Edaravone leads to proteome changes indicative of neuronal cell protection in response to oxidative stress

Neurochemistry International

Volumn 90, Issue , 2015, Pages 134-141

  Jami, Mohammad Saeid ^a,d   Salehi Najafabadi, Zahra ^a   Ahmadinejad, Fereshteh ^d   Hoedt, Esthelle ^b   Chaleshtori, Morteza Hashemzadeh ^d   Ghatrehsamani, Mahdi ^d   Neubert, Thomas A ^b   Larsen, Jan Petter ^c   Møller, Simon Geir ^a,c  

^a ST JOHN'S UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c STAVANGER UNIVERSITY HOSPITAL   (Norway)

^d SHAHREKORD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Edaravone; l Dopa; Oxidative stress; Parkinson's disease; Peroxiredoxin 2; Proteomics

Indexed keywords

3 HYDROXYBUTYRATE DEHYDROGENASE; ALPHA TROPOMYOSIN; CATHEPSIN X; CYCLOPHILIN D; DJ 1 PROTEIN; FUMARATE HYDRATASE; HYDROGEN PEROXIDE; LACTATE DEHYDROGENASE; LEVODOPA; LIPOCORTIN 1; MITOCHONDRIAL ENZYME; NORPHENAZONE; NUCLEOSIDE DIPHOSPHATE KINASE D; OXIDOREDUCTASE; PEROXIREDOXIN 2; PEROXIREDOXIN 6; PROTEOME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; STRUCTURAL PROTEIN; VIMENTIN; NEUROPROTECTIVE AGENT; PHENAZONE; PHENYLMETHYLPYRAZOLONE; REACTIVE OXYGEN METABOLITE; SCAVENGER;

APOPTOSIS; ARTICLE; CELL DAMAGE; CELL HYPOXIA; CELL PROTECTION; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CITRIC ACID CYCLE; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSKELETON; CYTOTOXICITY; DOPAMINERGIC SYSTEM; DOWN REGULATION; METABOLISM; NEUROBLASTOMA CELL; NEUROPROTECTION; NEUROTOXICITY; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION; ANALOGS AND DERIVATIVES; CELL LINE; DRUG EFFECTS; HUMAN; NERVE CELL;

ANTIPYRINE; APOPTOSIS; CELL LINE; CELL SURVIVAL; FREE RADICAL SCAVENGERS; HUMANS; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PROTEOME; REACTIVE OXYGEN SPECIES;

EID: 84947042458     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2015.07.024     Document Type: Article

References (47)

1. H. Ariga, K. Takahashi-Niki, I. Kato, H. Maita, T. Niki, and S.M.M. Iguchi-Ariga Neuroprotective function of DJ-1 in Parkinson's disease Oxidative Med. Cell. Longev. 2013 2013 683920 10.1155/2013/683920
2. M. Basso, S. Giraudo, D. Corpillo, B. Bergamasco, L. Lopiano, and M. Fasano Proteome analysis of human substantia nigra in Parkinson's disease Proteomics 4 2004 3943 3952 10.1002/pmic.200400848
3. H. Blessing, M. Bareiss, H. Zettlmeisl, J. Schwarz, and A. Storch Catechol-O-methyltransferase inhibition protects against 3,4-dihydroxyphenylalanine (DOPA) toxicity in primary mesencephalic cultures: new insights into levodopa toxicity Neurochem. Int. 42 2003 139 151
4. D.A. Bosco, D.M. Fowler, Q. Zhang, J. Nieva, E.T. Powers, P. Wentworth, R.A. Lerner, and J.W. Kelly Elevated levels of oxidized cholesterol metabolites in Lewy body disease brains accelerate alpha-synuclein fibrilization Nat. Chem. Biol. 2 2006 249 253 10.1038/nchembio782
5. M. Bourdi, D. Demady, J.L. Martin, S.K. Jabbour, B.M. Martin, J.W. George, and L.R. Pohl cDNA cloning and baculovirus expression of the human liver endoplasmic reticulum P58: characterization as a protein disulfide isomerase isoform, but not as a protease or a carnitine acyltransferase Archives Biochem. Biophys. 323 1995 397 403 10.1006/abbi.1995.0060
6. J.J. Bravo-Cordero, M.A.O. Magalhaes, R.J. Eddy, L. Hodgson, and J. Condeelis Functions of cofilin in cell locomotion and invasion Nat. rev. Mol. Cell Biol. 14 2013 405 415 10.1038/nrm3609
7. G. Candiano, M. Bruschi, L. Musante, L. Santucci, G.M. Ghiggeri, B. Carnemolla, P. Orecchia, L. Zardi, and P.G. Righetti Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis Electrophoresis 25 2004 1327 1333 10.1002/elps.200305844
8. J. Cox, and M. Mann MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 26 2008 1367 1372 10.1038/nbt.1511
9. C.A. Davie A review of Parkinson's disease Br. Med. Bull. 86 2008 109 127 10.1093/bmb/ldn013
10. T.M. Dawson, H.S. Ko, and V.L. Dawson Genetic animal models of Parkinson's disease Neuron 66 2010 646 661 10.1016/j.neuron.2010.04.034
11. A.M. Day, J.D. Brown, S.R. Taylor, J.D. Rand, B.A. Morgan, and E.A. Veal Inactivation of a peroxiredoxin by hydrogen peroxide is critical for thioredoxin-mediated repair of oxidized proteins and cell survival Mol. Cell 45 2012 398 408 10.1016/j.molcel.2011.11.027
12. L.M.L. De Lau, and M.M.B. Breteler Epidemiology of Parkinson's disease Lancet Neurol. 5 2006 525 535 10.1016/S1474-4422(06)70471-9
13. E.R. Dorsey, R. Constantinescu, J.P. Thompson, K.M. Biglan, R.G. Holloway, K. Kieburtz, F.J. Marshall, B.M. Ravina, G. Schifitto, A. Siderowf, and C.M. Tanner Projected number of people with Parkinson disease in the most populous nations, 2005 through 2030 Neurology 68 2007 384 386 10.1212/01.wnl.0000247740.47667.03
14. 2 activities Antioxid. Redox Signal. 15 2011 831 844 10.1089/ars.2010.3412
15. C. García-Estrada, C. Barreiro, M.-S. Jami, J. Martín-González, and J.-F. Martín The inducers 1,3-diaminopropane and spermidine cause the reprogramming of metabolism in Penicillium chrysogenum, leading to multiple vesicles and penicillin overproduction J. Proteomics 85 2013 129 159 10.1016/j.jprot.2013.04.028
16. R.D. Goldman, S. Khuon, Y.H. Chou, P. Opal, and P.M. Steinert The function of intermediate filaments in cell shape and cytoskeletal integrity J. Cell Biol. 134 1996 971 983
17. K.M. Gorecka, D. Konopka-Postupolska, J. Hennig, R. Buchet, and S. Pikula Peroxidase activity of annexin 1 from Arabidopsis thaliana Biochem. Biophys. Res. Commun. 336 2005 868 875 10.1016/j.bbrc.2005.08.181
18. B.G. Hoffstrom, A. Kaplan, R. Letso, R.S. Schmid, G.J. Turmel, D.C. Lo, and B.R. Stockwell Inhibitors of protein disulfide isomerase suppress apoptosis induced by misfolded proteins Nat. Chem. Biol. 6 2010 900 906 10.1038/nchembio.467
19. X. Hu, Z. Weng, C.T. Chu, L. Zhang, G. Cao, Y. Gao, A. Signore, J. Zhu, T. Hastings, J.T. Greenamyre, and J. Chen Peroxiredoxin-2 protects against 6-hydroxydopamine-induced dopaminergic neurodegeneration via attenuation of the apoptosis signal-regulating kinase (ASK1) signaling cascade J. Neurosci. Off. J. Soc. Neurosci. 31 2011 247 261 10.1523/JNEUROSCI.4589-10.2011
20. M.-S. Jami, C. Barreiro, C. García-Estrada, and J.-F. Martín Proteome analysis of the penicillin producer Penicillium chrysogenum: characterization of protein changes during the industrial strain improvement Mol. Cell. Proteomics MCP 9 2010 1182 1198
21. M.-S. Jami, C. García-Estrada, C. Barreiro, A.-A. Cuadrado, Z. Salehi-Najafabadi, and J.-F. Martín The Penicillium chrysogenum extracellular proteome. Conversion from a food-rotting strain to a versatile cell factory for white biotechnology Mol. Cell. Proteomics MCP 9 2010 2729 2744
22. M.-S. Jami, J. Hou, M. Liu, M.L. Varney, H. Hassan, J. Dong, L. Geng, J. Wang, F. Yu, X. Huang, H. Peng, K. Fu, Y. Li, R.K. Singh, and S.-J. Ding Functional proteomic analysis reveals the involvement of KIAA1199 in breast cancer growth, motility and invasiveness BMC Cancer 14 2014 194 10.1186/1471-2407-14-194
23. M.-S. Jami, R. Pal, E. Hoedt, T.A. Neubert, J.P. Larsen, and S.G. Møller Proteome analysis reveals roles of L-DOPA in response to oxidative stress in neurons BMC Neurosci. 15 2014 93 10.1186/1471-2202-15-93
24. M.-H. Jin, Y.-H. Lee, J.-M. Kim, H.-N. Sun, E.-Y. Moon, M.H. Shong, S.-U. Kim, S.H. Lee, T.-H. Lee, D.-Y. Yu, and D.-S. Lee Characterization of neural cell types expressing peroxiredoxins in mouse brain Neurosci. Lett. 381 2005 252 257 10.1016/j.neulet.2005.02.048
25. M. Kaste, S. Murayama, G.A. Ford, D.W.J. Dippel, M.R. Walters, and T. Tatlisumak Safety, tolerability and pharmacokinetics of MCI-186 in patients with acute ischemic stroke: new formulation and dosing regimen Cerebrovasc. Dis. (Basel, Switzerland) 36 2013 196 204 10.1159/000353680
26. T. Katsumoto, A. Mitsushima, and T. Kurimura The role of the vimentin intermediate filaments in rat 3Y1 cells elucidated by immunoelectron microscopy and computer-graphic reconstruction Biol. Cell/Under Auspices Eur. Cell Biol. Organ. 68 1990 139 146
27. K. Kikuchi, E. Tanaka, Y. Murai, and S. Tancharoen Clinical trials in acute ischemic stroke CNS Drugs 28 2014 929 938 10.1007/s40263-014-0199-6
28. K. Kiyoshi, K. Kiyoshi, M. Naoki, M. Yoko, I. Takashi, T. Salunya, M. Kei, K. Chiemi, I. Narumi, T. Nobuyuki, U. Hisaaki, M. Naohisa, S. Naoto, K. Terukazu, H. Teruto, M. Ikuro, M. Motohiro, and K. Ko-ichi Beneficial effects of the free radical scavenger edaravone (Radicut) in neurologic diseases J. Neurol. Neurophysiol. 2011 10.4172/2155-9562.S1-001 Special issue 1
29. K. Kosalková, C. García-Estrada, C. Barreiro, M.G. Flórez, M.S. Jami, M.A. Paniagua, and J.F. Martín Casein phosphopeptides drastically increase the secretion of extracellular proteins in Aspergillus awamori. Proteomics studies reveal changes in the secretory pathway Microb. Cell Factor. 11 2012 5 10.1186/1475-2859-11-5
30. P.A. Lapchak A critical assessment of edaravone acute ischemic stroke efficacy trials: is edaravone an effective neuroprotective therapy? Expert Opin. Pharmacother. 11 2010 1753 1763 10.1517/14656566.2010.493558
31. B.J. Lee, Y. Egi, K. van Leyen, E.H. Lo, and K. Arai Edaravone, a free radical scavenger, protects components of the neurovascular unit against oxidative stress in vitro Brain Res. 1307 2010 22 27 10.1016/j.brainres.2009.10.026 Epub 2009 Oct 17
32. A.M.L. Liekens, J. De Knijf, W. Daelemans, B. Goethals, P. De Rijk, and J. Del-Favero BioGraph: unsupervised biomedical knowledge discovery via automated hypothesis generation Genome Biol. 12 2011 R57 10.1186/gb-2011-12-6-r57
33. J.J.-C. Lin, R.D. Eppinga, K.S. Warren, and K.R. McCrae Human tropomyosin isoforms in the regulation of cytoskeleton functions Adv. Exp. Med. Biol. 644 2008 201 222
34. X. Liu, R. Shao, M. Li, and G. Yang Edaravone protects neurons in the rat substantia nigra against 6-hydroxydopamine-induced oxidative stress damage Cell Biochem. Biophys. 70 2014 1247 1254 10.1007/s12013-014-0048-8
35. C.L. Markert Lactate dehydrogenase. Biochemistry and function of lactate dehydrogenase Cell Biochem. Funct. 2 1984 131 134 10.1002/cbf.290020302
36. M.A. Mena, M.J. Casarejos, R.M. Solano, and J.G. de Yébenes Half a century of L-DOPA Curr. Top. Med. Chem. 9 2009 880 893
37. Y. Nakabeppu, D. Tsuchimoto, H. Yamaguchi, and K. Sakumi Oxidative damage in nucleic acids and Parkinson's disease J. Neurosci. Res. 85 2007 919 934 10.1002/jnr.21191
38. A.V. Peskin, N. Dickerhof, R.A. Poynton, L.N. Paton, P.E. Pace, M.B. Hampton, and C.C. Winterbourn Hyperoxidation of peroxiredoxins 2 and 3: rate constants for the reactions of the sulfenic acid of the peroxidatic cysteine J. Biol. Chem. 288 20 2013 14170 14177 10.1074/jbc.M113.460881
39. A. Pompella, A. Visvikis, A. Paolicchi, V. De Tata, and A.F. Casini The changing faces of glutathione, a cellular protagonist Biochem. Pharmacol. 66 2003 1499 1503
40. M. Ralser, M.M. Wamelink, A. Kowald, B. Gerisch, G. Heeren, E.A. Struys, E. Klipp, C. Jakobs, M. Breitenbach, H. Lehrach, and S. Krobitsch Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress J. Biol. 6 2007 10 10.1186/jbiol61
41. Y. Shinohara, and S. Inoue Cost-effectiveness analysis of the neuroprotective agent edaravone for noncardioembolic cerebral infarction J. Stroke Cerebrovasc. Dis. Off. J. Natl. Stroke Assoc. 22 2013 668 674 10.1016/j.jstrokecerebrovasdis.2012.04.002
42. J.D. Storey A direct approach to false discovery rates J. R. Stat. Soc. Ser. B (Statistical Methodology) 64 2002 479 498 10.1111/1467-9868.00346
43. V. Stresing, E. Baltziskueta, N. Rubio, J. Blanco, M.C. Arriba, J. Valls, M. Janier, P. Clézardin, R. Sanz-Pamplona, C. Nieva, M. Marro, D. Petrov, P. Dmitri, and A. Sierra Peroxiredoxin 2 specifically regulates the oxidative and metabolic stress response of human metastatic breast cancer cells in lungs Oncogene 32 2013 724 735 10.1038/onc.2012.93
44. Y. Yamamoto, M. Yanagisawa, N.W. Tak, K. Watanabe, C. Takahashi, A. Fujisawa, M. Kashiba, and M. Tanaka Repeated edaravone treatment reduces oxidative cell damage in rat brain induced by middle cerebral artery occlusion Redox Rep. Commun. Free Radic. Res. 14 2009 251 258 10.1179/135100009X12525712409779
45. H. Yoshida, H. Yanai, Y. Namiki, K. Fukatsu-Sasaki, N. Furutani, and N. Tada Neuroprotective effects of edaravone: a novel free radical scavenger in cerebrovascular injury CNS Drug Rev. 12 2006 9 20 10.1111/j.1527-3458.2006.00009.x
46. Zeevalk, G.D., Razmpour, R., Bernard, L.P., n.d. Glutathione and Parkinson's disease: is this the elephant in the room? Biomed. Pharmacother. Biomédecine pharmacothérapie 62, 236-249. doi:10.1016/j.biopha.2008.01.017.
47. Z.-Y. Zhao, P. Luan, S.-X. Huang, S.-H. Xiao, J. Zhao, B. Zhang, B.-B. Gu, R.-B. Pi, and J. Liu Edaravone protects HT22 neurons from H2O2-induced apoptosis by inhibiting the MAPK signaling pathway CNS Neurosci. Ther. 19 2013 163 169 10.1111/cns.12044