Stress-induced inhibition of translation independently of eIF2α phosphorylation

Journal of Cell Science

Volumn 128, Issue 23, 2015, Pages 4420-4427

  Knutsen, Jon Halvor Jonsrud ^a   Rødland, Gro Elise ^a   Bøe, Cathrine Arnason ^a   Håland, Tine Weise ^a   Sunnerhagen, Per ^b   Grallert, Beáta ^a   Boye, Erik ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

EIF2S1; eIF2 ; SPBC4B4.04; Stress; SUI2; Translation; Ultraviolet light

Indexed keywords

GENERAL CONTROL NONDEREPRESSIBLE 2 PROTEIN; HYDROGEN PEROXIDE; INITIATION FACTOR 2ALPHA; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 1; MESSENGER RNA; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG; GCN2 PROTEIN, S POMBE; INITIATION FACTOR 2; PROTEIN SERINE THREONINE KINASE; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; MAMMAL CELL; MOUSE; NONHUMAN; OXIDATIVE STRESS; POLYSOME; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RADIATION DOSE; RADIATION EXPOSURE; RIBOSOME; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; TRANSLATION REGULATION; ULTRAVIOLET IRRADIATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; RADIATION RESPONSE; SCHIZOSACCHAROMYCES; ULTRAVIOLET RADIATION;

EUKARYOTIC INITIATION FACTOR-2; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; STRESS, PHYSIOLOGICAL; ULTRAVIOLET RAYS;

EID: 84949870380     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.176545     Document Type: Article

References (44)

1. Aitken, C. E. and Lorsch, J. R. (2012). A mechanistic overview of translation initiation in eukaryotes. Nat. Struct. Mol. Biol. 19, 568-576.
2. Ashe, M. P., Slaven, J.W., De Long, S. K., Ibrahimo, S. and Sachs, A.B. (2001). A novel eIF2B-dependent mechanism of translational control in yeast as a response to fusel alcohols. EMBO J. 20, 6464-6474.
3. Beatty, K. E. and Tirrell, D. A. (2008). Two-color labeling of temporally defined protein populations in mammalian cells. Bioorg. Med. Chem. Lett. 18, 5995-5999.
4. Best, M. D. (2009). Click chemistry and bioorthogonal reactions: unprecedented selectivity in the labeling of biological molecules. Biochemistry 48, 6571-6584.
5. Browne, G. J. and Proud, C. G. (2002). Regulation of peptide-chain elongation in mammalian cells. Eur. J. Biochem. 269, 5360-5368.
6. Buffington, S. A., Huang, W. and Costa-Mattioli, M. (2014). Translational control in synaptic plasticity and cognitive dysfunction. Annu. Rev. Neurosci. 37, 17-38.
7. Casati, P. and Walbot, V. (2004). Crosslinking of ribosomal proteins to RNA in maize ribosomes by UV-B and its effects on translation. Plant Physiol. 136, 3319-3332.
8. Caspari, T., Dahlen, M., Kanter-Smoler, G., Lindsay, H. D., Hofmann, K., Papadimitriou, K., Sunnerhagen, P. and Carr, A. M. (2000). Characterization of Schizosaccharomyces pombe Hus1: a PCNA-related protein that associates with Rad1 and Rad9. Mol. Cell. Biol. 20, 1254-1262.
9. Castilho, B. A., Shanmugam, R., Silva, R. C., Ramesh, R., Himme, B. M. and Sattlegger, E. (2014). Keeping the eIF2 alpha kinase Gcn2 in check. Biochim. Biophys. Acta 1843, 1948-1968.
10. Chu, D., Kazana, E., Bellanger, N., Singh, T., Tuite, M. F. and von der Haar, T. (2013). Translation elongation can control translation initiation on eukaryotic mRNAs. EMBO J. 33, 21-34.
11. Clemens, M. J. (2001). Initiation factor eIF2 alpha phosphorylation in stress responses and apoptosis. Prog. Mol. Subcell. Biol. 27, 57-89.
12. Deng, J., Harding, H. P., Raught, B., Gingras, A.-C., Berlanga, J. J., Scheuner, D., Kaufman, R. J., Ron, D. and Sonenberg, N. (2002). Activation of GCN2 in UV-irradiated cells inhibits translation. Curr. Biol. 12, 1279-1286.
13. Dieterich, D. C., Hodas, J. J. L., Gouzer, G., Shadrin, I. Y., Ngo, J. T., Triller, A., Tirrell, D. A. and Schuman, E. M. (2010). In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat. Neurosci. 13, 897-905.
14. Dunand-Sauthier, I., Walker, C., Wilkinson, C., Gordon, C., Crane, R., Norbury, C. and Humphrey, T. (2002). Sum1, a component of the fission yeast eIF3 translation initiation complex, is rapidly relocalized during environmental stress and interacts with components of the 26S proteasome. Mol. Biol. Cell 13, 1626-1640.
15. Firczuk, H., Kannambath, S., Pahle, J., Claydon, A., Beynon, R., Duncan, J., Westerhoff, H., Mendes, P. and McCarthy, J. E. (2013). An in vivo control map for the eukaryotic mRNA translation machinery. Mol. Syst. Biol. 9, 635.
16. Fox, J. T., Shin, W. K., Caudill, M. A. and Stover, P. J. (2009). A UV-responsive internal ribosome entry site enhances serine hydroxymethyltransferase 1 expression for DNA damage repair. J. Biol. Chem. 284, 31097-31108.
17. Grallert, B. and Boye, E. (2007). The Gcn2 kinase as a cell cycle regulator. Cell Cycle 6, 2768-2772.
18. Grousl, T., Ivanov, P., Frydlova, I., Vasicova, P., Janda, F., Vojtova, J., Malinska, K., Malcova, I., Novakova, L., Janoskova, D. et al. (2009). Robust heat shock induces eIF2alpha-phosphorylation-independent assembly of stress granules containing eIF3 and 40S ribosomal subunits in budding yeast, Saccharomyces cerevisiae. J. Cell Sci. 122, 2078-2088.
19. Hamanaka, R. B., Bennett, B. S., Cullinan, S. B. and Diehl, J. A. (2005). PERK and GCN2 contribute to eIF2alpha phosphorylation and cell cycle arrest after activation of the unfolded protein response pathway. Mol. Biol. Cell 16, 5493-5501.
20. Hinnebusch, A. G. (2005). Translational regulation of GCN4 and the general amino acid control of yeast. Annu. Rev. Microbiol. 59, 407-450.
21. Iordanov, M. S., Pribnow, D., Magun, J. L., Dinh, T.-H., Pearson, J. A. and Magun, B. E. (1998). Ultraviolet radiation triggers the ribotoxic stress response in mammalian cells. J. Biol. Chem. 273, 15794-15803.
22. Knutsen, J. H. J., Rein, I. D., Rothe, C., Stokke, T., Grallert, B. and Boye, E. (2011). Cell-cycle analysis of fission yeast cells by flow cytometry. PLoS ONE 6, e17175.
23. Krieg, J., Hofsteenge, J. and Thomas, G. (1988). Identification of the 40 S ribosomal protein S6 phosphorylation sites induced by cycloheximide. J. Biol. Chem. 263, 11473-11477.
24. Krohn, M., Skjølberg, H. C., Soltani, H., Grallert, B. and Boye, E. (2008). The G1-S checkpoint in fission yeast is not a general DNA damage checkpoint. J. Cell Sci. 121, 4047-4054.
25. Leprivier, G., Remke, M., Rotblat, B., Dubuc, A., Mateo, A.-R. F., Kool, M., Agnihotri, S., El-Naggar, A., Yu, B., Prakash Somasekharan, S. et al. (2013). The eEF2 kinase confers resistance to nutrient deprivation by blocking translation elongation. Cell 153, 1064-1079.
26. Leupold, U. (1950). Die Vererbung von Homothallie und Heterothallie bei Schizosaccharomyces pombe. Cr. Trav. Lab. Carlsberg Ser. Physiol., 24, 381-480.
27. Liu, J., Xu, Y., Stoleru, D. and Salic, A. (2012). Imaging protein synthesis in cells and tissues with an alkyne analog of puromycin. Proc. Natl. Acad. Sci. USA 109, 413-418.
28. Loreni, F., Mancino, M. and Biffo, S. (2014). Translation factors and ribosomal proteins control tumor onset and progression: how? Oncogene 33, 2145-2156.
29. Moreno, S., Klar, A. and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
30. Nilsson, D. and Sunnerhagen, P. (2011). Cellular stress induces cytoplasmic RNA granules in fission yeast. RNA 17, 120-133.
31. Nilssen, E. A., Synnes, M., Kleckner, N., Grallert, B. and Boye, E. (2003). Intra-G1 arrest in response to UV irradiation in fission yeast. Proc. Natl. Acad. Sci. USA 100, 10758-10763.
32. Patel, J., McLeod, L. E., Vries, R. G. J., Flynn, A., Wang, X. and Proud, C. G. (2002). Cellular stresses profoundly inhibit protein synthesis and modulate the states of phosphorylation of multiple translation factors. Eur. J. Biochem. 269, 3076-3085.
33. Proud, C. G. (2004). mTOR-mediated regulation of translation factors by amino acids. Biochem. Biophys. Res. Commun. 313, 429-436.
34. Rødland, G. E., Tvegård, T., Boye, E. and Grallert, B. (2014). Crosstalk betweenthe Tor and Gcn2 pathways in response to different stresses. Cell Cycle 13, 453-461.
35. Shenton, D., Smirnova, J. B., Selley, J. N., Carroll, K., Hubbard, S. J., Pavitt, G. D., Ashe, M. P. and Grant, C. M. (2006). Global translational responses to oxidative stress impact upon multiple levels of protein synthesis. J. Biol. Chem. 281, 29011-29021.
36. Signer, R. A. J., Magee, J. A., Salic, A. and Morrison, S. J. (2014). Haematopoietic stem cells require a highly regulated protein synthesis rate. Nature 509, 49-54.
37. Sonenberg, N. and Hinnebusch, A. G. (2007). New modes of translational control in development, behavior, and disease. Mol. Cell 28, 721-729.
38. Sonenberg, N. and Hinnebusch, A. G. (2009). Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745.
39. Stark, C., Su, T.-C., Breitkreutz, A., Lourenco, P., Dahabieh, M., Breitkreutz, B.-J., Tyers, M. and Sadowski, I. (2010). PhosphoGRID: a database of experimentally verified in vivo protein phosphorylation sites from the budding yeast Saccharomyces cerevisiae. Database 2010, bap026.
40. Swaminathan, S., Masek, T., Molin, C., Pospisek, M. and Sunnerhagen, P. (2006). Rck2 is required for reprogramming of ribosomes during oxidative stress. Mol. Biol. Cell 17, 1472-1482.
41. Tvegård, T., Soltani, H., Skjølberg, H. C., Krohn, M., Nilssen, E. A., Kearsey, S. E., Grallert, B. and Boye, E. (2007). A novel checkpoint mechanismregulating the G1/S transition. Genes Dev. 21, 649-654.
42. Vattem, K. M. and Wek, R. C. (2004). Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. USA 101, 11269-11274.
43. Wells, D. G. (2012). mRNA translation: regulating an out of soma experience. Curr. Opin. Cell Biol. 24, 554-557.
44. Wu, S., Hu, Y., Wang, J.-L., Chatterjee, M., Shi, Y. and Kaufman, R. J. (2002). Ultraviolet light inhibits translation through activation of the unfolded protein response kinase PERK in the lumen of the endoplasmic reticulum. J. Biol. Chem. 277, 18077-18083.