Temporal activation of Nrf2 in the penumbra and Nrf2 activator-mediated neuroprotection in ischemia-reperfusion injury

Free Radical Biology and Medicine

Volumn 72, Issue , 2014, Pages 124-133

  Takagi, Toshinori ^a,b   Kitashoji, Akira ^a   Iwawaki, Takao ^c   Tsuruma, Kazuhiro ^a   Shimazawa, Masamitsu ^a   Yoshimura, Shinichi ^b   Iwama, Toru ^b   Hara, Hideaki ^a  

^a GIFU PHARMACEUTICAL UNIVERSITY   (Japan)

^b GIFU UNIVERSITY   (Japan)

^c GUNMA UNIVERSITY   (Japan)

Author keywords

Bardoxolone methyl; Free radicals; Ischemia reperfusion injury; Neuroprotection; Nrf2; Oxidative stress

Indexed keywords

BARDOXOLONE METHYL; HEME OXYGENASE 1; TRANSCRIPTION FACTOR NRF2; METHYL 2-CYANO-3,12-DIOXOOLEAN-1,9-DIEN-28-OATE; NEUROPROTECTIVE AGENT; OLEANOLIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN ISCHEMIA; CONTROLLED STUDY; HUMAN; IMMUNOHISTOCHEMISTRY; LUCIFERASE ASSAY; MALE; MOUSE; NERVE CELL; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; UPREGULATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; IMMUNOPRECIPITATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; BLOTTING, WESTERN; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; NEUROPROTECTIVE AGENTS; NF-E2-RELATED FACTOR 2; OLEANOLIC ACID; OXIDATIVE STRESS; REPERFUSION INJURY;

EID: 84900505499     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.04.009     Document Type: Article

References (39)

1. G.A. Donnan, M. Fisher, M. Macleod, and S.M. Davis Stroke. Lancet 371 2008 1612 1623
2. E.C. Jauch, J.L. Saver, H.P. Adams Jr, A. Bruno, J.J. Connors, B.M. Demaerschalk, P. Khatri, P.W. McMullan Jr, A.I. Qureshi, K. Rosenfield, P.A. Scott, D.R. Summers, D.Z. Wang, M. Wintermark, and H. Yonas Guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association Stroke 44 2013 870 947
3. J.L. Saver, R. Jahan, E.I. Levy, T.G. Jovin, B. Baxter, R.G. Nogueira, W. Clark, R. Budzik, and O.O. Zaidat Solitaire flow restoration device versus the Merci Retriever in patients with acute ischaemic stroke (SWIFT): a randomised, parallel-group, non-inferiority trial Lancet 380 2012 1241 1249
4. J.E. Jung, G.S. Kim, H. Chen, C.M. Maier, P. Narasimhan, Y.S. Song, K. Niizuma, M. Katsu, N. Okami, H. Yoshioka, H. Sakata, C.E. Goeders, and P.H. Chan Reperfusion and neurovascular dysfunction in stroke: from basic mechanisms to potential strategies for neuroprotection Mol. Neurobiol. 41 2010 172 179
5. A. Alfieri, S. Srivastava, R.C. Siow, M. Modo, P.A. Fraser, and G.E. Mann Targeting the Nrf2-Keap1 antioxidant defence pathway for neurovascular protection in stroke J. Physiol. 589 2011 4125 4136
6. M. Christophe, and S. Nicolas Mitochondria: a target for neuroprotective interventions in cerebral ischemia-reperfusion Curr. Pharm. Des. 12 2006 739 757
7. S. Cuzzocrea, D.P. Riley, A.P. Caputi, and D. Salvemini Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury Pharmacol. Rev. 53 2001 135 159
8. D.N. Granger, M.E. Hollwarth, and D.A. Parks Ischemia-reperfusion injury: role of oxygen-derived free radicals Acta Physiol. Scand. Suppl. 548 1986 47 63
9. P.H. Chan Role of oxidants in ischemic brain damage Stroke 27 1996 1124 1129
10. K. Irani Oxidant signaling in vascular cell growth, death, and survival: a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptotic signaling Circ. Res. 87 2000 179 183
11. T. Ishii, K. Itoh, S. Takahashi, H. Sato, T. Yanagawa, Y. Katoh, S. Bannai, and M. Yamamoto Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages J. Biol. Chem. 275 2000 16023 16029
12. J.W. Kaspar, S.K. Niture, and A.K. Jaiswal Nrf2:INrf2 (Keap1) signaling in oxidative stress Free Radic. Biol. Med. 47 2009 1304 1309
13. A.Y. Shih, D.A. Johnson, G. Wong, A.D. Kraft, L. Jiang, H. Erb, J.A. Johnson, and T.H. Murphy Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress J. Neurosci. 23 2003 3394 3406
14. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J.D. Engel, and M. Yamamoto Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev. 13 1999 76 86
15. M. McMahon, K. Itoh, M. Yamamoto, and J.D. Hayes Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression J. Biol. Chem. 278 2003 21592 21600
16. W.D. Holtzclaw, A.T. Dinkova-Kostova, and P. Talalay Protection against electrophile and oxidative stress by induction of phase 2 genes: the quest for the elusive sensor that responds to inducers Adv. Enzyme Regul. 44 2004 335 367
17. A. Kobayashi, T. Ohta, and M. Yamamoto Unique function of the Nrf2-Keap1 pathway in the inducible expression of antioxidant and detoxifying enzymes Methods Enzymol. 378 2004 273 286
18. H. Motohashi, and M. Yamamoto Nrf2-Keap1 defines a physiologically important stress response mechanism Trends Mol. Med. 10 2004 549 557
19. R. Stocker, Y. Yamamoto, A.F. McDonagh, A.N. Glazer, and B.N. Ames Bilirubin is an antioxidant of possible physiological importance Science 235 1987 1043 1046
20. M. Li, X. Zhang, L. Cui, R. Yang, L. Wang, L. Liu, and W. Du The neuroprotection of oxymatrine in cerebral ischemia/reperfusion is related to nuclear factor erythroid 2-related factor 2 (nrf2)-mediated antioxidant response: role of nrf2 and hemeoxygenase-1 expression Biol. Pharm. Bull. 34 2011 595 601
21. A.Y. Shih, P. Li, and T.H. Murphy A small-molecule-inducible Nrf2-mediated antioxidant response provides effective prophylaxis against cerebral ischemia in vivo J. Neurosci. 25 2005 10321 10335
22. F. Zhang, S. Wang, M. Zhang, Z. Weng, P. Li, Y. Gan, L. Zhang, G. Cao, Y. Gao, R.K. Leak, M.B. Sporn, and J. Chen Pharmacological induction of heme oxygenase-1 by a triterpenoid protects neurons against ischemic injury Stroke 43 2012 1390 1397
23. P.E. Pergola, P. Raskin, R.D. Toto, C.J. Meyer, J.W. Huff, E.B. Grossman, M. Krauth, S. Ruiz, P. Audhya, H. Christ-Schmidt, J. Wittes, and D.G. Warnock Bardoxolone methyl and kidney function in CKD with type 2 diabetes N. Engl. J. Med. 365 2011 327 336
24. N. Tanaka, Y. Ikeda, Y. Ohta, K. Deguchi, F. Tian, J. Shang, T. Matsuura, and K. Abe Expression of Keap1-Nrf2 system and antioxidative proteins in mouse brain after transient middle cerebral artery occlusion Brain Res. 1370 2011 246 253
25. J. Dang, L.O. Brandenburg, C. Rosen, A. Fragoulis, M. Kipp, T. Pufe, C. Beyer, and C.J. Wruck Nrf2 expression by neurons, astroglia, and microglia in the cerebral cortical penumbra of ischemic rats J. Mol. Neurosci. 46 2012 578 584
26. D. Oikawa, R. Akai, M. Tokuda, and T. Iwawaki A transgenic mouse model for monitoring oxidative stress Sci. Rep. 2 2012 229
27. Y. Kotani, Y. Nakajima, T. Hasegawa, M. Satoh, H. Nagase, M. Shimazawa, S. Yoshimura, T. Iwama, and H. Hara Propofol exerts greater neuroprotection with disodium edetate than without it J. Cereb. Blood Flow Metab. 28 2008 354 366
28. M. Lalancette-Hebert, D. Phaneuf, G. Soucy, Y.C. Weng, and J. Kriz Live imaging of Toll-like receptor 2 response in cerebral ischaemia reveals a role of olfactory bulb microglia as modulators of inflammation Brain 132 2009 940 954
29. J. Stohr, J.C. Watts, Z.L. Mensinger, A. Oehler, S.K. Grillo, S.J. DeArmond, S.B. Prusiner, and K. Giles Purified and synthetic Alzheimer's amyloid beta (Abeta) prions Proc. Natl. Acad. Sci. USA 109 2012 11025 11030
30. J.J. Auletta, J.L. Alabran, B.G. Kim, C.J. Meyer, and J.J. Letterio The synthetic triterpenoid, CDDO-Me, modulates the proinflammatory response to in vivo lipopolysaccharide challenge J. Interferon Cytokine Res. 30 2010 497 508
31. J.H. Garcia, S. Wagner, K.F. Liu, and X.J. Hu Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats: statistical validation Stroke 26 1995 627 634 (discussion 635)
32. S. Lee, M. Ueno, and T. Yamashita Axonal remodeling for motor recovery after traumatic brain injury requires downregulation of gamma-aminobutyric acid signaling Cell Death Dis. 2 2011 e133
33. S.E. Lakhan, A. Kirchgessner, and M. Hofer Inflammatory mechanisms in ischemic stroke: therapeutic approaches J. Transl. Med. 7 2009 97
34. T.W. Kensler, N. Wakabayashi, and S. Biswal Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway Annu. Rev. Pharmacol. Toxicol. 47 2007 89 116
35. S. Srivastava, A. Alfieri, R.C. Siow, G.E. Mann, and P.A. Fraser Temporal and spatial distribution of Nrf2 in rat brain following stroke: quantification of nuclear to cytoplasmic Nrf2 content using a novel immunohistochemical technique J. Physiol. 591 2013 3525 3538
36. T. Ichikawa, J. Li, C.J. Meyer, J.S. Janicki, M. Hannink, and T. Cui Dihydro-CDDO-trifluoroethyl amide (dh404), a novel Nrf2 activator, suppresses oxidative stress in cardiomyocytes PLoS One 4 2009 e8391
37. Y. Li, J.D. Paonessa, and Y. Zhang Mechanism of chemical activation of Nrf2 PLoS One 7 2012 e35122
38. Y. Miao, Y. Qiu, Y. Lin, Z. Miao, J. Zhang, and X. Lu Protection by pyruvate against glutamate neurotoxicity is mediated by astrocytes through a glutathione-dependent mechanism Mol. Biol. Rep. 38 2011 3235 3242
39. G. Barreto, R.E. White, Y. Ouyang, L. Xu, and R.G. Giffard Astrocytes: targets for neuroprotection in stroke Cent. Nerv. Syst. Agents Med. Chem 11 2011 164 173