Induction of ER stress in response to oxygen-glucose deprivation of cortical cultures involves the activation of the PERK and IRE-1 pathways and of caspase-12

Cell Death and Disease

Volumn 2, Issue 4, 2011, Pages

  Badiola, N ^a,b,c   Penas, C ^a,b,c   Minano Molina A ^a,c   Barneda Zahonero, B ^a,b,c   Fado R ^a,b,c   Sanchez Opazo G ^a,b,c   Comella, J X ^a,b,c   Sabria J ^a,b   Zhu, C ^d   Blomgren, K ^d,e   Casas, C ^a,b,c   Rodriguez Alvarez J ^a,b,c  

^a INSTITUT DE NEUROCIÈNCIES   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e QUEEN SILVIA CHILDREN'S HOSPITAL   (Sweden)

Author keywords

Apoptosis; Brain; Caspase 12; Cell culture; Endoplasmic reticulum stress; Ischemia

Indexed keywords

CALPAIN; CASPASE 12; CHAPERONE; GLUCOSE; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; INITIATION FACTOR 2ALPHA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OXYGEN; PROTEIN IRE1; PROTEIN KINASE; PROTEIN SUBUNIT; RNA ACTIVATED PROTEIN KINASE LIKE ER RESIDENT KINASE; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; ACTIVATING TRANSCRIPTION FACTOR 4; ATF4 PROTEIN, RAT; CASP12 PROTEIN, RAT; DIFFERENTIATION ANTIGEN; DNA BINDING PROTEIN; ERN2 PROTEIN, RAT; GLUCOSE REGULATED PROTEINS; GLUCOSE-REGULATED PROTEINS; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HSPA5 PROTEIN, RAT; INITIATION FACTOR 2; MEMBRANE PROTEIN; MYD116 PROTEIN, RAT; ONCOPROTEIN; PERK KINASE; PROTEIN KINASE R; PROTEIN SERINE THREONINE KINASE; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; FEMALE; FETUS; HYPOXIC ISCHEMIC ENCEPHALOPATHY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; RAT; RECEPTOR UPREGULATION; ANIMAL; BRAIN CORTEX; CELL CULTURE; CELL HYPOXIA; CULTURE TECHNIQUE; CYTOLOGY; ENDOPLASMIC RETICULUM; GENETICS; METABOLISM; NEWBORN; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; UPREGULATION; WISTAR RAT;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, DIFFERENTIATION; CALPAIN; CASPASE 12; CELL CULTURE TECHNIQUES; CELL HYPOXIA; CELLS, CULTURED; CEREBRAL CORTEX; DNA-BINDING PROTEINS; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; EUKARYOTIC INITIATION FACTOR-2; GLUCOSE; HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 79959979647     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2011.31     Document Type: Article

References (40)

1. Hara H, Fink K, Endres M, Friedlander RM, Gagliardini V, Moskowitz MA. Attenuation of transient focal cerebral ischemic injury in transgenic mice expressing a mutant ICE inhibitory protein. J Cereb Blood Flow Metab 1997; 17: 370-375. (Pubitemid 27188533)
2. Malagelada C, XIfrò X, Minano A, Sabría J, Rodriguez-Alvarez J. Contribution of caspasemediated apoptosis to the cell death caused by oxygen-glucose deprivation in cortical cell cultures. Neurobiol Dis 2005; 20: 27-37. (Pubitemid 41219200)
3. Rao RV, Ellerby HM, Bredesen DE. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 2004; 11: 372-380. (Pubitemid 38489415)
4. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000; 2: 326-332.
5. Shen J, Chen X, Hendershot L, Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 2002; 3: 99-111. (Pubitemid 34778399)
6. 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. (Pubitemid 30038529)
7. Shibata M, Hattori H, Sasaki T, Gotoh J, Hamada J, Fukuuchi Y. Activation of caspase-12 by endoplasmic reticulum stress induced by transient middle cerebral artery occlusion in mice. Neuroscience 2003; 118: 491-499. (Pubitemid 36423263)
8. Obeng EA, Boise LH. Caspase-12 and caspase-4 are not required for caspase-dependent endoplasmic reticulum stress-induced apoptosis. J Biol Chem 2005; 280: 29578-29587. (Pubitemid 41177033)
9. Paschen W, Doutheil J. Disturbances of the functioning of endoplasmic reticulum: a key mechanism underlying neuronal cell injury? J Cereb Blood Flow Metab 1999; 19: 1-18. (Pubitemid 29283575)
10. Tajiri S, Oyadomari S, Yano S, Morioka M, Gotoh T, Hamada JI et al. Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death Differ 2004; 11: 403-415. (Pubitemid 38489418)
11. Hayashi T, Saito A, Okuno S, Ferrand-Drake M, Dodd RL, Chan PH. Damage to the endoplasmic reticulum and activation of apoptotic machinery by oxidative stress in ischemic neurons. J Cereb Blood Flow Metab 2005; 25: 41-53. (Pubitemid 40096896)
12. 2+ dysregulation and endoplasmic reticulum stress following in vitro neuronal ischemia: role of Na+-K+-Cl- cotransporter. J Neurochem 2008; 106: 1563-1576.
13. Zhu C, Wang X, Xu F, Bahr BA, Shibata M, Uchiyama Y et al. The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ 2004; 12: 162-176.
14. Dever TE, Yang W, Astrom S, Bystrom AS, Hinnebusch AG. Modulation of tRNA(iMet), eIF-2, and eIF-2B expression shows that GCN4 translation is inversely coupled to the level of eIF-2.GTP.Met-tRNA(iMet) ternary complexes. Mol Cell Biol 1995; 15: 6351-6363.
15. Novoa I, Zeng H, Harding HP, Ron D. Feedback Inhibition of the Unfolded Protein Response by GADD34-mediated Dephosphorylation of eIF2{alpha}. J Cell Biol 2001; 153: 1011-1022.
16. Hong M, Luo S, Baumeister P, Huang JM, Gogia RK, Li M et al. Underglycosylation of ATF6 as a novel sensing mechanism for activation of the unfolded protein response. J Biol Chem 2004; 279: 11354-11363. (Pubitemid 38401633)
17. Hong M, Li M, Mao C, Lee AS. Endoplasmic reticulum stress triggers an acute proteasomedependent degradation of ATF6. J Cell Biochem 2004; 92: 723-732. (Pubitemid 44264263)
18. Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum Resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003; 23: 7448-7459. (Pubitemid 37271447)
19. Nakagawa T, Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J Cell Biol 2000; 150: 887-894. (Pubitemid 30663424)
20. Rao RV, Hermel E, Castro-Obregon S, del RG, Ellerby LM, Ellerby HM et al. Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. J Biol Chem 2001; 276: 33869-33874.
21. Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T et al. Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptorassociated factor 2-dependent mechanism in response to the ER stress. J Biol Chem 2001; 276: 13935-13940.
22. Blomgren K, Zhu C, Wang X, Karlsson JO, Leverin AL, Bahr BA et al. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of 'pathological apoptosis'? J Biol Chem 2001; 276: 10191-10198.
23. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000; 5: 897-904.
24. Althausen S, Mengesdorf T, Mies G, Olah L, Nairn AC, Proud CG et al. Changes in the phosphorylation of initiation factor eIF-2alpha, elongation factor eEF-2 and p70 S6 kinase after transient focal cerebral ischaemia in mice. J Neurochem 2001; 78: 779-787. (Pubitemid 32777979)
25. DeGracia DJ, Kumar R, Owen CR, Krause GS, White BC. Molecular pathways of protein synthesis inhibition during brain reperfusion: implications for neuronal survival or death. J Cereb Blood Flow Metab 2002; 22: 127-141. (Pubitemid 34135644)
26. Hayashi T, Saito A, Okuno S, Ferrand-Drake M, Dodd RL, Chan PH. Oxidative injury to the endoplasmic reticulum in mouse brains after transient focal ischemia. Neurobio Dis 2004; 15: 229-239. (Pubitemid 38296754)
27. Kumar R, Krause GS, Yoshida H, Mori K, DeGracia DJ. Dysfunction of the unfolded protein response during global brain ischemia and reperfusion. J Cereb Blood Flow Metab 2003; 23: 462-471. (Pubitemid 36403028)
28. Paschen W, Aufenberg C, Hotop S, Mengesdorf T. Transient cerebral ischemia activates processing of xbp1 messenger RNA indicative of endoplasmic reticulum stress. J Cereb Blood Flow Metab 2003; 23: 449-461. (Pubitemid 36403027)
29. Morimoto N, Oida Y, Shimazawa M, Miura M, Kudo T, Imaizumi K et al. Involvement of endoplasmic reticulum stress after middle cerebral artery occlusion in mice. Neuroscience 2007; 147: 957-967. (Pubitemid 47102538)
30. Ma Y, Hendershot LM. Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J Biol Chem 2003; 278: 34864-34873. (Pubitemid 37102245)
31. Mengesdorf T, Proud CG, Mies G, Paschen W. Mechanisms underlying suppression of protein synthesis induced by transient focal cerebral ischemia in mouse brain. Exp Neurol 2002; 177: 538-546. (Pubitemid 35366142)
32. Neumar RW, DeGracia DJ, Konkoly LL, Khoury JI, White BC, Krause GS. Calpain mediates eukaryotic initiation factor 4g degradation during global brain ischemia. J Cereb Blood Flow Metab 1998; 18: 876-881. (Pubitemid 28359905)
33. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001; 107: 881-891. (Pubitemid 34084979)
34. Olivari S, Galli C, Alanen H, Ruddock L, Molinari M. A novel stress-induced EDEM variant regulating endoplasmic reticulum-associated glycoprotein degradation. J Biol Chem 2005; 280: 2424-2428. (Pubitemid 40189341)
35. Morishima N, Nakanishi K, Tsuchiya K, Shibata T, Seiwa E. Translocation of Bim to the endoplasmic reticulum (ER) mediates ER stress signaling for activation of caspase-12 during ER stress-induced apoptosis. J Biol Chem 2004; 279: 50375-50381. (Pubitemid 39577855)
36. Tan Y, Dourdin N, Wu C, De VT, Elce JS, Greer PA. Ubiquitous calpains promote caspase-12 and JNK activation during endoplasmic reticulum stress-induced apoptosis. J Biol Che 2006; 281: 16016-16024. (Pubitemid 43848495)
37. Concannon CG, Ward MW, Bonner HP, Kuroki K, Tuffy LP, Bonner CT et al. NMDA receptor-mediated excitotoxic neuronal apoptosis in vitro and in vivo occurs in an ER stress and PUMA independent manner. J Neurochem 2008; 105: 891-903. (Pubitemid 351565712)
38. Goldberg MP, Choi DW. Combined oxygen and glucose deprivation in cortical cell cultured neurons: calcium-dependent and calcium-independent mechanisms of neuronal injury. J Neurosci 1993; 13: 3510-3524. (Pubitemid 23241187)
39. Malagelada C, Xifro X, Badiola N, Sabria J, Rodriguez-Alvarez J. Histamine H2-receptor antagonist ranitidine protects against neural death induced by oxygen-glucose deprivation. Stroke 2004; 35: 2396-2401. (Pubitemid 39311270)
40. Penas C, Guzman MS, Verdu E, Fores J, Navarro X, Casas C. Spinal cord injury induces endoplasmic reticulum stress with different cell-type dependent response. J Neurochem 2007; 102: 1242-1255. (Pubitemid 47174248)