Phosphorylation of 4E-BP1 predicts sensitivity to everolimus in gastric cancer cells

Cancer Letters

Volumn 331, Issue 2, 2013, Pages 220-229

  Nishi, Tetsuo ^a   Iwasaki, Kenta ^a   Ohashi, Norifumi ^b   Tanaka, Chie ^a   Kobayashi, Daisuke ^a   Nakayama, Goro ^a   Koike, Masahiko ^a   Fujiwara, Michitaka ^a   Kobayashi, Takaaki ^a   Kodera, Yasuhiro ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b AICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

4E BP1; ERK; Gastric cancer; MTOR inhibitor; Sensitivity

Indexed keywords

EVEROLIMUS; INITIATION FACTOR 4E BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER INHIBITION; CANCER RESISTANCE; CELL PROLIFERATION; CHEMOSENSITIVITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STOMACH CANCER; SUBCUTANEOUS TISSUE TUMOR; TUMOR XENOGRAFT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; PHOSPHOPROTEINS; PHOSPHORYLATION; SIROLIMUS; STOMACH NEOPLASMS; TOR SERINE-THREONINE KINASES;

MAMMALIA;

EID: 84875365774     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.01.004     Document Type: Article

References (41)

1. Ferlay J., Shin H.R., Bray F., Forman D., Mathers C., Parkin D.M. Estimates of worldwide burden of cancer in 2008: GLOBOCAN. Int. J. Cancer 2008, 127(2010):2893-2917.
2. Ajani J.A. Evolving chemotherapy for advanced gastric cancer. Oncologist 2005, 10(Suppl. 3):49-58.
3. Menges M., Hoehler T. Current strategies in systemic treatment of gastric cancer and cancer of the gastroesophageal junction. J. Cancer Res. Clin. Oncol. 2009, 135:29-38.
4. Webb A., Cunningham D., Scarffe J.H., Harper P., Norman A., Joffe J.K., Hughes M., Mansi J., Findlay M., Hill A., Oates J., Nicolson M., Hickish T., O'Brien M., Iveson T., Watson M., Underhill C., Wardley A., Meehan M. Randomized trial comparing epirubicin, cisplatin, and fluorouracil versus fluorouracil, doxorubicin, and methotrexate in advanced esophagogastric cancer. J. Clin. Oncol. 1997, 15:261-267.
5. Ross P., Nicolson M., Cunningham D., Valle J., Seymour M., Harper P., Price T., Anderson H., Iveson T., Hickish T., Lofts F., Norman A. Prospective randomized trial comparing mitomycin, cisplatin, and protracted venous-infusion fluorouracil (PVI 5-FU) with epirubicin, cisplatin, and PVI 5-FU in advanced esophagogastric cancer. J. Clin. Oncol. 2002, 20:1996-2004.
6. Kang Y.K., Kang W.K., Shin D.B., Chen J., Xiong J., Wang J., Lichinitser M., Guan Z., Khasanov R., Zheng L., Philco-Salas M., Suarez T., Santamaria J., Forster G., McCloud P.I. Capecitabine/cisplatin versus 5-fluorouracil/cisplatin as first-line therapy in patients with advanced gastric cancer: a randomised phase III noninferiority trial. Ann. Oncol. 2009, 20:666-673.
7. Van Cutsem E., Moiseyenko V.M., Tjulandin S., Majlis A., Constenla M., Boni C., Rodrigues A., Fodor M., Chao Y., Voznyi E., Risse M.L., Ajani J.A., Group V.S. Phase III study of docetaxel and cisplatin plus fluorouracil compared with cisplatin and fluorouracil as first-line therapy for advanced gastric cancer: a report of the V325 Study Group. J. Clin. Oncol. 2006, 24:4991-4997.
8. Cunningham D., Starling N., Rao S., Iveson T., Nicolson M., Coxon F., Middleton G., Daniel F., Oates J., Norman A.R. U.G.C.S.G.o.t.N.C.R.I.o.t.U. Kingdom, Capecitabine and oxaliplatin for advanced esophagogastric cancer. N. Engl. J. Med. 2008, 358:36-46.
9. Al-Batran S.E., Hartmann J.T., Probst S., Schmalenberg H., Hollerbach S., Hofheinz R., Rethwisch V., Seipelt G., Homann N., Wilhelm G., Schuch G., Stoehlmacher J., Derigs H.G., Hegewisch-Becker S., Grossmann J., Pauligk C., Atmaca A., Bokemeyer C., Knuth A., Jäger E., Onkologie A.I. Phase III trial in metastatic gastroesophageal adenocarcinoma with fluorouracil, leucovorin plus either oxaliplatin or cisplatin: a study of the Arbeitsgemeinschaft Internistische Onkologie. J. Clin. Oncol. 2008, 26:1435-1442.
10. Edinger A.L., Thompson C.B. Akt maintains cell size and survival by increasing mTOR-dependent nutrient uptake. Mol. Biol. Cell 2002, 13:2276-2288.
11. Fingar D.C., Richardson C.J., Tee A.R., Cheatham L., Tsou C., Blenis J. MTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol. Cell. Biol. 2004, 24:200-216.
12. Patel P.H., Chadalavada R.S., Chaganti R.S., Motzer R.J. Targeting von Hippel-Lindau pathway in renal cell carcinoma. Clin. Cancer Res. 2006, 12:7215-7220.
13. Hay N., Sonenberg N. Upstream and downstream of mTOR. Genes Dev. 2004, 18:1926-1945.
14. Vogt P.K. PI 3-kinase, mTOR, protein synthesis and cancer. Trends Mol. Med. 2001, 7:482-484.
15. Gingras A.C., Raught B., Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev. 2001, 15:807-826.
16. Fingar D.C., 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.
17. Mamane Y., Petroulakis E., Rong L., Yoshida K., Ler L.W., Sonenberg N. EIF4E-from translation to transformation. Oncogene 2004, 23:3172-3179.
18. Lang S.A., Gaumann A., Koehl G.E., Seidel U., Bataille F., Klein D., Ellis L.M., Bolder U., Hofstaedter F., Schlitt H.J., Geissler E.K., 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.
19. Kim M.A., Lee H.S., Lee H.E., Jeon Y.K., Yang H.K., Kim W.H. EGFR in gastric carcinomas: prognostic significance of protein overexpression and high gene copy number. Histopathology 2008, 52:738-746.
20. Lieto E., Ferraraccio F., Orditura M., Castellano P., Mura A.L., Pinto M., Zamboli A., De Vita F., Galizia G. Expression of vascular endothelial growth factor (VEGF) and epidermal growth factor receptor (EGFR) is an independent prognostic indicator of worse outcome in gastric cancer patients. Ann. Surg. Oncol. 2008, 15:69-79.
21. Matsubara J., Yamada Y., Hirashima Y., Takahari D., Okita N.T., Kato K., Hamaguchi T., Shirao K., Shimada Y., Shimoda T. Impact of insulin-like growth factor type 1 receptor, epidermal growth factor receptor, and HER2 expressions on outcomes of patients with gastric cancer. Clin. Cancer Res. 2008, 14:3022-3029.
22. Gravalos C., Jimeno A. HER2 in gastric cancer: a new prognostic factor and a novel therapeutic target. Ann. Oncol. 2008, 19:1523-1529.
23. Bjornsti M.A., Houghton P.J. The TOR pathway: a target for cancer therapy. Nat. Rev. Cancer 2004, 4:335-348.
24. Martín M.E., Pérez M.I., Redondo C., Alvarez M.I., Salinas M., Fando J.L. 4E binding protein 1 expression is inversely correlated to the progression of gastrointestinal cancers. Int. J. Biochem. Cell Biol. 2000, 32:633-642.
25. 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.
26. Okamoto I., Doi T., Ohtsu A., Miyazaki M., Tsuya A., Kurei K., Kobayashi K., Nakagawa K. Phase I clinical and pharmacokinetic study of RAD001 (everolimus) administered daily to Japanese patients with advanced solid tumors. Jpn. J. Clin. Oncol. 2010, 40:17-23.
27. Doi T., Muro K., Boku N., Yamada Y., Nishina T., Takiuchi H., Komatsu Y., Hamamoto Y., Ohno N., Fujita Y., Robson M., Ohtsu A. Multicenter phase II study of everolimus in patients with previously treated metastatic gastric cancer. J. Clin. Oncol. 2010, 28:1904-1910.
28. Eric Van Cutsem, K.-H. Yeh, Y.-J. Bang, L. Shen, J.A. Ajani, Y.-X. Bai, H.C. Chung, H.-M. Pan, K. Chin, K. Muro, Y.H. Kim, H. Smith, C. Costantini, S. Musalli, S. Rizvi, T. Sahmoud, A. Ohtsu, Phase III trial of everolimus (EVE) in previously treated patients with advanced gastric cancer (AGC): GRANITE-1, J. Clin. Oncol. (suppl. 4) (2012) (abstr LBA3).
29. Lee K.H., Hur H.S., Im S.A., Lee J., Kim H.P., Yoon Y.K., Han S.W., Song S.H., Oh D.Y., Kim T.Y., Bang Y.J. RAD001 shows activity against gastric cancer cells and overcomes 5-FU resistance by downregulating thymidylate synthase. Cancer Lett. 2010, 299:22-28.
30. Noh W.C., Mondesire W.H., Peng J., Jian W., Zhang H., Dong J., Mills G.B., Hung M.C., Meric-Bernstam F. Determinants of rapamycin sensitivity in breast cancer cells. Clin. Cancer Res. 2004, 10:1013-1023.
31. Mansure J.J., Nassim R., Chevalier S., Rocha J., Scarlata E., Kassouf W. Inhibition of mammalian target of rapamycin as a therapeutic strategy in the management of bladder cancer. Cancer Biol. Ther. 2009, 8:2339-2347.
32. Wang X., Hawk N., Yue P., Kauh J., Ramalingam S.S., Fu H., Khuri F.R., Sun S.Y. Overcoming mTOR inhibition-induced paradoxical activation of survival signaling pathways enhances mTOR inhibitors' anticancer efficacy. Cancer Biol. Ther. 2008, 7:1952-1958.
33. Dowling R.J., Topisirovic I., Alain T., Bidinosti M., Fonseca B.D., Petroulakis E., Wang X., Larsson O., Selvaraj A., Liu Y., Kozma S.C., Thomas G., Sonenberg N. MTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 2010, 328:1172-1176.
34. Gingras A.C., Gygi S.P., Raught B., Polakiewicz R.D., Abraham R.T., Hoekstra M.F., Aebersold R., Sonenberg N. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev. 1999, 13:1422-1437.
35. García-Martínez J.M., Moran J., Clarke R.G., Gray A., Cosulich S.C., Chresta C.M., Alessi D.R. Ku-0063794 is a specific inhibitor of the mammalian target of rapamycin. Biochem. J. 2009, 421:29-42.
36. Patursky-Polischuk I., Stolovich-Rain M., Hausner-Hanochi M., Kasir J., Cybulski N., Avruch J., Rüegg M.A., Hall M.N., Meyuhas O. The TSC-mTOR pathway mediates translational activation of TOP mRNAs by insulin largely in a raptor- or rictor-independent manner. Mol. Cell. Biol. 2009, 29:640-649.
37. Choo A.Y., Yoon S.O., Kim S.G., Roux P.P., Blenis J. Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc. Natl. Acad. Sci. USA 2008, 105:17414-17419.
38. O'Reilly K.E., Rojo F., She Q.B., Solit D., Mills G.B., Smith D., Lane H., Hofmann F., Hicklin D.J., Ludwig D.L., Baselga J., Rosen N. MTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res. 2006, 66:1500-1508.
39. Bang Y.J., Van Cutsem E., Feyereislova A., Chung H.C., Shen L., Sawaki A., Lordick F., Ohtsu A., Omuro Y., Satoh T., Aprile G., Kulikov E., Hill J., Lehle M., Rüschoff J., Kang Y.K., Investigators T.T. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet 2010, 376:687-697.
40. Ohtsu A., Shah M.A., Van Cutsem E., Rha S.Y., Sawaki A., Park S.R., Lim H.Y., Yamada Y., Wu J., Langer B., Starnawski M., Kang Y.K. Bevacizumab in combination with chemotherapy as first-line therapy in advanced gastric cancer: a randomized, double-blind, placebo-controlled phase III study. J. Clin. Oncol. 2011, 29:3968-3976.
41. Yoon D.H., Ryu M.H., Park Y.S., Lee H.J., Lee C., Ryoo B.Y., Lee J.L., Chang H.M., Kim T.W., Kang Y.K. Phase II study of everolimus with biomarker exploration in patients with advanced gastric cancer refractory to chemotherapy including fluoropyrimidine and platinum. Br. J. Cancer 2012, 106:1039-1044.