 29: 403-410.
18. To K, Fotovati A, Reipas KM, Law JH, Hu K, Wang J, Astanehe A, Davies AH, Lee L, Stratford AL, Raouf A, Johnson P, Berquin IM, Royer HD, Eaves CJ, Dunn SE,. Y-box binding protein-1 induces the expression of CD44 and CD49f leading to enhanced self-renewal, mammosphere growth, and drug resistance. Cancer Res 2010; 70: 2840-2851.
19. Toulany M, Schickfluss TA, Eicheler W, Kehlbach R, Schittek B, Rodemann HP,. Impact of oncogenic K-RAS on YB-1 phosphorylation induced by ionizing radiation. Breast Cancer Res 2011; 13: R28.
20. Shiota M, Izumi H, Tanimoto A, Takahashi M, Miyamoto N, Kashiwagi E, Kidani A, Hirano G, Masubuchi D, Fukunaka Y, Yasuniwa Y, Naito S, Nishizawa S, Sasaguri Y, Kohno K,. Programmed cell death protein 4 down-regulates Y-box binding protein-1 expression via a direct interaction with Twist1 to suppress cancer cell growth. Cancer Res 2009; 69: 3148-3156.
21. Shiota M, Yokomizo A, Itsumi M, Uchiumi T, Tada Y, Song Y, Kashiwagi E, Masubuchi D, Naito S,. Twist1 and Y-box-binding protein-1 promote malignant potential in bladder cancer cells. BJU Int 2011; 108: E142-E149.
22. Shiota M, Kashiwagi E, Yokomizo A, Takeuchi A, Dejima T, Song Y, Tatsugami K, Inokuchi J, Uchiumi T, Naito S,. Interaction between docetaxel resistance and castration resistance in prostate cancer: Implications of Twist1, YB-1, and androgen receptor. Prostate 2013; 73: 1336-1344.
23. Astanehe A, Finkbeiner MR, Krzywinski M, Fotovati A, Dhillon J, Berquin IM, Mills GB, Marra MA, Dunn SE,. MKNK1 is a YB-1 target gene responsible for imparting trastuzumab resistance and can be blocked by RSK inhibition. Oncogene 2012; 31: 4434-4446.
24. Coles LS, Lambrusco L, Burrows J, Hunter J, Diamond P, Bert AG, Vadas MA, Goodall GJ,. Phosphorylation of cold shock domain/Y-box proteins by ERK2 and GSK3β and repression of the human VEGF promoter. FEBS Lett 2005; 579: 5372-5378.
25. Jürchott K, Kuban RJ, Krech T, Blüthgen N, Stein U, Walther W, Friese C, Kiełbasa SM, Ungethüm U, Lund P, Knösel T, Kemmner W, Morkel M, Fritzmann J, Schlag PM, Birchmeier W, Krueger T, Sperling S, Sers C, Royer HD, Herzel H, Schäfer R,. Identification of Y-box binding protein 1 as a core regulator of MEK/ERK pathway-dependent gene signatures in colorectal cancer cells. PLoS Genet 2010; 6: e1001231.
26. Stratford AL, Fry CJ, Desilets C, Davies AH, Cho YY, Li Y, Dong Z, Berquin IM, Roux PP, Dunn SE,. Y-box binding protein-1 serine 102 is a downstream target of p90 ribosomal S6 kinase in basal-like breast cancer cells. Breast Cancer Res 2008; 10: R99.
27. Toulany M, Schickfluss TA, Eicheler W, Kehlbach R, Schittek B, Rodemann HP,. Impact of oncogenic K-RAS on YB-1 phosphorylation induced by ionizing radiation. Breast Cancer Res 2011; 13: R28.
28. Eisinger-Mathason TS, Andrade J, Lannigan DA,. RSK in tumorigenesis: Connections to steroid signaling. Steroids 2010; 75: 191-202.
29. Anjum R, Blenis J,. The RSK family of kinases: Emerging roles in cellular signalling. Nat Rev Mol Cell Biol 2008; 9: 747-758.
30. Stratford AL, Reipas K, Hu K, Fotovati A, Brough R, Frankum J, Takhar M, Watson P, Ashworth A, Lord CJ, Lasham A, Print CG, Dunn SE,. Targeting p90 ribosomal S6 kinase eliminates tumor-initiating cells by inactivating Y-box binding protein-1 in triple-negative breast cancers. Stem Cells 2012; 30: 1338-1348.
31. Steelman LS, Franklin RA, Abrams SL, Chappell W, Kempf CR, Bäsecke J, Stivala F, Donia M, Fagone P, Nicoletti F, Libra M, Ruvolo P, Ruvolo V, Evangelisti C, Martelli AM, McCubrey JA,. Roles of the Ras/Raf/MEK/ERK pathway in leukemia therapy. Leukemia 2011; 25: 1080-1094.
32. McCubrey JA, Steelman LS, Kempf CR, Chappell WH, Abrams SL, Stivala F, Malaponte G, Nicoletti F, Libra M, Bäsecke J, Maksimovic-Ivanic D, Mijatovic S, Montalto G, Cervello M, Cocco L, Martelli AM,. Therapeutic resistance resulting from mutations in Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR signaling pathways. J Cell Physiol 2011; 226: 2762-2781.
33. Smith JA, Poteet-Smith CE, Xu Y, Errington TM, Hecht SM, Lannigan DA,. Identification of the first specific inhibitor of p90 ribosomal S6 kinase (RSK) reveals an unexpected role for RSK in cancer cell proliferation. Cancer Res 2005; 65: 1027-1034.
34. Clark DE, Errington TM, Smith JA, Frierson HF Jr, Weber MJ, Lannigan DA,. The serine/threonine protein kinase, p90 ribosomal S6 kinase, is an important regulator of prostate cancer cell proliferation. Cancer Res 2005; 65: 3108-3116.
35. Romeo Y, Zhang X, Roux PP,. Regulation and function of the RSK family of protein kinases. Biochem J 2012; 441: 553-569.
36. Shiota M, Takeuchi A, Yokomizo A, Kashiwagi E, Tatsugami K, Kuroiwa K, Naito S,. Androgen receptor signaling regulates cell growth and vulnerability to doxorubicin in bladder cancer. J Urol 2012; 188: 276-286.
37. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Wong EW, Chang F, Lehmann B, Terrian DM, Milella M, Tafuri A, Stivala F, Libra M, Basecke J, Evangelisti C, Martelli AM, Franklin RA,. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta 2007; 1773: 1263-1284.
38. Cho YY, Yao K, Kim HG, Kang BS, Zheng D, Bode AM, Dong Z,. Ribosomal S6 kinase 2 is a key regulator in tumor promoter induced cell transformation. Cancer Res 2007; 67: 8104-8112.
39. Wang R, Jung SY, Wu CF, Qin J, Kobayashi R, Gallick GE, Kuang J,. Direct roles of the signaling kinase RSK2 in Cdc25C activation during Xenopus oocyte maturation. Proc Natl Acad Sci USA 2010; 107: 19885-19890.
40. Xing J, Ginty DD, Greenberg ME,. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 1996; 273: 959-963.
41. Zhang L, Cheng J, Ma Y, Thomas W, Zhang J, Du J,. Dual pathways for nuclear factor κB activation by angiotensin II in vascular smooth muscle: Phosphorylation of p65 by IκB kinase and ribosomal kinase. Circ Res 2005; 97: 975-982.
42. Buck M, Poli V, Hunter T, Chojkier M,. C/EBPβ phosphorylation by RSK creates a functional XEXD caspase inhibitory box critical for cell survival. Mol Cell 2001; 8: 807-816.
43. Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME,. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 1999; 286: 1358-1362.
44. Shimamura A, Ballif BA, Richards SA, Blenis J,. Rsk1 mediates a MEK-MAP kinase cell survival signal. Curr Biol 2000; 10: 127-135.
45. Anjum R, Roux PP, Ballif BA, Gygi SP, Blenis J,. The tumor suppressor DAP kinase is a target of RSK-mediated survival signaling. Curr Biol 2005; 15: 1762-1767.
46. Law JH, Li Y, To K, Wang M, Astanehe A, Lambie K, Dhillon J, Jones SJ, Gleave ME, Eaves CJ, Dunn SE,. Molecular decoy to the Y-box binding protein-1 suppresses the growth of breast and prostate cancer cells whilst sparing normal cell viability. PLoS ONE 2010; 5: e12661.
47. Mantwill K, Köhler-Vargas N, Bernshausen A, Bieler A, Lage H, Kaszubiak A, Surowiak P, Dravits T, Treiber U, Hartung R, Gansbacher B, Holm PS,. Inhibition of the multidrug-resistant phenotype by targeting YB-1 with a conditionally oncolytic adenovirus: Implications for combinatorial treatment regimen with chemotherapeutic agents. Cancer Res 2006; 66: 7195-7202.
48. Nguyen TL,. Targeting RSK: An overview of small molecule inhibitors. Anticancer Agents Med Chem 2008; 8: 710-716.
49. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P,. The selectivity of protein kinase inhibitors: A further update. Biochem J 2007; 408: 297-315.