Stable isotope-labelling analysis of the impact of inhibition of the mammalian target of rapamycin on protein synthesis

Biochemical Journal

Volumn 444, Issue 1, 2012, Pages 141-151

  Huo, Yilin ^a   Iadevaia, Valentina ^a   Yao, Zhong ^b,d   Kelly, Isabelle ^b,e   Cosulich, Sabina ^c   Guichard, Sylvie ^c   Foster, Leonard J ^b   Proud, Christopher G ^a,b  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c ASTRAZENECA   (United Kingdom)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITÉ LAVAL   (Canada)

Author keywords

AZD8055; Eukaryotic initiation factor (eIF); Mammalian target of rapamycin (mTOR); mRNA translation; Protein degradation; Stable isotope labelling with amino acids in cell culture (SILAC)

Indexed keywords

AZD 8055; ELONGATION FACTOR; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MESSENGER RNA; PP 242; RAPAMYCIN; RIBOSOME PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENCY; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; ISOTOPE LABELING; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN SYNTHESIS INHIBITION; REGULATORY MECHANISM; RNA TRANSLATION; SIGNAL TRANSDUCTION; STABLE ISOTOPE LABELING WITH AMINO ACIDS IN CELL CULTURE; TERMINAL OLIGOPYRIMIDINE TRACT; TRANSLATION REGULATION; UPREGULATION;

CARBON ISOTOPES; EUKARYOTIC INITIATION FACTOR-4E; HELA CELLS; HUMANS; INDOLES; ISOTOPE LABELING; MORPHOLINES; NITROGEN ISOTOPES; PROTEIN BIOSYNTHESIS; PURINES; RIBOSOMES; RNA, MESSENGER; SIROLIMUS; TOR SERINE-THREONINE KINASES;

EUKARYOTA; MAMMALIA;

EID: 84860805752     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20112107     Document Type: Article

References (40)

1. Wang, X. and Proud, C. G. (2011) mTORC1 signaling: what we still don't know. J. Mol. Cell Biol. 3, 206-220
2. Gingras, A.-C., Raught, B. and Sonenberg, N. (2001) Control of translation by the target of rapamycin proteins. Prog. Mol. Subcell. Biol. 27, 143-174
3. Manning, B. D. and Cantley, L. C. (2007) AKT/PKB signaling: navigating downstream. Cell 129, 1261-1274 (Pubitemid 46962095)
4. 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 mTOR inhibitor reveals rapamycin-insensitive functions of mTORC1. J. Biol. Chem. 284, 8023-8032
5. 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
6. Wang, X., Beugnet, A., Murakami, M., Yamanaka, S. and Proud, C. G. (2005) Distinct signaling events downstream of mTOR cooperate to mediate the effects of amino acids and insulin on initiation factor 4E-binding proteins. Mol. Cell. Biol. 25, 2558-2572 (Pubitemid 40381622)
7. Garcia-Martinez, J. M., Moran, J., Clarke, R. G., Gray, A., Cosulich, S. C., Chresta, C. M. and Alessi, D. R. (2009) Ku-0063794 is a specific inhibitor of the mammalian target of rapamycin (mTOR). Biochem. J. 421, 29-42
8. 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
9. Redpath, N. T., Foulstone, E. J. and Proud, C. G. (1996) Regulation of translation elongation factor-2 by insulin via a rapamycin-sensitive signalling pathway. EMBO J. 15, 2291-2297 (Pubitemid 26141145)
10. Iadevaia, V., Caldarola, S., Tino, E., Amaldi, F. and Loreni, F. (2008) All translation elongation factors and the e, f, and h subunits of translation initiation factor 3 are encoded by 5′-terminal oligopyrimidine (TOP) mRNAs. RNA 14, 1730-1736
11. Meyuhas, O. and Hornstein, E. (2000) In Translational Control of Gene Expression (Sonenberg, N., Hershey, J. W. B. and Mathews, M. B., eds), pp. 671-693, Cold Spring Harbor Laboratory Press, Cold Spring Harbor
12. Jefferies, H. B. J., Reinhard, G., Kozma, S. C. and Thomas, G. (1994) Rapamycin selectively represses translation of the 'polypyrimidine tract' mRNA family. Proc. Natl. Acad. Sci. U.S.A. 91, 4441-4445
13. Meyuhas, O. and Dreazen, A. (2009) Ribosomal protein s6 kinase from TOP mRNAs to cell size. Prog. Mol. Biol. Transl. Sci. 90, 109-153
14. Patursky-Polischuk, I., Stolovich-Rain, M., Hausner-Hanochi, M., Kasir, J., Cybulski, N., Avruch, J., Ruegg, M. A., Hall, M. N. and Meyuhas, O. (2009) The TSC-mTOR pathway mediates translational activation of TOP mRNAs by insulin largely in a raptor- or rictor-independent manner. Mol. Cell. Biol. 29, 640-649
15. Stolovich, M., Tang, H., Hornstein, E., Levy, G., Cohen, R., Bae, S. S., Birnbaum, M. J. and Meyuhas, O. (2002) Transduction of growth or mitogenic signals into translational activation of TOP mRNAs is fully reliant on the phosphatidylinositol 3-kinase-mediated pathway but requires neither S6K1 nor rpS6 phosphorylation. Mol. Cell. Biol. 22, 8101-8113 (Pubitemid 35304044)
16. Meyuhas, O. (2000) Synthesis of the translational apparatus is regulated at the translational level. Eur. J. Biochem. 267, 6321-6330
17. Waskiewicz, A. J., Johnson, J. C., Penn, B., Mahalingam, M., Kimball, S. R. and Cooper, J. A. (1999) Phosphorylation of the cap-binding protein eukaryotic translation factor 4E by protein kinase Mnk1 in vivo. Mol. Cell. Biol. 19, 1871-1880 (Pubitemid 29098245)
18. Wang, X., Campbell, L. E., Miller, C. M. and Proud, C. G. (1998) Amino acid availability regulates p70 S6 kinase and multiple translation factors. Biochem. J. 334, 261-267 (Pubitemid 28420997)
19. Chan, Q. W., Howes, C. G. and Foster, L. J. (2006) Quantitative comparison of caste differences in honeybee hemolymph. Mol. Cell. Proteomics 5, 2252-2262 (Pubitemid 46043025)
20. Rappsilber, J., Ishihama, Y. and Mann, M. (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663-670 (Pubitemid 36176744)
21. Mayer, C. and Grummt, I. (2006) Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 25, 6384-6391 (Pubitemid 44582283)
22. Schwanhausser, B., Gossen, M., Dittmar, G. and Selbach, M. (2009) Global analysis of cellular protein translation by pulsed SILAC. Proteomics 9, 205-209
23. Selbach, M., Schwanhäusser, B., Thierfelder, N., Fang, Z., Khanin, R. and Rajewsky, N. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58-63
24. Warburg, O. (1956) On the origin of cancer cells. Science 123, 309-314
25. Tennant, D. A., Duran, R. V. and Gottlieb, E. (2010) Targeting metabolic transformation for cancer therapy. Nat. Rev. Cancer 10, 267-277
26. Camacho-Vanegas, O., Weighardt, F., Ghigna, C., Amaldi, F., Riva, S. and Biamonti, G. (1997) Growth-dependent and growth-independent translation of messengers for heterogeneous nuclear ribonucleoproteins. Nucleic Acids Res. 25, 3950-3954 (Pubitemid 27420507)
27. Proud, C. G. (2007) Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem. J. 403, 217-234
28. RSK1 and p70 S6 kinase. EMBO J. 20, 4370-4379
29. 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
30. Mamane, Y., Petroulakis, E., Martineau, Y., Sato, T. A., Larsson, O., Rajasekhar, V. K. and Sonenberg, N. (2007) Epigenetic activation of a subset of mRNAs by eIF4E explains its effects on cell proliferation. PLoS ONE 2, e242
31. Shama, S., Avni, D., Frederickson, R. M., Sonenberg, N. and Meyuhas, O. (1995) Overexpression of initiation factor eIF-4E does not relieve the translational repression of ribosomal protein mRNAs in quiescent cells. Gene Expression 4, 241-252
32. Yang, Z. and Klionsky, D. J. (2010) Mammalian autophagy: core molecular machinery and signaling regulation. Curr. Opin. Cell Biol. 22, 124-131
33. Choo, A. Y., Yoon, S. O., Kim, S. G., Roux, P. P. and Blenis, J. (2008) Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc. Natl. Acad. Sci. U.S.A. 105, 17414-17419
34. Mikulits, W., Pradet-Balade, B., Habermann, B., Beug, H., Garcia-Sanz, J. G. and Müllner, E. W. (2000) Isolation of translationally controlled mRNAs by differential screening. FASEB J. 14, 1641-1652 (Pubitemid 30636567)
35. Johannes, G., Carter, M. S., Eisen, M. B., Brown, P. O. and Sarnow, P. (1999) Identification of eukaryotic mRNAs that are translated at reduced cap binding complex eIF4F concentrations using a cDNA microarray. Proc. Natl. Acad. Sci. U.S.A. 96, 13118-13123
36. Thermann, R. and Hentze, M. W. (2007) Drosophila miR2 induces pseudo-polysomes and inhibits translation initiation. Nature 447, 875-878 (Pubitemid 46920140)
37. Brunn, G. J., Williams, J., Sabers, C., Weiderrecht, G., Lawrence, J. C. and Abraham, R. T. (1996) Direct inhibition of the signalling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J. 15, 5256-5267 (Pubitemid 26336209)
38. Damgaard, C. K. and Lykke-Andersen, J. (2011) Translational coregulation of 5′TOP mRNAs by TIA-1 and TIAR. Genes Dev. 25, 2057-2068
39. Boisvert, F. M., Ahmad, Y., Gierlinski, M., Charriere, F., Lamond, D., Scott, M., Barton, G. and Lamond, A. I. (2011) A quantitative spatial proteomics analysis of proteome turnover in human cells. Mol. Cell. Proteomics 11, doi:10.1074mcp.M111.011429
40. Beau, I., Esclatine, A. and Codogno, P. (2008) Lost to translation: when autophagy targets mature ribosomes. Trends Cell Biol. 18, 311-314