Everolimus Enhances Gemcitabine-Induced Cytotoxicity in Bladder-Cancer Cell Lines

REFERENCES

• Anandappa , G. , Hollingdale , A. and Eisen , T. 2010 . Everolimus—A new approach in the treatment of renal cell carcinoma . Cancer Manage. Res. , 2 : 261 – 70 .
   Google Scholar
• Angelova , A. L. , Aprahamian , M. , Grekova , S. P. , Hajri , A. , Leuchs , B. , Giese , N. A. , Dinsart , C. , Herrmann , A. , Balboni , G. , Rommelaere , J. and Raykov , Z. 2009 . Improvement of gemcitabine-based therapy of pancreatic carcinoma by means of oncolytic parvovirus H-1PV . Clin. Cancer Res. , 15 : 511 – 19 .
   PubMed Web of Science ®Google Scholar
• Bergman , A. M. , Pinedo , H. M. and Peters , G. J. 2002 . Determinants of resistance to 2′,2′-difluorodeoxycytidine (gemcitabine) . Drug Resist. Update , 5 : 19 – 33 .
   PubMed Web of Science ®Google Scholar
• Boulay , A. , Zumstein-Mecker , S. , Stephan , C. , Beuvink , I. , Zilbermann , F. , Haller , R. , Tobler , S. , Heusser , C. , O'Reilly , T. , Stolz , B. , Marti , A. , Thomas , G. and Lane , H. A. 2004 . Antitumor efficacy of intermittent treatment schedules with the rapamycin derivative RAD001 correlates with prolonged inactivation of ribosomal protein S6 kinase 1 in peripheral blood mononuclear cells . Cancer Res. , 64 : 252 – 61 .
   PubMed Web of Science ®Google Scholar
• Bracho-Valdes , I. , Moreno-Alvarez , P. , Valencia-Martinez , I. , Robles-Molina , E. , Chavez-Vargas , L. and Vazquez-Prado , J. 2011 . mTORC1- and mTORC2-interacting proteins keep their multifunctional partners focused . IUBMB Life , 63 : 880 – 98 .
   Web of Science ®Google Scholar
• Chiang , C. T. , Yeh , P. Y. , Gao , M. , Chen , C. W. , Yeh , L. C. , Feng , W. C. , Kuo , S. H. , Hsu , C. H. , Lu , Y. S. and Cheng , A. L. 2010 . Combinations of mTORC1 inhibitor RAD001 with gemcitabine and paclitaxel for treating non-Hodgkin lymphoma . Cancer Lett. , 298 : 195 – 203 .
   PubMed Web of Science ®Google Scholar
• Chiong , E. , Lee , I. L. , Dadbin , A. , Sabichi , A. L. , Harris , L. , Urbauer , D. , McConkey , D. J. , Dickstein , R. J. , Cheng , T. and Grossman , H. B. 2011 . Effects of mTOR inhibitor everolimus (RAD001) on bladder cancer cells . Clin. Cancer Res. , 17 : 2863 – 73 .
   PubMed Web of Science ®Google Scholar
• Costello , B. A. , Qi , Y. , Borad , M. J. , Kim , G. P. , Northfelt , D. W. , Erlichman , C. , Alberts , S. R. , Rochester , M. N. , Scottsdale , A. Z. and Jacksonville , F. 2010 . Phase I trial of everolimus and gemcitabine for patients with solid tumors refractory to standard therapy and for a cohort of patients with cholangiocarcinoma/gallbladder cancer . J. Clin. Oncol. , 28 : 15s suppl.; abstr TPS166
   PubMed Web of Science ®Google Scholar
• da Silva , G. N. , de Castro Marcondes , J. P. , de Camargo , E. A. , da Silva Passos Junior , G. A , Sakamoto-Hojo , E. T. and Salvadori , D. M. 2010 . Cell cycle arrest and apoptosis in TP53 subtypes of bladder carcinoma cell lines treated with cisplatin and gemcitabine . Exp. Biol. Med. (Maywood) , 235 : 814 – 24 .
   PubMed Web of Science ®Google Scholar
• Dancey , J. E. 2006 . Therapeutic targets: MTOR and related pathways . Cancer Biol. Ther. , 5 : 1065 – 73 .
   PubMed Web of Science ®Google Scholar
• Donadelli , M. , Costanzo , C. , Beghelli , S. , Scupoli , M. T. , Dandrea , M. , Bonora , A. , Piacentini , P. , Budillon , A. , Caraglia , M. , Scarpa , A. and Palmieri , M. 2007 . Synergistic inhibition of pancreatic adenocarcinoma cell growth by trichostatin A and gemcitabine . Biochim. Biophys. Acta , 1773 : 1095 – 106 .
   PubMed Web of Science ®Google Scholar
• Flaig , T. W. , Su , L. J. , McCoach , C. , Li , Y. , Raben , D. , Varella-Garcia , M. and Bemis , L. T. 2009 . Dual epidermal growth factor receptor and vascular endothelial growth factor receptor inhibition with vandetanib sensitizes bladder cancer cells to cisplatin in a dose- and sequence-dependent manner . Br. J. Urol. Int. , 103 : 1729 – 37 .
   Google Scholar
• Garcia , J. A. and Danielpour , D. 2008 . Mammalian target of rapamycin inhibition as a therapeutic strategy in the management of urologic malignancies . Mol. Cancer Ther. , 7 : 1347 – 54 .
   PubMed Web of Science ®Google Scholar
• Gunelli , R. , Bercovich , E. , Nanni , O. , Ballardini , M. , Frassineti , G. L. , Giovannini , N. , Fiori , M. , Pasquini , E. , Ulivi , P. , Pappagallo , G. L. , Silvestrini , R. and Zoli , W. 2007 . Activity of endovesical gemcitabine in BCG-refractory bladder cancer patients: a translational study . Br. J. Cancer , 97 : 1499 – 504 .
   PubMed Web of Science ®Google Scholar
• Hadaschik , B. A. , ter Borg , M. G , Jackson , J. , Sowery , R. D. , So , A. I. , Burt , H. M. and Gleave , M. E. 2008 . Paclitaxel and cisplatin as intravesical agents against non-muscle-invasive bladder cancer . Br. J. Urol. Int. , 101 : 1347 – 55 .
   Google Scholar
• Haritunians , T. , Mori , A. , O'Kelly , J , Luong , Q. T. , Giles , F. J. and Koeffler , H. P. 2007 . Antiproliferative activity of RAD001 (everolimus) as a single agent and combined with other agents in mantle cell lymphoma . Leukemia , 21 : 333 – 39 .
   PubMed Web of Science ®Google Scholar
• Hayashi , H. , Kurata , T. and Nakagawa , K. 2011 . Gemcitabine: Efficacy in the treatment of advanced stage nonsquamous non-small cell lung cancer . Clin. Med. Insights Oncol. , 5 : 5177 – 84 .
   Google Scholar
• Huang , S. , Bjornsti , M. A. and Houghton , P. J. 2003 . Rapamycins: Mechanism of action and cellular resistance . Cancer Biol. Ther. , 2 : 222 – 32 .
   PubMed Web of Science ®Google Scholar
• Huang , Z. , Lin , L. , Gao , Y. , Chen , Y. , Yan , X. , Xing , J. and Hang , W. 2011 . Bladder cancer determination via two urinary metabolites: A biomarker pattern approach . Mol. Cell Proteomics. , doi: 10.1074/mcp.M111.007922
   Web of Science ®Google Scholar
• Hwang , S. K. and Kim , H. H. 2011 . The functions of mTOR in ischemic diseases . Biochem. Mol. Biol. Rep. , 44 : 506 – 11 .
   Google Scholar
• Iwata , K. , Aizawa , K. , Sakai , S. , Jingami , S. , Fukunaga , E. , Yoshida , M. , Hamada , A. and Saito , H. 2011 . The relationship between treatment time of gemcitabine and development of hematologic toxicity in cancer patients . Biol. Pharm. Bull. , 34 : 1765 – 68 .
   PubMed Web of Science ®Google Scholar
• Janus , A. , Robak , T. and Smolewski , P. 2005 . The mammalian target of the rapamycin (mTOR) kinase pathway: Its role in tumourigenesis and targeted antitumour therapy . Cell Mol. Biol. Lett. , 10 : 479 – 98 .
   PubMed Web of Science ®Google Scholar
• Jeon , H. G. , Yoon , C. Y. , Yu , J. H. , Park , M. J. , Lee , J. E. , Jeong , S. J. , Hong , S. K. , Byun , S. S. and Lee , S. E. 2011 . Induction of caspase mediated apoptosis and down-regulation of nuclear factor-kappaB and Akt signaling are involved in the synergistic antitumor effect of gemcitabine and the histone deacetylase inhibitor trichostatin A in human bladder cancer cells . J. Urol. , 186 : 2084 – 93 .
   PubMed Web of Science ®Google Scholar
• Kamat , A. M. and Mathew , P. 2011 . Bladder cancer: Imperatives for personalized medicine . Oncology , 25 : 951 – 58 .
   PubMed Web of Science ®Google Scholar
• Kilani , R. T. , Tamimi , Y. , Karmali , S. , Mackey , J. , Hanel , E. G. , Wong , K. K. and Moore , R. B. 2002 . Selective cytotoxicity of gemcitabine in bladder cancer cell lines . Anticancer Drugs , 13 : 557 – 66 .
   PubMed Web of Science ®Google Scholar
• Kirstein , M. N. , Brundage , R. C. , Moore , M. M. , Williams , B. W. , Hillman , L. A. , Dagit , J. W. , Fisher , J. E. , Marker , P. H. , Kratzke , R. A. and Yee , D. 2008 . Pharmacodynamic characterization of gemcitabine cytotoxicity in an in vitro cell culture bioreactor system . Cancer Chemother. Pharmacol. , 61 : 291 – 99 .
   PubMed Web of Science ®Google Scholar
• Ma , Y. , Yu , W. D. , Trump , D. L. and Johnson , C. S. 2010 . 1,25D3 enhances antitumor activity of gemcitabine and cisplatin in human bladder cancer models . Cancer , 116 : 3294 – 303 .
   PubMed Web of Science ®Google Scholar
• Macoska , J. A. , Adsule , S. , Tantivejkul , K. , Wang , S. , Pienta , K. J. and Lee , C. T. 2008 . -(-)Gossypol promotes the apoptosis of bladder cancer cells in vitro . Pharmacol Res , 58 : 323 – 31 .
   PubMed Web of Science ®Google Scholar
• Mansure , J. J. , Nassim , R. , Chevalier , S. , Rocha , J. , Scarlata , E. and Kassouf , W. 2009 . Inhibition of mammalian target of rapamycin as a therapeutic strategy in the management of bladder cancer . Cancer Biol Ther , 8 : 2339 – 47 .
   PubMed Web of Science ®Google Scholar
• Marinov , M. , Ziogas , A. , Pardo , O. E. , Tan , L. T. , Dhillon , T. , Mauri , F. A. , Lane , H. A. , Lemoine , N. R. , Zangemeister-Wittke , U. , Seckl , M. J. and Arcaro , A. 2009 . AKT/mTOR pathway activation and BCL-2 family proteins modulate the sensitivity of human small cell lung cancer cells to RAD001 . Clin. Cancer Res. , 15 : 1277 – 87 .
   PubMed Web of Science ®Google Scholar
• Mini , E. , Nobili , S. , Caciagli , B. , Landini , I. and Mazzei , T. 2006 . Cellular pharmacology of gemcitabine . Ann. Oncol. , 17 ( suppl. 5 ) : 7 – 12 .
   PubMed Web of Science ®Google Scholar
• Morgan , T. M. , Pitts , T. E. , Gross , T. S. , Poliachik , S. L. , Vessella , R. L. and Corey , E. 2008 . RAD001 (everolimus) inhibits growth of prostate cancer in the bone and the inhibitory effects are increased by combination with docetaxel and zoledronic acid . Prostate , 68 : 861 – 71 .
   PubMed Web of Science ®Google Scholar
• Muramaki , M. , Miyake , H. , Hara , I. , Kawabata , G. and Kamidono , S. 2004 . Synergistic inhibition of tumor growth and metastasis by combined treatment with TNP-470 and gemcitabine in a human bladder cancer KoTCC-1 model . J. Urol. , 172 : 1485 – 89 .
   PubMed Web of Science ®Google Scholar
• Nordentoft , I. , Dyrskjot , L. , Bodker , J. S. , Wild , P. J. , Hartmann , A. , Bertz , S. , Lehmann , J. , Orntoft , T. F. and Birkenkamp-Demtroder , K. 2011 . Increased expression of transcription factor TFAP2alpha correlates with chemosensitivity in advanced bladder cancer . BioMed Central Cancer , 11 : 135
   PubMed Web of Science ®Google Scholar
• O'Reilly , T. and McSheehy , P. M. 2010 . Biomarker development for the clinical activity of the mTOR inhibitor everolimus (RAD001): Processes, limitations, and further proposals . Translation Oncol. , 3 : 65 – 79 .
   PubMed Web of Science ®Google Scholar
• O'Reilly , T. , McSheehy , P. M. , Wartmann , M. , Lassota , P. , Brandt , R. and Lane , H. A. 2011 . Evaluation of the mTOR inhibitor, everolimus, in combination with cytotoxic antitumor agents using human tumor models in vitro and in vivo . Anticancer Drugs , 22 : 58 – 78 .
   PubMed Web of Science ®Google Scholar
• Pearce , H. L. and Miller , M. A. 2005 . The evolution of cancer research and drug discovery at Lilly Research Laboratories . Adv. Enzyme Regul. , 45 : 229 – 55 .
   PubMedGoogle Scholar
• Perabo , F. G. , Lindner , H. , Schmidt , D. , Huebner , D. , Blatter , J. , Fimmers , R. , Muller , S. C. and Albers , P. 2003 . Preclinical evaluation of gemcitabine/paclitaxel-interactions in human bladder cancer lines . Anticancer Res. , 23 : 4805 – 14 .
   PubMed Web of Science ®Google Scholar
• Pinto-Leite , R. , Botelho , P. , Ribeiro , E. , Oliveira , P. A. and Santos , L. 2009 . Effect of sirolimus on urinary bladder cancer T24 cell line . J. Exp. Clin. Cancer Res. 28: 3. ,
   PubMed Web of Science ®Google Scholar
• Roupret , M. , Zigeuner , R. , Palou , J. , Boehle , A. , Kaasinen , E. , Sylvester , R. , Babjuk , M. and Oosterlinck , W. 2011 . European guidelines for the diagnosis and management of upper urinary tract urothelial cell carcinomas: 2011 Update . Eur. Urol. , 59 : 584 – 94 .
   PubMed Web of Science ®Google Scholar
• Sehgal , S. N. 2003 . Sirolimus: Its discovery, biological properties, and mechanism of action . Transplant Proc. , 35 ( 3 suppl ) : 7S – 14S .
   PubMed Web of Science ®Google Scholar
• Siegel , R. , Ward , E. , Brawley , O. and Jemal , A. 2011 . Cancer statistics, 2011: The impact of eliminating socioeconomic and racial disparities on premature cancer deaths . CA Cancer J. Clin. , 61 : 212 – 36 .
   PubMed Web of Science ®Google Scholar
• Sonpavde , G. , Jian , W. , Liu , H. , Wu , M. F. , Shen , S. S. and Lerner , S. P. 2009 . Sunitinib malate is active against human urothelial carcinoma and enhances the activity of cisplatin in a preclinical model . Urol. Oncol. , 27 : 391 – 99 .
   PubMed Web of Science ®Google Scholar
• Spratlin , J. L. and Mulder , K. E. 2011 . Looking to the future: Biomarkers in the management of pancreatic adenocarcinoma . Int. J. Mol. Sci. , 12 : 5895 – 907 .
   PubMed Web of Science ®Google Scholar
• Su , B. and Jacinto , E. 2011 . Mammalian TOR signaling to the AGC kinases . Crit. Rev. Biochem. Mol. Biol. , 46 : 527 – 47 .
   PubMed Web of Science ®Google Scholar
• Toschi , L. , Finocchiaro , G. , Ceresoli , G. L. , Zucali , P. A. , Cavina , R. , Garassino , I. , De Vincenzo , F. , Santoro , A. and Cappuzzo , F. 2007 . Is gemcitabine cost effective in cancer treatment? . Expert Rev. Pharmacoecon. Outcomes Res. , 7 : 239 – 49 .
   PubMedGoogle Scholar
• Tuncyurek , P. , Mayer , J. M. , Klug , F. , Dillmann , S. , Henne-Bruns , D. , Keller , F. and Stracke , S. 2007 . Everolimus and mycophenolate mofetil sensitize human pancreatic cancer cells to gemcitabine in vitro: A novel adjunct to standard chemotherapy? . Eur. Surg. Res. , 39 : 380 – 87 .
   PubMed Web of Science ®Google Scholar
• Vasconcelos-Nóbrega , C. , Pinto-Leite , R. , Arantes-Rodrigues , R. , Ferreira , R. , Brochado , P. , Cardoso , M. L. , Palmeira , C. , Salvador , A. , Guedes-Teixeira , C. I. , Colaço , A , Palomino , L. F. , Lopes , C. , Santos , L. and Oliveira , P. A. 2011 . In vivo and in vitro effects of RAD001 on bladder cancer . Urol. Oncol. , doi: 10.1016/j.urolonc.2011.11.002
   PubMed Web of Science ®Google Scholar
• Veltkamp , S. A. , Pluim , D. , van Eijndhoven , M. A , Bolijn , M. J. , Ong , F. H. , Govindarajan , R. , Unadkat , J. D. , Beijnen , J. H. and Schellens , J. H. 2008 . New insights into the pharmacology and cytotoxicity of gemcitabine and 2′,2′-difluorodeoxyuridine . Mol. Cancer Ther. , 7 : 2415 – 25 .
   PubMed Web of Science ®Google Scholar
• Zoli , W. , Ricotti , L. , Tesei , A. , Ulivi , P. , Gasperi Campani , A. , Fabbri , F. , Gunelli , R. , Frassineti , G. L. and Amadori , D. 2004 . Schedule-dependent cytotoxic interaction between epidoxorubicin and gemcitabine in human bladder cancer cells in vitro . Clin. Cancer Res. , 10 : 1500 – 7 .
   PubMed Web of Science ®Google Scholar