MTOR signaling regulates the processing of pre-rRNA in human cells

Nucleic Acids Research

Volumn 40, Issue 6, 2012, Pages 2527-2539

  Iadevaia, Valentina ^a   Zhang, Ze ^a   Jan, Eric ^b   Proud, Christopher G ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEOME; RAPAMYCIN; RIBOSOME RNA; RNA 18S; RNA 28S; RNA 5S;

ARTICLE; CELL DISRUPTION; CELL FUNCTION; CELL METABOLISM; CELL NUCLEUS; CELL STRUCTURE; CHEMICAL LABELING; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; RNA INTERFERENCE; RNA PROCESSING; RNA SYNTHESIS; RNA TRANSCRIPTION; RNA TRANSLATION; SIGNAL TRANSDUCTION;

CELL NUCLEOLUS; HELA CELLS; HUMANS; PROTEIN BIOSYNTHESIS; PROTEINS; RIBOSOMAL PROTEINS; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, RIBOSOMAL; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES;

MAMMALIA; RAPTORES;

EID: 84859366546     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1040     Document Type: Article

References (37)

1. Wullschleger, S., Loewith, R. and Hall, M.N. (2006) TOR signaling in growth and metabolism. Cell, 124, 471-484 (Pubitemid 43199434)
2. 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)
3. White, R.J. (2005) RNA polymerases I and III, growth control and cancer. Nat. Rev. Mol. Cell Biol., 6, 69-78 (Pubitemid 40064900)
4. Meyuhas, O. (2000) Synthesis of the translational apparatus is regulated at the translational level. Eur. J. Biochem., 267, 6321-6330
5. Pianese, G. (1896) Beitraege zur Histologie und Aetiologie der Carconoms [Contributions to the histology and etiology of cancer]. Beitr. Pathol. Anat. Allgem. Pathol, 142, 1-193
6. Drygin, D., Rice, W.G. and Grummt, I. (2010) The RNA polymerase I transcription machinery: an emerging target for the treatment of cancer. Annu. Rev. Pharmacol. Toxicol., 50, 131-156
7. Montanaro, L., Trere, D. and Derenzini, M. (2008) Nucleolus, ribosomes, and cancer. Am. J. Pathol., 173, 301-310
8. Lohrum, M.A., Ludwig, R.L., Kubbutat, M.H., Hanlon, M. and Vousden, K.H. (2003) Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell, 3, 577-587 (Pubitemid 36808652)
9. Horn, H.F. and Vousden, K.H. (2008) Cooperation between the ribosomal proteins L5 and L11 in the p53 pathway. Oncogene, 27, 5774-5784
10. Cleary, M.D., Meiering, C.D., Jan, E., Guymon, R. and Boothroyd, J.C. (2005) Biosynthetic labeling of RNA with uracil phosphoribosyltransferase allows cell-specific microarray analysis of mRNA synthesis and decay. Nat. Biotechnol., 23, 232-237 (Pubitemid 40255335)
11. Woodford, T.A., Schlegel, R. and Pardee, A.B. (1988) Selective isolation of newly synthesized mammalian mRNA after in vivo labeling with 4-thiouridine or 6-thioguanosine. Anal. Biochem., 171, 166-172
12. del, S.B., Valdes, R., Mata, J., Felipe, A., Casado, F.J. and Pastor-Anglada, M. (1998) Differential expression and regulation of nucleoside transport systems in rat liver parenchymal and hepatoma cells. Hepatology, 28, 1504-1511 (Pubitemid 28549119)
13. Duflot, S., Riera, B., Fernandez-Veledo, S., Casado, V., Norman, R.I., Casado, F.J., Lluis, C., Franco, R. and Pastor-Anglada, M. (2004) ATP-sensitive K(+) channels regulate the concentrative adenosine transporter CNT2 following activation by A(1) adenosine receptors. Mol. Cell. Biol., 24, 2710-2719 (Pubitemid 38381263)
14. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York, USA
15. 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 50-terminal oligopyrimidine (TOP) mRNAs. RNA, 14, 1730-1736
16. Rouquette, J., Choesmel, V. and Gleizes, P.E. (2005) Nuclear export and cytoplasmic processing of precursors to the 40S ribosomal subunits in mammalian cells. EMBO J., 24, 2862-2872 (Pubitemid 43079890)
17. Hadjiolova, K.V., Nicoloso, M., Mazan, S., Hadjiolov, A.A. and Bachellerie, J.P. (1993) Alternative pre-rRNA processing pathways in human cells and their alteration by cycloheximide inhibition of protein synthesis. Eur. J. Biochem., 212, 211-215 (Pubitemid 23064619)
18. Lam, Y. and Lamond, A.I. (2006) Isolation of nucleoli. In: Celis, J.E. (ed.), Cell Biology: A Laboratory Handbook, Vol Elsevier Academic Press, Burlington, MA, pp. 103-108
19. Lorberg, A. and Hall, M.N. (2004) TOR: the first 10 years. In: Thomas, G., Sabatini, D.M. and Hall, M.N. (eds), TOR Target of rapamycin. Springer, Berlin, pp. 1-18 (Pubitemid 37047253)
20. Huang, M., Wang, Y., Cogut, S.B., Mitchell, B.S. and Graves, L.M. (2003) Inhibition of nucleoside transport by protein kinase inhibitors. J. Pharmacol. Exp. Ther., 304, 753-760 (Pubitemid 36152354)
21. Pende, M., Um, S.H., Mieulet, V., Sticker, M., Goss, V.L., Mestan, J., Mueller, M., Fumagalli, S., Kozma, S.C. and Thomas, G. (2004) S6K1(-/-)/S6K2(-/-) mice exhibit perinatal lethality and rapamycin-sensitive 50-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol. Cell. Biol., 24, 3112-3124 (Pubitemid 38452057)
22. Huang, B.P.H., Wang, Y., Wang, X. and Proud, C.G. (2009) Formation of eIF4F complexes is required for translation of structured mRNAs but not for the mTORC1-dependent activation of general protein synthesis in cardiomyocytes. Am. J. Physiol. Heart. Circ. Physiol., 296, H505-H514
23. Wang, X., Fonseca, B.D., Tang, H., Liu, R., Elia, A., Clemens, M.J., Bommer, U.A. and Proud, C.G. (2008) Re-evaluating the roles of proposed modulators of mammalian target of rapamycin complex 1 (mTORC1) signaling. J. Biol. Chem., 283, 30482-30492
24. 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
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. Robledo, S., Idol, R.A., Crimmins, D.L., Ladenson, J.H., Mason, P.J. and Bessler, M. (2008) The role of human ribosomal proteins in the maturation of rRNA and ribosome production. RNA, 14, 1918-1929
27. 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. USA, 91, 4441-4445
28. Strezoska, Z., Pestov, D.G. and Lau, L.F. (2000) Bop1 is a mouse WD40 repeat nucleolar protein involved in 28S and 5. 8S RRNA processing and 60S ribosome biogenesis. Mol. Cell. Biol., 20, 5516-5528 (Pubitemid 30482888)
29. Savkur, R.S. and Olson, M.O. (1998) Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease. Nucleic Acids Res., 26, 4508-4515 (Pubitemid 28442146)
30. Tsang, C.K., Liu, H. and Zheng, X.F. (2010) mTOR binds to the promoters of RNA polymerase I-and III-transcribed genes. Cell Cycle, 9, 953-957
31. Wei, Y. and Zheng, X.F. (2009) TORC1 association with rDNA chromatin as a mechanism to co-regulate Pol I and Pol III. Cell Cycle, 8, 3802-3803
32. Jastrzebski, K., Hannan, K.M., Tchoubrieva, E.B., Hannan, R.D. and Pearson, R.B. (2007) Coordinate regulation of ribosome biogenesis and function by the ribosomal protein S6 kinase, a key mediator of mTOR function. Growth Factors, 25, 209-226
33. Rosner, M., Schipany, K. and Hengstschlager, M. (2011) p70 S6K1 nuclear localization depends on its mTOR-mediated phosphorylation at T389, but not on its kinase activity towards S6. Amino Acids (in press). doi: 10.1007/s00726-011-0965-4
34. Rosner, M. and Hengstschlager, M. (2011) Nucleocytoplasmic localization of p70 S6K1, but not of its isoforms p85 and p31, is regulated by TSC2/mTOR. Oncogene, 30, 4509-4522
35. Powers, T. and Walter, P. (1999) Regulation of ribosome biogenesis by the rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae. Mol. Biol. Cell, 10, 987-1000 (Pubitemid 29193726)
36. Choesmel, V., Bacqueville, D., Rouquette, J., Noaillac-Depeyre, J., Fribourg, S., Cretien, A., Leblanc, T., Tchernia, G., Da, C.L. and Gleizes, P.E. (2007) Impaired ribosome biogenesis in Diamond-Blackfan anemia. Blood, 109, 1275-1283 (Pubitemid 46220680)
37. Reiter, A., Steinbauer, R., Philippi, A., Gerber, J., Tschochner, H., Milkereit, P. and Griesenbeck, J. (2011) Reduction in ribosomal protein synthesis is sufficient to explain major effects on ribosome production after short-term TOR inactivation in Saccharomyces cerevisiae. Mol. Cell. Biol., 31, 803-817.