The endoplasmic reticulum stress inhibitor salubrinal inhibits the activation of autophagy and neuroprotection induced by brain ischemic preconditioning

Acta Pharmacologica Sinica

Volumn 34, Issue 5, 2013, Pages 657-666

  Gao, Bo ^a   Zhang, Xiang Yang ^a   Han, Rong ^a   Zhang, Tong Tong ^a   Chen, Cheng ^a   Qin, Zheng Hong ^a   Sheng, Rui ^a  

^a MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

Author keywords

autophagy; caspase 12; cerebral ischemia; endoplasmic reticulum stress; glucose regulated protein 78 (GRP78); HSP70; ischemic preconditioning; LC3; p eIF2 ; p62; salubrinal

Indexed keywords

CASPASE 12; CELL PROTEIN; GLUCOSE REGULATED PROTEIN 78; HEAT SHOCK PROTEIN 70; INITIATION FACTOR 2ALPHA; PROTEIN LC3; PROTEIN P62; SALUBRINAL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BRAIN CORTEX; BRAIN INFARCTION SIZE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; ISCHEMIC PRECONDITIONING; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR DYSFUNCTION; NEUROPROTECTION; NONHUMAN; PROTEIN CLEAVAGE; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; APOPTOSIS; AUTOPHAGY; BRAIN; BRAIN ISCHEMIA; CINNAMATES; ENDOPLASMIC RETICULUM STRESS; ISCHEMIC PRECONDITIONING; MALE; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; THIOUREA;

EID: 84877590244     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2013.34     Document Type: Article

References (49)

1. Dirnagl U, Meisel A. Endogenous neuroprotection: mitochondria as gateways to cerebral preconditioning? Neuropharmacology 2008; 55: 334-44.
2. Obrenovitch TP. Molecular physiology of preconditioning-induced brain tolerance to ischemia. Physiol Rev 2008; 88: 211-47.
3. Perez-Pinzon MA. Mechanisms of neuroprotection during ischemic preconditioning: Lessons from anoxic tolerance. Compara Biochem Physiol 2007; 147: 291-9.
4. Liu XQ, Sheng R, Qin ZH. The neuroprotective mechanism of brain ischemic preconditioning. Acta Pharmacol Sin 2009; 30: 1071-80.
5. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005; 115: 2656-64.
6. Ma Y, Hendershot LM. The unfolding tale of the unfolded protein response. Cell 2001; 107: 827-30.
7. Boyce M, Yuan J. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ 2006; 13: 363-73.
8. Hayashi T, Saito A, Okuno S, Ferrand-Drake M, Chan PH. Induction of GRP78 by ischemic preconditioning reduces endoplasmic reticulum stress and prevents delayed neuronal cell death. J Cereb Blood Flow Metab 2003; 23: 949-61.
9. Reddy RK, Mao C, Baumeister P, Austin RC, Kaufman RJ, Lee AS. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J Biol Chem 2003; 278: 20915-24.
10. Oidaa Y, Izutaa H, Oyagi A, Shimazawaa M, Kudob T, Imaizumic K, et al. Induction of BiP, an ER-resident protein, prevents the neuronal death induced by transient forebrain ischemia in gerbil. Brain Res 2008; 1208: 217-24.
11. Yuan Y, Guo Q, Ye Z, Pingping X, Wang N, Song Z. Ischemic postconditioning protects brain from ischemia/reperfusion injury by attenuating endoplasmic reticulum stress-induced apoptosis through PI3K-Akt pathway. Brain Res 2011; 1367: 85-93.
12. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290: 1717-21.
13. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006; 441: 880-4.
14. McCray BA, Taylor JP. The role of autophagy in age-related neurodegeneration. Neurosignals 2008; 16: 75-84.
15. Yen WL, Klionsky DJ. How to live long and prosper: autophagy, mitochondria, and aging. Physiology 2008; 23: 248-62.
16. Adhami F, Liao G, Morozov YM, Schloemer A, Schmithorst VJ, Lorenz JN. Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am J Pathol 2006; 169: 566-83.
17. Carloni S, Buonocore G, Balduini W. Protective role of autophagy in neonatal hypoxia-ischemia induced brain injury. Neurobiol Dis 2008; 32: 329-39.
18. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S, et al. Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 2008; 172: 454-69.
19. Huang C, Yitzhaki S, Perry CN, Liu W, Giricz Z, Mentzer RM Jr, et al. Autophagy induced by ischemic preconditioning is essential for cardioprotection. J Cardiovasc Transl Res 2010; 3: 365-73.
20. Gurusamy N, Lekli I, Gorbunov NV, Gherghiceanu M, Popescu LM, Das DK. Cardioprotection by adaptation to ischaemia augments autophagy in association with BAG-1 protein. J Cell Mol Med 2009; 13: 373-87.
21. Yitzhaki S, Huang C, Liu W, Lee Y, Gustafsson AB, Mentzer RM Jr, et al. Autophagy is required for preconditioning by the adenosine A1 receptor-selective agonist CCPA. Basic Res Cardiol 2009; 104: 157-67.
22. Wu BX, Darden AG, Laser M, Li Y, Crosson CE, Hazard ES 3rd, et al. The rat Apg3p/Aut1p homolog is upregulated by ischemic preconditioning in the retina. Mol Vis 2006; 12: 1292-302.
23. Sheng R, Zhang LS, Han R, Liu XQ, Gao B, Qin ZH. Autophagy activation is associated with neuroprotection in a rat model of focal cerebral ischemic preconditioning. Autophagy 2010; 6: 482-94.
24. Sheng R, Liu XQ, Zhang LS, Gao B, Han R, Wu YQ, et al. Autophagy regulates endoplasmic reticulum stress in ischemic preconditioning. Autophagy 2012; 8: 310-25.
25. Yorimitsu T, Nair U, Yang Z, Klionsky DJ. Endoplasmic reticulum stress triggers autophagy. J Biol Chem 2006; 281: 30299-304.
26. Petrovski G, Das S, Juhasz B, Kertesz A, Tosaki A, Das DK. Cardioprotection by endoplasmic reticulum stress-induced autophagy. Antioxid Redox Signal 2011; 14: 2191-200.
27. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 2006; 26: 9220-31.
28. Oh SH, Lim SC. Endoplasmic reticulum stress-mediated autophagy/ apoptosis induced by capsaicin (8-methyl-N-vanillyl-6-nonenamide) and dihydrocapsaicin is regulated by the extent of c-Jun NH2-terminal kinase/extracellular signal-regulated kinase activation in WI38 lung epithelial fibroblast cells. J Pharmacol Exp Ther 2009; 329: 112-22.
29. Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989; 20: 84-91.
30. Lee SH, Kim YJ, Lee KM, Ryu S, Yoon BW. Ischemic preconditioning enhances neurogenesis in the subventricular zone. Neuroscience 2007; 146: 1020-31.
31. Tamura A, Graham DI, McCulloch J, Teasdale GM. Focal cerebral ischemia in the rat. 1 Description of technique and early neuropathological consequences following middle cerebral artery occlusion. J Cereb Blood Flow Metabol 1981; 1: 53-60.
32. Qin ZH, Chen RW, Wang Y, Nakai M, Chuang DM, Chase TN. Nuclear factor kappaB nuclear translocation upregulates c-Myc and p53 expression during NMDA receptor-mediated apoptosis in rat striatum. J Neurosci 1999; 19: 4023-33.
33. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, et al. A selective inhibitor of eIF2? dephosphorylation protects cells from ER stress. Science 2005; 307: 935-9.
34. Nakagawa, T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000; 403: 98-103.
35. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19: 5720-8.
36. Chakrabarti L, Eng J, Ivanov N, Garden GA, La Spada AR. Autophagy activation and enhanced mitophagy characterize the Purkinje cells of pcd mice prior to neuronal death. Mol Brain 2009; 2: 24.
37. Sokka AL, Putkonen N, Mudo G, Pryazhnikov E, Reijonen S, Khiroug L, et al. Endoplasmic reticulum stress inhibition protects against excitotoxic neuronal injury in the rat brain. J Neurosci 2007; 27: 901-8.
38. Tiwary R, Yu W, Li J, Park SK, Sanders BG, Kline K. Role of endoplasmic reticulum stress in alpha-TEA mediated TRAIL/DR5 death receptor dependent apoptosis. PLos One 2010; 5: e11865.
39. Chen J, Graham SH, Zhu RL, Simon RP. Stress proteins and tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 1996; 16: 566-77.
40. Currie RW, Ellison JA, White RF, Feuerstein GZ, Wang X, Barone FC. Benign focal ischemic preconditioning induces neuronal Hsp70 and prolonged astrogliosis with expression of Hsp27. Brain Res 2000; 863: 169-81.
41. Dhodda VK, Sailor KA, Bowen KK, Vemuganti R. Putative endogenous mediators of preconditioning-induced ischemic tolerance in rat brain identified by genomic and proteomic analysis. J Neurochem 2004; 89: 73-89.
42. Nishino K, Nowak TS Jr. Time course and cellular distribution of hsp27 and hsp72 stress protein expression in a quantitative gerbil model of ischemic injury and tolerance: thresholds for hsp72 induction and hilar lesioning in the context of ischemic preconditioning. J Cereb Blood Flow Metab 2004; 24: 167-78.
43. Massey AC, Kaushik S, Sovak G, Kiffin R, Cuervo AM. Consequences of the selective blockage of chaperone-mediated autophagy. Proc Natl Acad Sci U S A 2006; 103: 5805-10.
44. Meriin AB, Sherman MY. Role of molecular chaperones in neurodegenerative disorders. Int J Hyperthermia 2005; 21: 403-19.
45. Hoyer-Hansen M, Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 2007; 14: 1576-82.
46. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 2004; 117: 2805-12.
47. Kishi S, Shimoke K, Nakatani Y, Shimada T, Okumura N, Nagai K, et al. Nerve growth factor attenuates 2-deoxy-D-glucose-triggered endoplasmic reticulum stress-mediated apoptosis via enhanced expression of GRP78. Neurosci Res 2010; 66: 14-21.
48. Matus S, Lisbona F, Torres M, León C, Thielen P, Hetz C. The stress rheostat: an interplay between the unfolded protein response (UPR) and autophagy in neurodegeneration. Curr Mol Med 2008; 8: 157-72.
49. Choi CH, Jung YK, Oh SH. Autophagy induction by capsaicin in malignant human breast cells is modulated by p38 and extracellular signal-regulated mitogen-activated protein kinases and retards cell death by suppressing endoplasmic reticulum stress-mediated apoptosis. Mol Pharmacol 2010; 78: 114-25.