Rapamycin enhances chemotherapy-induced cytotoxicity by inhibiting the expressions of TS and ERK in gastric cancer cells

International Journal of Cancer

Volumn 126, Issue 11, 2010, Pages 2716-2725

  Shigematsu, Hideo ^a   Yoshida, Kazuhiro ^b   Sanada, Yuichi ^b   Osada, Shinnji ^b   Takahashi, Takao ^b   Wada, Yoshiyuki ^a   Konishi, Kazuo ^a   Okada, Morihito ^a   Fukushima, Masakazu ^c  

^a HIROSHIMA UNIVERSITY   (Japan)

^b GIFU UNIVERSITY   (Japan)

^c TAIHO PHARMACEUTICAL CO LTD   (Japan)

Author keywords

Apoptosis; Cisplatin; Docetaxel; ERK1 2; Fluorouracil; G1 arrest; Gastric cancer; JNK; Mtor; Rapamycin; S6K1

Indexed keywords

CASPASE; CISPLATIN; DOCETAXEL; FLUOROURACIL; INITIATION FACTOR 4E BINDING PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RAPAMYCIN; STRESS ACTIVATED PROTEIN KINASE; SYNTHETASE; THYMIDILATE SYNTHASE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; ANTINEOPLASTIC ANTIBIOTIC; MITOGEN ACTIVATED PROTEIN KINASE; TAXOID;

ARTICLE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CYTOTOXICITY; DRUG MECHANISM; DRUG POTENTIATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STOMACH CANCER; APOPTOSIS; CELL CYCLE; CELL DIVISION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; STOMACH TUMOR; TUMOR CELL LINE;

ANTIBIOTICS, ANTINEOPLASTIC; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE; CELL DIVISION; CELL LINE, TUMOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; SIGNAL TRANSDUCTION; SIROLIMUS; STOMACH NEOPLASMS; TAXOIDS;

EID: 77951221545     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24990     Document Type: Article

References (54)

1. Cunningham D, Starling N, Rao S, Iveson T, Nicolson M, Coxon F, Middleton G, Daniel F, Oates J, Norman AR. Capecitabine and oxaliplatin for advanced esophagogastric cancer. N Engl J Med 2008; 358:36-46.
2. Ajani JA, Moiseyenko VM, Tjulandin S, Majlis A, Constenla M, Boni C, Rodrigues A, Fodor M, Chao Y, Voznyi E, Marabotti C, Van Cutsem E. Clinical benefit with docetaxel plus fluorouracil and cisplatin compared with cisplatin and fluorouracil in a phase III trial of advanced gastric or gastroesophageal cancer adenocarcinoma: the V-325 Study Group. J Clin Oncol 2007; 25:3205-3209 (Pubitemid 47333732)
3. Koizumi W, Kurihara M, Nakano S, Hasegawa K. Phase II study of S-1, a novel oral derivative of 5-fluorouracil, in advanced gastric cancer. For the S-1 Cooperative Gastric Cancer Study Group. Oncology 2000;58:191-197 (Pubitemid 30189900)
4. Yoshida K, Ninomiya M, Takakura N, Hirabayashi N, Takiyama W, Sato Y, Todo S, Terashima M, Gotoh M, Sakamoto J, Nishiyama M. Phase II study of docetaxel and S-1 combination therapy for advanced or recurrent gastric cancer. Clin Cancer Res 2006;12(11 Pt 1):3402-3407 (Pubitemid 43917349)
5. Koizumi W, Narahara H, Hara T, Takagane A, Akiya T, Takagi M, Miyashita K, Nishizaki T, Kobayashi O, Takiyama W, Toh Y, Nagaie T, et al. S-1 plus cisplatin versus S-1 alone for first-line treatment of advanced gastric cancer (SPIRITS trial): a phase III trial. Lancet Oncol 2008;9:215-221
6. Chin KI, H.Imamura, H. Irinotecan plus S-1(IRIS) versus S-1 alone as first-line treatment for advanced gastric cancer: preliminary results of a randomized phase III study (GC0301/TOP002). J Clin Oncol 2007;25(18suppl):4524.
7. Wada Y, Yoshida K, Suzuki T, Mizuiri H, Konishi K, Ukon K, Tanabe K, Sakata Y, Fukushima M. Synergistic effects of docetaxel and S-1 by modulating the expression of metabolic enzymes of 5-fluorouracil in human gastric cancer cell lines. Int J Cancer 2006;119:783-791 (Pubitemid 44055889)
8. Yoshida K, Yamaguchi K, Osada S, Kawaguchi Y, Takahashi T, Sakashita F, Tanaka Y. Challenge for a better combination with basic evidence. Int J Clin Oncol 2008;13:212-219 (Pubitemid 351871900)
9. Martin ME, Perez MI, Redondo C, Alvarez MI, Salinas M, Fando JL. 4E binding protein 1 expression is inversely correlated to the progression of gastrointestinal cancers. Int J Biochem Cell Biol 2000;32: 633-642 (Pubitemid 30227360)
10. Nam SY, Lee HS, Jung GA, Choi J, Cho SJ, Kim MK, Kim WH, Lee BL. Akt/PKB activation in gastric carcinomas correlates with clinicopathologic variables and prognosis. APMIS 2003;111:1105-1113 (Pubitemid 38091249)
11. Lang SA, Gaumann A, Koehl GE, Seidel U, Bataille F, Klein D, Ellis LM, Bolder U, Hofstaedter F, Schlitt HJ, Geissler EK, Stoeltzing O. Mammalian target of rapamycin is activated in human gastric cancer and serves as a target for therapy in an experimental model. Int J Cancer 2007; 120:1803-1810 (Pubitemid 46399369)
12. Yu G, Wang J, Chen Y, Wang X, Pan J, Li G, Jia Z, Li Q, Yao JC, Xie K. Overexpression of phosphorylated mammalian target of rapamycin predicts lymph node metastasis and prognosis of chinese patients with gastric cancer. Clin Cancer Res 2009;15:1821-1829
13. Murayama T, Inokuchi M, Takagi Y, Yamada H, Kojima K, Kumagai J, Kawano T, Sugihara K. Relation between outcomes and localisation of p-mTOR expression in gastric cancer. Br J Cancer 2009;100:782-788
14. Bjornsti MA, Houghton PJ. The TOR pathway: a target for cancer therapy. Nat Rev Cancer 2004;4:335-348 (Pubitemid 38579480)
15. Janus A, Robak T, Smolewski P. The mammalian target of the rapamycin (mTOR) kinase pathway: its role in tumourigenesis and targeted antitumour therapy. Cell Mol Biol Lett 2005;10:479-498 (Pubitemid 41564520)
16. Sehgal SN, Baker H, Vezina C. Rapamycin (AY-22,989), a new antifungal antibiotic. II. Fermentation, isolation and characterization. J Antibiot (Tokyo) 1975; 28:727-732
17. Vezina C, Kudelski A, Sehgal SN. Rapamycin (AY-22,989), a new antifungal antibiotic. I. Taxonomy of the producing streptomycete and isolation of the active principle. J Antibiot (Tokyo) 1975;28:721-726
18. Brown EJ, Albers MW, Shin TB, Ichikawa K, Keith CT, Lane WS, Schreiber SL. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 1994;369:756-758 (Pubitemid 24225367)
19. Hashemolhosseini S, Nagamine Y, Morley SJ, Desrivieres S, Mercep L, Ferrari S. Rapamycin inhibition of the G1 to S transition is mediated by effects on cyclin D1 mRNA and protein stability. J Biol Chem 1998;273:14424-14429 (Pubitemid 28319162)
20. Del Bufalo D, Ciuffreda L, Trisciuoglio D, Desideri M, Cognetti F, Zupi G, Milella M. Antiangiogenic potential of the mammalian target of rapamycin inhibitor temsirolimus. Cancer Res 2006;66:5549-5554 (Pubitemid 43927103)
21. Shi Y, Frankel A, Radvanyi LG, Penn LZ, Miller RG, Mills GB. Rapamycin enhances apoptosis and increases sensitivity to cisplatin in vitro. Cancer Res 1995;55: 1982-1988
22. Grunwald V, DeGraffenried L, Russel D, Friedrichs WE, Ray RB, Hidalgo M. Inhibitors of mTOR reverse doxorubicin resistance conferred by PTEN status in prostate cancer cells. Cancer Res 2002;62: 6141-6145 (Pubitemid 35244463)
23. Mondesire WH, Jian W, Zhang H, Ensor J, Hung MC, Mills GB, Meric-Bernstam F. Targeting mammalian target of rapamycin synergistically enhances chemotherapy-induced cytotoxicity in breast cancer cells. Clin Cancer Res 2004;10:7031-7042 (Pubitemid 39383055)
24. Dancey JE. Clinical development of mammalian target of rapamycin inhibitors. Hematol Oncol Clin North Am 2002;16: 1101-1114 (Pubitemid 35462916)
25. Atkins MB, Hidalgo M, Stadler WM, Logan TF, Dutcher JP, Hudes GR, Park Y, Liou SH, Marshall B, Boni JP, Dukart G, Sherman ML. Randomized phase II study of multiple dose levels of CCI-779, a novel mammalian target of rapamycin kinase inhibitor, in patients with advanced refractory renal cell carcinoma. J Clin Oncol 2004;22:909-918 (Pubitemid 41103603)
26. Chan S, Scheulen ME, Johnston S, Mross K, Cardoso F, Dittrich C, Eiermann W, Hess D, Morant R, Semiglazov V, Borner M, Salzberg M, et al. Phase II study of temsirolimus (CCI-779), a novel inhibitor of mTOR, in heavily pretreated patients with locally advanced or metastatic breast cancer. J Clin Oncol 2005;23:5314-5322 (Pubitemid 46206985)
27. Chollet P, Abrial C, Tacca O, Mouret-Reynier MA, Leheurteur M, Durando X, Cure H. Mammalian target of rapamycin inhibitors in combination with letrozole in breast cancer. Clin Breast Cancer 2006;7: 336-338 (Pubitemid 44717767)
28. Ciaparrone M, Quirino M, Schinzari G, Zannoni G, Corsi DC, Vecchio FM, Cassano A, La Torre G, Barone C. Predictive role of thymidylate synthase, dihydropyrimidine dehydrogenase and thymidine phosphorylase expression in colorectal cancer patients receiving adjuvant 5-fluorouracil. Oncology 2006;70: 366-377 (Pubitemid 46066130)
29. Hara K, Yonezawa K, Kozlowski MT, Sugimoto T, Andrabi K, Weng QP, Kasuga M, Nishimoto I, Avruch J. Regulation of eIF-4E BP1 phosphorylation by mTOR. J Biol Chem 1997;272:26457-26463 (Pubitemid 27458864)
30. Van Triest B, Pinedo HM, Giaccone G, Peters GJ. Downstream molecular determinants of response to 5-fluorouracil and antifolate thymidylate synthase inhibitors. Ann Oncol 2000;11:385-391 (Pubitemid 30333539)
31. Kornmann M, Schwabe W, Sander S, Kron M, Strater J, Polat S, Kettner E, Weiser HF, Baumann W, Schramm H, Hausler P, Ott K, et al. Thymidylate synthase and dihydropyrimidine dehydrogenase mRNA expression levels: predictors for survival in colorectal cancer patients receiving adjuvant 5-fluorouracil. Clin Cancer Res 2003;9:4116-4124 (Pubitemid 37204028)
32. Taomoto J, Yoshida K, Wada Y, Tanabe K, Konishi K, Tahara H, Fukushima M. Overexpression of the orotate phosphoribosyl-transferase gene enhances the effect of 5-fluorouracil on gastric cancer cell lines. Oncology 2006;70:458-464 (Pubitemid 46333767)
33. Oeda M, Yoshida K, Sanada Y, Wada Y, Suzuki T, Mizuiri H, Konishi K, Shigematsu H, Tanabe K, Fukushima M. The expression profiles of orotate phosphoribosyltransferase and dihydropyrimidine dehydrogenase in gastric cancer and their clinical significance. Oncol Rep 2006;16:1165-1172
34. Abraham RT. Identification of TOR signaling complexes: more TORC for the cell growth engine. Cell 2002;111:9-12.
35. Volarevic S, Thomas G. Role of S6 phosphorylation and S6 kinase in cell growth. Prog Nucleic Acid Res Mol Biol 2001;65:101-127
36. Fingar DC, Salama S, Tsou C, Harlow E, Blenis J. Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev 2002; 16:1472-1487 (Pubitemid 34686329)
37. Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol 2001;21:3995-4004. (Pubitemid 32476461)
38. Klos KS, Wyszomierski SL, Sun M, Tan M, Zhou X, Li P, Yang W, Yin G, Hittelman WN, Yu D. ErbB2 increases vascular endothelial growth factor protein synthesis via activation of mammalian target of rapamycin/p70S6K leading to increased angiogenesis and spontaneous metastasis of human breast cancer cells. Cancer Res 2006;66:2028-2037 (Pubitemid 43294911)
39. Guba M, von Breitenbuch P, Steinbauer M, Koehl G, Flegel S, Hornung M, Bruns CJ, Zuelke C, Farkas S, Anthuber M, Jauch KW, Geissler EK. Rapamycin inhibits primary and metastatic tumor growth by antiangiogenesis: involvement of vascular endothelial growth factor. Nat Med 2002;8: 128-135 (Pubitemid 34155123)
40. Seeliger H, Guba M, Koehl GE, Doenecke A, Steinbauer M, Bruns CJ, Wagner C, Frank E, Jauch KW, Geissler EK. Blockage of 2-deoxy-D-ribose-induced angiogenesis with rapamycin counteracts a thymidine phosphorylase-based escape mechanism available for colon cancer under 5- fluorouracil therapy. Clin Cancer Res 2004; 10:1843-1852 (Pubitemid 38435576)
41. Haydon MS, Googe JD, Sorrells DS, Ghali GE, Li BD. Progression of eIF4e gene amplification and overexpression in benign and malignant tumors of the head and neck. Cancer 2000;88:2803-2810
42. Rosenwald IB, Chen JJ, Wang S, Savas L, London IM, Pullman J. Upregulation of protein synthesis initiation factor eIF-4E is an early event during colon carcinogenesis. Oncogene 1999;18:2507-2517 (Pubitemid 29206164)
43. Kerekatte V, Smiley K, Hu B, Smith A, Gelder F, De Benedetti A. The protooncogene/translation factor eIF4E: a survey of its expression in breast carcinomas. Int J Cancer 1995;64:27-31.
44. Pandya KJ, Dahlberg S, Hidalgo M, Cohen RB, Lee MW, Schiller JH, Johnson DH. A randomized, phase II trial of two dose levels of temsirolimus (CCI-779) in patients with extensive-stage small-cell lung cancer who have responding or stable disease after induction chemotherapy: a trial of the Eastern Cooperative Oncology Group (E1500). J Thorac Oncol 2007;2: 1036-1041 (Pubitemid 350059580)
45. Hudes G, Carducci M, Tomczak P, Dutcher J, Figlin R, Kapoor A, Staroslawska E, Sosman J, McDermott D, Bodrogi I, Kovacevic Z, Lesovoy V, et al. Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma. N Engl J Med 2007;356:2271-2281 (Pubitemid 46849157)
46. Hahn M, Li W, Yu C, Rahmani M, Dent P, Grant S. Rapamycin and UCN-01 synergistically induce apoptosis in human leukemia cells through a process that is regulated by the Raf-1/MEK/ERK, Akt, and JNK signal transduction pathways. Mol Cancer Ther 2005;4:457-470
47. Goudar RK, Shi Q, Hjelmeland MD, Keir ST, McLendon RE, Wikstrand CJ, Reese ED, Conrad CA, Traxler P, Lane HA, Reardon DA, Cavenee WK, et al. Combination therapy of inhibitors of epidermal growth factor receptor/vascular endothelial growth factor receptor 2 (AEE788) and the mammalian target of rapamycin (RAD001) offers improved glioblastoma tumor growth inhibition. Mol Cancer Ther 2005;4:101-112 (Pubitemid 40268071)
48. Cejka D, Preusser M, Fuereder T, Sieghart W, Werzowa J, Strommer S, Wacheck V. mTOR inhibition sensitizes gastric cancer to alkylating chemotherapy in vivo. Anticancer Res 2008;28(6A):3801-3808
49. Cejka D, Preusser M, Woehrer A, Sieghart W, Strommer S, Werzowa J, Fuereder T, Wacheck V. Everolimus (RAD001) and anti-angiogenic cyclophosphamide show long-term control of gastric cancer growth in vivo. Cancer Biol Ther 2008;7:1377-1385
50. Harada H, Andersen JS, Mann M, Terada N, Korsmeyer SJ. p70S6 kinase signals cell survival as well as growth, inactivating the pro-apoptotic molecule BAD. Proc Natl Acad Sci U S A 2001;98:9666-9670 (Pubitemid 32769360)
51. Huang S, Liu LN, Hosoi H, Dilling MB, Shikata T, Houghton PJ. p53/p21(CIP1) cooperate in enforcing rapamycin-induced G(1) arrest and determine the cellular response to rapamycin. Cancer Res 2001; 61:3373-3381
52. Huang S, Shu L, Dilling MB, Easton J, Harwood FC, Ichijo H, Houghton PJ. Sustained activation of the JNK cascade and rapamycin-induced apoptosis are suppressed by p53/p21(Cip1). Mol Cell 2003;11:1491-1501 (Pubitemid 36776536)
53. Zhou B, Wang ZX, Zhao Y, Brautigan DL, Zhang ZY. The specificity of extracellular signal-regulated kinase 2 dephosphorylation by protein phosphatases. J Biol Chem 2002;277: 31818-31825 (Pubitemid 34968988)
54. Herbert TP, Tee AR, Proud CG. The extracellular signal-regulated kinase pathway regulates the phosphorylation of 4E-BP1 at multiple sites. J Biol Chem 2002; 277:11591-11596