Response to mTOR inhibition: Activity of eIF4E predicts sensitivity in cell lines and acquired changes in eIF4E regulation in breast cancer

Molecular Cancer

Volumn 10, Issue , 2011, Pages

  Satheesha, Sampoorna ^a   Cookson, Victoria J ^a   Coleman, Louise J ^a   Ingram, Nicola ^a   Madhok, Brijesh ^a   Hanby, Andrew M ^a   Suleman, Charlotte A B ^a   Sabine, Vicky S ^b   Macaskill, E Jane ^b   Bartlett, John M S ^b   Dixon, J Michael ^b   McElwaine, Jim N ^c   Hughes, Thomas A ^a  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EVEROLIMUS; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; RAPAMYCIN; DRUG DERIVATIVE; EIF4EBP1 PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TARGET OF RAPAMYCIN KINASE;

ARTICLE; BREAST CANCER; CANCER CELL; COLON CANCER; DRUG SENSITIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG CANCER; 5' UNTRANSLATED REGION; BREAST TUMOR; CELL PROLIFERATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PREOPERATIVE CARE; PROTEIN SYNTHESIS; REPORTER GENE; TISSUE CULTURE TECHNIQUE; TUMOR CELL LINE;

5' UNTRANSLATED REGIONS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG SCREENING ASSAYS, ANTITUMOR; EUKARYOTIC INITIATION FACTOR-4E; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, REPORTER; HUMANS; PHOSPHOPROTEINS; PHOSPHORYLATION; PREOPERATIVE CARE; PROTEIN BIOSYNTHESIS; SIROLIMUS; TISSUE CULTURE TECHNIQUES; TOR SERINE-THREONINE KINASES;

EID: 79851510771     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-10-19     Document Type: Article

References (46)

1. Mulay AV, Cockfield S, Stryker R, Fergusson D, Knoll GA. Conversion from calcineurin inhibitors to sirolimus for chronic renal allograft dysfunction: a systematic review of the evidence. Transplantation 2006, 82:1153-1162. 10.1097/01.tp.0000237101.58974.43, 17102766.
2. Meric-Bernstam F, Gonzalez-Angulo AM. Targeting the mTOR signaling network for cancer therapy. J Clin Oncol 2009, 27:2278-2287. 10.1200/JCO.2008.20.0766, 2738634, 19332717.
3. Hudes G, Carducci M, Tomczak P, Dutcher J, Figlin R, Kapoor A, Staroslawska E, Sosman J, McDermott D, Bodrogi I, et al. Temsirolimus, interferon alfa, or both for advanced renal-cell carcinoma. N Engl J Med 2007, 356:2271-2281. 10.1056/NEJMoa066838, 17538086.
4. Motzer RJ, Escudier B, Oudard S, Hutson TE, Porta C, Bracarda S, Grunwald V, Thompson JA, Figlin RA, Hollaender N, et al. Efficacy of everolimus in advanced renal cell carcinoma: a double-blind, randomised, placebo-controlled phase III trial. Lancet 2008, 372:449-456. 10.1016/S0140-6736(08)61039-9, 18653228.
5. Stallone G, Schena A, Infante B, Di Paolo S, Loverre A, Maggio G, Ranieri E, Gesualdo L, Schena FP, Grandaliano G. Sirolimus for Kaposi's sarcoma in renal-transplant recipients. N Engl J Med 2005, 352:1317-1323. 10.1056/NEJMoa042831, 15800227.
6. Oshiro N, Yoshino K, Hidayat S, Tokunaga C, Hara K, Eguchi S, Avruch J, Yonezawa K. Dissociation of raptor from mTOR is a mechanism of rapamycin-induced inhibition of mTOR function. Genes Cells 2004, 9:359-366. 10.1111/j.1356-9597.2004.00727.x, 15066126.
7. Chen J, Zheng XF, Brown EJ, Schreiber SL. Identification of an 11-kDa FKBP12-rapamycin-binding domain within the 289-kDa FKBP12-rapamycin-associated protein and characterization of a critical serine residue. Proc Natl Acad Sci USA 1995, 92:4947-4951. 10.1073/pnas.92.11.4947, 41824, 7539137.
8. Shor B, Zhang WG, Toral-Barza L, Lucas J, Abraham RT, Gibbons JJ, Yu K. A new pharmacologic action of CCI-779 involves FKBP12-independent inhibition of mTOR kinase activity and profound repression of global protein synthesis. Cancer Res 2008, 68:2934-2943. 10.1158/0008-5472.CAN-07-6487, 18413763.
9. Dowling RJ, Topisirovic I, Fonseca BD, Sonenberg N. Dissecting the role of mTOR: Lessons from mTOR inhibitors. Biochim Biophys Acta 2010, 1804:433-439.
10. Shaw RJ, Bardeesy N, Manning BD, Lopez L, Kosmatka M, DePinho RA, Cantley LC. The LKB1 tumor suppressor negatively regulates mTOR signaling. Cancer Cell 2004, 6:91-99. 10.1016/j.ccr.2004.06.007, 15261145.
11. Feng Z, Zhang H, Levine AJ, Jin S. The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci USA 2005, 102:8204-8209. 10.1073/pnas.0502857102, 1142118, 15928081.
12. 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. 10.1074/jbc.272.42.26457, 9334222.
13. von Manteuffel SR, Dennis PB, Pullen N, Gingras AC, Sonenberg N, Thomas G. The insulin-induced signalling pathway leading to S6 and initiation factor 4E binding protein 1 phosphorylation bifurcates at a rapamycin-sensitive point immediately upstream of p70s6k. Mol Cell Biol 1997, 17:5426-5436. 232392, 9271419.
14. Beretta L, Gingras AC, Svitkin YV, Hall MN, Sonenberg N. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. E M B O J 1996, 15:658-664.
15. Koromilas AE, Lazaris-Karatzas A, Sonenberg N. mRNAs containing extensive secondary structure in their 5' non-coding region translate efficiently in cells overexpressing initiation factor eIF-4E. E M B O J 1992, 11:4153-4158.
16. Gray NK, Hentze MW. Regulation of protein synthesis by mRNA structure. Mol Biol Rep 1994, 19:195-200. 10.1007/BF00986961, 7969107.
17. Kozak M. An analysis of vertebrate mRNA sequences: intimations of translational control. J Cell Biol 1991, 115:887-903. 10.1083/jcb.115.4.887, 2289952, 1955461.
18. Culjkovic B, Topisirovic I, Borden KL. Controlling gene expression through RNA regulons: the role of the eukaryotic translation initiation factor eIF4E. Cell Cycle 2007, 6:65-69. 10.4161/cc.6.1.3688, 17245113.
19. Culjkovic B, Topisirovic I, Skrabanek L, Ruiz-Gutierrez M, Borden KL. eIF4E promotes nuclear export of cyclin D1 mRNAs via an element in the 3'UTR. J Cell Biol 2005, 169:245-256. 10.1083/jcb.200501019, 2171863, 15837800.
20. Raught B, Peiretti F, Gingras AC, Livingstone M, Shahbazian D, Mayeur GL, Polakiewicz RD, Sonenberg N, Hershey JW. Phosphorylation of eucaryotic translation initiation factor 4B Ser422 is modulated by S6 kinases. E M B O J 2004, 23:1761-1769.
21. Tabernero J, Rojo F, Calvo E, Burris H, Judson I, Hazell K, Martinelli E, Ramon y Cajal S, Jones S, Vidal L, et al. Dose- and schedule-dependent inhibition of the mammalian target of rapamycin pathway with everolimus: a phase I tumor pharmacodynamic study in patients with advanced solid tumors. J Clin Oncol 2008, 26:1603-1610. 10.1200/JCO.2007.14.5482, 18332469.
22. O'Donnell A, Faivre S, Burris HA, Rea D, Papadimitrakopoulou V, Shand N, Lane HA, Hazell K, Zoellner U, Kovarik JM, et al. Phase I pharmacokinetic and pharmacodynamic study of the oral mammalian target of rapamycin inhibitor everolimus in patients with advanced solid tumors. J Clin Oncol 2008, 26:1588-1595.
23. Duran I, Kortmansky J, Singh D, Hirte H, Kocha W, Goss G, Le L, Oza A, Nicklee T, Ho J, et al. A phase II clinical and pharmacodynamic study of temsirolimus in advanced neuroendocrine carcinomas. Br J Cancer 2006, 95:1148-1154. 10.1038/sj.bjc.6603419, 2360568, 17031397.
24. Darb-Esfahani S, Faggad A, Noske A, Weichert W, Buckendahl AC, Muller B, Budczies J, Roske A, Dietel M, Denkert C. Phospho-mTOR and phospho-4EBP1 in endometrial adenocarcinoma: association with stage and grade in vivo and link with response to rapamycin treatment in vitro. J Cancer Res Clin Oncol 2009, 135:933-941. 10.1007/s00432-008-0529-5, 19107520.
25. Dilling MB, Germain GS, Dudkin L, Jayaraman AL, Zhang X, Harwood FC, Houghton PJ. 4E-binding proteins, the suppressors of eukaryotic initiation factor 4E, are down-regulated in cells with acquired or intrinsic resistance to rapamycin. J Biol Chem 2002, 277:13907-13917. 10.1074/jbc.M110782200, 11847216.
26. Iwenofu OH, Lackman RD, Staddon AP, Goodwin DG, Haupt HM, Brooks JS. Phospho-S6 ribosomal protein: a potential new predictive sarcoma marker for targeted mTOR therapy. Mod Pathol 2008, 21:231-237. 10.1038/modpathol.3800995, 18157089.
27. Cho D, Signoretti S, Dabora S, Regan M, Seeley A, Mariotti M, Youmans A, Polivy A, Mandato L, McDermott D, et al. Potential histologic and molecular predictors of response to temsirolimus in patients with advanced renal cell carcinoma. Clin Genitourin Cancer 2007, 5:379-385. 10.3816/CGC.2007.n.020, 17956710.
28. Hughes TA, Brady HJ. Cross-talk between pRb/E2F and Wnt/beta-catenin pathways: E2F1 induces axin2 leading to repression of Wnt signalling and to increased cell death. Exp Cell Res 2005, 303:32-46. 10.1016/j.yexcr.2004.09.014, 15572025.
29. Hughes TA, Brady HJM. Expression of axin2 is regulated by the alternative 5' untranslated regions of its mRNA. J Biol Chem 2005, 280:8581-8588. 10.1074/jbc.M410806200, 15611123.
30. Pyronnet S, Imataka H, Gingras AC, Fukunaga R, Hunter T, Sonenberg N. Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E. EMBO J 1999, 18:270-279. 10.1093/emboj/18.1.270, 1171121, 9878069.
31. Coleman LJ, Peter MB, Teall TJ, Brannan RA, Hanby AM, Honarpisheh H, Shaaban AM, Smith L, Speirs V, Verghese ET, et al. Combined analysis of eIF4E and 4E-binding protein expression predicts breast cancer survival and estimates eIF4E activity. Br J Cancer 2009, 100:1393-1399. 10.1038/sj.bjc.6605044, 2694424, 19367274.
32. Smith L, Brannan RA, Hanby AM, Shaaban AM, Verghese ET, Peter M, Pollock S, Satheesha S, Szynkiewicz M, Speirs V, Hughes TA. Differential regulation of estrogen receptor β isoforms by 5' untranslated regions in cancer. Journal of Cellular and Molecular Medicine 2010, 14:2172-2184. 10.1111/j.1582-4934.2009.00867.x, 20920096.
33. Smith L, Coleman LJ, Cummings M, Satheesha S, Shaw SO, Speirs V, Hughes TA. Expression of oestrogen receptor beta isoforms is regulated by transcriptional and post-transcriptional mechanisms. Biochem J 2010, 429:283-290. 10.1042/BJ20100373, 20462399.
34. Akamine R, Yamamoto T, Watanabe M, Yamazaki N, Kataoka M, Ishikawa M, Ooie T, Baba Y, Shinohara Y. Usefulness of the 5' region of the cDNA encoding acidic ribosomal phosphoprotein P0 conserved among rats, mice, and humans as a standard probe for gene expression analysis in different tissues and animal species. J Biochem Biophys Methods 2007, 70:481-486. 10.1016/j.jbbm.2006.11.008, 17196660.
35. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
36. Macaskill EJ, Bartlett JM, Sabine VS, Faratian D, Renshaw L, White S, Campbell FM, Young O, Williams L, Thomas JS, Barber MD, Dixon JM. The mammalian target of rapamycin inhibitor everolimus (RAD001) in early breast cancer: results of a pre-operative study. Breast Cancer Res Treat
37. Going JJ. Efficiently estimated histologic cell counts. Hum Pathol 1994, 25:333-336. 10.1016/0046-8177(94)90139-2, 8163265.
38. Hsieh AC, Costa M, Zollo O, Davis C, Feldman ME, Testa JR, Meyuhas O, Shokat KM, Ruggero D. Genetic dissection of the oncogenic mTOR pathway reveals druggable addiction to translational control via 4EBP-eIF4E. Cancer Cell 2010, 17:249-261. 10.1016/j.ccr.2010.01.021, 2901095, 20227039.
39. Gingras AC, Raught B, Gygi SP, Niedzwiecka A, Miron M, Burley SK, Polakiewicz RD, Wyslouch-Cieszynska A, Aebersold R, Sonenberg N. Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev 2001, 15:2852-2864. 10.1101/gad.887201, 312813, 11691836.
40. Mothe-Satney I, Yang D, Fadden P, Haystead TA, Lawrence JC. Multiple mechanisms control phosphorylation of PHAS-I in five (S/T)P sites that govern translational repression. Mol Cell Biol 2000, 20:3558-3567. 10.1128/MCB.20.10.3558-3567.2000, 85648, 10779345.
41. Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT, Hoekstra MF, Aebersold R, Sonenberg N. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 1999, 13:1422-1437. 10.1101/gad.13.11.1422, 316780, 10364159.
42. Noh WC, Mondesire WH, Peng J, Jian W, Zhang H, Dong J, Mills GB, Hung MC, Meric-Bernstam F. Determinants of rapamycin sensitivity in breast cancer cells. Clin Cancer Res 2004, 10:1013-1023. 10.1158/1078-0432.CCR-03-0043, 14871980.
43. Chang SB, Miron P, Miron A, Iglehart JD. Rapamycin inhibits proliferation of estrogen-receptor-positive breast cancer cells. J Surg Res 2007, 138:37-44. 10.1016/j.jss.2006.07.003, 17109887.
44. Hosoi H, Dilling MB, Liu LN, Danks MK, Shikata T, Sekulic A, Abraham RT, Lawrence JC, Houghton PJ. Studies on the mechanism of resistance to rapamycin in human cancer cells. Mol Pharmacol 1998, 54:815-824.
45. Wu GJ, Sinclair CS, Paape J, Ingle JN, Roche PC, James CD, Couch FJ. 17q23 amplifications in breast cancer involve the PAT1, RAD51C, PS6K, and SIGma1B genes. Cancer Res 2000, 60:5371-5375.
46. Jastrzebski K, Hannan KM, Tchoubrieva EB, Hannan RD, Pearson RB. Coordinate regulation of ribosome biogenesis and function by the ribosomal protein S6 kinase, a key mediator of mTOR function. Growth Factors 2007, 25:209-226. 10.1080/08977190701779101, 18092230.