The free radical scavenger edaravone rescues rats from cerebral infarction by attenuating the release of high-mobility group box-1 in neuronal cells

Journal of Pharmacology and Experimental Therapeutics

Volumn 329, Issue 3, 2009, Pages 865-874

  Kikuchi, Kiyoshi ^a,e   Kawahara, Ko Ichi ^a   Tancharoen, Salunya ^b   Matsuda, Fumiyo ^c   Morimoto, Yoko ^a   Ito, Takashi ^a   Biswas, Kamal Krishna ^a   Takenouchi, Kazunori ^a   Miura, Naoki ^d   Oyama, Yoko ^a   Nawa, Yuko ^a   Arimura, Noboru ^a   Iwata, Masahiro ^a   Tajima, Yutaka ^e   Kuramoto, Terukazu ^e   Nakayama, Kenji ^e   Shigemori, Minoru ^f   Yoshida, Yoshihiro ^c   Hashiguchi, Teruto ^a   Maruyama, Ikuro ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

^b MAHIDOL UNIVERSITY   (Thailand)

^c KAGOSHIMA UNIVERSITY   (Japan)

^d KAGOSHIMA UNIVERSITY   (Japan)

^e Omuta City General Hospital   (Japan)

^f KURUME UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; NORPHENAZONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN INFARCTION; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG MECHANISM; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TRANSPORT; RAT; REPERFUSION INJURY;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTIPYRINE; APOPTOSIS; BUTADIENES; CELL HYPOXIA; CELL NUCLEUS; CEREBRAL INFARCTION; CEREBRUM; CYTOCHROMES C; CYTOPLASM; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FREE RADICAL SCAVENGERS; GLUCOSE; HMGB1 PROTEIN; HYDROGEN PEROXIDE; MALE; NEURONS; NEUROPROTECTIVE AGENTS; NITRILES; OXIDATIVE STRESS; PC12 CELLS; RATS; RATS, WISTAR; S100 PROTEINS;

EID: 66749132080     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.108.149484     Document Type: Article

References (55)

1. Alessandrini A, Namura S, Moskowitz MA, and Bonventre JV (1999) MEK1 protein kinase inhibition protects against damage resulting from focal cerebral ischemia. Proc Natl Acad Sci U S A 96:12866-12869. (Pubitemid 29513594)
2. Ando K, Nishi H, Watanabe T, Watanabe Y, Yuki S, Sugasawa K, Horii D, Ishibashi A, Kimura A, Nakano D, et al. (1997) General pharmacological studies of 3-methyl-1-phenyl-2-pyrazolin-5-one (MCI-186), a novel radical scavenging agent. Jpn Pharmacol Ther 25 (Suppl):S1723-S1753. (Pubitemid 28030794)
3. Benchoua A, Guégan C, Couriaud C, Hosseini H, Sampaïo N, Morin D, and Onténiente B (2001) Specific caspase pathways are activated in the two stages of cerebral infarction. J Neurosci 21:7127-7134. (Pubitemid 32846960)
4. Delaney ML and Onderdonk AB (1997) Evaluation of the AnaeroPack system for growth of clinically significant anaerobes. J Clin Microbiol 35:558-562. (Pubitemid 27083837)
5. - generation by mononuclear phagocytes in diabetes. J Leukoc Biol 81:520-527. (Pubitemid 46198404)
6. Dohi K, Satoh K, Nakamachi T, Yofu S, Hiratsuka K, Nakamura S, Ohtaki H, Yoshikawa T, Shioda S, and Aruga T (2007) Does edaravone (MCI-186) act as an antioxidant and a neuroprotector in experimental traumatic brain injury? Antioxid Redox Signal 9:281-287. (Pubitemid 46105426)
7. Donato R (1999) Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta 1450:191-231. (Pubitemid 29295473)
8. Edaravone Acute Brain Infarction Study Group (2003) Effect of a novel free radical scavenger, edaravone (MCI-186), on acute brain infarction. Randomized, placebo-controlled, double-blind study at multicenters. Cerebrovasc Dis 15:222-229. (Pubitemid 36351210)
9. Fagan SC, Hess DC, Machado LS, Hohnadel EJ, Pollock DM, and Ergul A (2005) Tactics for vascular protection after acute ischemic stroke. Pharmacotherapy 25:387-395. (Pubitemid 40300326)
10. Fan J, Li Y, Levy RM, Fan JJ, Hackam DJ, Vodovotz Y, Yang H, Tracey KJ, Billiar TR, and Wilson MA (2007) Hemorrhagic shock induces NAD(P)H oxidase activation in neutrophils: role of HMGB1-TLR4 signaling. J Immunol 178:6573-6580. (Pubitemid 46717441)
11. Fisher M (2006) The ischemic penumbra: a new opportunity for neuroprotection. Cerebrovasc Dis 21 (Suppl 2:64-70.
12. Gechev TS, Van Breusegem F, Stone JM, Denev I, and Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28:1091-1101. (Pubitemid 44714119)
13. Goldstein RS, Gallowitsch-Puerta M, Yang L, Rosas-Ballina M, Huston JM, Czura CJ, Lee DC, Ward MF, Bruchfeld AN, Wang H, et al. (2006) Elevated high-mobility group box 1 levels in patients with cerebral and myocardial ischemia. Shock 25:571-574. (Pubitemid 44297016)
14. Gonzalez-Martinez T, Perez-Piñera P, Díaz-Esnal B, and Vega JA (2003) S-100 proteins in the human peripheral nervous system. Microsc Res Tech 60:633-638.
15. Green AR and Shuaib A (2006) Therapeutic strategies for the treatment of stroke. Drug Discov Today 11:681-693. (Pubitemid 44056287)
16. Håberg A, Qu H, Saether O, Unsgård G, Haraldseth O, and Sonnewald U (2001) Differences in neurotransmitter synthesis and intermediary metabolism between glutamatergic and GABAergic neurons during 4 hours of middle cerebral artery occlusion in the rat: the role of astrocytes in neuronal survival. J Cereb Blood Flow Metab 21:1451-1463. (Pubitemid 33117185)
17. Haddad JJ (2004) Hypoxia and the regulation of mitogen-activated protein kinases: gene transcription and the assessment of potential pharmacologic therapeutic interventions. Int Immunopharmacol 4:1249-1285. (Pubitemid 39094402)
18. Harada H, Wang Y, Mishima Y, Uehara N, Makaya T, and Kano T (2005) A novel method of detecting rCBF with laser-Doppler flowmetry without cranial window through the skull for a MCAO rat model. Brain Res Brain Res Protoc 14:165-170. (Pubitemid 40431696)
19. Hillion JA, Takahashi K, Maric D, Ruetzler C, Barker JL, and Hallenbeck JM (2005) Development of an ischemic tolerance model in a PC12 cell line. J Cereb Blood Flow Metab 25:154-162. (Pubitemid 40171198)
20. Huang YH, Chang AY, Huang CM, Huang SW, and Chan SH (2002) Proteomic analysis of lipopolysaccharide-induced apoptosis in PC12 cells. Proteomics 2:1220-1228.
21. Ito T, Kawahara K, Nakamura T, Yamada S, Nakamura T, Abeyama K, Hashiguchi T, and Maruyama I (2007) High-mobility group box 1 protein promotes development of microvascular thrombosis in rats. J Thromb Haemost 5:109-116. (Pubitemid 44921075)
22. Jiang W, Bell CW, and Pisetsky DS (2007) The relationship between apoptosis and high-mobility group protein 1 release from murine macrophages stimulated with lipopolysaccharide or polyinosinic-polycytidylic acid. J Immunol 178:6495-6503. (Pubitemid 46717433)
23. Kawahara K, Watanabe S, Ohshima T, Soejima Y, Oishi T, Aratani S, Nakata M, Shibata M, Inoue K, Amano T, et al. (1999) Hypernuclear acetylation in atherosclerotic lesions and activated vascular smooth muscle cells. Biochem Biophys Res Commun 266:417-424. (Pubitemid 30028683)
24. Kawasaki T, Kitao T, Nakagawa K, Fujisaki H, Takegawa Y, Koda K, Ago Y, Baba A, and Matsuda T (2007) Nitric oxide-induced apoptosis in cultured rat astrocytes: protection by edaravone, a radical scavenger. Glia 55:1325-1333. (Pubitemid 47328936)
25. Kim JB, Sig Choi J, Yu YM, Nam K, Piao CS, Kim SW, Lee MH, Han PL, Park JS, and Lee JK (2006) HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J Neurosci 26:6413-6421. (Pubitemid 44318322)
26. Kim JY, Park JS, Strassheim D, Douglas I, Diaz del Valle F, Asehnoune K, Mitra S, Kwak SH, Yamada S, Maruyama I, et al. (2005) HMGB1 contributes to the development of acute lung injury after hemorrhage. Am J Physiol Lung Cell Mol Physiol 288:L958-L965. (Pubitemid 40547924)
27. Liu K, Mori S, Takahashi HK, Tomono Y, Wake H, Kanke T, Sato Y, Hiraga N, Adachi N, Yoshino T, et al. (2007) Anti-high mobility group box 1 monoclonal antibody ameliorates brain infarction induced by transient ischemia in rats. FASEB J 21:3904-3916. (Pubitemid 350232348)
28. Longa EZ, Weinstein PR, Carlson S, and Cummins R (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20:84-91. (Pubitemid 19040218)
29. Menzies SA, Hoff JT, and Betz AL (1992) Middle cerebral artery occlusion in rats: a neurological and pathological evaluation of a reproducible model. Neurosurgery 31:100-106; discussion 106-107.
30. Mills EM, Gunasekar PG, Pavlakovic G, and Isom GE (1996) Cyanide-induced apoptosis and oxidative stress in differentiated PC12 cells. J Neurochem 67:1039-1046. (Pubitemid 26277916)
31. Nakamura T, Kuroda Y, Yamashita S, Zhang X, Miyamoto O, Tamiya T, Nagao S, Xi G, Keep RF, and Itano T (2008) Edaravone attenuates brain edema and neurologic deficits in a rat model of acute intracerebral hemorrhage. Stroke 39:463-469.
32. Nishi H, Watanabe T, Sakurai H, Yuki S, and Ishibashi A (1989) Effect of MCI-186 on brain edema in rats. Stroke 20:1236-1240. (Pubitemid 19226920)
33. Qi X, Okuma Y, Hosoi T, and Nomura Y (2004) Edaravone protects against hypoxia/ischemia-induced endoplasmic reticulum dysfunction. J Pharmacol Exp Ther 311:388-393. (Pubitemid 39287820)
34. Qiu J, Nishimura M, Wang Y, Sims JR, Qiu S, Savitz SI, Salomone S, and Moskowitz MA (2008) Early release of HMGB-1 from neurons after the onset of brain ischemia. J Cereb Blood Flow Metab 28:927-938.
35. Riuzzi F, Sorci G, and Donato R (2006) The amphoterin (HMGB1)/receptor for advanced glycation end products (RAGE) pair modulates myoblast proliferation, apoptosis, adhesiveness, migration, and invasiveness. Functional inactivation of RAGE in L6 myoblasts results in tumor formation in vivo. J Biol Chem 281:8242-8253. (Pubitemid 43847445)
36. Sahu D, Debnath P, Takayama Y, and Iwahara J (2008) Redox properties of the A-domain of the HMGB1 protein. FEBS Lett 582:3973-3978.
37. Sekine Y, Takeda K, and Ichijo H (2006) The ASK1-MAP kinase signaling in ER stress and neurodegenerative diseases. Curr Mol Med 6:87-97.
38. Shuaib A, Lees KR, Lyden P, Grotta J, Davalos A, Davis SM, Diener HC, Ashwood T, Wasiewski WW, and Emeribe U (2007) NXY-059 for the treatment of acute ischemic stroke. N Engl J Med 357:562-571. (Pubitemid 47236281)
39. Slevin M, Krupinski J, Slowik A, Rubio F, Szczudlik A, and Gaffney J (2000) Activation of MAP kinase (ERK-1/ERK-2), tyrosine kinase and VEGF in the human brain following acute ischaemic stroke. Neuroreport 11:2759-2764.
40. Takamatsu Y, Yuki S, and Watanabe T (1997) Studies on the concentrations of 3-methyl-1-phenyl-2-pyrazolin-5-one (MCI-186) in MCA occlusion and reperfusion model of rats. Jpn Pharmacol Ther 25 (Suppl):S1785-S1791. (Pubitemid 128725979)
41. Tancharoen S, Sarker KP, Imamura T, Biswas KK, Matsushita K, Tatsuyama S, Travis J, Potempa J, Torii M, and Maruyama I (2005) Neuropeptide release from dental pulp cells by RgpB via proteinase-activated receptor-2 signaling. J Immunol 174:5796-5804. (Pubitemid 40593224)
42. Tang D, Shi Y, Kang R, Li T, Xiao W, Wang H, and Xiao X (2007) Hydrogen peroxide stimulates macrophages and monocytes to actively release HMGB1. J Leukoc Biol 81:741-747. (Pubitemid 46393551)
43. Taniguchi N, Kawahara K, Yone K, Hashiguchi T, Yamakuchi M, Goto M, Inoue K, Yamada S, Ijiri K, Matsunaga S, et al. (2003) High mobility group box chromosomal protein 1 plays a role in the pathogenesis of rheumatoid arthritis as a novel cytokine. Arthritis Rheum 48:971-981. (Pubitemid 36418239)
44. Tsung A, Sahai R, Tanaka H, Nakao A, Fink MP, Lotze MT, Yang H, Li J, Tracey KJ, Geller DA, et al. (2005) The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 201:1135-1143. (Pubitemid 40524681)
45. van der Worp HB, Kappelle LJ, Algra A, Bär PR, Orgogozo JM, Ringelstein EB, Bath PM, and van Gijn J (2002) The effect of tirilazad mesylate on infarct volume of patients with acute ischemic stroke. Neurology 58:133-135. (Pubitemid 34041952)
46. Wang CX and Shuaib A (2007) Neuroprotective effects of free radical scavengers in stroke. Drugs Aging 24:537-546. (Pubitemid 47195673)
47. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, et al. (1999) HMG-1 as a late mediator of endotoxin lethality in mice. Science 285:248-251. (Pubitemid 29329996)
48. Watanabe T, Morita I, Nishi H, and Murota S (1988) Preventive effect of MCI-186 on 15-HPETE induced vascular endothelial cell injury in vitro. Prostaglandins Leukot Essent Fatty Acids 33:81-87. (Pubitemid 18175123)
49. Watanabe T, Tanaka M, Watanabe K, Takamatsu Y, and Tobe A (2004) Research and development of the free radical scavenger edaravone as a neuroprotectant. Yakugaku Zasshi 124:99-111. (Pubitemid 41350513)
50. Wu DC, Ye W, Che XM, and Yang GY (2000) Activation of mitogen-activated protein kinases after permanent cerebral artery occlusion in mouse brain. J Cereb Blood Flow Metab 20:1320-1330.
51. Yamagishi S and Takeuchi M (2004) Nifedipine inhibits gene expression of receptor for advanced glycation end products (RAGE) in endothelial cells by suppressing reactive oxygen species generation. Drugs Exp Clin Res 30:169-175. (Pubitemid 39487685)
52. Yokota S, Kumagai Y, Uchiumi M, Isawa S, Murasaki M, Akimoto K, Iwamoto M, Yuasa T, and Iwano M (1997). A pharmacokinetic study of MCI-186, a novel drug for cerebrovascular disease in elderly and young healthy subjects. Jpn J Clin Pharmacol Ther 28:693-702.
53. Yung HW, Korolchuk S, Tolkovsky AM, Charnock-Jones DS, and Burton GJ (2007) Endoplasmic reticulum stress exacerbates ischemia-reperfusion-induced apoptosis through attenuation of Akt protein synthesis in human choriocarcinoma cells. FASEB J 21:872-884. (Pubitemid 46348260)
54. Zhang N, Komine-Kobayashi M, Tanaka R, Liu M, Mizuno Y, and Urabe T (2005) Edaravone reduces early accumulation of oxidative products and sequential inflammatory responses after transient focal ischemia in mice brain. Stroke 36:2220-2225. (Pubitemid 41429250)
55. Zhao Q, Wang X, Nelin LD, Yao Y, Matta R, Manson ME, Baliga RS, Meng X, Smith CV, Bauer JA, et al. (2006) MAP kinase phosphatase 1 controls innate immune responses and suppresses endotoxic shock. J Exp Med 203:131-140. (Pubitemid 43139652)