Endoplasmic reticulum stress induced by tunicamycin and thapsigargin protects against transient ischemic brain injury: Involvement of PARK2-dependent mitophagy

Autophagy

Volumn 10, Issue 10, 2014, Pages 1801-1813

  Zhang, Xiangnan ^a   Yuan, Yang ^a   Jiang, Lei ^a   Zhang, Jingying ^a   Gao, Jieqiong ^b   Shen, Zhe ^a   Zheng, Yanrong ^a   Deng, Tian ^a   Yan, Haijing ^a   Li, Wenlu ^a,c   Hou, Wei Wei ^a   Lu, Jianxin ^b   Shen, Yao ^b   Dai, Haibing ^c   Hu, Wei Wei ^a   Zhang, Zhuohua ^d   Chen, Zhong ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b WENZHOU MEDICAL UNIVERSITY   (China)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Cerebral ischemia; Endoplasmic reticulum stress; Mitophagy; Neuroprotection; PARK2

Indexed keywords

3 METHYLADENINE; ACTIVATING TRANSCRIPTION FACTOR 4; CHLOROQUINE; GLUCOSE; OXYGEN; PROTEIN; PROTEIN EIF2S1; PROTEIN PARK2; REACTIVE OXYGEN METABOLITE; THAPSIGARGIN; TUNICAMYCIN; UNCLASSIFIED DRUG; NEUROPROTECTIVE AGENT; PARKIN; UBIQUITIN PROTEIN LIGASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BRAIN CELL CULTURE; BRAIN INFARCTION SIZE; BRAIN INJURY; BRAIN PROTECTION; CELL DEATH; CONTROLLED STUDY; CYTOSOL; EMBRYO; ENDOPLASMIC RETICULUM STRESS; FETUS; GENE SILENCING; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; IMMUNOHISTOCHEMISTRY; MALE; MICRO POSITRON EMISSION TOMOGRAPHY; MIDDLE CEREBRAL ARTERY OCCLUSION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MITOPHAGY; MOUSE; NERVE CELL; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIMARY CULTURE; PROTEIN DEPLETION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REPERFUSION; REPERFUSION INJURY; TRANSIENT ISCHEMIC BRAIN INJURY; TRANSIENT MIDDLE CEREBRAL ARTERY OCCLUSION; WESTERN BLOTTING; ANIMAL; BRAIN ISCHEMIA; DEFICIENCY; DRUG EFFECTS; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BRAIN ISCHEMIA; ENDOPLASMIC RETICULUM STRESS; GLUCOSE; MICE; MITOCHONDRIAL DEGRADATION; NEUROPROTECTIVE AGENTS; OXYGEN; REPERFUSION INJURY; SIGNAL TRANSDUCTION; THAPSIGARGIN; TUNICAMYCIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84907892583     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.32136     Document Type: Article

References (51)

1. Roussel BD, Kruppa AJ, Miranda E, Crowther DC, Lomas DA, Marciniak SJ. Endoplasmic reticulum dysfunction in neurological disease. Lancet Neurol 2013; 12:105-18; PMID:23237905; http://dx.doi.org/10.1016/S1474-4422(12)70238-7
2. Paschen W. Endoplasmic reticulum dysfunction in brain pathology: critical role of protein synthesis. Curr Neurovasc Res 2004; 1:173-81; PMID:16185192; http://dx.doi.org/10.2174/1567202043480125
3. Chen X, Kintner DB, Luo J, Baba A, Matsuda T, Sun D. Endoplasmic reticulum Ca2+ dysregulation and endoplasmic reticulum stress following in vitro neuronal ischemia: role of Na+-K+-Cl-cotransporter. J Neurochem 2008; 106:1563-76; PMID:18507737; http://dx.doi.org/10.1111/j.1471-4159.2008.05501.x
4. 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; PMID:9886350; http://dx.doi.org/10.1097/00004647-199901000-00001
5. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, Hetz C, Danial NN, Moskowitz MA, Korsmeyer SJ. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci U S A 2005; 102:12005-10; PMID:16103352; http://dx.doi.org/10.1073/pnas.0505294102
6. Qi X, Hosoi T, Okuma Y, Kaneko M, Nomura Y. Sodium 4-phenylbutyrate protects against cerebral ischemic injury. Mol Pharmacol 2004; 66:899-908; PMID:15226415; http://dx.doi.org/10.1124/mol.104.001339
7. Sokka AL, Putkonen N, Mudo G, Pryazhnikov E, Reijonen S, Khiroug L, Belluardo N, Lindholm D, Korhonen L. Endoplasmic reticulum stress inhibition protects against excitotoxic neuronal injury in the rat brain. J Neurosci 2007; 27:901-8; PMID:17251432; http://dx.doi.org/10.1523/JNEUROSCI.4289-06.2007
8. Nakka VP, Gusain A, Raghubir R. Endoplasmic reticulum stress plays critical role in brain damage after cerebral ischemia/reperfusion in rats. Neurotox Res 2010; 17:189-202; PMID:19763736; http://dx.doi.org/10.1007/s12640-009-9110-5
9. Rissanen A, Sivenius J, Jolkkonen J. Prolonged bihemispheric alterations in unfolded protein response related gene expression after experimental stroke. Brain Res 2006; 1087:60-6; PMID:16684512; http://dx.doi.org/10.1016/j.brainres.2006.02.095
10. Badiola N, Penas C, Miñano-Molina A, Barneda- Zahonero B, Fadó R, Sánchez-Opazo G, Comella JX, Sabriá J, Zhu C, Blomgren K, et al. 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 Dis 2011; 2:e149; PMID:21525936; http://dx.doi.org/10.1038/cddis.2011.31
11. 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; PMID:10882126; http:// dx.doi.org/10.1016/S1097-2765(00)80330-5
12. Ibuki T, Yamasaki Y, Mizuguchi H, Sokabe M. Protective effects of XBP1 against oxygen and glucose deprivation/reoxygenation injury in rat primary hippocampal neurons. Neurosci Lett 2012; 518:45-8; PMID:22580202; http://dx.doi.org/10.1016/j. neulet.2012.04.053
13. 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; PMID:20726815; http://dx.doi.org/10.1089/ars.2010.3486
14. Tooze SA, Yoshimori T. The origin of the autophagosomal membrane. Nat Cell Biol 2010; 12:831-5; PMID:20811355; http://dx.doi.org/10.1038/ncb0910-831
15. Decuypere JP, Kindt D, Luyten T, Welkenhuyzen K, Missiaen L, De Smedt H, Bultynck G, Parys JB. mTOR-Controlled Autophagy Requires Intracellular Ca(2+) Signaling. PLoS One 2013; 8:e61020; PMID:23565295; http://dx.doi.org/10.1371/journal.pone.0061020
16. Crawford SE, Estes MK. Viroporin-mediated calcium-activated autophagy. Autophagy 2013; 9:797-8; PMID:23442576; http://dx.doi.org/10.4161/auto.23959
17. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 2006; 26:9220-31; PMID:17030611; http:// dx.doi.org/10.1128/MCB.01453-06
18. Ding WX, Ni HM, Gao W, Hou YF, Melan MA, Chen X, Stolz DB, Shao ZM, Yin XM. Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival. J Biol Chem 2007; 282:4702-10; PMID:17135238; http://dx.doi.org/10.1074/jbc.M609267200
19. Fouillet A, Levet C, Virgone A, Robin M, Dourlen P, Rieusset J, Belaidi E, Ovize M, Touret M, Nataf S, et al. ER stress inhibits neuronal death by promoting autophagy. Autophagy 2012; 8:915-26; PMID:22660271; http://dx.doi.org/10.4161/auto.19716
20. Wen YD, Sheng R, Zhang LS, Han R, Zhang X, Zhang XD, Han F, Fukunaga K, Qin ZH. Neuronal injury in rat model of permanent focal cerebral ischemia is associated with activation of autophagic and lysosomal pathways. Autophagy 2008; 4:762-9; PMID:18567942; http://dx.doi.org/10.4161/auto.6412
21. Adhami F, Liao G, Morozov YM, Schloemer A, Schmithorst VJ, Lorenz JN, Dunn RS, Vorhees CV, Wills-Karp M, Degen JL, et al. Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am J Pathol 2006; 169:566-83; PMID:16877357; http://dx.doi.org/10.2353/ajpath.2006.051066
22. Zhang X, Yan H, Yuan Y, Gao J, Shen Z, Cheng Y, Shen Y, Wang RR, Wang X, Hu WW, et al. Cerebral ischemia-reperfusion-induced autophagy protects against neuronal injury by mitochondrial clearance. Autophagy 2013; 9:1321-33; PMID:23800795; http://dx.doi.org/10.4161/auto.25132
23. Geisler S, Holmström KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ, Springer W. PINK1/ Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 2010; 12:119-31; PMID:20098416; http://dx.doi.org/10.1038/ncb2012
24. Huang C, Andres AM, Ratliff EP, Hernandez G, Lee P, Gottlieb RA. Preconditioning involves selective mitophagy mediated by Parkin and p62/SQSTM1. PLoS One 2011; 6:e20975; PMID:21687634; http://dx.doi.org/10.1371/journal.pone.0020975
25. Paschen W. Dependence of vital cell function on endoplasmic reticulum calcium levels: implications for the mechanisms underlying neuronal cell injury in different pathological states. Cell Calcium 2001; 29:1-11; PMID:11133351; http://dx.doi.org/10.1054/ceca.2000.0162
26. Reimertz C, Kögel D, Rami A, Chittenden T, Prehn JH. Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J Cell Biol 2003; 162:587-97; PMID:12913114; http://dx.doi.org/10.1083/jcb.200305149
27. Rao RV, Ellerby HM, Bredesen DE. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 2004; 11:372-80; PMID:14765132; http://dx.doi.org/10.1038/sj.cdd.4401378
28. Szydlowska K, Tymianski M. Calcium, ischemia and excitotoxicity. Cell Calcium 2010; 47:122-9; PMID:20167368; http://dx.doi.org/10.1016/j.ceca.2010.01.003
29. 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; 23:449-61; PMID:12679722; http://dx.doi.org/10.1097/00004647-200304000-00009
30. Althausen S, Mengesdorf T, Mies G, Oláh L, Nairn AC, Proud CG, Paschen W. 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; 78:779-87; PMID:11520898; http://dx.doi.org/10.1046/j.1471-4159.2001.00462.x
31. Mouw G, Zechel JL, Gamboa J, Lust WD, Selman WR, Ratcheson RA. Activation of caspase-12, an endoplasmic reticulum resident caspase, after permanent focal ischemia in rat. Neuroreport 2003; 14:183-6; PMID:12598725; http://dx.doi.org/10.1097/00001756-200302100-00004
32. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. Caspase-12 mediates endo-plasmic- reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000; 403:98-103; PMID:10638761; http://dx.doi.org/10.1038/47513
33. Appenzeller-Herzog C, Hall MN. Bidirectional crosstalk between endoplasmic reticulum stress and mTOR signaling. Trends Cell Biol 2012; 22:274-82; PMID:22444729; http://dx.doi.org/10.1016/j.tcb.2012.02.006
34. Li Y, Zhao Y, Hu J, Xiao J, Qu L, Wang Z, Ma D, Chen Y. A novel ER-localized transmembrane protein, EMC6, interacts with RAB5A and regulates cell autophagy. Autophagy 2013; 9:150-63; PMID:23182941; http://dx.doi.org/10.4161/auto.22742
35. Sheng R, Liu XQ, Zhang LS, Gao B, Han R, Wu YQ, Zhang XY, Qin ZH. Autophagy regulates endoplasmic reticulum stress in ischemic preconditioning. Autophagy 2012; 8:310-25; PMID:22361585; http://dx.doi.org/10.4161/auto.18673
36. Hamasaki M, Furuta N, Matsuda A, Nezu A, Yamamoto A, Fujita N, Oomori H, Noda T, Haraguchi T, Hiraoka Y, et al. Autophagosomes form at ER-mitochondria contact sites. Nature 2013; 495:389-93; PMID:23455425; http://dx.doi.org/10.1038/nature11910
37. Mengesdorf T, Jensen PH, Mies G, Aufenberg C, Paschen W. Down-regulation of parkin protein in transient focal cerebral ischemia: A link between stroke and degenerative disease? Proc Natl Acad Sci U S A 2002; 99:15042-7; PMID:12415119; http://dx.doi.org/10.1073/pnas.232588799
38. Vincow ES, Merrihew G, Thomas RE, Shulman NJ, Beyer RP, MacCoss MJ, Pallanck LJ. The PINK1- Parkin pathway promotes both mitophagy and selective respiratory chain turnover in vivo. Proc Natl Acad Sci U S A 2013; 110:6400-5; PMID:23509287; http://dx.doi.org/10.1073/pnas.1221132110
39. Bouman L, Schlierf A, Lutz AK, Shan J, Deinlein A, Kast J, Galehdar Z, Palmisano V, Patenge N, Berg D, et al. Parkin is transcriptionally regulated by ATF4: evidence for an interconnection between mitochondrial stress and ER stress. Cell Death Differ 2011; 18:769-82; PMID:21113145; http://dx.doi.org/10.1038/cdd.2010.142
40. Olzmann JA, Li L, Chudaev MV, Chen J, Perez FA, Palmiter RD, Chin LS. Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6. J Cell Biol 2007; 178:1025-38; PMID:17846173; http://dx.doi.org/10.1083/jcb.200611128
41. Olzmann JA, Chin LS. Parkin-mediated K63-linked polyubiquitination: a signal for targeting misfolded proteins to the aggresome-autophagy pathway. Autophagy 2008; 4:85-7; PMID:17957134; http://dx.doi.org/10.4161/auto.5172
42. Shimura H, Hattori N, Kubo Si, Mizuno Y, Asakawa S, Minoshima S, Shimizu N, Iwai K, Chiba T, Tanaka K, et al. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat Genet 2000; 25:302-5; PMID:10888878; http://dx.doi.org/10.1038/77060
43. Hu BR, Martone ME, Jones YZ, Liu CL. Protein aggregation after transient cerebral ischemia. J Neurosci 2000; 20:3191-9; PMID:10777783
44. Wang HQ, Imai Y, Kataoka A, Takahashi R. Cell type-specific upregulation of Parkin in response to ER stress. Antioxid Redox Signal 2007; 9:533-42; PMID:17465879; http://dx.doi.org/10.1089/ars.2006.1522
45. Fan YY, Zhang XN, He P, Shen Z, Shen Y, Wang XF, Hu WW, Chen Z. Transient lack of glucose but not O2 is involved in ischemic postconditioning-induced neuroprotection. CNS Neurosci Ther 2013; 19:30-7; PMID:23167958; http://dx.doi.org/10.1111/cns.12033
46. Fan YY, Hu WW, Dai HB, Zhang JX, Zhang LY, He P, Shen Y, Ohtsu H, Wei EQ, Chen Z. Activation of the central histaminergic system is involved in hypoxiainduced stroke tolerance in adult mice. J Cereb Blood Flow Metab 2011; 31:305-14; PMID:20588322; http://dx.doi.org/10.1038/jcbfm.2010.94
47. Gao F, Guo Y, Zhang H, Wang S, Wang J, Wu JM, Chen Z, Ding MP. Anterior thalamic nucleus stimulation modulates regional cerebral metabolism: an FDG-MicroPET study in rats. Neurobiol Dis 2009; 34:477-83; PMID:19303441; http://dx.doi.org/10.1016/j.nbd.2009.03.001
48. Zhang CH, Fan YY, Wang XF, Xiong JY, Tang YY, Gao JQ, Shen Z, Song XH, Zhang JY, Shen Y, et al. Acidic preconditioning protects against ischemiainduced brain injury. Neurosci Lett 2012; 523:3-8; PMID:22583767; http://dx.doi.org/10.1016/j.neulet.2012.05.015
49. Du L, Hickey RW, Bayir H, Watkins SC, Tyurin VA, Guo F, Kochanek PM, Jenkins LW, Ren J, Gibson G, et al. Starving neurons show sex difference in autophagy. J Biol Chem 2009; 284:2383-96; PMID:19036730; http://dx.doi.org/10.1074/jbc.M804396200
50. Zhang X, Wu J, Dou Y, Xia B, Rong W, Rimbach G, Lou Y. Asiatic acid protects primary neurons against C2-ceramide-induced apoptosis. Eur J Pharmacol 2012; 679:51-9; PMID:22296759; http://dx.doi.org/10.1016/j.ejphar.2012.01.006
51. Zinchuk V, Zinchuk O, Okada T. Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena. Acta Histochem Cytochem 2007; 40:101-11; PMID:17898874; http://dx.doi.org/10.1267/ahc.07002