Selenite targets eIF4E-binding protein-1 to inhibit translation initiation and induce the assembly of non-canonical stress granules

Nucleic Acids Research

Volumn 40, Issue 16, 2012, Pages 8099-8110

  Fujimura, Ken ^a   Sasaki, Atsuo T ^b   Anderson, Paul ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 2ALPHA; INITIATION FACTOR 4E BINDING PROTEIN 1; SODIUM SELENITE;

ANIMAL CELL; ARTICLE; CELL ACTIVITY; CELL GRANULE; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; STRESS GRANULE; TRANSLATION INITIATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTINEOPLASTIC AGENTS; CELLS, CULTURED; CYTOPLASMIC GRANULES; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTOR-4F; HUMANS; MICE; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PEPTIDE INITIATION FACTORS; PHOSPHOPROTEINS; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; RIBONUCLEOPROTEINS; SODIUM SELENITE; STRESS, PHYSIOLOGICAL;

MAMMALIA;

EID: 84870270861     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks566     Document Type: Article

References (43)

1. Sonenberg, N. and Hinnebusch, A.G. (2009) Regulation of translation initiation in eukaryotes: mechanism and biological targets. Cell, 136, 731-745.
2. Anderson, P. and Kedersha, N. (2008) Stress granules: the tao of RNA triage. Trends Biochem. Sci., 33, 141-150.
3. Kim, W.J., Back, S.H., Kim, V., Ryu, I. and Jang, S.K. (2005) Sequestration of TRAF2 into stress granules interrupts tumor necrosis factor signaling under stress conditions. Mol. Cell. Biol., 25, 2450-2462.
4. Arimoto, K., Fukuda, H., Imajoh-Ohmi, S., Saito, H. and Takekawa, M. (2008) Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK signaling. Nat. Cell Biol., 10, 1324-1332.
5. Hoffman, I., Casella, M., Schnolzer, M., Schlechter, T., Spring, H. and Franke, W.W. (2006) Identification of the junctional plaque protein plakophilin 3 in cytoplasmic particles containing RNA binding proteins and the recruitment of plakophilins 1 and 3 to stress granules. Mol. Biol. Cell, 17, 1388-1398.
6. Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fritzler, M.J., Scheuner, D., Kaufman, R.J., Golan, D.E. and Anderson, P. (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol., 169, 871-884.
7. McEwen, E., Kedersha, N., Song, B., Scheuner, D., Gilks, N., Han, A., Chen, J.-J., Anderson, P. and Kaufman, R.J. (2005) Heme-regulated inhibitor kinase-mediated 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.
8. Kwon, S., Zhang, Y. and Matthias, P. (2007) The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev., 21, 3381-3394.
9. Eisinger-Mathason, T.S., Andrade, J., Groehler, A.L., Clark, D.E., Muratore-Schroeder, T.L., Pasic, L., Smith, J.A., Shabanowitz, J., Hunt, D.F. et al. (2008) Codependent functions of RSK2 and the apoptosis-promoting factor TIA-1 in stress granule assembly and cell survival. Mol. Cell, 31, 722-736.
10. Kim, B., Cooke, H.J. and Rhee, K. (2012) DAZL is essential for stress granule formation implicated in germ cell survival upon heat stress. Development, 139, 568-578.
11. Moeller, B.J., Cao, Y., Liu, C.Y. and Dewhirst, M.W. (2004) Radiation activates HIF1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell, 5, 429-441.
12. Fournier, M.J., Gareau, C. and Mazroui, R. (2010) The chemotherapeutic agent bortezomib induces the formation of stress granules. Cancer Cell Int., 10, 12.
13. Selenius, M., Rundlof, A.-K., Olm, E., Fernandes, A.P. and Bjornstedt, M. (2010) Selenium and selenoprotein thioredoxin reductase in the prevention, treatment and diagnostics of cancer. Antioxid. Redox Signaling, 12, 867-880.
14. Husbeck, B., Nonn, L., Peehl, D.M. and Knox, S.J. (2006) Tumor-selective killing by selenite in patient-matched pairs of normal and malignant prostate cells. Prostate, 66, 218-225.
15. Olm, E., Fernandes, A.P., Hebert, C., Rundlof, A.-K., Larsen, E.H., Danielsson, O. and Bjornstedt, M. (2009) Extracellular thiol-assisted selenium uptake dependent on the xc -cystine transporter explains the cancer-specific cytotoxicity of selenite. Proc. Natl. Acad. Sci. USA, 106, 11400-11405.
16. Guan, L., Han, B., Li, Z., Hua, F., Huang, F., Wei, W., Yang, Y. and Xu, C. (2009) Sodium selenite induces apoptosis by ROS-mediated endoplasmic reticulum stress and mitochondrial dysfunction in human acute promyelocytic leukemia NB4 cells. Apoptosis, 14, 218-225.
17. Suzuki, M., Endo, M., Shinohara, F., Echigo, S. and Rikiishi, H. (2010) Differential apoptotic response of human cancer cells to organoselenium compounds. Cancer Chemother. Pharmacol., 66, 475-484.
18. Kedersha, N., Tisdale, S., Hickman, T. and Anderson, P. (2008) Real-time and quantitative imaging of mammalian stress granules and processing bodies. Methods Enzymol., 448, 521-551.
19. Ohn, T., Kedersha, N., Hickman, T., Tisdale, S. and Anderson, P. (2008) A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell Biol., 10, 1224-1231.
20. Kedersha, N., Cho, M.R., Li, W., Yacono, P.W., Chen, S., Gilks, N., Golan, D.E. and Anderson, P. (2000) Dynamic shuttling of TIA-1 accompanies recruitment of mRNA to mammalian stress granules. J. Cell Biol., 151, 1257-1268.
21. Fujimura, K., Katahira, J., Kano, F., Yoneda, Y. and Murata, M. (2009) Microscopic dissection of the process of stress granule assembly. Biochim. Biophys. Acta, 1793, 1728-1737.
22. Fujimura, K., Suzuki, T., Yasuda, Y., Murata, M., Katahira, J. and Yoneda, Y. (2010) Identification of importin a1 as a novel constituent of RNA stress granules. Biochim. Biophys. Acta, 1803, 865-871.
23. Kedersha, N., Chen, S., Gilks, N., Li, W., Miller, I.J., Stahl, J. and Anderson, P. (2002) Evidence that ternary complex (eIF2-GTP-tRNAi Met)-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell, 13, 195-210.
24. Leung, A.K.L., Calabrese, J.M. and Sharp, P.A. (2006) Quantitative analysis of Argonaute proteins reveal microRNA-dependent localization to stress granules. Proc. Natl. Acad. Sci. USA, 103, 18125-18130.
25. Mazroui, R., Huot, M.-E., Tremblay, S., Filion, C., Labelle, Y. and Khandjian, E.W. (2002) Trapping of messenger RNA by fragile mental X retardation into cytoplasmic granules induces translational repression. Hum. Mol. Genet., 11, 3007-3017.
26. Gallouzi, I.E., Brennan, C.M., Stenberg, M.G., Swanson, M.S., Eversole, A., Maizels, N. and Steitz, J.A. (2000) HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc. Natl. Acad. Sci. USA, 97, 3073-3078.
27. Fujimura, K., Kano, F. and Murata, M. (2008) Identification of PCBP2, a facilitator of IRES-mediated translation, as a novel constituent of stress granules and processing bodies. RNA, 14, 425-431.
28. Li, C.-H., Ohn, T., Ivanov, P., Tisdale, S. and Anderson, P. (2010) eIF5A promotes translation elongation, polysome disassembly and stress granule assembly. PLoS One, 5, e9942.s.
29. Chang, W.-L. and Tarn, W.-Y. (2009) A role for transportin in deposition of TTP to cytoplasmic RNA granules and mRNA decay. Nucl. Acids Res., 37, 6600-6612.
30. Scheuner, D., Song, B., McEwen, E., Liu, C., Laybutt, R., Gillespie, P., Saunders, T., Bonner-Weir, S. and Kaufman, R.J. (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell, 7, 1165-1176.
31. Dang, Y., Kedersha, N., Low, W.-K., Romo, D., Gorospe, M., Kaufman, R.J., Anderson, P. and Liu, J.O. (2006) Eukaryotic initiation factor 2 a-independent pathway of stress granule induction by the natural product pateamine A. J. Biol. Chem., 281, 32870-32878.
32. Marissen, W.E. and Lloyd, R.E. (1998) Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol. Cell. Biol., 18, 7565-7574.
33. Zhao, R., Xiang, N., Domann, F.E. and Zhong, W. (2006) Expression of p53 enhances selenite-induced superoxide production and apoptosis in human prostate cancer cells. Cancer Res., 66, 2296-2304.
34. Hoyle, N.P., Castelli, L.M., Campbell, S.G., Holmes, L.E. and Ashe, M.P. (2007) Stress-dependent relocalization of translationally primed mRNPs to cytoplasmic granules that are kinetically and spatially distinct from P-bodies. J. Cell Biol., 179, 65-74.
35. Buchan, J.R., Muhlrad, D. and Parker, R. (2008) P bodies promote stress granule assembly in Saccharomyces cerevisiae. J. Cell Biol., 183, 441-455.
36. Buchan, J.R., Yoon, J.H. and Parker, R. (2011) Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae. J. Cell Sci., 124, 228-239.
37. Love, D.C. and Hanover, J.A. (2005) The hexosamine signaling pathway: deciphering the ''O-GlcNAc code''. Sci. STKE, 312, re13.
38. Ren, Y., Huang, F., Liu, Y., Yang, Y., Jiang, Q. and Xu, C. (2009) Autophagy inhibition through PI3K/Akt increases apoptosis by sodium selenite in NB4 cells. BMB Rep., 42, 599-604.
39. Harris, T.E., Chi, A., Shabanowitz, J., Hunt, D.F., Rhoads, R.E. and Lawrence, J.C. Jr (2006) mTOR-dependent stimulation of the association of eIF4G and eIF3 by insulin. EMBO J., 25, 1659-1668.
40. Rong, L., Livingstone, M., Sukarieh, R., Petroulakis, E., Gingras, A.-C., Crosby, K., Smith, B., Polakiewicz, R.D., Pelletier, J., Ferraiuolo, M.A. et al. (2008) Control of eIF4E cellular localization by eIF4E-binding proteins, 4 E-BPs. RNA, 14, 1318-1327.
41. Hagner, P.R., Mazan-Mamczarz, K., Dai, B., Balzer, E.M., Corl, S., Martin, S.S., Zhao, X.F. and Gartenhaus, R.B. (2011) Ribosomal protein S6 is highly expressed in non-Hodgkin lymphoma and associates with mRNA containing a 50 terminal oligopyrimidine tract. Oncogene, 30, 1531-1541.
42. Zhang, H., Cicchetti, G., Onda, H., Koon, H.B., Asrican, K., Bajraszewski, N., Vazquez, F., Carpenter, C.L. and Kwiatkowski, D.J. (2003) Loss of Tsc1/Tsc2 activates mTOR and disrupts PI3K-Akt signaling through downregulation of PDGFR. J. Clin. Invest., 112, 1223-1233.
43. Damgaard, C.K. and Lykke-Andersen, J. (2011) Translational coregulation of 50TOP mRNAs by TIA-1 and TIAR. Genes Dev., 25, 2057-2068.