Short Chemical Ischemia Triggers Phosphorylation of eIF2α and Death of SH-SY5Y Cells but not Proteasome Stress and Heat Shock Protein Response in both SH-SY5Y and T98G Cells

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• 作者：Katarina Klacanova ; Ivana Pilchova ; Katarina Klikova…
• 关键词：Ischemia ; Proteasome ; Ubiquitin ; Heat shock proteins ; Unfolded protein response ; Cell death
• 刊名：Journal of Molecular Neuroscience
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：58
• 期：4
• 页码：497-506
• 全文大小：863 KB
• 参考文献：Asai A, Tanahashi N, Qiu JH, Saito N, Chi S, Kawahara N, Tanaka K, Kirino T (2002) Selective proteasome dysfunction in the hippocampal CA1 region after transient forebrain ischemia. J Cereb Blood Flow Metab 22:705–710CrossRef PubMed
  Baou M, Kohlhaas SL, Butterworth M, Vogler M, Dinsdale D, Walewska R, Majid A, Eldering E, Dyer MJ, Cohen GM (2010) Role of NOXA and its ubiquitination in proteasome inhibitor-induced apoptosis in chronic lymphocytic leukemia cells. Haematologica 95:1510–1518CrossRef PubMed PubMedCentral
  Burda J, Martin EM, Garcia A, Alcazar A, Fando JL, Salinas M (1994) Phosphorylation of the a subunit of initiation factor 2 correlates with the inhibition of translation following transient cerebral ischaemia in the rat. Biochem J 302:335–338CrossRef PubMed PubMedCentral
  Caldeira MV, Curcio M, Leal G, Salazar IL, Mele M, Santos AR, Melo CV, Pereira P, Canzoniero LM, Duarte CB (2013) Excitotoxic stimulation downregulates the ubiquitin-proteasome system through activation of NMDA receptors in cultured hippocampal neurons. Biochim Biophys Acta 1832:263–274CrossRef PubMed
  Caldeira MV, Salazar IL, Curcio M, Canzoniero LM, Duarte CB (2014) Role of the ubiquitin-proteasome system in brain ischemia: friend or foe? Prog Neurobiol 112:50–69CrossRef PubMed
  Chen T, Ozel D, Qiao Y, Harbinski F, Chen L, Denoyelle S, He X, Zvereva N, Supko JG, Chorev M, Halperin JA, Aktas BH (2011) Chemical genetics identify eIF2alpha kinase heme-regulated inhibitor as an anticancer target. Nat Chem Biol 7:610–616CrossRef PubMed PubMedCentral
  Ciechanover A, Kwon YT (2015) Degradation of misfolded proteins in neurodegenerative diseases: therapeutic targets and strategies. Exp Mol Med 47, e147CrossRef PubMed PubMedCentral
  DeGracia DJ, Hu BR (2007) Irreversible translation arrest in the reperfused brain. J Cereb Blood Flow Metab 27:875–893PubMed PubMedCentral
  DeGracia DJ, Neumar RW, White BC, Krause GS (1996) Global brain ischemia and reperfusion: modifications in eukaryotic initiation factors are associated with inhibition of translation initiation. J Neurochem 67:2005–2012CrossRef PubMed
  Deval C, Chaveroux C, Maurin AC, Cherasse Y, Parry L, Carraro V, Milenkovic D, Ferrara M, Bruhat A, Jousse C, Fafournoux P (2009) Amino acid limitation regulates the expression of genes involved in several specific biological processes through GCN2-dependent and GCN2-independent pathways. FEBS J 276:707–718CrossRef PubMed
  Donnelly N, Gorman AM, Gupta S, Samali A (2013) The eIF2α kinases: their structures and functions. Cell Mol Life Sci 70:3493–3511CrossRef PubMed
  Garnier P, Ying W, Swanson RA (2003) Ischemic preconditioning by caspase cleavage of poly(ADP-ribose) polymerase-1. J Neurosci 23:7967–7973PubMed
  Ge P, Luo Y, Liu CL, Hu B (2007) Protein aggregation and proteasome dysfunction after brain ischemia. Stroke 38:3230–3236CrossRef PubMed PubMedCentral
  Gomez E, Powell ML, Bevington A, Herbert TP (2008) A decrease in cellular energy status stimulates PERK-dependent eIF2alpha phosphorylation and regulates protein synthesis in pancreatic beta-cells. Biochem J 410:485–493CrossRef PubMed
  Gubellini P, Bisso GM, Ciofi-Luzzatto A, Fortuna S, Lorenzini P, Michalek H, Scarsella G (1997) Ubiquitin-mediated stress response in a rat model of brain transient ischemia/hypoxia. Neurochem Res 22:93–100CrossRef PubMed
  Hamanaka RB, Bennett BS, Cullinan SB, Diehl JA (2005) PERK and GCN2 contribute to eIF2alpha phosphorylation and cell cycle arrest after activation of the unfolded protein response pathway. Mol Biol Cell 16:5493–5501CrossRef PubMed PubMedCentral
  Hayashi T, Takada K, Matsuda M (1991) Changes in ubiquitin and ubiquitin-protein conjugates in the CA1 neurons after transient sublethal ischemia. Mol Chem Neuropathol 151:75–82CrossRef
  He C, Stroink A, Vogel L, Wang CX (2013) Temperature increase exacerbates apoptotic neuronal death in chemically-induced ischemia. PLoS One 8, e68796CrossRef PubMed PubMedCentral
  Hetz C, Mollereau B (2014) Disturbance of endoplasmic reticulum proteostasis in neurodegenerative diseases. Nat Rev Neurosci 15:233–249CrossRef PubMed
  Holcik M, Sonenberg N (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6:318–327CrossRef PubMed
  Hossmann KA (1993) Disturbances of cerebral protein synthesis and ischemic cell death. Prog Brain Res 96:161–177CrossRef PubMed
  Hossmann KA (1999) The hypoxic brain. Insights from ischemia research. Adv Exp Med Biol 474:155–169CrossRef PubMed
  Hu BR, Martone ME, Jones YZ, Liu CL (2000) Protein aggregation after transient cerebral ischemia. J Neurosci 20:3191–3199PubMed
  Ide T, Takada K, Qiu JH, Saito N, Kawahara N, Asai A, Kirino T (1999) Ubiquitin stress response in postischemic hippocampal neurons under nontolerant and tolerant conditions. J Cereb Blood Flow Metab 19:750–756CrossRef PubMed
  Iwabuchi M, Sheng H, Thompson JW, Wang L, Dubois LG, Gooden D, Moseley M, Paschen W, Yang W (2014) Characterization of the ubiquitin-modified proteome regulated by transient forebrain ischemia. J Cereb Blood Flow Metab 34:425–432CrossRef PubMed PubMedCentral
  Iwaki K, Chi SH, Dillmann WH, Mestril R (1993) Induction of HSP70 in cultured rat neonatal cardiomyocytes by hypoxia and metabolic stress. Circulation 87:2023–2032CrossRef PubMed
  Jiang HY, Wek RC (2005) Phosphorylation of the α-subunit of the eukaryotic initiation factor-2 (eIF2α) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J Biol Chem 280:14189–14202CrossRef PubMed
  Kabakov AE, Budagova KR, Latchman DS, Kampinga HH (2002) Stressful preconditioning and HSP70 overexpression attenuate proteotoxicity of cellular ATP depletion. Am J Physiol Cell Physiol 283:C521–C534CrossRef PubMed
  Kamikubo T, Hayashi T (1996) Changes in proteasome activity following transient ischemia. Neurochem Int 28:209–212CrossRef PubMed
  Kirino T (2000) Delayed neuronal death. Neuropathology 20:S95–S97CrossRef PubMed
  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 77:1418–1421CrossRef PubMed
  Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431–1568PubMed
  Liu CL, Ge P, Zhang F, Hu BR (2005) Co-translational protein aggregation after transient cerebral ischemia. Neuroscience 134:1273–1284CrossRef PubMed PubMedCentral
  Liu C, Gao Y, Barrett J, Hu B (2010) Autophagy and protein aggregation after brain ischemia. J Neurochem 115:68–78CrossRef PubMed PubMedCentral
  Luo T, Park Y, Sun X, Liu C, Hu B (2013) Protein misfolding, aggregation, and autophagy after brain ischemia. Trans Stroke Res 4:581–588CrossRef
  Martín de la Vega C, Burda J, Nemethova M, Quevedo C, Alcázar A, Martín ME, Danielisova V, Fando JL, Salinas M (2001) Possible mechanisms involved in the down-regulation of translation during transient global ischaemia in the rat brain. Biochem J 357:819–826CrossRef PubMed PubMedCentral
  Nawrocki ST, Carew JS, Dunner K Jr, Boise LH, Chiao PJ, Huang P, Abbruzzese JL, McConkey DJ (2005) Bortezomib inhibits PKR-like endoplasmic reticulum (ER) kinase and induces apoptosis via ER stress in human pancreatic cancer cells. Cancer Res 65:11510–11519CrossRef PubMed
  Obeng EA, Carlson LM, Gutman DM, Harrington WJ Jr, Lee KP, Boise LH (2006) Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 107:4907–4916CrossRef PubMed PubMedCentral
  Racay P (2012) Ischaemia-induced protein ubiquitinylation is differentially accompanied with heat-shock protein 70 expression after naïve and preconditioned ischaemia. Cell Mol Neurobiol 32:107–119CrossRef PubMed
  Roussel BD, Kruppa AJ, Miranda E, Crowther DC, Lomas DA, Marciniak SJ (2013) Endoplasmic reticulum dysfunction in neurological disease. Lancet Neurol 12:105–118CrossRef PubMed
  Sanderson TH, Deogracias MP, Nangia KK, Wang J, Krause GS, Kumar R (2010) PKR-like endoplasmic reticulum kinase (PERK) activation following brain ischemia is independent of unfolded nascent proteins. Neuroscience 169:1307–1314CrossRef PubMed
  Sanderson TH, Gallaway M, Kumar R (2015) Unfolding the unfolded protein response: unique insights into brain ischemia. Int J Mol Sci 16:7133–7142CrossRef PubMed PubMedCentral
  Selvatici R, Previati M, Marino S, Marani L, Falzarano S, Lanzoni I, Siniscalchi A (2009) Sodium azide induced neuronal damage in vitro: evidence for non-apoptotic cell death. Neurochem Res 34:909–916CrossRef PubMed
  Seo JW, Kim Y, Hur J, Park KS, Cho YW (2013) Proteomic analysis of primary cultured rat cortical neurons in chemical ischemia. Neurochem Res 38:1648–1660CrossRef PubMed
  Szydlowska K, Tymianski M (2010) Calcium, ischemia and excitotoxicity. Cell Calcium 47:122–129CrossRef PubMed
  Ye J, Kumanova M, Hart LS, Sloane K, Zhang H, De Panis DN, Bobrovnikova-Marjon E, Diehl JA, Ron D, Koumenis C (2010) The GCN2-ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation. EMBO J 29:2082–2096CrossRef PubMed PubMedCentral
  Yerlikaya A, Kimball SR, Stanley BA (2008) Phosphorylation of eIF2alpha in response to 26S proteasome inhibition is mediated by the heme-regulated inhibitor (HRI) kinase. Biochem J 412:579–588CrossRef PubMed PubMedCentral
  
• 作者单位：Katarina Klacanova (1)
  Ivana Pilchova (1)
  Katarina Klikova (1)
  Peter Racay (1)
  
  1. Department of Medical Biochemistry and Division Neuroscience of Biomedical Center, Jessenius Faculty of Medicine in Martin, Comenius University in Bratislava, Mala Hora 4D, Martin, SK-03601, Slovak Republic
  
• 刊物主题：Neurosciences; Neurochemistry; Cell Biology; Proteomics; Neurology;
• 出版者：Springer US
• ISSN：1559-1166

文摘

Both translation arrest and proteasome stress associated with accumulation of ubiquitin-conjugated protein aggregates were considered as a cause of delayed neuronal death after transient global brain ischemia; however, exact mechanisms as well as possible relationships are not fully understood. The aim of this study was to compare the effect of chemical ischemia and proteasome stress on cellular stress responses and viability of neuroblastoma SH-SY5Y and glioblastoma T98G cells. Chemical ischemia was induced by transient treatment of the cells with sodium azide in combination with 2-deoxyglucose. Proteasome stress was induced by treatment of the cells with bortezomib. Treatment of SH-SY5Y cells with sodium azide/2-deoxyglucose for 15 min was associated with cell death observed 24 h after treatment, while glioblastoma T98G cells were resistant to the same treatment. Treatment of both SH-SY5Y and T98G cells with bortezomib was associated with cell death, accumulation of ubiquitin-conjugated proteins, and increased expression of Hsp70. These typical cellular responses to proteasome stress, observed also after transient global brain ischemia, were not observed after chemical ischemia. Finally, chemical ischemia, but not proteasome stress, was in SH-SY5Y cells associated with increased phosphorylation of eIF2α, another typical cellular response triggered after transient global brain ischemia. Our results showed that short chemical ischemia of SH-SY5Y cells is not sufficient to induce both proteasome stress associated with accumulation of ubiquitin-conjugated proteins and stress response at the level of heat shock proteins despite induction of cell death and eIF2α phosphorylation.