PERK is responsible for the increased phosphorylation of eIF2α and the severe inhibition of protein synthesis after transient global brain ischemia

Journal of Neurochemistry

Volumn 94, Issue 5, 2005, Pages 1235-1242

  Owen, Cheri R ^a   Kumar, Rita ^a   Zhang, Peichuan ^b   McGrath, Barbara C ^b   Cavener, Douglas R ^b   Krause, Gary S ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Eukaryotic initiation factor 2; RNA dependent protein kinase like endoplasmic reticulum kinase; Transgenic mice; Transient cerebral ischemia; Translation initiation factors

Indexed keywords

INITIATION FACTOR 2ALPHA; PROTEIN KINASE; PROTEIN KINASE R; RNA DEPENDENT PROTEIN KINASE LIKE ENDOPLASMIC RETICULUM KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CELL SURVIVAL; CONTROLLED STUDY; GENE DISRUPTION; HIGH ENERGY PHOSPHATE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; REPERFUSION INJURY; TRANSGENIC MOUSE; TRANSLATION INITIATION; WILD TYPE;

ANIMALS; EIF-2 KINASE; EUKARYOTIC INITIATION FACTOR-2; ISCHEMIC ATTACK, TRANSIENT; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PHOSPHORYLATION; REPERFUSION INJURY;

EUKARYOTA; MUS MUSCULUS; TRIXIS;

EID: 24144440965     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03276.x     Document Type: Article

References (61)

1. Althausen S., Mengesdorf T., Mies G., Olah L., Nairn A. C., Proud C. G. and Paschen W. (2001) Changes in the phosphorylation of initiation factor eIF-2α, elongation factor eEF-2 and p70 S6 kinase after transient focal cerebral ischaemia in mice. J. Neurochem. 78, 779-787.
2. Ames A. III, Wright L., Kowada M., Thurston J. and Majno G. (1968) Cerebral ischemia II. Am. J. Pathol. 52, 437-442.
3. Araki T., Kato H., Inoue T. and Kogure K. (1990) Regional impairment of protein synthesis following brief cerebral ischemia in the gerbil. Acta Neuropathol. (Berl.) 79, 501-505.
4. Bedard K., MacDonald N., Collins J. and Cribb A. (2004) Cytoprotection following endoplasmic reticulum stress protein induction in continuous cell lines. Pharmacol. Toxicol. 94, 124-131.
5. Bertolotti A., Zhang Y., Hendershot L. M., Harding H. P. and Ron D. (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell. Biol. 2, 326-332.
6. Brostrom C. O. and Brosrrom M. A. (1998) Regulation of translational initiation during cellular responses to stress. Prog. Nucl. Acid Res. Mol. Biol. 58, 79-125.
7. Browne G. J. and Proud C. G. (2002) Regulation of peptide-chain elongation in mammalian cells. Eur. J. Biochem. 269, 5360-5368.
8. Burda J., Martin E. M., Garcia A., Alcazar A., Fando J. L. and Saunas M. (1994) Phosphorylation of the α subunit of initiation factor 2 correlates with the inhibition of translation following transient cerebral ischaemia in the rat. Biochem. J. 302, 335-338.
9. Clemens M. J. (2001) Initiation factor eIF2α phosphorylation in stress responses and apoptosis. Prog. Mol. Subcell. Biol. 27, 57-89.
10. Cosgrove J. W. and Rapoport S. I. (1986) Preparation of a cell-free extract from rat brain which can initiate protein synthesis in vitro. Neurochem. Res. 11, 1289-1301.
11. Crosby J. S., Lee K., London I. M. and Chen J. J. (1994) Erythroid expression of the heme-regulated eIF-2α kinase. Mol. Cell Biol. 14, 3906-3914.
12. Csermely P., Schnaider T., Soti C., Prohaszka Z. and Nardai G. (1998) The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol Ther. 79, 129-168.
13. DeGracia D. J., Neumar R. W., White B. C. and Krause G. S. (1996) Global brain ischemia and reperfusion: Modifications in eukaryotic initiation factors are associated with inhibition of translation initiation. J. Neurochem. 67, 2005-2012.
14. DeGracia D. J., Sullivan J. M., Neumar R. W., Alousi S. S., Hikade K. R., Pittman J. E., White B. C., Rafols J. A. and Krause G. S. (1997) Effect of brain ischemia and reperfusion on the localization of phosphorylated eukaryotic initiation factor 2α. J. Cereb. Blood Flow Metab. 17, 1291-1302.
15. DeGracia D. J., Adamczyk S., Folbe A. J. et al. (1999) Eukaryotic initiation factor 2α kinase and phosphatase activity during post-ischemic brain reperfusion. Exp. Neurol. 155, 221-227.
16. Djuricic B., Rohn G., Paschen W. and Hossmann K. A. (1995) Calcium activity and post-ischemic suppression of protein synthesis. Experientia 51, 245-248.
17. Fresno M., Carrasco L. and Vazquez D. (1976) Initiation of the polypeptide chain by reticulocyte cell-free systems: Survey of different inhibitors of translation. Eur. J. Biochem. 68, 353-364.
18. Harding H. P., Zhang Y. and Ron D. (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274.
19. Harding H. P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M. and Ron D. (2000a) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6, 1099-1108.
20. Harding H. P., Zhang Y., Bertolotti A., Zeng H. and Ron D. (2000b) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5, 897-904.
21. Hossmann K. A. (1993) Disturbances of cerebral protein synthesis and ischemic cell death. Prog. Brain Res. 96, 161-177.
22. Hu B. R., Martone M. E., Jones Y. Z. and Liu C. L. (2000) Protein aggregation after transient cerebral ischemia. J. Neurosci. 20, 3191-3199.
23. Hu B. R., Janelidze S., Ginsberg M. D., Busto R., Perez-Pinzon M., Sick T. J., Siesjo B. K. and Liu C. L. (2001) Protein aggregation after focal brain ischemia and reperfusion. J. Cereb. Blood Flow Metab. 21, 865-875.
24. Ito T., Warnken S. P. and May W. S. (1999) Protein synthesis inhibition by flavonoids; roles of eukaryotic initiation factor 2α kinases. Biochem. Biophys. Res. Commun. 265, 589-594.
25. Jiang H. Y., Wek S. A., McGrath B. C., Scheuner D., Kaufman R. J., Cavener D. R. and Wek R. C. (2003) Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-κB in response to diverse cellular stresses. Mol Cell Biol. 23, 5651-5663.
26. Kimata Y., Kimata Y. I., Shimizu Y., Abe H., Farcasanu I. C., Takeuchi M., Rose M. D. and Kohno K. (2003) Genetic evidence for a role of BiP/Kar2 that regulates Irel in response to accumulation of unfolded proteins. Mol. Biol. Cell. 14, 2559-2569.
27. Kleihues P. and Hossmann K. (1971) Protein synthesis in the cat brain after prolonged cerebral ischemia. Brain Res. 35, 409-418.
28. Koch G., Smith M., Macer D., Webster P. and Mortara R. (1986) Endoplasmic reticulum contains a common, abundant calcium-binding glycoprotein, endoplasmin. J. Cell Sci. 86, 217-232.
29. Kohno K., Higuchi T., Ohta S., Kohno K., Kumon Y. and Sakaki S. (1997) Neuroprotective nitric oxide synthase inhibitor reduces intracellular calcium accumulation following transient global ischemia in the gerbil. Neurosci. Lett. 224, 17-20.
30. Krause G. S. and Tiffany B. R. (1993) Suppression of protein synthesis in the reperfused brain. Stroke 24, 747-755.
31. Kumar R., Azam S., Sullivan J. M. et al. (2001) Brain ischemia and reperfusion activates the eukaryotic initiation factor 2α kinase, PERK. J. Neurochem. 77, 1418-1421.
32. Li Y., Iida K., O'Neil J. et al. (2003) PERK eIF2α kinase regulates neonatal growth by controlling the expression of circulating insulin-like growth factor-I derived from the liver. Endocrinology 144, 3505-3513.
33. 2+. J. Biol. Chem. 272, 30 873-30 879.
34. Lipton P. (1999) Ischemic cell death in brain neurons. Physiol. Rev. 79, 1431-1568.
35. Liu C. Y., Wong H. N., Schauerte J. A. and Kaufman R. J. (2002) The protein kinase/endoribonuclease IRE1α that signals the unfolded protein response has a luminal N-terminal ligand-independent dimerization domain. J. Biol. Chem. 277, 18 346-18 356.
36. Lu P. D., Jousse C., Marciniak S. J., Zhang Y., Novoa I., Scheuner D., Kaufman R. J., Ron D. and Harding H. P. (2004) Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J. 23, 169-179.
37. Ma K., Vattem K. M. and Wek R. C. (2002) Dimerization and release of molecular chaperone inhibition facilitate activation of eukaryotic initiation factor-2 (eIF2) kinase in response to endoplasmic reticulum stress. J. Biol. Chem. 277, 18 728-18 735.
38. Mengesdorf T., Proud C. G., Mies G. and Paschen W. (2002) Mechanisms underlying suppression of protein synthesis induced by transient focal cerebral ischemia in mouse brain. Exp. Neurol. 177, 538-546.
39. Murakami K., Kondo T., Kawase M. and Chan P. H. (1998) The development of a new mouse model of global ischemia: focus on the relationships between ischemia duration, anesthesia, cerebral vasculature, and neuronal injury following global ischemia in mice. Brain Res. 780, 304-310.
40. Murtha-Riel P., Davies M. V., Scherer B. J., Choi S. Y., Hershey J. W. and Kaufman R. J. (1993) Expression of a phosphorylation-resistant eukaryotic initiation factor 2α-subunit mitigates heat shock inhibition of protein synthesis. J. Biol. Chem. 268, 12 946-12 951.
41. Novoa I., Zhang Y., Zeng H., Jungreis R., Harding H. P. and Ron D. (2003) Stress-induced gene expression requires programmed recovery from translational repression. EMBO J. 22, 1180-1187.
42. Nowak T. S. Jr, Fried R. L., Lust D. and Passonneau J. V. (1985) Changes in brain energy metabolism and protein synthesis following transient bilateral ischemia in the gerbil. J. Neurochem. 44, 487-494.
43. Pain V. M. (1996) Initiation of protein synthesis in eukaryotic cells. Eur. J. Biochem. 236, 747-771.
44. Pal J. K., Chen J. J. and London I. M. (1991) Tissue distribution of heme-regulated eIF-2α kinase determined by monoclonal antibodies. Biochemistry 30, 2555-2562.
45. 2+ ATPase. J. Neurochem. 68, 1124-1134.
46. Paschen W. (2000) Role of calcium in neuronal cell injury: Which subcellular compartment is involved? Brain Res. Bull. 53, 409-413.
47. Paschen W. (2003a) Mechanisms of neuronal cell death: diverse roles of calcium in the various subcellular compartments. Cell Calcium 34, 305-310.
48. Paschen W. (2003b) Shutdown of translation: lethal or protective? Unfolded protein response versus apoptosis. J. Cereb. Blood Flow Metab. 23, 773-779.
49. Paschen W. and Doutheil J. (1999) Disturbances of the functioning of endoplasmic reticulum: a key mechanism underlying neuronal cell injury? J. Cereb. Blood Flow Metab. 19, 1-18.
50. Paschen W., Doutheil J., Gissel C. and Treiman M. (1996) Depletion of neuronal endoplasmic reticulum calcium stores by thapsigargin: effect on protein synthesis. J. Neurochem. 67, 1735-1743.
51. Shi Y., Vattem K. M., Sood R., An J., Liang J., Stramm L. and Wek R. C. (1998) Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol. Cell Biol. 18, 7499-7509.
52. Siesjo B. and Ljunggren B. (1973) Cerebral energy reserves after prolonged hypoxia and ischemia. Arch. Neurol. 29, 400-407.
53. Srivastava S. P., Kumar K. U. and Kaufman R. J. (1998) Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J. Biol. Chem. 273, 2416-2423.
54. Stewart M. L., Grollman A. P. and Huang M. T. (1971) Aurintricarboxylic acid: Inhibitor of initiation of protein synthesis. Proc. Natl Acad. Sci. USA 68, 97-101.
55. Sullivan J. M., Alousi S. S., Hikade K. R., Rafols J. A., Krause G. S. and White B. C. (1999) Insulin induces dephosphorylation of eIF2α and restores protein synthesis in vulnerable hippocampal neurons following transient brain ischemia. J. Cereb. Blood Flow Metab. 19, 1010-1019.
56. 2+)-dependent association with GRP78. J. Cell Biol. 114, 189-205.
57. Thilmann R., Xie Y., Kleihues P. and Kiessling M. (1986) Persistent inhibition of protein synthesis precedes delayed neuronal death in postischemic gerbil hippocampus. Acta Neuropathol (Berl.) 71, 88-93.
58. Van P. N., Peter F. and Soling H. D. (1989) Four intracistemal calcium-binding glycoproteins from rat liver microsomes with high affinity for calcium. No indication for calsequestrin-like proteins in inositol 1,4,5-trisphosphate-sensitive calcium sequestering rat liver vesicles. J. Biol. Chem. 264, 17 494-17 501.
59. White B. C., Sullivan J. M., DeGracia D. J., O'Neil B. J., Neumar R. W., Grossman L. I., Rafols J. A. and Krause G. S. (2000) Brain ischemia and reperfusion: Molecular mechanisms of neuronal injury. J. Neurol. Sci. 179, 1-33.
60. Xie Y., Seo K. and Hossmann K. A. (1989) Effect of barbiturate treatment on post-ischemic protein biosynthesis in gerbil brain. J. Neurol. Sci. 92, 317-328.
61. Zhang P., McGrath B., Li S., Frank A., Zambito F., Reinert J., Gannon M., Ma K., McNaughton K. and Cavener D. R. (2002) The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol. Cell Biol. 22, 3864-3874.