XInhibition of mTORC1 by astrin and stress granules prevents apoptosis in cancer cells

Cell

Volumn 154, Issue 4, 2013, Pages

  Thedieck, Kathrin ^a,b,g   Holzwarth, Birgit ^a   Prentzell, Mirja Tamara ^a   Boehlke, Christopher ^b   Kläsener, Kathrin ^a,c   Ruf, Stefanie ^a   Sonntag, Annika Gwendolin ^a   Maerz, Lars ^a   Grellscheid, Sushma Nagaraja ^d   Kremmer, Elisabeth ^e   Nitschke, Roland ^a   Kuehn, E Wolfgang ^a,b   Jonker, Johan W ^g   Groen, Albert K ^g   Reth, Michael ^a,c   Hall, Michael N ^f   Baumeister, Ralf ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^d DURHAM UNIVERSITY   (United Kingdom)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

^f UNIVERSITY OF BASEL   (Switzerland)

^g UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1;

APOPTOSIS; ARTICLE; ASTRIN; CANCER CELL; CELL STRESS; CELLULAR STRESS RESPONSE; GRANULE CELL; HUMAN; HUMAN CELL; NEOPLASM; PRIORITY JOURNAL; REGULATOR GENE; UPREGULATION;

MAMMALIA; RAPTORES;

EID: 84882800242     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.07.031     Document Type: Article

References (67)

1. A. Alexander, S.L. Cai, J. Kim, A. Nanez, M. Sahin, K.H. MacLean, K. Inoki, K.L. Guan, J. Shen, and M.D. Person ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS Proc. Natl. Acad. Sci. USA 107 2010 4153 4158
2. P. Anderson, and N. Kedersha Stress granules: the Tao of RNA triage Trends Biochem. Sci. 33 2008 141 150
3. P. Anderson, and N. Kedersha RNA granules: post-transcriptional and epigenetic modulators of gene expression Nat. Rev. Mol. Cell Biol. 10 2009 430 436
4. C. Appenzeller-Herzog, and M.N. Hall Bidirectional crosstalk between endoplasmic reticulum stress and mTOR signaling Trends Cell Biol. 22 2012 274 282
5. K. Arimoto, H. Fukuda, S. Imajoh-Ohmi, H. Saito, and M. Takekawa Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways Nat. Cell Biol. 10 2008 1324 1332
6. G.U. Bae, D.W. Seo, H.K. Kwon, H.Y. Lee, S. Hong, Z.W. Lee, K.S. Ha, H.W. Lee, and J.W. Han Hydrogen peroxide activates p70(S6k) signaling pathway J. Biol. Chem. 274 1999 32596 32602
7. D. Benjamin, M. Colombi, C. Moroni, and M.N. Hall Rapamycin passes the torch: a new generation of mTOR inhibitors Nat. Rev. Drug Discov. 10 2011 868 880
8. M.E. Bordeleau, A. Mori, M. Oberer, L. Lindqvist, L.S. Chard, T. Higa, G.J. Belsham, G. Wagner, J. Tanaka, and J. Pelletier Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A Nat. Chem. Biol. 2 2006 213 220
9. J.R. Buchan, and R. Parker Eukaryotic stress granules: the ins and outs of translation Mol. Cell 36 2009 932 941
10. S. Buechler Low expression of a few genes indicates good prognosis in estrogen receptor positive breast cancer BMC Cancer 9 2009 243
11. M.S. Chang, C.J. Huang, M.L. Chen, S.T. Chen, C.C. Fan, J.M. Chu, W.C. Lin, and Y.C. Yang Cloning and characterization of hMAP126, a new member of mitotic spindle-associated proteins Biochem. Biophys. Res. Commun. 287 2001 116 121
12. S.D. Chou, T. Prince, J. Gong, and S.K. Calderwood mTOR is essential for the proteotoxic stress response, HSF1 activation and heat shock protein synthesis PLoS ONE 7 2012 e39679
13. N. Dai, J. Rapley, M. Angel, M.F. Yanik, M.D. Blower, and J. Avruch mTOR phosphorylates IMP2 to promote IGF2 mRNA translation by internal ribosomal entry Genes Dev. 25 2011 1159 1172
14. P. Dalle Pezze, A.G. Sonntag, A. Thien, M.T. Prentzell, M. Gödel, S. Fischer, E. Neumann-Haefelin, T.B. Huber, R. Baumeister, D.P. Shanley, and K. Thedieck A dynamic network model of mTOR signaling reveals TSC-independent mTORC2 regulation Sci. Signal. 5 2012 ra25
15. M.D. Dennis, S.R. Kimball, and L.S. Jefferson Mechanistic target of rapamycin complex 1 (mTORC1)-mediated phosphorylation is governed by competition between substrates for interaction with raptor J. Biol. Chem. 288 2013 10 19
16. M.M. Emara, K. Fujimura, D. Sciaranghella, V. Ivanova, P. Ivanov, and P. Anderson Hydrogen peroxide induces stress granule formation independent of eIF2α phosphorylation Biochem. Biophys. Res. Commun. 423 2012 763 769
17. N.G. Farny, N.L. Kedersha, and P.A. Silver Metazoan stress granule assembly is mediated by P-eIF2alpha-dependent and -independent mechanisms RNA 15 2009 1814 1821
18. M.J. Fournier, L. Coudert, S. Mellaoui, P. Adjibade, C. Gareau, M.F. Côté, N. Sonenberg, R.C. Gaudreault, and R. Mazroui Inactivation of the mTORC1-eukaryotic translation initiation factor 4E pathway alters stress granule formation Mol. Cell. Biol. 33 2013 2285 2301
19. J.P. Fruehauf, and F.L. Meyskens Jr. Reactive oxygen species: a breath of life or death? Clin. Cancer Res. 13 2007 789 794
20. J. Gruber, J. Harborth, J. Schnabel, K. Weber, and M. Hatzfeld The mitotic-spindle-associated protein astrin is essential for progression through mitosis J. Cell Sci. 115 2002 4053 4059
21. M. Grzmil, and B.A. Hemmings Translation regulation as a therapeutic target in cancer Cancer Res. 72 2012 3891 3900
22. D.M. Gwinn, J.M. Asara, and R.J. Shaw Raptor is phosphorylated by cdc2 during mitosis PLoS ONE 5 2010 e9197
23. V.A. Halim, M. Alvarez-Fernández, Y.J. Xu, M. Aprelia, H.W. van den Toorn, A.J. Heck, S. Mohammed, and R.H. Medema Comparative phosphoproteomic analysis of checkpoint recovery identifies new regulators of the DNA damage response Sci. Signal. 6 2013 rs9
24. M. Holcik, and N. Sonenberg Translational control in stress and apoptosis Nat. Rev. Mol. Cell Biol. 6 2005 318 327
25. A.C. Hsieh, Y. Liu, M.P. Edlind, N.T. Ingolia, M.R. Janes, A. Sher, E.Y. Shi, C.R. Stumpf, C. Christensen, and M.J. Bonham The translational landscape of mTOR signalling steers cancer initiation and metastasis Nature 485 2012 55 61
26. C. Huang, J. Li, Q. Ke, S.S. Leonard, B.H. Jiang, X.S. Zhong, M. Costa, V. Castranova, and X. Shi Ultraviolet-induced phosphorylation of p70(S6K) at Thr(389) and Thr(421)/Ser(424) involves hydrogen peroxide and mammalian target of rapamycin but not Akt and atypical protein kinase C Cancer Res. 62 2002 5689 5697
27. Y. Huo, V. Iadevaia, Z. Yao, I. Kelly, S. Cosulich, S. Guichard, L.J. Foster, and C.G. Proud Stable isotope-labelling analysis of the impact of inhibition of the mammalian target of rapamycin on protein synthesis Biochem. J. 444 2012 141 151
28. N. Karimian Pour, and K. Adeli Insulin silences apolipoprotein B mRNA translation by inducing intracellular traffic into cytoplasmic RNA granules Biochemistry 50 2011 6942 6950
29. N. Kedersha, and P. Anderson Mammalian stress granules and processing bodies Methods Enzymol. 431 2007 61 81
30. N. Kedersha, M.R. Cho, W. Li, P.W. Yacono, S. Chen, N. Gilks, D.E. Golan, and P. Anderson Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules J. Cell Biol. 151 2000 1257 1268
31. D.H. Kim, D.D. Sarbassov, S.M. Ali, J.E. King, R.R. Latek, H. Erdjument-Bromage, P. Tempst, and D.M. Sabatini mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery Cell 110 2002 163 175
32. M. Laplante, and D.M. Sabatini mTOR signaling in growth control and disease Cell 149 2012 274 293
33. C.H. Lee, K. Inoki, M. Karbowniczek, E. Petroulakis, N. Sonenberg, E.P. Henske, and K.L. Guan Constitutive mTOR activation in TSC mutants sensitizes cells to energy starvation and genomic damage via p53 EMBO J. 26 2007 4812 4823
34. M. Li, L. Zhao, J. Liu, A. Liu, C. Jia, D. Ma, Y. Jiang, and X. Bai Multi-mechanisms are involved in reactive oxygen species regulation of mTORC1 signaling Cell. Signal. 22 2010 1469 1476
35. X. Luo, N. Talarek, and C. De Virgilio Initiation of the yeast G0 program requires Igo1 and Igo2, which antagonize activation of decapping of specific nutrient-regulated mRNAs RNA Biol. 8 2011 14 17
36. G.J. Mack, and D.A. Compton Analysis of mitotic microtubule-associated proteins using mass spectrometry identifies astrin, a spindle-associated protein Proc. Natl. Acad. Sci. USA 98 2001 14434 14439
37. A.L. Manning, S.F. Bakhoum, S. Maffini, C. Correia-Melo, H. Maiato, and D.A. Compton CLASP1, astrin and Kif2b form a molecular switch that regulates kinetochore-microtubule dynamics to promote mitotic progression and fidelity EMBO J. 29 2010 3531 3543
38. M.M. Mihaylova, and R.J. Shaw The AMPK signalling pathway coordinates cell growth, autophagy and metabolism Nat. Cell Biol. 13 2011 1016 1023
39. S.S. Myatt, J.J. Brosens, and E.W. Lam Sense and sensitivity: FOXO and ROS in cancer development and treatment Antioxid. Redox Signal. 14 2011 675 687
40. A. Nakashima, Y. Maruki, Y. Imamura, C. Kondo, T. Kawamata, I. Kawanishi, H. Takata, A. Matsuura, K.S. Lee, and U. Kikkawa The yeast Tor signaling pathway is involved in G2/M transition via polo-kinase PLoS ONE 3 2008 e2223
41. P. Polak, and M.N. Hall mTOR and the control of whole body metabolism Curr. Opin. Cell Biol. 21 2009 209 218
42. F. Ramírez-Valle, S. Braunstein, J. Zavadil, S.C. Formenti, and R.J. Schneider eIF4GI links nutrient sensing by mTOR to cell proliferation and inhibition of autophagy J. Cell Biol. 181 2008 293 307
43. F. Ramírez-Valle, M.L. Badura, S. Braunstein, M. Narasimhan, and R.J. Schneider Mitotic raptor promotes mTORC1 activity, G(2)/M cell cycle progression, and internal ribosome entry site-mediated mRNA translation Mol. Cell. Biol. 30 2010 3151 3164
44. J. Rapley, N. Oshiro, S. Ortiz-Vega, and J. Avruch The mechanism of insulin-stimulated 4E-BP protein binding to mammalian target of rapamycin (mTOR) complex 1 and its contribution to mTOR complex 1 signaling J. Biol. Chem. 286 2011 38043 38053
45. D. Rübsamen, J.S. Blees, K. Schulz, C. Döring, M.L. Hansmann, H. Heide, A. Weigert, T. Schmid, and B. Brüne IRES-dependent translation of egr2 is induced under inflammatory conditions RNA 18 2012 1910 1920
46. Y. Sancak, L. Bar-Peled, R. Zoncu, A.L. Markhard, S. Nada, and D.M. Sabatini Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids Cell 141 2010 290 303
47. D.D. Sarbassov, and D.M. Sabatini Redox regulation of the nutrient-sensitive raptor-mTOR pathway and complex J. Biol. Chem. 280 2005 39505 39509
48. D.D. Sarbassov, S.M. Ali, S. Sengupta, J.H. Sheen, P.P. Hsu, A.F. Bagley, A.L. Markhard, and D.M. Sabatini Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB Mol. Cell 22 2006 159 168
49. O.J. Shah, Z. Wang, and T. Hunter Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies Curr. Biol. 14 2004 1650 1656
50. X. Shao, J. Xue, and F.A. van der Hoorn Testicular protein Spag5 has similarity to mitotic spindle protein Deepest and binds outer dense fiber protein Odf1 Mol. Reprod. Dev. 59 2001 410 416
51. O. Söderberg, K.J. Leuchowius, M. Gullberg, M. Jarvius, I. Weibrecht, L.G. Larsson, and U. Landegren Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay Methods 45 2008 227 232
52. A.G. Sonntag, P. Dalle Pezze, D.P. Shanley, and K. Thedieck A modelling-experimental approach reveals insulin receptor substrate (IRS)-dependent regulation of adenosine monosphosphate-dependent kinase (AMPK) by insulin FEBS J. 279 2012 3314 3328
53. V. Sosa, T. Moliné, R. Somoza, R. Paciucci, H. Kondoh, and M.E. LLeonart Oxidative stress and cancer: an overview Ageing Res. Rev. 12 2013 376 390
54. T. Takahara, and T. Maeda Transient sequestration of TORC1 into stress granules during heat stress Mol. Cell 47 2012 242 252
55. N. Talarek, E. Cameroni, M. Jaquenoud, X. Luo, S. Bontron, S. Lippman, G. Devgan, M. Snyder, J.R. Broach, and C. De Virgilio Initiation of the TORC1-regulated G0 program requires Igo1/2, which license specific mRNAs to evade degradation via the 5′-3′ mRNA decay pathway Mol. Cell 38 2010 345 355
56. K. Thedieck, P. Polak, M.L. Kim, K.D. Molle, A. Cohen, P. Jenö, C. Arrieumerlou, and M.N. Hall PRAS40 and PRR5-like protein are new mTOR interactors that regulate apoptosis PLoS ONE 2 2007 e1217
57. K.H. Thein, J. Kleylein-Sohn, E.A. Nigg, and U. Gruneberg Astrin is required for the maintenance of sister chromatid cohesion and centrosome integrity J. Cell Biol. 178 2007 345 354
58. M.G. Thomas, M. Loschi, M.A. Desbats, and G.L. Boccaccio RNA granules: the good, the bad and the ugly Cell. Signal. 23 2011 324 334
59. C.C. Thoreen, L. Chantranupong, H.R. Keys, T. Wang, N.S. Gray, and D.M. Sabatini A unifying model for mTORC1-mediated regulation of mRNA translation Nature 485 2012 109 113
60. H. Tourrière, K. Chebli, L. Zekri, B. Courselaud, J.M. Blanchard, E. Bertrand, and J. Tazi The RasGAP-associated endoribonuclease G3BP assembles stress granules J. Cell Biol. 160 2003 823 831
61. K. Välk, T. Vooder, R. Kolde, M.A. Reintam, C. Petzold, J. Vilo, and A. Metspalu Gene expression profiles of non-small cell lung cancer: survival prediction and new biomarkers Oncology 79 2010 283 292
62. K.M. Vattem, and R.C. Wek Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells Proc. Natl. Acad. Sci. USA 101 2004 11269 11274
63. X. Wang, and C.G. Proud p70 S6 kinase is activated by sodium arsenite in adult rat cardiomyocytes: roles for phosphatidylinositol 3-kinase and p38 MAP kinase Biochem. Biophys. Res. Commun. 238 1997 207 212
64. G. Wickman, L. Julian, and M.F. Olson How apoptotic cells aid in the removal of their own cold dead bodies Cell Death Differ. 19 2012 735 742
65. F. Wippich, B. Bodenmiller, M.G. Trajkovska, S. Wanka, R. Aebersold, and L. Pelkmans Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling Cell 152 2013 791 805
66. S. Yamasaki, and P. Anderson Reprogramming mRNA translation during stress Curr. Opin. Cell Biol. 20 2008 222 226
67. S. Yoshida, S. Hong, T. Suzuki, S. Nada, A.M. Mannan, J. Wang, M. Okada, K.L. Guan, and K. Inoki Redox regulates mammalian target of rapamycin complex 1 (mTORC1) activity by modulating the TSC1/TSC2-Rheb GTPase pathway J. Biol. Chem. 286 2011 32651 32660