Integrated stress response of vertebrates is regulated by four eIF2α kinases

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Taniuchi, Shusuke ^a,b   Miyake, Masato ^a,b   Tsugawa, Kazue ^a   Oyadomari, Miho ^a   Oyadomari, Seiichi ^a,b  

^a Otsuka Pharmaceutical   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EIF2AK4 PROTEIN, MOUSE; EIF2ALPHA KINASE, MOUSE; PERK KINASE; PROTEIN KINASE R; PROTEIN KINASE R, MOUSE; PROTEIN SERINE THREONINE KINASE;

ANIMAL; CAENORHABDITIS ELEGANS; CELL LINE; CRISPR CAS SYSTEM; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; FIBROBLAST; GENE EDITING; METABOLISM; MOUSE; PHOSPHORYLATION; PHYLOGENY;

ANIMALS; CAENORHABDITIS ELEGANS; CELL LINE; CRISPR-CAS SYSTEMS; DROSOPHILA MELANOGASTER; EIF-2 KINASE; ENDOPLASMIC RETICULUM; FIBROBLASTS; GENE EDITING; MICE; PHOSPHORYLATION; PHYLOGENY; PROTEIN-SERINE-THREONINE KINASES;

EID: 84988352997     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep32886     Document Type: Article

References (48)

1. Wek, R. C., Jiang, H. Y., Anthony, T. G. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34, 7-11, doi: 10. 1042/BST20060007 (2006).
2. Pathak, V. K., Schindler, D., Hershey, J. W. Generation of a mutant form of protein synthesis initiation factor eIF-2 lacking the site of phosphorylation by eIF-2 kinases. Mol Cell Biol 8, 993-995 (1988).
3. Harding, H. P. et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11, 619-633 (2003).
4. Ron, D. Translational control in the endoplasmic reticulum stress response. Journal of Clinical Investigation 110, 1383-1388, doi: 10. 1172/jc0200216784 (2002).
5. Oyadomari, S., Harding, H. P., Zhang, Y., Oyadomari, M., Ron, D. Dephosphorylation of translation initiation factor 2alpha enhances glucose tolerance and attenuates hepatosteatosis in mice. Cell Metab 7, 520-532, doi: 10. 1016/j. cmet. 2008. 04. 011 (2008).
6. Baird, T. D., Wek, R. C. Eukaryotic initiation factor 2 phosphorylation and translational control in metabolism. Adv Nutr 3, 307-321, doi: 10. 3945/an. 112. 002113 (2012).
7. Costa-Mattioli, M. et al. Translational control of hippocampal synaptic plasticity and memory by the eIF2alpha kinase GCN2. Nature 436, 1166-1173, doi: 10. 1038/nature03897 (2005).
8. Sidrauski, C. et al. Pharmacological brake-release of mRNA translation enhances cognitive memory. Elife 2, e00498, doi: 10. 7554/eLife. 00498 (2013).
9. Dey, S. et al. ATF4-dependent induction of heme oxygenase 1 prevents anoikis and promotes metastasis. J Clin Invest 125, 2592-2608, doi: 10. 1172/JCI78031 (2015).
10. Munn, D. H. et al. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2, 3-dioxygenase. Immunity 22, 633-642, doi: 10. 1016/j. immuni. 2005. 03. 013 (2005).
11. Chen, J. J., London, I. M. Regulation of protein synthesis by heme-regulated eIF-2 alpha kinase. Trends Biochem Sci 20, 105-108 (1995).
12. Chen, J. J. et al. Cloning of the cDNA of the heme-regulated eukaryotic initiation factor 2 alpha (eIF-2 alpha) kinase of rabbit reticulocytes: homology to yeast GCN2 protein kinase and human double-stranded-RNA-dependent eIF-2 alpha kinase. Proc Natl Acad Sci USA 88, 7729-7733 (1991).
13. Levin, D. H., Petryshyn, R., London, I. M. Characterization of double-stranded-RNA-activated kinase that phosphorylates alpha subunit of eukaryotic initiation factor 2 (eIF-2 alpha) in reticulocyte lysates. Proc Natl Acad Sci USA 77, 832-836 (1980).
14. Meurs, E. et al. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 62, 379-390 (1990).
15. Harding, H. P., Zhang, Y., Ron, D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274, doi: 10. 1038/16729 (1999).
16. Bertolotti, A., Zhang, Y., Hendershot, L. M., Harding, H. P., Ron, D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2, 326-332, doi: 10. 1038/35014014 (2000).
17. Dever, T. E. et al. Phosphorylation of initiation factor 2 alpha by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68, 585-596 (1992).
18. Zhang, P. et al. The GCN2 eIF2alpha kinase is required for adaptation to amino acid deprivation in mice. Mol Cell Biol 22, 6681-6688 (2002).
19. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., Sudarsanam, S. The protein kinase complement of the human genome. Science 298, 1912-1934, doi: 10. 1126/science. 1075762 (2002).
20. Manning, G., Plowman, G. D., Hunter, T., Sudarsanam, S. Evolution of protein kinase signaling from yeast to man. Trends Biochem Sci 27, 514-520 (2002).
21. Narasimhan, J. et al. Translation regulation by eukaryotic initiation factor-2 kinases in the development of latent cysts in Toxoplasma gondii. Journal of Biological Chemistry 283, 16591-16601, doi: 10. 1074/jbc. M800681200 (2008).
22. Konrad, C., Wek, R. C., Sullivan, W. J. A GCN2-Like Eukaryotic Initiation Factor 2 Kinase Increases the Viability of Extracellular Toxoplasma gondii Parasites. Eukaryotic Cell 10, 1403-1412, doi: 10. 1128/ec. 05117-11 (2011).
23. Konrad, C., Wek, R. C., Sullivan, W. J. GCN2-like eIF2 alpha kinase manages the amino acid starvation response in Toxoplasma gondii. International Journal for Parasitology 44, 139-146, doi: 10. 1016/j. ijpara. 2013. 08. 005 (2014).
24. Patel, C. V., Handy, I., Goldsmith, T., Patel, R. C. PACT, a stress-modulated cellular activator of interferon-induced doublestranded RNA-activated protein kinase, PKR. Journal of Biological Chemistry 275, 37993-37998, doi: 10. 1074/jbc. M004762200 (2000).
25. Lu, L. R., Han, A. P., Chen, J. J. Translation initiation control by heme-regulated eukaryotic initiation factor 2 alpha kinase in erythroid cells under cytoplasmic stresses. Molecular and Cellular Biology 21, 7971-7980, doi: 10. 1128/mcb. 21. 23. 7971-7980. 2001 (2001).
26. McEwen, E. et al. Heme-regulated inhibitor kinase-mediated phosphorylation of eukaryotic translation initiation factor 2 inhibits translation, induces stress granule formation, mediates survival upon arsenite exposure. Journal of Biological Chemistry 280, 16925-16933, doi: 10. 1074/jbc. M412882200 (2005).
27. Zhan, K., Narasimhan, J., Wek, R. C. Differential activation of eIF2 kinases in response to cellular stresses in Schizosaccharomyces pombe. Genetics 168, 1867-1875, doi: 10. 1534/genetics. 104. 031443 (2004).
28. Cosentino, G. P. et al. Double-stranded-RNA-dependent protein kinase and TAR RNA-binding protein form homo-and heterodimers in vivo. Proc Natl Acad Sci USA 92, 9445-9449 (1995).
29. Kimball, S. R., Antonetti, D. A., Brawley, R. M., Jefferson, L. S. Mechanism of inhibition of peptide chain initiation by amino acid deprivation in perfused rat liver. Regulation involving inhibition of eukaryotic initiation factor 2 alpha phosphatase activity. J Biol Chem 266, 1969-1976 (1991).
30. Wu, S. Y. et al. Ultraviolet light inhibits translation through activation of the unfolded protein response kinase PERK in the lumen of the endoplasmic reticulum. Journal of Biological Chemistry 277, 18077-18083, doi: 10. 1074/jbc. M110164200 (2002).
31. Deng, J. et al. Activation of GCN2 in UV-irradiated cells inhibits translation. Current Biology 12, 1279-1286, doi: 10. 1016/s0960-9822(02)01037-0 (2002).
32. Hofmann, S., Cherkasova, V., Bankhead, P., Bukau, B., Stoecklin, G. Translation suppression promotes stress granule formation and cell survival in response to cold shock. Molecular Biology of the Cell 23, 3786-3800, doi: 10. 1091/mbc. E12-04-0296 (2012).
33. Gomez, E., Powell, M. L., Bevington, A., Herbert, T. P. A decrease in cellular energy status stimulates PERK-dependent eIF2 alpha phosphorylation and regulates protein synthesis in pancreatic beta-cells. Biochemical Journal 410, 485-493, doi: 10. 1042/bj20071367 (2008).
34. Moore, C. E., Omikorede, O., Gomez, E., Willars, G. B., Herbert, T. P. PERK Activation at Low Glucose Concentration Is Mediated by SERCA Pump Inhibition and Confers Preemptive Cytoprotection to Pancreatic beta-Cells. Molecular Endocrinology 25, 315-326, doi: 10. 1210/me. 2010-0309 (2011).
35. Berlanga, J. J., Santoyo, J., de Haro, C. Characterization of a mammalian homolog of the GCN2 eukaryotic initiation factor 2 alpha kinase. European Journal of Biochemistry 265, 754-762, doi: 10. 1046/j. 1432-1327. 1999. 00780. x (1999).
36. Srivastava, S. P., Kumar, K. U., Kaufman, R. J. Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. Journal of Biological Chemistry 273, 2416-2423, doi: 10. 1074/jbc. 273. 4. 2416 (1998).
37. Koumenis, C. et al. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2 alpha. Molecular and Cellular Biology 22, 7405-7416, doi: 10. 1128/mcb. 22. 21. 7405-7416. 2002 (2002).
38. Liu, Y. et al. Regulation of G(1) arrest and apoptosis in hypoxia by PERK and GCN2-mediated eIF2alpha phosphorylation. Neoplasia 12, 61-68 (2010).
39. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823, doi: 10. 1126/science. 1231143 (2013).
40. Wang, H. et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910-918, doi: 10. 1016/j. cell. 2013. 04. 025 (2013).
41. Lageix, S. et al. Arabidopsis eIF2 alpha kinase GCN2 is essential for growth in stress conditions and is activated by wounding. Bmc Plant Biology 8, 9, doi: 10. 1186/1471-2229-8-134 (2008).
42. Uma, S., Yun, B. G., Matts, R. L. The heme-regulated eukaryotic initiation factor 2alpha kinase. A potential regulatory target for control of protein synthesis by diffusible gases. J Biol Chem 276, 14875-14883, doi: 10. 1074/jbc. M011476200 (2001).
43. Joshi, M., Kulkarni, A., Pal, J. K. Small molecule modulators of eukaryotic initiation factor 2alpha kinases, the key regulators of protein synthesis. Biochimie 95, 1980-1990, doi: 10. 1016/j. biochi. 2013. 07. 030 (2013).
44. Kitamura, T. et al. Retrovirus-mediated gene transfer and expression cloning: powerful tools in functional genomics. Exp Hematol 31, 1007-1014 (2003).
45. Ran, F. A. et al. Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8, 2281-2308, doi: 10. 1038/nprot. 2013. 143 (2013).
46. Oyadomari, S. et al. Cotranslocational degradation protects the stressed endoplasmic reticulum from protein overload. Cell 126, 727-739, doi: 10. 1016/j. cell. 2006. 06. 051 (2006).
47. Thompson, J. D., Higgins, D. G., Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680 (1994).
48. Kumar, S., Tamura, K., Jakobsen, I. B., Nei, M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244-1245 (2001).