Hydrogen peroxide induces stress granule formation independent of eIF2α phosphorylation

Biochemical and Biophysical Research Communications

Volumn 423, Issue 4, 2012, Pages 763-769

  Emara, Mohamed M ^a,b,c   Fujimura, Ken ^a   Sciaranghella, Daniele ^a   Ivanova, Victoria ^a   Ivanov, Pavel ^a   Anderson, Paul ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HAMAD BIN KHALIFA UNIVERSITY   (Qatar)

^c Cairo University   (Egypt)

Author keywords

EIF2; EIF4E; Oxidative stress; RNA; Stress granules; Translation

Indexed keywords

EMETINE; HYDROGEN PEROXIDE; INITIATION FACTOR 2ALPHA;

ANIMAL CELL; ARTICLE; CYTOPLASM; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STRESS GRANULE; TRANSLATION INITIATION; WESTERN BLOTTING;

ANIMALS; CELL LINE, TUMOR; CYTOPLASMIC GRANULES; EUKARYOTIC INITIATION FACTOR-2; GENE KNOCKDOWN TECHNIQUES; HUMANS; HYDROGEN PEROXIDE; MICE; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; RNA, SMALL INTERFERING; RNA, UNTRANSLATED;

MAMMALIA;

EID: 84863827090     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.06.033     Document Type: Article

References (38)

1. Yamasaki S., Anderson P. Reprogramming mRNA translation during stress. Curr. Opin. Cell Biol. 2008, 20:222-226.
2. Sonenberg N., Hinnebusch A.G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009, 136:731-745.
3. Anderson P., Kedersha N. Stress granules: the Tao of RNA triage. Trends. Biochem. Sci. 2008, 33:141-150.
4. Anderson P., Kedersha N. Stress granules. Curr. Biol. 2009, 19:397-408.
5. Anderson P., Kedersha N. RNA granules. J. Cell Biol. 2006, 172:803-808.
6. Arimoto K., Fukuda H., Imajoh-Ohmi S., Saito H., Takekawa M. Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat. Cell Biol. 2008, 10:1324-1332.
7. Kim W.J., Back S.H., Kim V., Ryu I., Jang S.K. Sequestration of TRAF2 into stress granules interrupts tumor necrosis factor signaling under stress conditions. Mol. Cell Biol. 2005, 25:2450-2462.
8. Brown J.A., Roberts T.L., Richards R., Woods R., Birrell G., Lim Y.C., Ohno S., Yamashita A., Abraham R.T., Gueven N., Lavin M.F. A novel role for hSMG-1 in stress granule formation. Mol. Cell Biol. 2011, 31:4417-4429.
9. Pothof J., Verkaik N.S., Hoeijmakers J.H., van Gent D.C. MicroRNA responses and stress granule formation modulate the DNA damage response. Cell Cycle 2009, 8:3462-3468.
10. Wolf A., Krause-Gruszczynska M., Birkenmeier O., Ostareck-Lederer A., Huttelmaier S., Hatzfeld M. Plakophilin 1 stimulates translation by promoting eIF4A1 activity. J. Cell Biol. 2010, 188:463-471.
11. Kedersha N., Anderson P. Mammalian stress granules and processing bodies. Methods Enzymol. 2007, 431:61-81.
12. Emara M.M., Ivanov P., Hickman T., Dawra N., Tisdale S., Kedersha N., Hu G.F., Anderson P. Angiogenin-induced tRNA-derived stress-induced RNAs promote stress-induced stress granule assembly. J. Biol. Chem. 2010, 285:10959-10968.
13. Kedersha N., Tisdale S., Hickman T., Anderson P. Real-time and quantitative imaging of mammalian stress granules and processing bodies. Methods Enzymol. 2008, 448:521-552.
14. Chen L., Xu B., Liu L., Luo Y., Yin J., Zhou H., Chen W., Shen T., Han X., Huang S. Hydrogen peroxide inhibits mTOR signaling by activation of AMPKalpha leading to apoptosis of neuronal cells. Lab. Invest. 2010, 90:762-773.
15. Kedersha N., Chen S., Gilks N., Li W., Miller I.J., Stahl J., Anderson P. Evidence that ternary complex (eIF2-GTP-tRNA(i)(Met))-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell 2002, 13:195-210.
16. Ohn T., Kedersha N., Hickman T., Tisdale S., Anderson P. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell Biol. 2008, 10:1224-1231.
17. Yamasaki S., Ivanov P., Hu G.F., Anderson P. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J. Cell Biol. 2009, 185:35-42.
18. Ivanov P., Emara M.M., Villen J., Gygi S.P., Anderson P. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol. Cell 2011, 43:613-623.
19. Zafarullah M., Li W.Q., Sylvester J., Ahmad M. Molecular mechanisms of N-acetylcysteine actions. Cell. Mol. Life Sci. 2003, 60:6-20.
20. Kedersha N., Cho M.R., Li W., Yacono P.W., Chen S., Gilks N., Golan D.E., Anderson P. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 2000, 151:1257-1268.
21. Grant C.M. Regulation of translation by hydrogen peroxide. Antioxid Redox Signal 2011, 15:191-203.
22. MacCallum P.R., Jack S.C., Egan P.A., McDermott B.T., Elliott R.M., Chan S.W. Cap-dependent and hepatitis C virus internal ribosome entry site-mediated translation are modulated by phosphorylation of eIF2alpha under oxidative stress. J. Gen. Virol. 2006, 87:3251-3262.
23. Patel J., McLeod L.E., Vries R.G., Flynn A., Wang X., Proud C.G. Cellular stresses profoundly inhibit protein synthesis and modulate the states of phosphorylation of multiple translation factors. Eur. J. Biochem. 2002, 269:3076-3085.
24. Shenton D., Smirnova J.B., Selley J.N., Carroll K., Hubbard S.J., Pavitt G.D., Ashe M.P., Grant C.M. Global translational responses to oxidative stress impact upon multiple levels of protein synthesis. J. Biol. Chem. 2006, 281:29011-29021.
25. Kedersha N.L., Gupta M., Li W., Miller I., Anderson P. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J. Cell Biol. 1999, 147:1431-1442.
26. Scheuner D., Song B., McEwen E., Liu C., Laybutt R., Gillespie P., Saunders T., Bonner-Weir S., Kaufman R.J. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 2001, 7:1165-1176.
27. Godon C., Lagniel G., Lee J., Buhler J.M., Kieffer S., Perrot M., Boucherie H., Toledano M.B., Labarre J. The H2O2 stimulon in Saccharomyces cerevisiae. J. Biol. Chem. 1998, 273:22480-22489.
28. Mascarenhas C., Edwards-Ingram L.C., Zeef L., Shenton D., Ashe M.P., Grant C.M. Gcn4 is required for the response to peroxide stress in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 2008, 19:2995-3007.
29. Gingras A.C., Raught B., Gygi S.P., Niedzwiecka A., Miron M., Burley S.K., Polakiewicz R.D., Wyslouch-Cieszynska A., Aebersold R., Sonenberg N. Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev. 2001, 15:2852-2864.
30. Oulhen N., Boulben S., Bidinosti M., Morales J., Cormier P., Cosson B. A variant mimicking hyperphosphorylated 4E-BP inhibits protein synthesis in a sea urchin cell-free, cap-dependent translation system. PLoS ONE 2009, 4:e5070.
31. Buchan J.R., Yoon J.H., Parker R. Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae. J Cell Sci 2011, 124:228-239.
32. Hoyle N.P., Castelli L.M., Campbell S.G., Holmes L.E., Ashe M.P. Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. J. Cell Biol. 2007, 179:65-74.
33. Bordeleau M.E., Mori A., Oberer M., Lindqvist L., Chard L.S., Higa T., Belsham G.J., Wagner G., Tanaka J., Pelletier J. Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat. Chem. Biol. 2006, 2:213-220.
34. Kim W.J., Kim J.H., Jang S.K. Anti-inflammatory lipid mediator 15d-PGJ2 inhibits translation through inactivation of eIF4A. EMBO J. 2007, 26:5020-5032.
35. Dang Y., Kedersha N., Low W.K., Romo D., Gorospe M., Kaufman R., Anderson P., Liu J.O. Eukaryotic initiation factor 2alpha-independent pathway of stress granule induction by the natural product pateamine A. J. Biol. Chem. 2006, 281:32870-32878.
36. Low W.K., Dang Y., Schneider-Poetsch T., Shi Z., Choi N.S., Merrick W.C., Romo D., Liu J.O. Inhibition of eukaryotic translation initiation by the marine natural product pateamine A. Mol. Cell 2005, 20:709-722.
37. Damgaard C.K., Lykke-Andersen J. Translational coregulation of 5'TOP mRNAs by TIA-1 and TIAR. Genes Dev. 2011, 25:2057-2068.
38. Ivanov P., Kedersha N., Anderson P. Stress puts TIA on TOP. Genes Dev. 2011, 25:2119-2124.