Adaptation to chronic mTOR inhibition in cancer and in aging

Biochemical Society Transactions

Volumn 41, Issue 4, 2013, Pages 956-961

  Gilley, Rebecca ^a   Balmanno, Kathryn ^a   Cope, Claire L ^a   Cook, Simon J ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

Acquired resistance; Cap dependent translation; Eukaryotic initiation factor 4E (eIF4E); Eukaryotic initiation factor 4E binding protein (4E BP); Mammalian target of rapamycin (mTOR); Rapamycin

Indexed keywords

2 (4 AMINO 1 ISOPROPYL 1H PYRAZOLO[3,4 D]PYRIMIDIN 3 YL) 1H INDOL 5 OL; 4 (4 AMINO 5 (7 METHOXY 1H INDOL 2 YL)IMIDAZO[5,1 F][1,2,4]TRIAZIN 7 YL)CYCLOHEXANECARBOXYLIC ACID; ANTINEOPLASTIC AGENT; AZD 2014; AZD 8055; GROWTH FACTOR; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MLN 0128; RAPAMYCIN; UNCLASSIFIED DRUG;

ADAPTATION; AGING; ARTICLE; BIOSYNTHESIS; CANCER RESISTANCE; CARCINOGENESIS; CATABOLISM; CELL PROLIFERATION; CELL SURVIVAL; DOWNSTREAM PROCESSING; DRUG TARGETING; ENZYME PHOSPHORYLATION; HUMAN; LIFESPAN; NEMATODE; NEOPLASM; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TUMOR CELL;

AGING; ANTINEOPLASTIC AGENTS; HUMANS; LONGEVITY; NEOPLASMS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84880559637     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20130080     Document Type: Article

References (43)

1. Laplante, M and Sabatini, D.M. (2012) mTOR signaling in growth control and disease. Cell 149, 274-293
2. Oh, W.J. and Jacinto, E. (2011) mTOR complex 2 signaling and functions. Cell Cycle 10, 2305-2316
3. De Benedetti, A. and Graff, J.R. (2004) eIF-4E expression and its role in malignancies and metastases. Oncogene 23, 3189-3199
4. Ben-Sahra, I., Howell, J.J., Asara, J.M. and Manning, B.D. (2013) Stimulation of de novo pyrimidine synthesis by growth signaling through mTOR and S6K1. Science 339, 1323-1328
5. Fenton, T.R. and Gout, I.T. (2011) Functions and regulation of the 70kDa ribosomal S6 kinases. Int. J. Biochem. Cell Biol. 43, 45-59
6. Kim, J., Kundu, M., Viollet, B. and Guan, K.L. (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of UlK1. Nat. Cell Biol. 13, 132-141
7. Menon, S. and Manning, B.D. (2008) Common corruption of the mTOR signaling network in human tumors. Oncogene 27, S43-51
8. Lu, Z.H., Shvartsman, M.B., Lee, A.Y., Shao, J.M., Murray, M.M., Kladney, R.D., Fan, D., Krajewski, S., Chiang, G.G., Mills, G.B. and Arbeit, J.M. (2010) Mammalian target of rapamycin activator RHEB is frequently overexpressed in human carcinomas and is critical and sufficient for skin epithelial carcinogenesis. Cancer Res. 70, 3287-3298
9. van Veelen, W., Korsse, S.E., van de Laar, L. and Peppelenbosch, M.P. (2011) The long and winding road to rational treatment of cancer associated with LKB1/AMPK/TSC/mTORC1 signaling. Oncogene 30, 2289-2303
10. Masri, J., Bernath, A., Martin, J., Jo, O.D., Vartanian, R., Funk, A. and Gera, J. (2007) mTORC2 activity is elevated in gliomas and promotes growth and cell motility via overexpression of rictor. Cancer Res. 67, 11712-11720
11. Dowling, R.J., Topisirovic, I., Alain, T., Bidinosti, M., Fonseca, B.D., Petroulakis, E., Wang, X., Larsson, O., Selvaraj, A., Liu, Y. et al. (2010) mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 328, 1172-1176
12. Hsieh, A.C., Costa, M., Zollo, O., Davis, C., Feldman, M.E., Testa, J.R., Meyuhas, O., Shokat, K.M. and Ruggero, D. (2010) Genetic dissection of the oncogenic mTOR pathway reveals druggable addiction to translational control via 4EBP-eIF4E. Cancer Cell 17, 249-261
13. Sorrells, D.L., Black, D.R., Meschonat, C., Rhoads, R., De Benedetti, A., Gao, M., Williams, B.J. and Li, B.D. (1998) Detection of eIF4E gene amplification in breast cancer by competitive PCR. Ann. Surg. Oncol. 5, 232-237
14. Haydon, M.S., Googe, J.D., Sorrells, D.S., Ghali, G.E. and Li, B.D. (2000) Progression of eIF4e gene amplification and overexpression in benign and malignant tumors of the head and neck. Cancer 88, 2803-2810
15. Ruggero, D., Montanaro, L., Ma, L., Xu, W., Londei, P., Cordon-Cardo, C. and Pandolfi, P.P. (2004) The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat. Med. 10, 484-486
16. Furic, L., Rong, L., Larsson, O., Koumakpayi, I.H., Yoshida, K., Brueschke, A., Petroulakis, E., Robichaud, N., Pollak, M., Gaboury, L.A. et al. (2010) eIF4E phosphorylation promotes tumorigenesis and is associated with prostate cancer progression. Proc. Natl. Acad. Sci. U.S.A. 107, 14134-14139
17. Mamane, Y., Petroulakis, E., Rong, L., Yoshida, K., Ler, L.W. and Sonenberg, N. (2004) eIF4E: from translation to transformation. Oncogene 23, 3172-3179
18. Hsieh, A.C., Liu, Y., Edlind, M.P., Ingolia, N.T., Janes, M.R., Sher, A., Shi, E.Y., Stumpf, C.R., Christensen, C., Bonham, M.J. et al. (2012) The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature 485, 55-61
19. Thoreen, C.C., Chantranupong, L., Keys, H.R., Wang, T., Gray, N.S. and Sabatini, D.M. (2012) A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485, 109-113
20. Huang, S., Bjornsti, M.A. and Houghton, P.J. (2003) Rapamycins: mechanism of action and cellular resistance. Cancer Biol. Ther. 2, 222-232
21. Guertin, D.A. and Sabatini, D.M. (2009) The pharmacology of mTOR inhibition. Sci. Signaling 2, pe24
22. Harrington, L.S., Findlay, G.M., Gray, A., Tolkacheva, T., Wigfield, S., Rebholz, H., Barnett, J., Leslie, N.R., Cheng, S., Shepherd, P.R. et al. (2004) The TSC1-1/2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS1 proteins. J. Cell Biol. 166, 213-223
23. Hsu, P.P., Kang, S.A., Rameseder, J., Zhang, Y., Ottina, K.A., Lim, D., Peterson, T.R., Choi, Y., Gray, N.S., Yaffe, M.B. et al. (2011) The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling. Science 332, 1317-1322
24. Yu, Y., Yoon, S.O., Poulogiannis, G., Yang, Q., Ma, X.M., Villén, J., Kubica, N., Hoffman, G.R., Cantley, L.C., Gygi, S.P. and Blenis, J. (2011) Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 332, 1322-1326
25. Feldman, M.E., Apsel, B., Uotila, A., Loewith, R., Knight, Z.A., Ruggero, D. and Shokat, K.M. (2009) Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol. 7, e38
26. Thoreen, C.C., Kang, S.A., Chang, J.W., Liu, Q., Zhang, J., Gao, Y., Reichling, L.J., Sim, T., Sabatini, D.M. and Gray, N.S. (2009) An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J. Biol. Chem. 284, 8023-8032
27. Chresta, C.M., Davies, B.R., Hickson, I., Harding, T., Cosulich, S., Critchlow, S.E., Vincent, J.P., Ellston, R., Jones, D., Sini, P. et al. (2010) AZD8055 is a potent, selective, and orally bioavailable ATP-competitive mammalian target of rapamycin kinase inhibitor with in vitro and in vivo antitumor activity. Cancer Res. 70, 288-298
28. Benjamin, D., Colombi, M., Moroni, C. and Hall, M.N. (2011) Rapamycin passes the torch: a new generation of mTOR inhibitors. Nat. Rev. Drug Discovery 10, 868-880
29. Dilling, M.B., Germain, G.S., Dudkin, L., Jayaraman, A.L., Zhang, X., Harwood, F.C. and Houghton, P.J. (2002) 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. 277, 13907-13917
30. Alain, T., Morita, M., Fonseca, B.D., Yanagiya, A., Siddiqui, N., Bhat, M., Zammit, D., Marcus, V., Metrakos, P., Voyer, L.A. et al. (2012) eIF4E/4E-BP ratio predicts the efficacy of mTOR targeted therapies. Cancer Res. 72, 6468-6476
31. Hou, J., Lam, F., Proud, C. and Wang, S. (2012) Targeting Mnks for cancer therapy. Oncotarget 3, 118-31
32. Hands, L., Proud, C.G. and Wyttenbach, A. (2009) mTOR's role in ageing: protein synthesis or autophagy? Aging 1, 586-597
33. Harrison, D.E., Strong, R., Sharp, Z.D., Nelson, J.F., Astle, C.M., Flurkey, K., Nadon, N.L., Wilkinson, J.E., Frenkel, K., Carter, C.S. et al. (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460, 392-395
34. Hansen, M., Taubert, S., Crawford, D., Libina, N., Lee, S.J. and Kenyon, C. (2007) Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 6, 95-110
35. Pan, K.Z., Palter, J.E., Rogers, A.N., Olsen, A., Chen, D., Lithgow, G.J. and Kapahi, P. (2007) Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell 6, 111-119
36. Syntichaki, P., Troulinaki, K. and Tavernarakis, N. (2007) eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans. Nature 445, 922-926
37. Kapahi, P., Zid, B.M., Harper, T., Koslover, D., Sapin, V. and Benzer, S. (2004) Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr. Biol. 14, 885-890
38. Bjedov, I., Toivonen, J.M., Kerr, F., Slack, C., Jacobson, J., Foley, A. and Partridge, L. (2010) Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab. 11, 35-46
39. Rogers, A.N., Chen, D., McColl, G., Czerwieniec, G., Felkey, K., Gibson, B.W., Hubbard, A., Melov, S., Lithgow, G.J. and Kapahi, P. (2011) Life span extension via eIF4G inhibition is mediated by posttranscriptional remodeling of stress response gene expression in C. elegans. Cell Metab. 14, 55-66
40. Hars, E.S., Qi, H., Ryazanov, A.G., Jin, S., Cai, L., Hu, C. and Liu, L.F. (2007) Autophagy regulates ageing in C. elegans. Autophagy 3, 93-95
41. Tóth, M.L., Sigmond, T., Borsos, E., Barna, J., Erdélyi, P., Takács-Vellai, K., Orosz, L., Kovács, A.L., Csikós, G., Sass, M. and Vellai, T. (2008) Longevity pathways converge on autophagy genes to regulate life span in Caenorhabditis elegans. Autophagy 4, 330-338
42. Hansen, M., Chandra, A., Mitic, L.L., Onken, B., Driscoll, M. and Kenyon, C. (2008) A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet. 4, e24
43. Haigis, M.C. and Yankner, B.A. (2010) The aging stress response. Mol. Cell 40, 333-344