Control of paip1-eukayrotic translation initiation factor 3 interaction by amino acids through S6 kinase

Molecular and Cellular Biology

Volumn 34, Issue 6, 2014, Pages 1046-1053

  Martineau, Yvan ^a,b   Wang, Xiaoshan ^a   Alain, Tommy ^a   Petroulakis, Emmanuel ^a   Shahbazian, David ^a,d   Fabre, Bertrand ^c   Bousquet Dubouch, Marie Pierre ^c   Monsarrat, Bernard ^c   Pyronnet, Stéphane ^b   Sonenberg, Nahum ^a  

^a MCGILL UNIVERSITY   (Canada)

^b CANCER RESEARCH CENTER OF TOULOUSE   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d YALE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL LINE; CELL LINE, TUMOR; EUKARYOTIC INITIATION FACTOR-3; HEK293 CELLS; HELA CELLS; HUMANS; PEPTIDE INITIATION FACTORS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84894256995     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01079-13     Document Type: Article

References (38)

1. Holcik M, Sonenberg N. 2005. Translational control in stress and apoptosis. Nat. Rev. Mol. Cell. Biol. 6:318-327. http://dx.doi.org/10.1038/nrm1618.
2. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136:731-745. http://dx.doi.org/10.1016/j.cell.2009.01.042.
3. Laplante M, Sabatini DM. 2012. mTOR signaling in growth control and disease. Cell 149:274-293. http://dx.doi.org/10.1016/j.cell.2012.03.017.
4. Ma XM, Blenis J. 2009. Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell. Biol. 10:307-318. http://dx.doi.org/10.1038/nrm2672.
5. Kimball SR, Jefferson LS. 2000. Regulation of translation initiation in mammalian cells by amino acids, p 561-579. In Sonenberg N, Hershey JWB, Mathews MB (ed), Translational control of gene expression, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
6. Sengupta S, Peterson TR, Sabatini DM. 2010. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol. Cell 40:310-322. http://dx.doi.org/10.1016/j.molcel.2010.09.026.
7. Dodd KM, Tee AR. 2012. Leucine and mTORC1: a complex relationship. Am. J. Physiol. Endocrinol. Metab. 302:E1329-E1342. http://dx.doi.org/10.1152/ajpendo.00525.2011.
8. Jastrzebski K, Hannan KM, Tchoubrieva EB, Hannan RD, Pearson RB. 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. http://dx.doi.org/10.1080/08977190701779101.
9. Shahbazian D, Parsyan A, Petroulakis E, Hershey J, Sonenberg N. 2010. eIF4B controls survival and proliferation and is regulated by protooncogenic signaling pathways. Cell Cycle 9:4106-4109. http://dx.doi.org/10.4161/cc.9.20.13630.
10. Dorrello NV, Peschiaroli A, Guardavaccaro D, Colburn NH, Sherman NE, Pagano M. 2006. S6K1- and βTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth. Science 314:467-471. http://dx.doi.org/10.1126/science.1130276.
11. Raught B, Peiretti F, Gingras AC, Livingstone M, Shahbazian D, Mayeur GL, Polakiewicz RD, Sonenberg N, Hershey JW. 2004. Phosphorylation of eucaryotic translation initiation factor 4B Ser422 is modulated by S6 kinases. EMBO J. 23:1761-1769. http://dx.doi.org/10.1038/sj.emboj.7600193.
12. Wang L, Gout I, Proud CG. 2001. Cross-talk between the ERK and p70 S6 kinase (S6K) signaling pathways. MEK-dependent activation of S6K2 in cardiomyocytes. J. Biol. Chem. 276:32670-32677. http://dx.doi.org/10.1074/jbc.M102776200.
13. Csibi A, Cornille K, Leibovitch MP, Poupon A, Tintignac LA, Sanchez AM, Leibovitch SA. 2010. The translation regulatory subunit eIF3f controls the kinase-dependent mTOR signaling required for muscle differentiation and hypertrophy in mouse. PLoS One 5:e8994. http://dx.doi.org/10.1371/journal.pone.0008994.
14. Harris TE, Chi A, Shabanowitz J, Hunt DF, Rhoads RE, Lawrence JC, Jr. 2006. mTOR-dependent stimulation of the association of eIF4G and eIF3 by insulin. EMBO J. 25:1659-1668. http://dx.doi.org/10.1038/sj.emboj.7601047.
15. Holz MK, Ballif BA, Gygi SP, Blenis J. 2005. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123:569-580. http://dx.doi.org/10.1016/j.cell.2005.10.024.
16. Hinnebusch AG. 2006. eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem. Sci. 31:553-562. http://dx.doi.org/10.1016/j.tibs.2006.08.005.
17. Damoc E, Fraser CS, Zhou M, Videler H, Mayeur GL, Hershey JW, Doudna JA, Robinson CV, Leary JA. 2007. Structural characterization of the human eukaryotic initiation factor 3 protein complex by mass spectrometry. Mol. Cell. Proteomics 6:1135-1146. http://dx.doi.org/10.1074/mcp.M600399-MCP200.
18. Zhang L, Smit-McBride Z, Pan X, Rheinhardt J, Hershey JW. 2008. An oncogenic role for the phosphorylated h-subunit of human translation initiation factor eIF3. J. Biol. Chem. 283:24047-24060. http://dx.doi.org/10.1074/jbc.M800956200.
19. Martineau Y, Derry MC, Wang X, Yanagiya A, Berlanga JJ, Shyu AB, Imataka H, Gehring K, Sonenberg N. 2008. Poly(A)-binding proteininteracting protein 1 binds to eukaryotic translation initiation factor 3 to stimulate translation. Mol. Cell. Biol. 28:6658-6667. http://dx.doi.org/10.1128/MCB.00738-08.
20. Zhou M, Sandercock AM, Fraser CS, Ridlova G, Stephens E, Schenauer MR, Yokoi-Fong T, Barsky D, Leary JA, Hershey JW, Doudna JA, Robinson CV. 2008. Special feature: mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc. Natl. Acad. Sci. U. S. A. 105:18139-18144. http://dx.doi.org/10.1073/pnas.0801313105.
21. Craig AW, Haghighat A, Yu AT, Sonenberg N. 1998. Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature 392:520-523. http://dx.doi.org/10.1038/33198.
22. Alain T, Lun X, Martineau Y, Sean P, Pulendran B, Petroulakis E, Zemp FJ, Lemay CG, Roy D, Bell JC, Thomas G, Kozma SC, Forsyth PA, Costa-Mattioli M, Sonenberg N. 2010. Vesicular stomatitis virus oncolysis is potentiated by impairing mTORC1-dependent type I IFN production. Proc. Natl. Acad. Sci. U. S. A. 107:1576-1581. http://dx.doi.org/10.1073/pnas.0912344107.
23. Dowling RJ, Topisirovic I, Alain T, Bidinosti M, Fonseca BD, Petroulakis E, Wang X, Larsson O, Selvaraj A, Liu Y, Kozma SC, Thomas G, Sonenberg N. 2010. mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 328:1172-1176. http://dx.doi.org/10.1126/science.1187532.
24. Mamane Y, Petroulakis E, Martineau Y, Sato TA, Larsson O, Rajasekhar VK, Sonenberg N. 2007. Epigenetic activation of a subset of mRNAs by eIF4E explains its effects on cell proliferation. PLoS One 2:e242. http://dx.doi.org/10.1371/journal.pone.0000242.
25. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, Sabatini DM. 2008. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320:1496-1501. http://dx.doi.org/10.1126/science.1157535.
26. Feldman ME, Apsel B, Uotila A, Loewith R, Knight ZA, Ruggero D, Shokat KM. 2009. Active-site inhibitors of mTOR target rapamycinresistant outputs of mTORC1 and mTORC2. PLoS Biol. 7:e38. http://dx.doi.org/10.1371/journal.pbio.1000038.
27. Okuzumi T, Fiedler D, Zhang C, Gray DC, Aizenstein B, Hoffman R, Shokat KM. 2009. Inhibitor hijacking of Akt activation. Nat. Chem. Biol. 5:484-493. http://dx.doi.org/10.1038/nchembio.183.
28. Pisarev AV, Unbehaun A, Hellen CU, Pestova TV. 2007. Assembly and analysis of eukaryotic translation initiation complexes. Methods Enzymol. 430:147-177. http://dx.doi.org/10.1016/S0076-6879(07)30007-4.
29. Sun CM, Todorovic A, Querol-Audi J, Bai Y, Villa N, Snyder M, Ashchyan J, Lewis CS, Hartland A, Gradia S, Fraser CS, Doudna JA, Nogales E, Cate JHD. 2011. Functional reconstitution of human eukaryotic translation initiation factor 3 (eIF3). Proc. Natl. Acad. Sci. U. S. A. 108:20473-20478. http://dx.doi.org/10.1073/pnas.1116821108.
30. Siridechadilok B, Fraser CS, Hall RJ, Doudna JA, Nogales E. 2005. Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310:1513-1515. http://dx.doi.org/10.1126/science.1118977.
31. -/- mice exhibit perinatal lethality and rapamycin-sensitive 5'-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol. Cell. Biol. 24:3112-3124. http://dx.doi.org/10.1128/MCB.24.8.3112-3124.2004.
32. Ruvinsky I, Sharon N, Lerer T, Cohen H, Stolovich-Rain M, Nir T, Dor Y, Zisman P, Meyuhas O. 2005. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev. 19:2199-2211. http://dx.doi.org/10.1101/gad.351605.
33. Schmid T, Jansen AP, Baker AR, Hegamyer G, Hagan JP, Colburn NH. 2008. Translation inhibitor Pdcd4 is targeted for degradation during tumor promotion. Cancer Res. 68:1254-1260. http://dx.doi.org/10.1158/0008-5472.CAN-07-1719.
34. Schepetilnikov M, Dimitrova M, Mancera-Martinez E, Geldreich A, Keller M, Ryabova LA. 2013. TOR and S6K1 promote translation reinitiation of uORF-containing mRNAs via phosphorylation of eIF3h. EMBO J. 32:1087-1102. http://dx.doi.org/10.1038/emboj.2013.61.
35. Farley AR, Powell DW, Weaver CM, Jennings JL, Link AJ. 2011. Assessing the components of the eIF3 complex and their phosphorylation status. J. Proteome Res. 10:1481-1494. http://dx.doi.org/10.1021/pr100877m.
36. Tuazon PT, Merrick WC, Traugh JA. 1989. Comparative analysis of phosphorylation of translational initiation and elongation factors by seven protein kinases. J. Biol. Chem. 264:2773-2777.
37. Shahbazian D, Roux PP, Mieulet V, Cohen MS, Raught B, Taunton J, Hershey JW, Blenis J, Pende M, Sonenberg N. 2006. The mTOR/PI3K and MAPK pathways converge on eIF4B to control its phosphorylation and activity. EMBO J. 25:2781-2791. http://dx.doi.org/10.1038/sj.emboj.7601166.
38. Pearce LR, Alton GR, Richter DT, Kath JC, Lingardo L, Chapman J, Hwang C, Alessi DR. 2010. Characterization of PF-4708671, a novel and highly specific inhibitor of p70 ribosomal S6 kinase (S6K1). Biochem. J. 431:245-255. http://dx.doi.org/10.1042/BJ20101024.