Cyclooxygenase-2 Inhibitor NS398 Enhances Radiosensitivity of Radioresistant Esophageal Cancer Cells by Inhibiting AKT Activation and Inducing Apoptosis

REFERENCES

• Blot, W.J.; McLaughlin, J.K. The changing epidemiology of esophageal cancer. Semin Oncol 1999, 26(5 Suppl 15), 2–8.
   PubMed Web of Science ®Google Scholar
• Ng, T.; Dipetrillo, T.; Purviance, J.; Safran, H. Multimodality treatment of esophageal cancer: a review of the current status and future directions. Curr Oncol Rep 2006, 8(3), 174–182.
   PubMedGoogle Scholar
• Fukuda, K.; Sakakura, C.; Miyagawa, K.; Kuriu, Y.; Kin, S.; Nakase, Y.; Hagiwara, A.; Mitsufuji, S.; Okazaki, Y.; Hayashizaki, Y.; Yamagishi, H. Differential gene expression profiles of radioresistant oesophageal cancer cell lines established by continuous fractionated irradiation. Br J Cancer 2004, 91(8), 1543–1550.
   PubMed Web of Science ®Google Scholar
• Rich, T.A.; Shepard, R. COX-2 inhibitors as radiation sensitizers for upper GI tract cancers: esophagus, stomach, and pancreas. Am J Clin Oncol 2003, 26(4), S110–S113.
   PubMed Web of Science ®Google Scholar
• Zhang, X.; Morham, S.G.; Langenbach, R.; Young, D.A. Malignant transformation and antineoplastic actions of nonsteroidal antiinflammatory drugs (NSAIDs) on cyclooxygenase-null embryo fibroblasts. J Exp Med 1999, 190(4), 451–459.
   PubMed Web of Science ®Google Scholar
• Liu, J.F.; Jamieson, G.; Wu, T.C.; Zhang, S.W.; Wang, Q.Z.; Drew, P. Cyclooxygenase-2 expression in squamous cell carcinoma of the esophagus. Dis Esophagus 2006, 19(5), 350–354.
   PubMed Web of Science ®Google Scholar
• Terakado, N.; Shintani, S.; Yano, J.; Chunnan, L.; Mihara, M.; Nakashiro, K.; Hamakawa, H. Overexpression of cyclooxygenase-2 is associated with radioresistance in oral squamous cell carcinoma. Oral Oncol 2004, 40(4), 383–389.
   PubMed Web of Science ®Google Scholar
• Zhi, H.; Wang, L.; Zhang, J.; Zhou, C.; Ding, F.; Luo, A.; Wu, M.; Zhan, Q.; Liu, Z. Significance of COX-2 expression in human esophageal squamous cell carcinoma. Carcinogenesis 2006, 27(6), 1214–1221.
   PubMed Web of Science ®Google Scholar
• Heeren, P.; Plukker, J.; van Dullemen, H.; Nap, R.; Hollema, H. Prognostic role of cyclooxygenase-2 expression in esophageal carcinoma. Cancer Lett 2005, 225(2), 283–289.
   PubMed Web of Science ®Google Scholar
• Takatori, H.; Natsugoe, S.; Okumura, H.; Matsumoto, M.; Uchikado, Y.; Setoyama, T.; Sasaki, K.; Tamotsu, K.; Owaki, T.; Ishiqami, S.; Aikou, T. Cyclooxygenase-2 expression is related to prognosis in patients with esophageal squamous cell carcinoma. Eur J Surg Oncol 2008, 34(4), 397–402.
   PubMed Web of Science ®Google Scholar
• Huang, W.Z.; Fu, J.H.; Wang, D.K.; Hu, Y.; Liu, M.Z.; Yang, H.; Feng, Y.F.; Zheng, B.; Wang, G.; Luo, K.J.; Wen, J.; Rong, T.H. Overexpression of cyclooxygenase-2 is associated with chemoradiotherapy resistance and prognosis in esophageal squamous cell carcinoma patients. Dis Esophagus 2008, 21(8), 679–684.
   PubMed Web of Science ®Google Scholar
• Nix, P.; Lind, M.; Greenman, J.; Stafford, N.; Cawkwell, L. Expression of Cox-2 protein in radioresistant laryngeal cancer. Ann Oncol 2004, 15(5), 797–801.
   PubMed Web of Science ®Google Scholar
• Li, S.; Tong, Q.; Zhang, W.; Wang, Q.; Chen, Z.; Wu, Q. Mechanism of growth inhibitory effects of cyclooxygenase-2 inhibitor-NS398 on cancer cells. Cancer Invest 2008, 26(4), 333–337.
   PubMed Web of Science ®Google Scholar
• Liu, X.; Li, P.; Zhang, S.T.; You, H.; Jia, J.D.; Yu, Z.L. COX-2 mRNA expression in esophageal squamous cell carcinoma (ESCC) and effect by NSAID. Dis Esophagus 2008, 21(1), 9–14.
   PubMed Web of Science ®Google Scholar
• Gore, E. Celecoxib and radiation therapy in non-small-cell lung cancer. Oncology 2004, 18(14 Suppl 14), 10–14.
   PubMedGoogle Scholar
• Kim, N.; Kim, C.H.; Ahn, D.W.; Lee, K.S.; Cho, S.J.; Park, J.H.; Lee, M.K.; Kim, J.S.; Jung, H.C.; Song, I.S. Anti-gastric cancer effects of celecoxib, a selective COX-2 inhibitor, through inhibition of Akt signaling. J Gastroenterol Hepatol 2009, 24(3), 480–487.
   PubMed Web of Science ®Google Scholar
• Liu, B.; Shi, Z.L.; Feng, J.; Tao, H.M. Celecoxib, a cyclooxygenase-2 inhibitor, induces apoptosis in human osteosarcoma cell line MG-63 via down-regulation of PI3K/Akt. Cell Biol Int 2008, 32(5), 494–501.
   PubMed Web of Science ®Google Scholar
• Kulp, S.K.; Yang, Y.T.; Hung, C.C.; Chen, K.F.; Lai, J.P.; Tseng, P.H.; Fowble, J.W.; Ward, P.J.; Chen, C.S. 3-Phosphoinositide-dependent protein kinase-1/Akt signaling represents a major cyclooxygenase-2-independent target for celecoxib in prostate cancer cells. Cancer Res 2004, 64(4), 1444–1451.
   PubMed Web of Science ®Google Scholar
• Sinha-Datta, U.; Taylor, J.M.; Brown, M.; Nicot, C. Celecoxib disrupts the canonical apoptotic network in HTLV-I cells through activation of Bax and inhibition of PKB/Akt. Apoptosis 2008, 13(1), 33–40.
   PubMed Web of Science ®Google Scholar
• Shin, Y.K.; Park, J.S.; Kim, H.S.; Jun, H.J.; Kim, G.E.; Suh, C.O.; Yun, Y.S.; Pyo, H. Radiosensitivity enhancement by celecoxib, a cyclooxygenase (COX)-2 selective inhibitor, via COX-2-dependent cell cycle regulation on human cancer cells expressing differential COX-2 levels. Cancer Res 2005, 65(20), 9501–9509.
   PubMed Web of Science ®Google Scholar
• Deasy, B.M.; O’Sullivan-Coyne, G.; O’Donovan, T.R.; McKenna, S.L.; O’Sullivan, G.C. Cyclooxygenase-2 inhibitors demonstrate anti-proliferative effects in oesophageal cancer cells by prostaglandin E(2)-independent mechanisms. Cancer Lett 2007, 256(2), 246–258.
   PubMed Web of Science ®Google Scholar
• Liu, J.F.; Zhu, G.J.; Jamieson, G.G.; Wu, T.C.; Zhu, T.N.; Shan, B.E.; Drew, P.A. NS-398 induces apoptosis in human esophageal cancer cells through inhibition of NF-kappa B downstream regulation of cyclooxygenase-2. Cancer Invest 2009, 27(1), 17–23.
   PubMed Web of Science ®Google Scholar
• Brognard, J.; Clark, A.S.; Ni, Y.; Dennis, P.A. Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation. Cancer Res 2001, 61(10), 3986–3997.
   PubMed Web of Science ®Google Scholar
• Dent, P.; Yacoub, A.; Contessa, J.; Caron, R.; Amorino, G.; Valerie, K.; Hagan, M.P.; Grant, S.; Schmidt-Ullrich, R. Stress and radiation-induced activation of multiple intracellular signaling pathways. Radiat Res 2003, 159(3), 283–300.
   PubMed Web of Science ®Google Scholar
• Kulik, G.; Klippel, A.; Weber, M.J. Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol Cell Biol 1997, 17(3), 1595–1606.
   PubMed Web of Science ®Google Scholar
• Toulany, M.; Kehlbach, R.; Florczak, U.; Sak, A.; Wang, S.; Chen, J.; Lobrich, M.; Rodemann, H.P. Targeting of AKT1 enhances radiation toxicity of human tumor cells by inhibiting DNA-PKcs-dependent DNA double-strand break repair. Mol Cancer Ther 2008, 7(7), 1772–1781.
   PubMed Web of Science ®Google Scholar
• Bussink, J.; Van Der Kogel, A.J.; Kaanders, J.H. Activation of the PI3-K/AKT pathway and implications for radioresistance mechanisms in head and neck cancer. Lancet Oncol 2008, 9(3), 288–296.
   PubMed Web of Science ®Google Scholar
• Ward, S.; Sotsios, Y.; Dowden, J.; Bruce, I.; Finan, P. Therapeutic potential of phosphoinositide 3-kinase inhibitors. Chem Biol 2003, 10(3), 207–213.
   PubMed Web of Science ®Google Scholar
• Liao, Z.; Milas, L.; Komaki, R.; Stevens, C.; Cox, J.D. Combination of a COX-2 inhibitor with radiotherapy or radiochemotherapy in the treatment of thoracic cancer. Am J Clin Oncol 2003, 26(4), S85–S91.
   PubMed Web of Science ®Google Scholar
• Pyo, H.; Choy, H.; Amorino, G.P.; Kim, J.S.; Cao, Q.; Hercules, S.K.; DuBois, R.N. A selective cyclooxygenase-2 inhibitor, NS-398, enhances the effect of radiation in vitro and in vivo preferentially on the cells that express cyclooxygenase-2. Clin Cancer Res 2001, 7(10), 2998–3005.
   PubMed Web of Science ®Google Scholar
• Palayoor, S.T.; Arayankalayil, M.J.; Shoaibi, A.; Coleman, C.N. Radiation sensitivity of human carcinoma cells transfected with small interfering RNA targeted against cyclooxygenase-2. Clin Cancer Res 2005, 11(19 pt 1), 6980–6986.
   PubMed Web of Science ®Google Scholar
• Liu, W.; Chen, Y.; Wang, W.; Keng, P.; Finkelstein, J.; Hu, D.; Liang, L.; Guo, M.; Fenton, B.; Okunieff, P.; Ding, I. Combination of radiation and celebrex (celecoxib) reduce mammary and lung tumor growth. Am J Clin Oncol 2003, 26(4), S103–S109.
   PubMed Web of Science ®Google Scholar
• Sminia, P.; Kuipers, G.; Geldof, A.; Lafleur, V.; Slotman, B. COX-2 inhibitors act as radiosensitizer in tumor treatment. Biomed Pharmacother 2005, 59(Suppl 2), S272–S275.
   PubMedGoogle Scholar
• Lieber, M.R.; Ma, Y.; Pannicke, U.; Schwarz, K. Mechanism and regulation of human non-homologous DNA end-joining. Nat Rev Mol Cell Biol 2003, 4(9), 712–720.
   PubMed Web of Science ®Google Scholar
• Driscoll, M.; Jeggo, P.A. The role of double-strand break repair—insights from human genetics. Nat Rev Genet 2006, 7(1), 45–54.
   PubMed Web of Science ®Google Scholar
• Hsu, A.L.; Ching, T.T.; Wang, D.S.; Song, X.; Rangnekar, V.M.; Chen, C.S. The cyclooxygenase-2 inhibitor celecoxib induces apoptosis by blocking Akt activation in human prostate cancer cells independently of Bcl-2. J Biol Chem 2000, 275(15), 11397–11403.
   PubMed Web of Science ®Google Scholar
• Song, K.; Cornelius, S.C.; Reiss, M.; Danielpour, D. Insulin-like growth factor-I inhibits transcriptional responses of transforming growth factor-beta by phosphatidylinositol 3-kinase/Akt-dependent suppression of the activation of Smad3 but not Smad2. J Biol Chem 2003, 278(40), 38342–38351.
   PubMed Web of Science ®Google Scholar
• Davis, T.W.; O’Neal, J.M.; Pagel, M.D.; Zweifel, B.S.; Mehta, P.P.; Heuvelman, D.M.; Masferrer, J.L. Synergy between celecoxib and radiotherapy results from inhibition of cyclooxygenase-2-derived prostaglandin E2, a survival factor for tumor and associated vasculature. Cancer Res 2004, 64(1), 279–285.
   PubMed Web of Science ®Google Scholar
• Kang, K.B.; Wang, T.T.; Woon, C.T.; Cheah, E.S.; Moore, X.L.; Zhu, C.; Wong, M.C. Enhancement of glioblastoma radioresponse by a selective COX-2 inhibitor celecoxib: inhibition of tumor angiogenesis with extensive tumor necrosis. Int J Radiat Oncol Biol Phys 2007, 67(3), 888–896.
   PubMed Web of Science ®Google Scholar
• Dormond, O.; Foletti, A.; Paroz, C.; Rüegg, C. NSAIDs inhibit alpha V beta 3 integrin-mediated and Cdc42/Rac-dependent endothelial-cell spreading, migration and angiogenesis. Nat Med 2001, 7(9), 1041–1047.
   PubMed Web of Science ®Google Scholar
• Banu, N.; Buda, A.; Chell, S.; Elder, D.; Moorghen, M.; Paraskeva, C.; Qualtrough, D.; Pignatelli, M. Inhibition of COX-2 with NS-398 decreases colon cancer cell motility through blocking epidermal growth factor receptor transactivation: possibilities for combination therapy. Cell Prolif 2007, 40(5), 768–779.
   PubMed Web of Science ®Google Scholar
• Mehta, S.; Boddy, A.; Johnson, I.T.; Rhodes, M. Systematic review: Cyclo-oxygenase-2 in human oesophageal adenocarcinogenesis. Aliment Pharmacol Ther 2006, 24(9), 1321–1331.
   PubMed Web of Science ®Google Scholar