Cerebral ischemia and the unfolded protein response

Journal of Neurochemistry

Volumn 91, Issue 1, 2004, Pages 1-8

  DeGracia, Donald J ^a   Montie, Heather L ^a  

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

Author keywords

Brain ischemia and brain reperfusion; CHOP; IRE1; PERK; Protein synthesis inhibition; Unfolded protein response

Indexed keywords

APOPTOSIS; BRAIN ISCHEMIA; ENDOPLASMIC RETICULUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INDUCTION; PROTEIN SYNTHESIS INHIBITION; REPERFUSION; REVIEW; STRESS; UPREGULATION;

ANIMALS; BRAIN ISCHEMIA; DNA-BINDING PROTEINS; EIF-2 KINASE; ENDOPLASMIC RETICULUM; HUMANS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; PHOSPHORYLATION; PROTEIN FOLDING; REPERFUSION INJURY; TRANSCRIPTION FACTORS;

EID: 4744344331     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02703.x     Document Type: Review

References (62)

1. Althausen S., Mengesdorf T., Mies G., Olah L., Naim 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. Bertolotti A., Zhang Y., Hendershot L. M., Harding H. P. and Ron D. (2000) Dynamic interaction of GRP78 and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2, 326-332.
3. Brodsky J. L. and McCracken A. A. (1999) ER protein quality control and proteasome-mediated protein degradation. Semin. Cell Dev. Biol. 10, 507-513.
4. Brostrom C. O. and Brostrom M. A. (1998) Regulation of translational initiation during cellular responses to stress. Prog. Nucleic Acid Res. Mol. Biol. 58, 79-125.
5. Calfon M., Zeng H., Urano F., Till J. H., Hubbard S. R., Harding H. P., Clark S. G. and Ron D. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96.
6. 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.
7. 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.
8. DeGracia D. J., Kumar R., Owen C., Krause G. S. and White B. C. (2002) Molecular pathways of protein synthesis inhibition during brain reperfusion: implications for neuronal survival or death. J. Cereb. Blood Flow Metab. 22, 127-141.
9. Dever T. E., Yang W., Astrom S., Bystrom A. S. and Hinnebusch A. G. (1995) Modulation of tRNAiMet, eIF-2, and eIF-2B expression shows that GCN4 translation is inversely coupled to the levels of eIF-2-GTP-Met-tRNAiMet temary complexes. Mol. Cell Biol. 15, 6351-6363.
10. Doutheil J., Althausen S., Gissel C. and Paschen W. (1999) Activation of MYD116 (gadd34) expression following transient forebrain ischemia of rat: implications for a role of disturbances of endoplasmic reticulum calcium homeostasis. Brain Res. Mol. Brain Res. 63, 225-232.
11. Doutheil J., Althausen S., Treiman M. and Paschen W. (2000) Effect of nitric oxide on endoplasmic reticulum calcium homeostasis, protein synthesis and energy metabolism. Cell Calcium 27, 107-115.
12. Garcia L., Burda J., Hrehorovska M., Burda R., Martin M. E. and Salinas M. (2004) Ischaemic preconditioning in the rat brain: effect on the activity of several initiation factors, Akt and extracellular signal-regulated protein kinase phosphorylation, and GRP78 and GADD34 expression. J. Neurochem. 88, 136-147.
13. Gonzalez T. N., Sidrauski C., Dorfler S. and Walter P. (1999) Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway. EMBO J. 18, 3119-3132.
14. Harding H., I. Novoa Y., Zhang H., Zeng M., Schapira and D. Ron. (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell. 6, 1099-1108.
15. Harding H. P., Calfon M., Urano F., Novoa I. and Ron D. (2002) Transcriptional and translational control in the mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18, 575-599.
16. Hayashi T., Saito A., Okuno S., Ferrand-Drake M., Dodd R. L., Nishi T., Maier C. M., Kinouchi H. and Chan P. H. (2003) Oxidative damage to the endoplasmic reticulum is implicated in ischemic neuronal cell death. J. Cereb. Blood Flow Metab. 23, 1117-1128.
17. Hayashi T., Saito A., Okuno S., Ferrand-Drake M., Dodd R. L. and Chan P. H. (2004) Oxidative injury to the endoplasmic reticulum in mouse brains after transient focal ischemia. Neurobiol. Dis. 15, 229-239.
18. Haze K., Yoshida H., Yanagi H., Yura T. and Mori K. (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell. 10, 3787-3799.
19. Hossmann K. A. (1993) Disturbances of cerebral protein synthesis and ischemic cell death. Prog. Brain Res. 96, 161-177.
20. 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.
21. 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.
22. Imai H., Harland J., McCulloch J., Graham D. I., Brown S. M. and Macrae I. M. (2002) Specific expression of the cell cycle regulation proteins, GADD34 and PCNA, in the peri-infarct zone after focal cerebral ischaemia in the rat. Eur. J. Neurosci. 2002, 1929-1936.
23. Jin K., Mao X. O., Eshoo M. W., Nagayama T., Minami M., Simon R. P. and Greenberg D. A. (2001) Microarray analysis of hippocampal gene expression in global cerebral ischemia. Ann. Neurol. 50, 93-103.
24. Kaufman R. J. (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13, 1211-1233.
25. Kim S. W., Park S., You K. H. and Kwon O. Y. (2003) Expression of the endoplasmic reticulum chaperone GRP94 gene in ischemic gerbil brain. Z. Naturforsch. [C]. 58, 736-739.
26. Kim Y. M., Son K., Hong S. J., Green A., Chen J. J., Tzeng E., Hierholzer C. and Billiar T. R. (1998) Inhibition of protein synthesis by nitric oxide correlates with cytostatic activity: nitric oxide induces phosphorylation of initiation factor eIF-2α. Mol. Med. 4, 179-190.
27. Kleihues P. and Hossmann K. (1971) Protein synthesis in the cat brain after prolonged cerebral ischemia. Brain Res. 35, 409-418.
28. 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.
29. Kumar R., Azam S., Sullivan J. M. et al. (2001) Brain ischemia and reperfusion activates the eukaryotic initiation factor 2alpha kinase, PERK. J. Neurochem. 77, 1418-1421.
30. Kumar R., Krause G. S., Yoshida H., Mori K. and DeGracia D. J. (2003) Dysfunction of the unfolded protein response during global brain ischemia and reperfusion. J. Cereb. Blood Flow Metab. 23, 462-471.
31. Lee A. H., Iwakoshi N. N. and Glimcher L. H. (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23, 7448-7459.
32. Lee K., Tirasophon W., Shen X., Michalak M., Prywes R., Okada T., Yoshida H., Mori K. and Kaufman R. J. (2002) IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Devel. 16, 452-466.
33. Ma Y., Brewer J. W., Diehl J. A. and Hendershot L. M. (2002) Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318, 1351-1365.
34. McCullough K. D., Martindale J. L., Klotz L. O., Aw T. Y. and Holbrook N. J. (2001) GADD153 sensitizes cells to endoplasmic reticulum stress by downregulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 21, 1249-1259.
35. Martin de la Vega C., Burda J., Nemethova M., Quevedo C., Alcazar A., Martin M. E., Danielisova V., Fando J. L. and Salinas M. (2001) Possible mechanisms involved in the downregulation of translation during transient global ischaemia in the rat brain. Biochem. J. 357, 819-826.
36. 2+-ATPase: relationship between global protein synthesis and expression and translation of individual genes. Biochem. J. 356, 805-812.
37. 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.
38. Mouw G., Zechel J. L., Gamboa J., Lust W. D., Selman W. R. and Ratcheson R. A. (2003) Activation of caspase-12, an endoplasmic reticulum resident caspase, after permanent focal ischemia in rat. Neuroreport. 14, 183-186.
39. Novoa I., Zeng H., Handing H. P. and Ron D. (2001) Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol. 28, 1011-1022.
40. Okada T., Yoshida H., Akazawa R., Negishi M. and Mori K. (2002) Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem. J. 366, 585-594.
41. Oyadomari S. and Mori M. (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11, 381-389.
42. 2+ ATPase. J. Neurochem. 68, 1124-1134.
43. 2+ ATPase. Brain Res. 834, 32-41.
44. Paschen W. (1996) Disturbances of calcium homeostasis within the endoplasmic reticulum may contribute to the development of ischemic-cell damage. Med. Hypotheses 47, 283-288.
45. Paschen W. (2003) Shutdown of translation: lethal or protective? unfolded protein response versus apoptosis. J. Cereb. Blood Flow Metab. 23, 773-779.
46. Paschen W., Gissel C., Linden T., Althausen S. and Doutheil J. (1998) Activation of gadd153 expression through transient cerebral ischemia: evidence that ischemia causes endoplasmic reticulum dysfunction. Brain Res. Mol. Brain Res. 60, 115-122.
47. Paschen W., Mengesdorf T., Althausen S. and Hotop S. (2001) Peroxidative stress selectively downregulates the neuronal stress response activated under conditions of endoplasmic reticulum dysfunction. J. Neurochem. 76, 1916-1924.
48. Paschen W., Aufenberg C., Hotop S. and Mengesdorf T. (2003) Transient cerebral ischemia activates processing of xbp1 messenger RNA indicative of endoplasmic reticulum stress. J. Cereb. Blood Flow Metab. 23, 449-461.
49. Petito C. K. and Pulsinelli W. A. (1984) Delayed neuronal recovery and neuronal death in rat hippocampus following severe cerebral ischemia: possible relationship to abnormalities in neuronal processes. J. Cereb. Blood Flow Metab. 4, 194-205.
50. Ron D. and Harding H. P. (2000) PERK and translational control by stress in the endoplasmic reticulum. In: Translational Control. of Gene Expression (Sonenberg N., Hershey J. W. B., Mathews M. B., eds), pp. 547-560. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
51. Roy B. and Lee A. S. (1999) The mammalian endoplasmic reticulum stress response element consists of an evolutionarily conserved tripartite structure and interacts with a novel stress-inducible complex. Nucleic Acids Res. 27, 1437-1443.
52. Schmidt-Kastner R., Zhang B., Belayev L., Khoutorova L., Amin R., Busto R. and Ginsberg M. D. (2002) DNA microarray analysis of cortical gene expression during early recirculation after focal brain ischemia in rat. Brain Res. Mol. Brain Res. 108, 81-93.
53. Shen J., Chen X., Hendershot L. and Prywes R. (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell. 3, 99-111.
54. Shibata M., Hattori H., Sasaki T., Gotoh J., Hamada J. and Fukuuchi Y. (2003) Activation of caspase-12 by endoplasmic reticulum stress induced by transient middle cerebral artery occlusion in mice. Neuroscience. 118, 491-499.
55. Tajiri S., Oyadomari S., Yano S., Morioka M., Gotoh T., Hamada J. I., Ushio Y. and Mori M. (2004) Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death Differ. (advanced online publication).
56. Ubeda M., Vallejo M. and Habener J. F. (1999) CHOP enhancement of gene transcription by interactions with Jun/Fos AP-1 complex proteins. Mol. Cell. Biol. 19, 7589-7599.
57. White B. C., Daya A., DeGracia D. J., O'Neil B. J., Skjaerlund J. M., Trumble S., Krause G. S. and Rafols J. A. (1993) Fluorescent histochemical localization of lipid peroxidation during brain reperfusion following cardiac arrest. Acta. Neuropathol. 86, 1-9.
58. 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.
59. Yoneda T., Imaizumi K., Oono K., Yui D., Gomi F., Katayama T. and Tohyama M. (2001) Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J. Biol. Chem. 27, 13935-13940.
60. Yoshida H., Matsui T., Yamamoto A., Okada T. and Mori K. (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891.
61. Yoshida H., Matsui T., Hosokawa N., Kaufman R. J., Nagata K. and Mori K. (2003) A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell. 4, 265-271.
62. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R. T., Remotti H., Stevens J. L. and Ron D. (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12, 982-995.