Crosstalk Between Endoplasmic Reticulum Stress, Oxidative Stress, and Autophagy: Potential Therapeutic Targets for Acute CNS Injuries

Molecular Neurobiology

Volumn 53, Issue 1, 2016, Pages 532-544

  Nakka, Venkata Prasuja ^a,b   Prakash babu, Phanithi ^b   Vemuganti, Raghu ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF HYDERABAD   (India)

Author keywords

Acute CNS injury; Autophagy; Crosstalk; ER stress; Oxidative stress

Indexed keywords

2 [[4 [2,6 BIS(1 PYRROLIDINYL) 4 PYRIMIDINYL] 1 PIPERAZINYL]METHYL] 3,4 DIHYDRO 2,5,7,8 TETRAMETHYL 2H 1 BENZOPYRAN 6 OL; 4 PHENYLBUTYRIC ACID; 7 CHLORO 3 IMINO 5 METHYL 2 AZABICYCLO[4.1.0]HEPTANE; ACTIVATING TRANSCRIPTION FACTOR 6; APOCYNIN; BINDING IMMUNOGLOBULIN PROTEIN INDUCER X; CARNOSIC ACID; CURCUMIN; DOCOSAHEXAENOIC ACID; FUSED HETEROCYCLIC RINGS; HYDROQUINONE DERIVATIVE; MELATONIN; N(G) METHYLARGININE; N(G) NITROARGININE METHYL ESTER; NEUROPROTECTIVE AGENT; NITRIC OXIDE SYNTHASE INHIBITOR; NITRO LEVO ARGININE; NORPHENAZONE; OPC 14177; PANCREATIC ENDOPLASMIC RETICULUM KINASE; PROTEIN IRE1; PROTEIN KINASE R; RESVERATROL; SALUBRINAL; SULFORAPHANE; TAUROURSODEOXYCHOLIC ACID; TERTBUTYLHYDROQUINONE; THIOCTIC ACID; TRITERPENOID; UNCLASSIFIED DRUG;

AUTOPHAGY; BRAIN HYPOXIA; BRAIN INJURY; BRAIN ISCHEMIA; CELL NUCLEUS; CELL STRESS; CEREBROVASCULAR ACCIDENT; CYTOSOL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG TARGETING; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMAN; MOLECULAR INTERACTION; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PROTEIN FOLDING; REVIEW; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; SUBARACHNOID HEMORRHAGE; TRAUMATIC BRAIN INJURY; UNFOLDED PROTEIN RESPONSE; ANIMAL; CENTRAL NERVOUS SYSTEM DISEASES; DRUG DELIVERY SYSTEM; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; TRENDS;

ANIMALS; AUTOPHAGY; CENTRAL NERVOUS SYSTEM DISEASES; DRUG DELIVERY SYSTEMS; ENDOPLASMIC RETICULUM STRESS; HUMANS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 84953347508     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-014-9029-6     Document Type: Review

References (161)

1. Kaufman RJ (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13:1211–1233
2. Paschen W, 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
3. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404:770–774
4. Lai E, Teodoro T, Volchuk A (2007) Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology 22:193–201
5. Kaufman RJ (2002) Orchestrating the unfolded protein response in health and disease. J Clin Invest 110:1389–1398
6. Hu BR, Martone ME, Yones YZ, Liu CL (2000) Protein aggregation after transient cerebral ischemia. J Neurosci 20:3191–3199
7. Xu C, Bailly-Maitre B, Reed JC (2005) Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 115:2656–2664
8. Viner RI, Ferrington DA, Williams TD, Bigelow DJ, Schoneich C (1999) Protein modification during biological aging: selective tyrosine nitration of the SERCA2a isoform of the sarcoplasmic reticulum Ca2+-ATPase in skeletal muscle. Biochem J 340:657–669
9. Gotoh T, Mori M (2006) Nitric oxide and endoplasmic reticulum stress. Arterioscler Thromb Vasc Biol 26:1439–1446
10. Høyer-Hansen M, Jäättelä M (2007) Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 14:1576–1582
11. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519–529
12. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2:326–332
13. Kumar R, Azam S, Sullivan JM, Owen C, Cavener DR, Zhang P, Ron D, Harding HP, Chen JJ, Han A, White BC, Krause GS, DeGracia DJ (2001) Brain ischemia and reperfusion activates the eukaryotic initiation factor 2alpha kinase, PERK. J Neurochem 77:1418–1421
14. Prostko CR, Brostrom MA, Brostrom CO (1993) Reversible phosphorylation of eukaryotic initiation factor 2 alpha in response to endoplasmic reticular signaling. Mol Cell Biochem 128:255–265
15. Ron D (2002) Translational control in the endoplasmic reticulum stress response. J Clin Invest 110:1383–1388
16. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5:897–904
17. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM, Ron D (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11:619–633
18. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, Nagata K, Harding HP, Ron D (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 18:3066–3077
19. Hamanaka RB, Bennett BS, Cullinan SB, Alan Diehl J (2005) PERK and GCN2 contribute to eIF2α phosphorylation and cell cycle arrest after activation of the unfolded protein response pathway. Mol Biol Cell 16:5493–5501
20. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, Kaufman RJ, Ma D, Coen DM, Ron D, Yuan J (2005) A selective inhibitor of eIF2a dephosphorylation protects cells from ER stress. Science 307:935–939
21. Sokka AL, Putkonen N, Mudo G, Pryazhnikov E, Reijonen S, Khiroug L, Belluardo N, Lindholm D, Korhonen L (2007) Endoplasmic reticulum stress inhibition protects against excitotoxic neuronal injury in the rat brain. J Neurosci 27:901–908
22. Nakka VP, Gusain A, Raghubir R (2010) Endoplasmic reticulum stress plays critical role in brain damage after cerebral ischemia/reperfusion in rats. Neurotox Res 17:189–202
23. Gorman AM, Healy SJ, Jäger R, Samali A (2012) Stress management at the ER: regulators of ER stress-induced apoptosis. Pharmacol Ther 134:306–316
24. Hetz C, Mollereau B (2014) Disturbance of endoplasmic reticulum proteostasis in neurodegenerative diseases. Nat Rev Neurosci 15:233–249
25. Kim I, Xu W, Reed JC (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7:1013–1030
26. Calfon M, Zeng H, Urano F, Till JH, Hubbart SR, Harding HP, Clark SG, Ron D (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing XBP-1 mRNA. Nature 415:92–96
27. Lee AH, Iwakoshi NN, Glimcher LH (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23:7448–7459
28. Paschen W, Aufenberg C, Hotop S, 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
29. Tajiri S, Oyadomari S, Yano S, Morioka M, Gotoh T, Hamada JI, Ushio Y, Mori M (2004) Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death Differ 11:403–415
30. Han D, Lerner AG, Vande Walle L, Upton JP, Xu W, Hagen A, Backes BJ, Oakes SA, Papa FR (2009) IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138:562–575
31. Hollien J, Weissman JS (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313:104–107
32. Lerner AG, Upton JP, Praveen PV, Ghosh R, Nakagawa Y, Igbaria A, Shen S, Nguyen V, Backes BJ, Heiman M et al (2012) IRE1a induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab 16:250–264
33. Upton JP, Wang L, Han D, Wang ES, Huskey NE, Lim L, Truitt M, McManus MT, Ruggero D, Goga A et al (2012) IRE1a cleaves select microRNAs during ER stress to derepress translation of proapoptotic caspase-2. Science 338:818–822
34. Ghosh R, Wang L, Wang ES, Perera BG, Igbaria A, Morita S, Prado K, Thamsen M, Caswell D, Macias H et al (2014) Allosteric inhibition of the IRE1α RNase preserves cell viability and function during endoplasmic reticulum stress. Cell 158:534–548
35. Shibata M, Hattori H, Sasaki T, Gotoh J, Hamada J, Fukuuchi Y (2003) Activation of caspase-12 by endoplasmic reticulum stress induced by transient middle cerebral artery occlusion in mice. Neuroscience 118:491–499
36. Mouw G, Zechel JL, Gamboa J, Lust WD, Selman WR, Ratcheson RA (2003) Activation of caspase-12, an endoplasmic reticulum resident caspase, after permanent focal ischemia in rat. Neuroreport 14:183–186
37. Larner SF, Hayes RL, McKinsey DM, Pike BR, Wang KK (2004) Increased expression and processing of caspase-12 after traumatic brain injury in rats. J Neurochem 88:78–90
38. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J (2000) Caspase-12 mediates endoplasmic-reticulum specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98–103
39. Rao RV, Castro-Obregon S, Frankowski H, Schuler M, Stoka V, del Rio G, Bredesen DE, Ellerby HM (2002) Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J Biol Chem 277:21836–21842
40. Aoyama K, Burns DM, Suh SW, Garnier P, Matsumori Y, Shiina H, Swanson RA (2005) Acidosis causes endoplasmic reticulum stress and caspase-12-mediated astrocyte death. J Cereb Blood Flow Metab 25:358–370
41. Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, 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 276:13935–13940
42. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664–666
43. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, Hori S, Kakizuka A, Ichijo H (2002) ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 16:1345–1355
44. Nishitoh H, Saitoh M, Mochida Y, Takeda K, Nakano H, Rothe M, Miyazono K, Ichijo H (1998) ASK1 is essential for JNK/SAPK activation by TRAF2. Mol Cell 2:389–395
45. Borsello T, Clarke PG, Hirt L, Vercelli A, Repici M, Schorderet DF, Bogousslavsky J, Bonny C (2003) A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat Med 9:1180–1186
46. Gao Y, Signore AP, Yin W, Cao G, Yin X, Sun F, Luo Y, Graham SH, Chen J (2005) Neuroprotection against focal ischemic brain injury by inhibition of c-Jun N-terminal kinase and attenuation of the mitochondrial apoptosis-signaling pathway. J Cereb Blood Flow Metab 25:694–712
47. Haze K, Yoshida H, Yanagi H, Yura T, 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
48. Wu J, Rutkowski DT, Dubois M, Swathirajan J, Saunders T, Wang J, Song B, Yau GD, Kaufman RJ (2007) ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell 13:351–364
49. Egawa N, Yamamoto K, Inoue H, Hikawa R, Nishi K, Mori K, Takahashi R (2011) The endoplasmic reticulum stress sensor, ATF6α, protects against neurotoxin-induced dopaminergic neuronal death. J Biol Chem 286:7947–7957
50. Moroa MA, Almeida A, Bolanos JP, Lizasoain I (2005) Mitochondrial respiratory chain and free radical generation in stroke. Free Radic Biol Med 39:1291–1304
51. Chong ZZ, Li F, Maiese K (2005) Oxidative stress in the brain: novel cellular targets that govern survival during neurodegenerative disease. Prog Neurobiol 75:207–246
52. Anderson JK (2004) Oxidative stress in neurodegeneration: a cause or consequence? Nat Rev Neurosci 5:S18–S25
53. Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245–313
54. Murphy AN, Fiskum G, Beal MF (1999) Mitochondria in neurodegeneration: bioenergetic function in cell life and death. J Cereb Blood Flow Metab 19:231–245
55. Brennan AM, Suh SW, Won SJ, Narasimhan P, Kauppinen TM, Lee H, Edling Y, Chan PH, Swanson RA (2009) NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat Neurosci 12:857–863
56. Kahles T, Brandes RP (2012) NADPH oxidases as therapeutic targets in ischemic stroke. Cell Mol Life Sci 69:2345–2363
57. Wei H, Kim SJ, Zhang Z, Tsai PC, Wisniewski KE, Mukherjee AB (2008) ER and oxidative stresses are common mediators of apoptosis in both neurodegenerative and non-neurodegenerative lysosomal storage disorders and are alleviated by chemical chaperones. Hum Mol Genet 17:469–477
58. Martínez JA (2006) Mitochondrial oxidative stress and inflammation: an slalom to obesity and insulin resistance. J Physiol Biochem 62:303–306
59. Kregel KC, Zhang HJ (2007) An integrated view of oxidative stress in aging: basic mechanisms, functional effects, and pathological considerations. Am J Physiol Regul Integr Comp Physiol 292:R18–R36
60. Li G, Scull C, Ozcan L, Tabas I (2010) NADPH oxidase links endoplasmic reticulum stress, oxidative stress, and PKR activation to induce apoptosis. J Cell Biol 191:1113–1125
61. Malhotra JD, Kaufman RJ (2007) Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 9:2277–2294
62. Gorrini C, Harris IS, Mak TW (2013) Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discov 12:931–947
63. Cullinan SB, Zhang D, Hannink M, Arvisais E, Kaufman RJ, Diehl JA (2003) Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol 23:7198–7209
64. He CH, Gong P, Hu B, Stewart D, Choi ME, Choi AM, Alam J (2001) Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation. J Biol Chem 276:20858–20865
65. Zhao L, Ackerman SL (2006) Endoplasmic reticulum stress in health and disease. Curr Opin Cell Biol 18:444–452
66. Li G, Mongillo M, Chin KT, Harding H, Ron D, Marks AR, Tabas I (2009) Role of ERO1-α-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. J Cell Biol 186:783–792
67. Gorlach A, Klappa P, Kietzmann T (2006) The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid Redox Signal 8:1391–1418
68. Jacobson J, Duchen MR (2002) Mitochondrial oxidative stress and cell death in astrocytes—requirement for stored Ca2+ and sustained opening of the permeability transition pore. J Cell Sci 115:1175–1188
69. Boehning D, Patterson RL, Sedaghat L, Glebova NO, Kurosaki T, Snyder SH (2003) Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat Cell Biol 5:1051–1061
70. Bhandary B, Marahatta A, Kim HR, Chae HJ (2012) An involvement of oxidative stress in endoplasmic reticulum stress and its associated diseases. Int J Mol Sci 14:434–456
71. Cooper LL, Li W, Lu Y, Centracchio J, Terentyeva R, Koren G, Terentyev D (2013) Redox modification of ryanodine receptors by mitochondria-derived reactive oxygen species contributes to aberrant Ca2+ handling in ageing rabbit hearts. J Physiol 591:5895–5911
72. Berridge MJ (2002) The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32:235–249
73. Ruiz A, Matute C, Alberdi E (2009) Endoplasmic reticulum Ca(2+) release through ryanodine and IP (3) receptors contributes to neuronal excitotoxicity. Cell Calcium 46:273–281
74. Lipton SA, Rosenberg PA (1994) Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 330:613–622
75. Choi DW (1998) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623–634
76. Ruiz A, Matute C, Alberdi E (2010) Intracellular Ca2+ release through ryanodine receptors contributes to AMPA receptor-mediated mitochondrial dysfunction and ER stress in oligodendrocytes. Cell Death Dis 15(1):e54
77. Horbinski C, Chu CT (2005) Kinase signaling cascades in the mitochondrion: a matter of life or death. Free Radic Biol Med 38:2–11
78. Nakka VP, Gusain A, Mehta SL, Raghubir R (2008) Molecular mechanisms of apoptosis in cerebral ischemia: multiple neuroprotective opportunities. Mol Neurobiol 37:7–38
79. Ouyang YB, Tan Y, Comb M, Liu CL, Martone ME, Siesjo BK, Hu BR (1999) Survival and death-promoting events after transient cerebral ischemia: phosphorylation of Akt, release of cytochrome C, and activation of caspase-like proteases. J Cereb Blood Flow Metab 19:1126–1135
80. Fujimura M, Morita-Fujimura Y, Murakami K, Kawase M, Chan PH (1998) Cytosolic distribution of cytochrome c after transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab 8:1239–1247
81. Perez-Pinzon MA, Xu GP, Born J, Lorenzo J, Busto R, Rosenthal M, Sick TJ (1999) Cytochrome C is released from mitochondria into the cytosol after cerebral anoxia or ischemia. J Cereb Blood Flow Metab 19:39–43
82. Cao G, Minami M, Pei W, Yan C, Chen D, O’Horo C, Graham SH, Chen J (2001) Intracellular Bax translocation after transient cerebral ischemia: implications for a role of the mitochondrial apoptotic signaling pathway in ischemic neuronal death. J Cereb Blood Flow Metab 21:321–333
83. Sugawara T, Fujimura M, Morita-Fujimura Y, Kawase M, Chan PH (1999) Mitochondrial release of cytochrome c corresponds to the selective vulnerability of hippocampal CA1 neurons in rats after transient forebrain ischemia. J Neurosci 19:RC39
84. Vosler PS, Graham SH, Wechsler LR, Chen J (2009) Mitochondrial targets for stroke: focusing basic science research toward development of clinically translatable therapeutics. Stroke 40:3149–3155
85. Gogvadze V, Orrenius S, Zhivotovsky B (2006) Multiple pathways of cytochrome c release from mitochondria in apoptosis. Biochim Biophys Acta 1757:639–647
86. Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9:47–59
87. Ferrer I, Planas AM (2003) Signaling of cell death and cell survival following focal cerebral ischemia: life and death struggle in the penumbra. J Neuropathol Exp Neurol 62:329–339
88. Szegezdi E, Logue SE, Gorman AM, Samali A (2006) Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 7:880–885
89. Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA, Pozzan T (1998) Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280:1763–1766
90. Gupta S, Cuffe L, Szegezdi E, Logue SE, Neary C, Healy S, Samali A (2010) Mechanisms of ER stress-mediated mitochondrial membrane permeabilization. Int J Cell Biol 2010:170215
91. Klee M, Pallauf K, Alcalá S, Fleischer A, Pimentel-Muiños FX (2009) Mitochondrial apoptosis induced by BH3-only molecules in the exclusive presence of endoplasmic reticular Bak. EMBO J 28:1757–1768
92. Mengesdorf T, Proud CG, Mies G, Paschen W (2002) Mechanisms underlying suppression of protein synthesis induced by transient focal cerebral ischemia in mouse brain. Exp Neurol 177:538–546
93. Owen CR, Kumar R, Zhang P, McGrath BC, Cavener DR, Krause GS (2005) PERK is responsible for the increased phosphorylation of eIF2alpha and the severe inhibition of protein synthesis after transient global brain ischemia. J Neurochem 94:1235–1242
94. Beresewicz M, Kowalczyk JE, Zablocka B (2006) Cytochrome c binds to inositol (1,4,5) trisphosphate and ryanodine receptors in vivo after transient brain ischemia in gerbils. Neurochem Int 48:568–571
95. Hacki J, Egger L, Monney L, Conus S, Rosse T, Fellay I, Borner C (2000) Apoptotic crosstalk between the endoplasmic reticulum and mitochondria controlled by Bcl-2. Oncogene 19:2286–2295
96. Sanges D, Marigo V (2006) Cross-talk between two apoptotic pathways activated by endoplasmic reticulum stress: differential contribution of caspase-12 and AIF. Apoptosis 11:1629–1641
97. Yorimitsu T, Nair U, Yang Z, Klionsky DJ (2006) Endoplasmic reticulum stress triggers autophagy. J Biol Chem 281:30299–30304
98. Kolattukudy PE, Niu J (2012) Inflammation, endoplasmic reticulum stress, autophagy, and the monocyte chemoattractant protein-1/CCR2 pathway. Circ Res 6(110):174–189
99. Harraz MM, Dawson TM, Dawson VL (2008) Advances in neuronal cell death. Stroke 39:286–288
100. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, Shiosaka S, Hammarback JA, Urano F, Imaizumi K (2006) Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26:9220–9231
101. Boland B, Nixon RA (2006) Neuronal macroautophagy: from development to degeneration. Mol Aspects Med 27:503–519
102. Rami A, Kogel D (2008) Apoptosis meets autophagy-like cell death in the ischemic penumbra: two sides of the same coin? Autophagy 4:422–426
103. Semenza GL (2008) Mitochondrial autophagy: life and breath of the cell. Autophagy 4:534–536
104. Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, Ron D, Yin XM (2007) Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 171:513–524
105. Xilouri M, Stefanis L (2010) Autophagy in the central nervous system: implications for neurodegenerative disorders. CNS Neurol Disord Drug Targets 9:701–719
106. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S, Kawahara N, Kuida K, Nagata S, Kominami E, Tanaka K, Uchiyama Y (2008) Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 172:454–469
107. Wen YD, Sheng R, Zhang LS, Han R, Zhang X, Zhang XD, Han F, Fukunaga K, Qin ZH (2008) Neuronal injury in rat model of permanent focal cerebral ischemia is associated with activation of autophagic and lysosomal pathways. Autophagy 4:762–769
108. Sheng R, Zhang LS, Han R, Liu XQ, Gao B, Qin ZH (2010) Autophagy activation is associated with neuroprotection in a rat model of focal cerebral ischemic preconditioning. Autophagy 6:482–494
109. Adhami F, Schloemer A, Kuan C (2007) The roles of autophagy in cerebral ischemia. Autophagy 3:42–44
110. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, Ogawa S, Kaufman RJ, Kominami E, Momoi T (2007) ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 14:230–239
111. Fujita E, Kouroku Y, Isoai A, Kumagai H, Mizutani A, Matsuda C et al (2007) Two endoplasmic reticulum-associated degradation systems (ERAD) for the novel variant of the mutant dysferlin; ubiquitin/proteasome ERAD(I) and autophagy/lysosome ERAD(II). Hum Mol Genet 16:618–629
112. Vidal RL, Figueroa A, Court FA, Thielen P et al (2012) Targeting the UPR transcription factor XBP1 protects against Huntington’s disease through the regulation of FoxO1 and autophagy. Mol Genet 21:2245–2262
113. Hetz C, Thielen P, Matus S et al (2009) XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy. Genes Dev 23:2294–2306
114. Gao B, Zhang XY, Han R, Zhang TT, Chen C, Qin ZH, Sheng R (2013) The endoplasmic reticulum stress inhibitor salubrinal inhibits the activation of autophagy and neuroprotection induced by brain ischemic preconditioning. Acta Pharmacol Sin 34:657–666
115. Szydlowska K, Tymianskia M (2010) Calcium, ischemia and excitotoxicity. Cell Calcium 47:122–129
116. Tabas I (2010) The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ Res 107:839–850
117. DeGracia DJ, Kumar R, Owen CR, Krause GS, White BC (2002) Molecular pathways of protein synthesis inhibition during brain reperfusion: implications for neuronal survival or death. J Cereb Blood Flow Metab 22:127–141
118. Paschen W, Gissel C, Linden T, Althausen S, 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
119. Niizuma K, Endo H, Nito C, Myer DJ, Chan PH (2009) Potential role of PUMA in delayed death of hippocampal CA1 neurons after transient global cerebral ischemia. Stroke 40:618–625
120. Ness JM, Harvey CA, Strasser A, Bouillet P, Klocke BJ, Roth KA (2006) Selective involvement of BH3-only Bcl-2 family members Bim and Bad in neonatal hypoxia-ischemia. Brain Res 1099:150–159
121. Chan PH (2001) Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab 21:2–14
122. Cherubini A, Ruggiero C, Polidori MC, Mecocci P (2005) Potential markers of oxidative stress in stroke. Free Radic Biol Med 39:841–852
123. Hayashi T, Saito A, Okuno S, Ferrand-Drake M, Dodd RL, Chan PK (2005) Damage to the endoplasmic reticulum and activation of apoptotic machinery by oxidative stress in ischemic neurons. J Cereb Blood Flow Metab 25:41–53
124. Santos CX, Tanaka LY, Wosniak J, Laurindo FR (2009) Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid Redox Signal 11:2409–2427
125. Lehotský J, Urban P, Pavlíková M, Tatarková Z, Kaminska B, Kaplán P (2009) Molecular mechanisms leading to neuroprotection/ischemic tolerance: effect of preconditioning on the stress reaction of endoplasmic reticulum. Cell Mol Neurobiol 29:917–925
126. Roussel BD, Kruppa AJ, Miranda E, Crowther DC, Lomas DA, Marciniak SJ (2013) Endoplasmic reticulum dysfunction in neurological disease. Lancet Neurol 12:105–118
127. Lange PS, Chavez JC, Pinto JT, Coppola G, Sun CW, Townes TM, Geschwind DH, Ratan RR (2007) ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J Exp Med 205:1227–1242
128. Srinivasan K, Sharma SS (2011) Sodium phenylbutyrate ameliorates focal cerebral ischemic/reperfusion injury associated with comorbid type 2 diabetes by reducing endoplasmic reticulum stress and DNA fragmentation. Behav Brain Res 225:110–116
129. Yao C, Zhang J, Liu G, Chen F, Lin Y (2014) Neuroprotection by (−)-epigallocatechin-3-gallate in a rat model of stroke is mediated through inhibition of endoplasmic reticulum stress. Mol Med Rep 9:69–76
130. Shoichet MS, Tate CC, Baumann MD, LaPlaca MC (2008) Strategies for regeneration and repair in the injured central nervous system. In: Reichert WM (ed) Indwelling neural implants: strategies for contending with the in vivo environment. CRC Press, Boca Raton, Chapter 8
131. Krajewska M, Xu L, Xu W, Krajewski S, Kress CL, Cui J, Yang L, Irie F, Yamaguchi Y, Lipton SA, Reed JC (2011) Endoplasmic reticulum protein BI-1 modulates unfolded protein response signaling and protects against stroke and traumatic brain injury. Brain Res 1370:227–237
132. Begum G, Yan HQ, Li L, Singh A, Dixon CE, Sun D (2014) Docosahexaenoic acid reduces ER stress and abnormal protein accumulation and improves neuronal function following traumatic brain injury. J Neurosci 34:3743–3755
133. Cheng G, Kong RH, Zhang LM, Zhang JN (2012) Mitochondria in traumatic brain injury and mitochondrial-targeted multipotential therapeutic strategies. Br J Pharmacol 167:699–719
134. Truettner JS, Hu B, Alonso OF, Bramlett HM, Kokame K, Dietrich WD (2007) Subcellular stress response after traumatic brain injury. J Neurotrauma 24:599–612
135. Lee HY, Lee GH, Marahatta A, Lin SM, Lee MR, Jang KY, Kim KM, Lee HJ, Lee JW, Bagalkot TR, Chung YC, Lee YC, Kim HR, Chae HJ (2013) The protective role of Bax inhibitor-1 against chronic mild stress through the inhibition of monoamine oxidase A. Sci Rep 3:3398
136. Nakka VP, Bodden LO, Vemuganti R (2014) ER stress inhibitor salubrinal is neuroprotective after TBI. J Neurotrauma 31(12):A107
137. Yan F, Li J, Chen J, Hu Q, Gu C, Lin W, Chen G (2014) Endoplasmic reticulum stress is associated with neuroprotection against apoptosis via autophagy activation in a rat model of subarachnoid hemorrhage. Neurosci Lett 563:160–165
138. Jing CH, Wang L, Liu PP, Wu C, Ruan D, Chen G (2012) Autophagy activation is associated with neuroprotection against apoptosis via a mitochondrial pathway in a rat model of subarachnoid hemorrhage. Neuroscience 213:144–153
139. He Z, Ostrowski RP, Sun X, Ma Q, Tang J, Zhang JH (2012) Targeting C/EBP homologous protein with siRNA attenuates cerebral vasospasm after experimental subarachnoid hemorrhage. Exp Neurol 238:218–224
140. Zhang HY, Wang ZG, Lu XH, Kong XX, Wu FZ, Lin L, Tan X, Ye LB, Xiao J (2014) Endoplasmic reticulum stress: relevance and therapeutics in central nervous system diseases. Mol Neurobiol
141. Ohri SS, Maddie MA, Zhao Y, Qiu MS, Hetman M, Whittemore SR (2011) Attenuating the endoplasmic reticulum stress response improves functional recovery after spinal cord injury. Glia 59:1489–1502
142. Matsuyama D, Watanabe M, Suyama K, Kuroiwa M, Mochida J (2014) Endoplasmic reticulum stress response in the rat contusive spinal cord injury model-susceptibility in specific cell types. Spinal Cord 52:9–16
143. Penas C, Guzmán MS, Verdú E, Forés J, Navarro X, Casas C (2007) Spinal cord injury induces endoplasmic reticulum stress with different cell-type dependent response. J Neurochem 102:1242–1255
144. Kohno K, Higuchi T, Ohta S, Kumon Y, Sakaki S (1997) Neuroprotective nitric oxide synthase inhibitor reduces intracellular calcium accumulation following transient global ischemia in the gerbil. Neurosci Lett 224:17–20
145. Sekiguchi F et al (2004) The potent inducible nitric oxide synthase inhibitor ONO-1714 inhibits neuronal NOS and exerts antinociception in rats. Neurosci Lett 365:111–115
146. Terpolilli NA, Moskowitz MA, Plesnila N (2012) Nitric oxide: considerations for the treatment of ischemic stroke. J Cereb Blood Flow Metab 32:1332–1346
147. Ding K, Wang H, Xu J, Li T, Zhang L, Ding Y, Zhu L, He J, Zhou M (2014) Melatonin stimulates antioxidant enzymes and reduces oxidative stress in experimental traumatic brain injury: the Nrf2-ARE signaling pathway as a potential mechanism. Free Radic Biol Med 73:1–11
148. Satoh T, Kosaka K, Itoh K, Kobayashi A, Yamamoto M, Shimojo Y, Kitajima C, Cui J, Kamins J, Okamoto S, Izumi M, Shirasawa T, Lipton SA (2008) Carnosic acid, a catechol-type electrophilic compound, protects neurons both in vitro and in vivo through activation of the Keap1/Nrf2 pathway via S-alkylation of targeted cysteines on Keap1. J Neurochem 104:1116–1131
149. Shih AY, Li P, Murphy TH (2005) A small-molecule inducible Nrf2-mediated antioxidant response provides effective prophylaxis against cerebral ischemia in vivo. J Neurosci 25:10321–10335
150. Itoh T, Satou T, Nishida S, Tsubaki M, Hashimoto S, Ito H (2009) The novel free radical scavenger, edaravone, increases neural stem cell number around the area of damage following rat traumatic brain injury. Neurotox Res 16:378–389
151. Qi X, Okuma Y, Hosoi T, Nomura Y (2004) Edaravone protects against hypoxia/ischemia-induced endoplasmic reticulum dysfunction. Pharmacol Exp Ther 311:388–393
152. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Görgün CZ, Hotamisligil GS (2006) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313:1137–1140
153. Rodrigues CM, Spellman SR, Solá S, Grande AW, Linehan-Stieers C, Low WC, Steer CJ (2002) Neuroprotection by a bile acid in an acute stroke model in the rat. Cereb Blood Flow Metab 22:463–471
154. Lu XY, Wang HD, Xu JG, Ding K, Li T (2014) NADPH oxidase inhibition improves neurological outcome in experimental traumatic brain injury. Neurochem Int 69:14–19
155. Ferreira AP, Rodrigues FS, Della-Pace ID, Mota BC, Oliveira SM et al (2013) The effect of NADPH-oxidase inhibitor apocynin on cognitive impairment induced by moderate lateral fluid percussion injury: role of inflammatory and oxidative brain damage. Neurochem Int 63:583–593
156. Chen H, Song YS, Chan PH (2009) Inhibition of NADPH oxidase is neuroprotective after ischemia-reperfusion. J Cereb Blood Flow Metab 29:1262–1272
157. Uchikawa O, Sakai N, Terao Y, Suzuki H (2008) Fused heterocyclic compound. WO2008016131
158. Hall ED, Vaishnav RA, Mustafa AG (2010) Antioxidant therapies for traumatic brain injury. Neurotherapeutics 7:51–61
159. Kudo T et al (2008) A molecular chaperone inducer protects neurons from ER stress. Cell Death Differ 15:364–375
160. Ladecola C, Zhang F, Casey R, Nagayama M, Ross ME (1997) Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J Neurosci 17:9157–9164
161. Mesenge C, Margaill I, Verrecchia C, Allix M, Boulu RG, Plotkine M (1998) Protective effect of melatonin in a model of traumatic brain injury in mice. J Pineal Res 25:41–46