Inactivation of the mTORC1-eukaryotic translation initiation factor 4E pathway alters stress granule formation

Molecular and Cellular Biology

Volumn 33, Issue 11, 2013, Pages 2285-2301

  Fournier, Marie Josée ^a   Coudert, Laetitia ^a   Mellaoui, Samia ^a   Adjibade, Pauline ^a   Gareau, Cristina ^a   Côté, Marie France ^a   Sonenberg, Nahum ^b   Gaudreault, René C ^a   Mazroui, Rachid ^a  

^a LAVAL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 (4 AMINO 1 ISOPROPYL 1H PYRAZOLO[3,4 D]PYRIMIDIN 3 YL) 1H INDOL 5 OL; INITIATION FACTOR 4E; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1;

ARTICLE; CELL STRESS; CONTROLLED STUDY; FEMALE; GENE INACTIVATION; GENE INTERACTION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; STRESS GRANULE; TRANSLATION INITIATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BORONIC ACIDS; CHICK EMBRYO; CYTOPLASMIC GRANULES; EUKARYOTIC INITIATION FACTOR-4E; HELA CELLS; HUMANS; INDOLES; PHOSPHOPROTEINS; PHOSPHORYLATION; PURINES; PYRAZINES; TOR SERINE-THREONINE KINASES;

EUKARYOTA;

EID: 84878994383     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01517-12     Document Type: Article

References (86)

1. Moeller BJ, Cao Y, Li CY, Dewhirst MW. 2004. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 5:429-441.
2. Gardner LB. 2008. Hypoxic inhibition of nonsense-mediated RNA decay regulates gene expression and the integrated stress response. Mol. Cell. Biol. 28:3729 -3741.
3. Mazroui R, Sukarieh R, Bordeleau ME, Kaufman RJ, Northcote P, Tanaka J, Gallouzi I, Pelletier J. 2006. Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation. Mol. Biol. Cell 17:4212- 4219.
4. McInerney GM, Kedersha NL, Kaufman RJ, Anderson P, Liljestrom P. 2005. Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation. Mol. Biol. Cell 16:3753-3763.
5. Fournier MJ, Gareau C, Mazroui R. 2010. The chemotherapeutic agent bortezomib induces the formation of stress granules. Cancer Cell Int. 10: 12. doi:10.1186/1475-2867-10-12.
6. Gareau C, Fournier MJ, Filion C, Coudert L, Martel D, Labelle Y, Mazroui R. 2011. p21(WAF1/CIP1) upregulation through the stress granule-associated protein CUGBP1 confers resistance to bortezomibmediated apoptosis. PLoS One 6:e20254. doi:10.1371/journal.pone .0020254.
7. Mazroui R, Di Marco S, Kaufman RJ, Gallouzi IE. 2007. Inhibition of the ubiquitin-proteasome system induces stress granule formation. Mol. Biol. Cell 18:2603-2618.
8. Anderson P, Kedersha N. 2006. RNA granules. J. Cell Biol. 172:803- 808.
9. Anderson P, Kedersha N. 2008. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33:141-150.
10. Arimoto K, Fukuda H, Imajoh-Ohmi S, Saito H, Takekawa M. 2008. Formation of stress granules inhibits apoptosis by suppressing stressresponsive MAPK pathways. Nat. Cell Biol. 10:1324 -1332.
11. Kim WJ, Back SH, Kim V, Ryu I, Jang SK. 2005. Sequestration of TRAF2 into stress granules interrupts tumor necrosis factor signaling under stress conditions. Mol. Cell. Biol. 25:2450 -2462.
12. Morita T, Satoh R, Umeda N, Kita A, Sugiura R. 2012. The stress granule protein Vgl1 and poly(A)-binding protein Pab1 are required for doxorubicin resistance in the fission yeast Schizosaccharomyces pombe. Biochem. Biophys. Res. Commun. 417:399-403.
13. McConkey DJ, Zhu K. 2008. Mechanisms of proteasome inhibitor action and resistance in cancer. Drug Resist. Updat. 11:164 -179.
14. Richardson PG, Mitsiades C, Schlossman R, Ghobrial I, Hideshima T, Munshi N, Anderson KC. 2008. Bortezomib in the front-line treatment of multiple myeloma. Expert Rev. Anticancer Ther. 8:1053-1072.
15. Sterz J, von Metzler I, Hahne JC, Lamottke B, Rademacher J, Heider U, Terpos E, Sezer O. 2008. The potential of proteasome inhibitors in cancer therapy. Expert Opin. Invest. Drugs 17:879-895.
16. Caravita T, de Fabritiis P, Palumbo A, Amadori S, Boccadoro M. 2006. Bortezomib: efficacy comparisons in solid tumors and hematologic malignancies. Nat. Clin. Pract. Oncol. 3:374 -387.
17. Codony-Servat J, Tapia MA, Bosch M, Oliva C, Domingo-Domenech J, Mellado B, Rolfe M, Ross JS, Gascon P, Rovira A, Albanell J. 2006. Differential cellular and molecular effects of bortezomib, a proteasome inhibitor, in human breast cancer cells. Mol. Cancer Ther. 5:665- 675.
18. Guertin DA, Sabatini DM. 2009. The pharmacology of mTOR inhibition. Sci. Signal. 2:pe24. doi:10.1126/scisignal.267pe24.
19. Laplante M, Sabatini DM. 2012. mTOR signaling in growth control and disease. Cell 149:274 -293.
20. Jacinto E, Loewith R, Schmidt A, Lin S, Ruegg MA, Hall A, Hall MN. 2004. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat. Cell Biol. 6:1122-1128.
21. Peterson TR, Laplante M, Thoreen CC, Sancak Y, Kang SA, Kuehl WM, Gray NS, Sabatini DM. 2009. DEPTOR is an mTOR inhibitor frequently overexpressed in multiple myeloma cells and required for their survival. Cell 137:873- 886.
22. Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. 2004. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptorindependent pathway that regulates the cytoskeleton. Curr. Biol. 14: 1296-1302.
23. Takahara T, Hara K, Yonezawa K, Sorimachi H, Maeda T. 2006. Nutrient-dependent multimerization of the mammalian target of rapamycin through the N-terminal HEAT repeat region. J. Biol. Chem. 281: 28605-28614.
24. Wang L, Rhodes CJ, Lawrence JC, Jr. 2006. Activation of mammalian target of rapamycin (mTOR) by insulin is associated with stimulation of 4EBP1 binding to dimeric mTOR complex 1. J. Biol. Chem. 281:24293-24303.
25. Yip CK, Murata K, Walz T, Sabatini DM, Kang SA. 2010. Structure of the human mTOR complex I and its implications for rapamycin inhibition. Mol. Cell 38:768 -774.
26. Zhang HH, Lipovsky AI, Dibble CC, Sahin M, Manning BD. 2006. S6K1 regulates GSK3 under conditions of mTOR-dependent feedback inhibition of Akt. Mol. Cell 24:185-197.
27. Hara K, Maruki Y, Long X, Yoshino K, Oshiro N, Hidayat S, Tokunaga C, Avruch J, Yonezawa K. 2002. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110:177-189.
28. Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. 2002. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110:163-175.
29. Zhou H, Huang S. 2010. The complexes of mammalian target of rapamycin. Curr. Protein Pept. Sci. 11:409-424.
30. Richter JD, Sonenberg N. 2005. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433:477-480.
31. Sonenberg N. 2008. eIF4E, the mRNA cap-binding protein: from basic discovery to translational research. Biochem. Cell Biol. 86:178 -183.
32. Haghighat A, Sonenberg N. 1997. eIF4G dramatically enhances the binding of eIF4E to the mRNA 5=-cap structure. J. Biol. Chem. 272:21677-21680.
33. Haghighat A, Svitkin Y, Novoa I, Kuechler E, Skern T, Sonenberg N. 1996. The eIF4G-eIF4E complex is the target for direct cleavage by the rhinovirus 2A proteinase. J. Virol. 70:8444-8450.
34. Haghighat A, Mader S, Pause A, Sonenberg N. 1995. Repression of cap-dependent translation by 4E-binding protein 1: competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J. 14:5701-5709.
35. Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT, Hoekstra MF, Aebersold R, Sonenberg N. 1999. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev. 13:1422-1437.
36. Mamane Y, Petroulakis E, Rong L, Yoshida K, Ler LW, Sonenberg N. 2004. eIF4E-from translation to transformation. Oncogene 23:3172-3179.
37. Rong L, Livingstone M, Sukarieh R, Petroulakis E, Gingras AC, Crosby K, Smith B, Polakiewicz RD, Pelletier J, Ferraiuolo MA, Sonenberg N. 2008. Control of eIF4E cellular localization by eIF4E-binding proteins, 4E-BPs. RNA 14:1318 -1327.
38. Rousseau D, Gingras AC, Pause A, Sonenberg N. 1996. The eIF4Ebinding proteins 1 and 2 are negative regulators of cell growth. Oncogene 13:2415-2420.
39. Averous J, Proud CG. 2006. When translation meets transformation: the mTOR story. Oncogene 25:6423-6435.
40. Huang S, Houghton PJ. 2003. Targeting mTOR signaling for cancer therapy. Curr. Opin. Pharmacol. 3:371-377.
41. Janus A, Robak T, Smolewski P. 2005. The mammalian target of the rapamycin (mTOR) kinase pathway: its role in tumourigenesis and targeted antitumour therapy. Cell. Mol. Biol. Lett. 10:479-498.
42. Petroulakis E, Mamane Y, Le Bacquer O, Shahbazian D, Sonenberg N. 2006.mTORsignaling: implications for cancer and anticancer therapy. Br. J. Cancer 94:195-199.
43. Graff JR, Konicek BW, Carter JH, Marcusson EG. 2008. Targeting the eukaryotic translation initiation factor 4E for cancer therapy. Cancer Res. 68:631-634.
44. Graff JR, Konicek BW, Vincent TM, Lynch RL, Monteith D, Weir SN, Schwier P, Capen A, Goode RL, Dowless MS, Chen Y, Zhang H, Sissons S, Cox K, McNulty AM, Parsons SH, Wang T, Sams L, Geeganage S, Douglass LE, Neubauer BL, Dean NM, Blanchard K, Shou J, Stancato LF, Carter JH, Marcusson EG. 2007. Therapeutic suppression of translation initiation factor eIF4E expression reduces tumor growth without toxicity. J. Clin. Invest. 117:2638 -2648.
45. Konicek BW, Dumstorf CA, Graff JR. 2008. Targeting the eIF4F translation initiation complex for cancer therapy. Cell Cycle 7:2466 -2471.
46. Mamane Y, Petroulakis E, LeBacquer O, Sonenberg N. 2006. mTOR, translation initiation and cancer. Oncogene 25:6416-6422.
47. Nathan CO, Amirghahari N, Rong X, Giordano T, Sibley D, Nordberg M, Glass J, Agarwal A, Caldito G. 2007. Mammalian target of rapamycin inhibitors as possible adjuvant therapy for microscopic residual disease in head and neck squamous cell cancer. Cancer Res. 67:2160 -2168.
48. 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. doi:10 .1371/journal.pbio.1000038.
49. Thoreen CC, Kang SA, Chang JW, Liu Q, Zhang J, Gao Y, Reichling LJ, Sim T, Sabatini DM, Gray NS. 2009. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J. Biol. Chem. 284:8023-8032.
50. Grosso S, Pesce E, Brina D, Beugnet A, Loreni F, Biffo S. 2011. Sensitivity of global translation to mTOR inhibition in REN cells depends on the equilibrium between eIF4E and 4E-BP1. PLoS One 6:e29136. doi: 10.1371/journal.pone.0029136.
51. Hsieh AC, Costa M, Zollo O, Davis C, Feldman ME, Testa JR, Meyuhas O, Shokat KM, Ruggero D. 2010. Genetic dissection of the oncogenic mTOR pathway reveals druggable addiction to translational control via 4EBP-eIF4E. Cancer Cell 17:249 -261.
52. Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS, Sabatini DM. 2012. A unifying model for mTORC1-mediated regulation ofmRNA translation. Nature 485:109 -113.
53. Mokas S, Mills JR, Garreau C, Fournier MJ, Robert F, Arya P, Kaufman RJ, Pelletier J, Mazroui R. 2009. Uncoupling stress granule assembly and translation initiation inhibition. Mol. Biol. Cell 20:2673-2683.
54. Chen L, Aktas BH, Wang Y, He X, Sahoo R, Zhang N, Denoyelle S, Kabha E, Yang H, Freedman RY, Supko JG, Chorev M, Wagner G, Halperin JA. 2012. Tumor suppression by small molecule inhibitors of translation initiation. Oncotarget 3:869-881.
55. Moerke NJ, Aktas H, Chen H, Cantel S, Reibarkh MY, Fahmy A, Gross JD, Degterev A, Yuan J, Chorev M, Halperin JA, Wagner G. 2007. Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 128:257-267.
56. Mazroui R, Huot ME, Tremblay S, Filion C, Labelle Y, Khandjian EW. 2002. Trapping of messenger RNA by Fragile X Mental Retardation protein into cytoplasmic granules induces translation repression. Hum. Mol. Genet. 11:3007-3017.
57. Tourrière H, Chebli K, Zekri L, Courselaud B, Blanchard JM, Bertrand E, Tazi J. 2003. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 160:823-831.
58. Kedersha N, Chen S, Gilks N, Li W, Miller IJ, Stahl J, Anderson P. 2002. Evidence that ternary complex (eIF2-GTP-tRNA(i)(Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell 13:195-210.
59. Kedersha N, Cho MR, Li W, Yacono PW, Chen S, Gilks N, Golan DE, Anderson P. 2000. Dynamic shuttling of TIA-1 accompanies the recruitment ofmRNAto mammalian stress granules. J. Cell Biol. 151:1257-1268.
60. Kedersha NL, Gupta M, Li W, Miller I, Anderson P. 1999. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J. Cell Biol. 147:1431-1442.
61. McEwen E, Kedersha N, Song B, Scheuner D, Gilks N, Han A, Chen JJ, Anderson P, Kaufman RJ. 2005. Heme-regulated inhibitor kinasemediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, and mediates survival upon arsenite exposure. J. Biol. Chem. 280:16925-16933.
62. Holcik M, Sonenberg N. 2005. Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol. 6:318 -327.
63. Wippich F, Bodenmiller B, Trajkovska MG, Wanka S, Aebersold R, Pelkmans L. 2013. Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling. Cell 152:791-805.
64. Dowling RJ, Topisirovic I, Fonseca BD, Sonenberg N. 2010. Dissecting the role of mTOR: lessons frommTORinhibitors. Biochim. Biophys. Acta 1804:433-439.
65. Sukarieh R, Sonenberg N, Pelletier J. 2009. The eIF4E-binding proteins are modifiers of cytoplasmic eIF4E relocalization during the heat shock response. Am. J. Physiol. Cell Physiol. 296:C1207-C1217.
66. 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.
67. Patel J, McLeod LE, Vries RG, Flynn A, Wang X, Proud CG. 2002. Cellular stresses profoundly inhibit protein synthesis and modulate the states of phosphorylation of multiple translation factors. Eur. J. Biochem. 269:3076 -3085.
68. Wu XN, Wang XK, Wu SQ, Lu J, Zheng M, Wang YH, Zhou H, Zhang H, Han J. 2011. Phosphorylation of Raptor by p38beta participates in arsenite-induced mammalian target of rapamycin complex 1 (mTORC1) activation. J. Biol. Chem. 286:31501-31511.
69. Alain T, Morita M, Fonseca BD, Yanagiya A, Siddiqui N, Bhat M, Zammit D, Marcus V, Metrakos P, Voyer LA, Gandin V, Liu Y, Topisirovic I, Sonenberg N. 2012. eIF4E/4E-BP ratio predicts the efficacy of mTOR targeted therapies. Cancer Res. 72:6468-6476.
70. Lin TA, Kong X, Haystead TA, Pause A, Belsham G, Sonenberg N, Lawrence JC, Jr. 1994. PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science 266:653-656.
71. Pause A, Belsham GJ, Gingras AC, Donze O, Lin TA, Lawrence JC, Jr, Sonenberg N. 1994. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5=-cap function. Nature 371:762-767.
72. Poulin F, Gingras AC, Olsen H, Chevalier S, Sonenberg N. 1998. 4E-BP3, a new member of the eukaryotic initiation factor 4E-binding protein family. J. Biol. Chem. 273:14002-14007.
73. Buchan JR, Parker R. 2009. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 36:932-941.
74. Bragado P, Estrada Y, Sosa MS, Avivar-Valderas A, Cannan D, Genden E, Teng M, Ranganathan AC, Wen HC, Kapoor A, Bernstein E, Aguirre-Ghiso JA. 2012. Analysis of marker-defined HNSCC subpopulations reveals a dynamic regulation of tumor initiating properties. PLoS One 7:e29974. doi:10.1371/journal.pone.0029974.
75. Gloesenkamp CR, Nitzsche B, Ocker M, Di Fazio P, Quint K, Hoffmann B, Scherubl H, Hopfner M. 2012. AKT inhibition by triciribine alone or as combination therapy for growth control of gastroenteropancreatic neuroendocrine tumors. Int. J. Oncol. 40:876-888.
76. Petitclerc E, Deschesnes RG, Cote MF, Marquis C, Janvier R, Lacroix J, Miot-Noirault E, Legault J, Mounetou E, Madelmont JC, C-Gaudreault R. 2004. Antiangiogenic and antitumoral activity of phenyl-3-(2-chloroethyl)ureas: a class of soft alkylating agents disrupting microtubules that are unaffected by cell adhesion-mediated drug resistance. Cancer Res. 64:4654-4663.
77. Ribatti D, Nico B, Cimpean AM, Raica M, Crivellato E, Ruggieri S, Vacca A. 19 April 2012. B16-F10 melanoma cells contribute to the new formation of blood vessels in the chick embryo chorioallantoic membrane through vasculogenic mimicry. Clin. Exp. Med. [Epub ahead of print.]
78. Fujimura K, Sasaki AT, Anderson P. 2012. Selenite targets eIF4E-binding protein-1 to inhibit translation initiation and induce the assembly of noncanonical stress granules. Nucleic Acids Res. 40:8099-8110.
79. Hsieh AC, Liu Y, Edlind MP, Ingolia NT, Janes MR, Sher A, Shi EY, Stumpf CR, Christensen C, Bonham MJ, Wang S, Ren P, Martin M, Jessen K, Feldman ME, Weissman JS, Shokat KM, Rommel C, Ruggero D. 2012. The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature 485:55-61.
80. Larsson O, Morita M, Topisirovic I, Alain T, Blouin MJ, Pollak M, Sonenberg N. 2012. Distinct perturbation of the translatome by the antidiabetic drug metformin. Proc. Natl. Acad. Sci. U. S. A. 109:8977-8982.
81. Hilliker A, Gao Z, Jankowsky E, Parker R. 2011. The DEAD-box protein Ded1 modulates translation by the formation and resolution of an eIF4FmRNA complex. Mol. Cell 43:962-972.
82. Rajyaguru P, She M, Parker R. 2012. Scd6 targets eIF4G to repress translation: RGG motif proteins as a class of eIF4G-binding proteins. Mol. Cell 45:244 -254.
83. Shih JW, Wang WT, Tsai TY, Kuo CY, Li HK, Wu Lee YH. 2012. Critical roles of RNA helicase DDX3 and its interactions with eIF4E/ PABP1 in stress granule assembly and stress response. Biochem. J. 441: 119-129.
84. Svitkin YV, Herdy B, Costa-Mattioli M, Gingras AC, Raught B, Sonenberg N. 2005. Eukaryotic translation initiation factor 4E availability controls the switch between cap-dependent and internal ribosomal entry sitemediated translation. Mol. Cell. Biol. 25:10556 -10565.
85. Yanagiya A, Suyama E, Adachi H, Svitkin YV, Aza-Blanc P, Imataka H, Mikami S, Martineau Y, Ronai ZA, Sonenberg N. 2012. Translational homeostasis via the mRNA cap-binding protein, eIF4E. Mol. Cell 46:847-858.
86. Di Marco S, Hel Z, Lachance C, Furneaux H, Radzioch D. 2001. Polymorphism in the 3=-untranslated region of TNFalpha mRNA impairs binding of the posttranscriptional regulatory protein HuR to TNFalpha mRNA. Nucleic Acids Res. 29:863-871.