Uncoupling stress granule assembly and translation initiation inhibition

Molecular Biology of the Cell

Volumn 20, Issue 11, 2009, Pages 2673-2683

  Mokas, Sophie ^a   Mills, John R ^b   Garreau, Cristina ^a   Fournier, Marie Josée ^a   Robert, Francis ^b   Arya, Prabhat ^c   Kaufman, Randal J ^d   Pelletier, Jerry ^b   Mazroui, Rachid ^a  

^a LAVAL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (4 METHYL 2,6 DINITROANILINO) N METHYLPROPIONAMIDE; CAP BINDING PROTEIN; GUANOSINE TRIPHOSPHATE; INITIATION FACTOR; INITIATION FACTOR 2; INITIATION FACTOR 2ALPHA; INITIATION FACTOR 4B; INITIATION FACTOR 4E; INITIATION FACTOR 4H; MESSENGER RNA; METHIONINE; POLYADENYLIC ACID BINDING PROTEIN; PROTEIN L28; TRANSFER RNA; TRANSFER RNA METHYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL GRANULE; CELL STRESS; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RIBOSOME; RIBOSOME SUBUNIT; TRANSLATION INITIATION; TRANSLATION REGULATION;

EUKARYOTA;

EID: 66349136830     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-10-1061     Document Type: Article

References (48)

1. Anderson, P., and Kedersha, N. (2006). RNA granules. J. Cell Biol. 172, 803-808.
2. Anderson, P., and Kedersha, N. (2008). Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33, 141-150.
3. Arimoto, K., Fukuda, H., Imajoh-Ohmi, S., Saito, H., and Takekawa, M. (2008). Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat. Cell Biol. 10, 1324-1332.
4. Baxter, R., Knell, V. C., Somerville, H. J., Swain, H. M., and Weeks, D. P. (1973). Effect of MDMP on protein synthesis in wheat and bacteria. Nat. New Biol. 243, 139-142.
5. Blume, J. E., and Shapiro, D. J. (1989). Ribosome loading, but not protein synthesis, is required for estrogen stabilization of Xenopus laevis vitellogenin mRNA. Nucleic Acids Res. 17, 9003-9014.
6. Brengues, M., Teixeira, D., and Parker, R. (2005). Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310, 486-489. (Pubitemid 41507961)
7. Cencic, R., Robert, F., and Pelletier, J. (2007). Identifying small molecule inhibitors of eukaryotic translation initiation. Methods Enzymol. 431, 269-302.
8. Craig, A. W., Haghighat, A., Yu, A. T., and Sonenberg, N. (1998). Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature 392, 520-523. (Pubitemid 28168986)
9. Dang, Y., Kedersha, N., Low, W. K., Romo, D., Gorospe, M., Kaufman, R., Anderson, P., and Liu, J. O. (2006). Eukaryotic initiation factor 2α-independent pathway of stress granule induction by the natural product pateamine A. J. Biol. Chem. 281, 32870-32878.
10. De Gregorio, E., Preiss, T., and Hentze, M. W. (1999). Translation driven by an eIF4G core domain in vivo. EMBO J. 18, 4865-4874. (Pubitemid 29415539)
11. Emara, M. M., and Brinton, M. A. (2007). Interaction of TIA-1/TIAR with West Nile and dengue virus products in infected cells interferes with stress granule formation and processing body assembly. Proc. Natl. Acad. Sci. USA 104, 9041-9046.
12. 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.
13. Gebauer, F., and Hentze, M. W. (2004). Molecular mechanisms of translational control. Nat. Rev. 5, 827-835.
14. Gingras, A. C., Raught, B., and Sonenberg, N. (1999). eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68, 913-963.
15. Kahvejian, A., Roy, G., and Sonenberg, N. (2001). The mRNA closed-loop model: the function of PABP and PABP-interacting proteins in mRNA translation. Cold Spring Harb. Symp. Quant. Biol. 66, 293-300.
16. Kapp, L. D., and Lorsch, J. R. (2004). The molecular mechanics of eukaryotic translation. Annu. Rev. Biochem. 73, 657-704.
17. Kedersha, N., and Anderson, P. (2007). Mammalian stress granules and processing bodies. Methods Enzymol. 431, 61-81.
18. Kedersha, N., Chen, S., Gilks, N., Li, W., Miller, I. J., Stahl, J., and 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.
19. 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 the recruitment of mRNA to mammalian stress granules. J. Cell Biol. 151, 1257-1268.
20. Kedersha, N. L., Gupta, M., Li, W., Miller, I., and 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. (Pubitemid 30027399)
21. 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. (Pubitemid 41002864)
22. Lin, C. J., Cencic, R., Mills, J. R., Robert, F., and Pelletier, J. (2008). c-Myc and eIF4F are components of a feedforward loop that links transcription and translation. Cancer Res. 68, 5326-5334.
23. Marintchev, A., and Wagner, G. (2004). Translation initiation: structures, mechanisms and evolution. Q. Rev. Biophys. 37, 197-284.
24. Mazroui, R., Di Marco, S., Clair, E., von Roretz, C., Tenenbaum, S. A., Keene, J. D., Saleh, M., and Gallouzi, I. E. (2008). Caspase-mediated cleavage of HuR in the cytoplasm contributes to pp32/PHAP-I regulation of apoptosis. J. Cell Biol. 180, 113-127.
25. Mazroui, R., Di Marco, S., Kaufman, R. J., and Gallouzi, I. E. (2007). Inhibition of the ubiquitin-proteasome system induces stress granule formation. Mol. Biol. Cell 18, 2603-2618.
26. Mazroui, R., Huot, M. E., Tremblay, S., Boilard, N., Labelle, Y., and Khandjian, E. W. (2003). Fragile X Mental Retardation protein determinants required for its association with polyribosomal mRNPs. Hum. Mol. Genet. 12, 3087-3096.
27. Mazroui, R., Huot, M. E., Tremblay, S., Filion, C., Labelle, Y., and Khandjian, E. W. (2002). Trapping of messenger RNA by fragile X mental retardation protein into cytoplasmic granules induces translation repression. Hum. Mol. Genet. 11, 3007-3017.
28. Mazroui, R., Sukarieh, R., Bordeleau, M. E., Kaufman, R. J., Northcote, P., Tanaka, J., Gallouzi, I., and Pelletier, J. (2006). Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation. Mol. Biol. Cell 17, 4212-4219.
29. McInerney, G. M., Kedersha, N. L., Kaufman, R. J., Anderson, P., and Liljestrom, P. (2005). Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation. Mol. Biol. Cell 16, 3753-3763.
30. Michel, Y. M., Poncet, D., Piron, M., Kean, K. M., and Borman, A. M. (2000). Cap-Poly(A) synergy in mammalian cell-free extracts. Investigation of the requirements for poly(A)-mediated stimulation of translation initiation. J. Biol. Chem. 275, 32268-32276.
31. Moeller, B. J., Cao, Y., Li, C. Y., and Dewhirst, M. W. (2004). Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 5, 429-441. (Pubitemid 38610245)
32. Moerke, N. J., et al. (2007). Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 128, 257-267.
33. Montero, H., Rojas, M., Arias, C. F., and Lopez, S. (2008). Rotavirus infection induces the phosphorylation of eIF2alpha but prevents the formation of stress granules. J. Virol. 82, 1496-1504.
34. 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.
35. Pestova, T. V., Kolupaeva, V. G., Lomakin, I. B., Pilipenko, E. V., Shatsky, I. N., Agol, V. I., and Hellen, C. U. (2001). Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. USA 98, 7029-7036.
36. Pisarev, A. V., Shirokikh, N. E., and Hellen, C. U. (2005). Translation initiation by factor-independent binding of eukaryotic ribosomes to internal ribosomal entry sites. C. R. Biol. 328, 589-605.
37. Pyronnet, S., Dostie, J., and Sonenberg, N. (2001). Suppression of cap-dependent translation in mitosis. Genes Dev. 15, 2083-2093. (Pubitemid 32762052)
38. Pyronnet, S., Pradayrol, L., and Sonenberg, N. (2000). A cell cycle-dependent internal ribosome entry site. Mol. Cell 5, 607-616.
39. Robert, F., et al. (2006). Initiation of protein synthesis by hepatitis C virus is refractory to reduced eIF2.GTP. Met-tRNA (i) (Met) ternary complex availability. Mol. Biol. Cell 17, 4632-4644.
40. 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. (Pubitemid 32607351)
41. Sivan, G., Kedersha, N., and Elroy-Stein, O. (2007). Ribosomal slowdown mediates translational arrest during cellular division. Mol. Cell. Biol. 27, 6639-6646.
42. Sonenberg, N. (2008). eIF4E, the mRNA cap-binding protein: from basic discovery to translational research. Biochem. Cell Biol. 86, 178-183.
43. Sonenberg, N., and Dever, T. E. (2003). Eukaryotic translation initiation factors and regulators. Curr. Opin. Struct. Biol. 13, 56-63.
44. Svitkin, Y. V., Herdy, B., Costa-Mattioli, M., Gingras, A. C., Raught, B., and Sonenberg, N. (2005). Eukaryotic translation initiation factor 4E availability controls the switch between cap-dependent and internal ribosomal entry site-mediated translation. Mol. Cell. Biol. 25, 10556-10565.
45. Svitkin, Y. V., and Sonenberg, N. (2006). Translational control by the poly(A) binding protein: a check for mRNA integrity. Mol. Biol. 40, 684-693.
46. Teixeira, D., Sheth, U., Valencia-Sanchez, M. A., Brengues, M., and Parker, R. (2005). Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 11, 371-382. (Pubitemid 40397171)
47. Wakiyama, M., Imataka, H., and Sonenberg, N. (2000). Interaction of eIF4G with poly(A)-binding protein stimulates translation and is critical for Xenopus oocyte maturation. Curr. Biol. 10, 1147-1150.
48. Wek, R. C., Jiang, H. Y., and Anthony, T. G. (2006). Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34, 7-11.