Mutation of ATF4 mediates resistance of neuronal cell lines against oxidative stress by inducing xCT expression

Cell Death and Differentiation

Volumn 19, Issue 5, 2012, Pages 847-858

  Lewerenz, J ^a   Sato, H ^b   Albrecht, P ^c   Henke, N ^c   Noack, R ^c   Methner, A ^c   Maher, P ^d  

^a UNIVERSITY OF ULM   (Germany)

^b YAMAGATA UNIVERSITY   (Japan)

^c Department of Orthopedic Surgery   (Germany)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

ATF4; glutamate; glutathione; oxidative stress; xCT

Indexed keywords

AMYLOID BETA PROTEIN; ATF4 TRANSCRIPTION FACTOR; GLUTAMIC ACID; GLUTATHIONE DERIVATIVE; ISOPROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MOLECULAR WEIGHT; NERVE CELL MEMBRANE CONDUCTANCE; OPEN READING FRAME; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSLATION INITIATION; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 4; AMINO ACID TRANSPORT SYSTEM Y+; ANIMALS; BLOTTING, WESTERN; CELL LINE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GLUTATHIONE; MICE; MUTATION; NEURONS; OXIDATIVE STRESS; PC12 CELLS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84859582963     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2011.165     Document Type: Article

References (42)

1. Schulz JB, Lindenau J, Seyfried J, Dichgans J. Glutathione, oxidative stress and neurodegeneration. Eur J Biochem 2000; 267: 4904-4911. (Pubitemid 30641286)
2. Hayes JD, McLellan LI. Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radic Res 1999; 31: 273-300. (Pubitemid 29452854)
3. Liu YH, Di YM, Zhou ZW, Mo SL, Zhou SF. Multidrug resistance-associated proteins and implications in drug development. Clin Exp Pharmacol Physiol 2010; 37: 115-120.
4. Schafer FQ, Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 2001; 30: 1191-1212. (Pubitemid 32463931)
5. Martindale JL, Holbrook NJ. Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 2002; 192: 1-15. (Pubitemid 34587382)
6. Pani G, Galeotti T, Chiarugi P. Metastasis: cancer cell's escape from oxidative stress. Cancer Metastasis Rev 2010; 29: 351-378.
7. Behl C, Davis JB, Lesley R, Schubert D. Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 1994; 77: 817-827. (Pubitemid 24187680)
8. Sagara Y, Dargusch R, Klier FG, Schubert D, Behl C. Increased antioxidant enzyme activity in amyloid beta protein-resistant cells. J Neurosci 1996; 16: 497-505. (Pubitemid 26028810)
9. - protects from oxidative glutamate toxicity. J Neurochem 2006; 98: 916-925.
10. Soucek T, Cumming R, Dargusch R, Maher P, Schubert D. The regulation of glucose metabolism by HIF-1 mediates a neuroprotective response to amyloid beta peptide. Neuron 2003; 39: 43-56. (Pubitemid 36830947)
11. Denko NC. Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer 2008; 8: 705-713.
12. Albrecht P, Lewerenz J, Dittmer S, Noack R, Maher P, Methner A. Mechanisms of oxidative glutamate toxicity: the glutamate/cystine antiporter system x(c)- as a neuroprotective drug target. CNS Neurol Disord Drug Targets 2010; 9: 373-382.
13. Bannai S. Exchange of cystine and glutamate across plasma membrane of human fibroblasts. J Biol Chem 1986; 261: 2256-2263. (Pubitemid 17205155)
14. Sato H, Tamba M, Ishii T, Bannai S. Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J Biol Chem 1999; 274: 11455-11458.
15. Qin S, Colin C, Hinners I, Gervais A, Cheret C, Mallat M. System Xc- and apolipoprotein E expressed by microglia have opposite effects on the neurotoxicity of amyloid-beta peptide 1-40. J Neurosci 2006; 26: 3345-3356.
16. Savaskan NE, Heckel A, Hahnen E, Engelhorn T, Doerfler A, Ganslandt O et al. Small interfering RNA-mediated xCT silencing in gliomas inhibits neurodegeneration and alleviates brain edema. Nat Med 2008; 14: 629-632. (Pubitemid 351809547)
17. Dai Z, Huang Y, Sadee W, Blower P. Chemoinformatics analysis identifies cytotoxic compounds susceptible to chemoresistance mediated by glutathione and cystine/glutamate transport system xc. J Med Chem 2007; 50: 1896-1906. (Pubitemid 46626599)
18. Sato H, Nomura S, Maebara K, Sato K, Tamba M, Bannai S. Transcriptional control of cystine/glutamate transporter gene by amino acid deprivation. Biochem Biophys Res Commun 2004; 325: 109-116. (Pubitemid 39441168)
19. Lewerenz J, Maher P. Basal levels of eIF2alpha phosphorylation determine cellular antioxidant status by regulating ATF4 and xCT expression. J Biol Chem 2009; 284: 1106-1115.
20. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 2003; 11: 619-633. (Pubitemid 36385118)
21. Ameri K, Harris AL. Activating transcription factor 4. Int J Biochem Cell Biol 2008; 40: 14-21. (Pubitemid 350064577)
22. Siu F, Bain PJ, LeBlanc-Chaffin R, Chen H, Kilberg MS. ATF4 is a mediator of the nutrient-sensing response pathway that activates the human asparagine synthetase gene. J Biol Chem 2002; 277: 24120-24127. (Pubitemid 34951925)
23. Vattem KM, Wek RC. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci USA 2004; 101: 11269-11274. (Pubitemid 39038336)
24. Bi M, Naczki C, Koritzinsky M, Fels D, Blais J, Hu N et al. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. Embo J 2005; 24: 3470-3481. (Pubitemid 41486784)
25. Igarashi T, Izumi H, Uchiumi T, Nishio K, Arao T, Tanabe M et al. Clock and ATF4 transcription system regulates drug resistance in human cancer cell lines. Oncogene 2007; 26: 4749-4760. (Pubitemid 47093179)
26. Sasaki H, Sato H, Kuriyama-Matsumura K, Sato K, Maebara K, Wang H et al. Electrophile response element-mediated induction of the cystine/glutamate exchange transporter gene expression. J Biol Chem 2002; 277: 44765-44771. (Pubitemid 36159069)
27. Shih AY, Johnson DA, Wong G, Kraft AD, Jiang L, Erb H et al. Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J Neurosci 2003; 23: 3394-3406. (Pubitemid 36531981)
28. Lassot I, Estrabaud E, Emiliani S, Benkirane M, Benarous R, Margottin-Goguet F. p300 modulates ATF4 stability and transcriptional activity independently of its acetyltransferase domain. J Biol Chem 2005; 280: 41537-41545. (Pubitemid 41832215)
29. Lassot I, Segeral E, Berlioz-Torrent C, Durand H, Groussin L, Hai T et al. ATF4 degradation relies on a phosphorylation-dependent interaction with the SCF(betaTrCP) ubiquitin ligase. Mol Cell Biol 2001; 21: 2192-2202. (Pubitemid 32479639)
30. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D et al. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 2005; 307: 935-939. (Pubitemid 40229232)
31. Lu PD, Harding HP, Ron D. Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J Cell Biol 2004; 167: 27-33. (Pubitemid 39363411)
32. Dargusch R, Schubert D. Specificity of resistance to oxidative stress. J Neurochem 2002; 81: 1394-1400. (Pubitemid 34809272)
33. Novoa I, Zeng H, Harding HP, Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 2001; 153: 1011-1022.
34. Lange PS, Chavez JC, Pinto JT, Coppola G, Sun CW, Townes TM et al. ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J Exp Med 2008; 205: 1227-1242. (Pubitemid 351679695)
35. Galehdar Z, Swan P, Fuerth B, Callaghan SM, Park DS, Cregan SP. Neuronal apoptosis induced by endoplasmic reticulum stress is regulated by ATF4-CHOP-mediated induction of the Bcl-2 homology 3-only member PUMA. J Neurosci 2010; 30: 16938-16948.
36. Ord D, Meerits K, Ord T. TRB3 protects cells against the growth inhibitory and cytotoxic effect of ATF4. Exp cell res 2007; 313: 3556-3567. (Pubitemid 47404553)
37. Mielnicki LM, Hughes RG, Chevray PM, Pruitt SC. Mutated Atf4 suppresses c-Ha-ras oncogene transcript levels and cellular transformation in NIH3T3 fibroblasts. Biochem Biophys Res Commun 1996; 228: 586-595. (Pubitemid 26396115)
38. Hayes JD, McMahon M. NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends Biochem Sci 2009; 34: 176-188.
39. Maher P, Lewerenz J, Lozano C, Torres JL. A novel approach to enhancing cellular glutathione levels. J Neurochem 2008; 107: 690-700.
40. Cordey M, Pike CJ. Conventional protein kinase C isoforms mediate neuroprotection induced by phorbol ester and estrogen. J Neurochem 2006; 96: 204-217.
41. Cumming RC, Dargusch R, Fischer WH, Schubert D. Increase in expression levels and resistance to sulfhydryl oxidation of peroxiredoxin isoforms in amyloid beta-resistant nerve cells. J Biol Chem 2007; 282: 30523-30534. (Pubitemid 350035173)
42. Maher P. Proteasome inhibitors prevent oxidative stress-induced nerve cell death by a novel mechanism. Biochem Pharmacol 2008; 75: 1994-2006.