Edaravone protects rats and human pulmonary alveolar epithelial cells against hyperoxia injury: heme oxygenase-1 and PI3K/Akt pathway may be involved

REFERENCES

• Wispe JR, Roberts RJ: Molecular basis of pulmonary oxygen toxicity. Clin Perinatol. 1987;14:651–666.
   PubMed Web of Science ®Google Scholar
• Barazzone C, Horowitz S, Donati YR, Rodriguez I, Piguet PF: Oxygen toxicity in mouse lung. Pathways to cell death. Am J Respir Cell Mol Biol. 1998;19:573–581.
   PubMed Web of Science ®Google Scholar
• Saikumar P, Dong Z, Weinberg JM, Venkatachalam MA: Mechanisms of cell death in hypoxia/reoxygenation injury. Oncogene. 1998;17:3341–3349.
   PubMed Web of Science ®Google Scholar
• O'Reilly MA, Staversky RJ, Huyck HL, Watkins RH, LoMonaco MB, D'Angio CT, Baggs RB, Maniscalco WM, Pryhuber GS: Bcl-2 family gene expression during severe hyperoxia induced lung injury. Lab Invest. 2000;80:1845–1854.
   PubMed Web of Science ®Google Scholar
• Pace PW, Yao LJ, Wilson JX, Possmayer F, Veldhuizen RA, Lewis JF: The effects of hyperoxia exposure on lung function and pulmonary surfactant in a rat model of acute lung injury. Exp Lung Res. 2009;35:380–398.
   PubMed Web of Science ®Google Scholar
• Reddy NM, Kleeberger SR, Kensler TW, Yamamoto M, Hassoun PM, Reddy SP: Disruption of Nrf2 impairs the resolution of hyperoxia-induced acute lung injury and inflammation in mice. J Immunol. 2009;182:7264–7271.
   PubMed Web of Science ®Google Scholar
• Watanabe T, Tanaka M, Watanabe K, Takamatsu Y, Tobe A: Research and development of the free radical scavenger edaravone as a neuroprotectant. Yakugaku Zasshi. 2004;124:99–111.
   PubMed Web of Science ®Google Scholar
• Kaur C, Ling EA: Antioxidants and neuroprotection in the adult and developing central nervous system. Curr Med Chem. 2008;15:3068–3080.
   PubMed Web of Science ®Google Scholar
• Yoshida H, Yanai H, Namiki Y, Fukatsu-Sasaki K, Furutani N, Tada N: Neuroprotective effects of edaravone: a novel free radical scavenger in cerebrovascular injury. CNS Drug Rev. 2006;12:9–20.
   PubMedGoogle Scholar
• Wu Z, Ming Y, Zhang Z, Wu J, Wu Z, Yao S: Edaravone rescues the lung by inhibiting lipid peroxidation and pro-inflammatory cytokines in a rat model. Chin Med J (Engl). 2014;127:968–970.
   PubMed Web of Science ®Google Scholar
• Liu S, Li R, Ni X, Cai Z, Zhang R, Sun X, Quock RM, Xu W: Perfluorocarbon-facilitated CNS oxygen toxicity in rats. reversal by edaravone. Brain Res. 2012;1471:56–65.
   PubMed Web of Science ®Google Scholar
• Cheng B, Guo Y, Li C, Ji B, Pan Y, Chen J, Bai B: Edaravone protected PC12 cells against MPP(+)-cytoxicity via inhibiting oxidative stress and up-regulating heme oxygenase-1 expression. J Neurol Sci. 2014;343:115–9.
   PubMed Web of Science ®Google Scholar
• Wang C, Ye Z, Zheng J, Liu K, Sun X, Tao H, Liu W: Targeting reactive oxygen species by edaravone inhalation in a rat hyperoxic lung injury model. role of inflammasome. Undersea Hyperb Med. 2013;40:505–11.
   PubMed Web of Science ®Google Scholar
• Siner JM, Jiang G, Cohen ZI, Shan P, Zhang X, Lee CG, Elias JA, Lee PJ: VEGF-induced heme oxygenase-1 confers cytoprotection from lethal hyperoxia in vivo. FASEB J. 2007;21:1422–32.
   PubMed Web of Science ®Google Scholar
• Bai L, Pang WJ, Yang YJ, Yang GS: Modulation of Sirt1 by resveratrol and nicotinamide alters proliferation and differentiation of pig preadipocytes. Mol Cell Biochem. 2008;307:129–40.
   PubMed Web of Science ®Google Scholar
• Chang Y, Yang ST, Liu JH, Dong E, Wang Y, Cao A, Liu Y, Wang H: In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol Lett. 2011;200:201–210.
   PubMed Web of Science ®Google Scholar
• Ohkawa H, Ohishi N, Yagi K: Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95:351–358.
   PubMed Web of Science ®Google Scholar
• Valls-Belles V, Torres Mdel C, Boix L, Muñiz P, Gonzalez-Sanjose ML, Codoñer-Franch P: Alpha-Tocopherol, MDA-HNE and 8-OHdG levels in liver and heart mitochondria of adriamycin-treated rats fed with alcohol-free beer. Toxicology. 2008;249:97–101.
   PubMed Web of Science ®Google Scholar
• Tzaneva V, Perry SF: Heme oxygenase-1 (HO-1) mediated respiratory responses to hypoxia in the goldfish, Carassius auratus. Respir Physiol Neurobiol. 2014;199:1–8.
   PubMed Web of Science ®Google Scholar
• Slutsky AS: Lung injury caused by mechanical ventilation. Chest. 1999;116:9–15.
   PubMed Web of Science ®Google Scholar
• Buccellato LJ, Tso M, Akinci OI, Chandel NS, Budinger GR: Reactive oxygen species are required for hyperoxia-induced Bax activation and cell death in alveolar epithelial cells. J Biol Chem. 2004;279:6753–6760.
   PubMed Web of Science ®Google Scholar
• Freeman BA, Crapo JD: Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J Biol Chem. 1981;256:10986–10992.
   PubMed Web of Science ®Google Scholar
• Sanders SP, Zweier JL, Kuppusamy P, Harrison SJ, Bassett DJ, Gabrielson EW, Sylvester JT: Hyperoxic sheep pulmonary microvascular endothelial cells generate free radicals via mitochondrial electron transport. J Clin Invest. 1993;91: 46–52.
   PubMed Web of Science ®Google Scholar
• Zhang X, Shan P, Sasidhar M, Chupp GL, Flavell RA, Choi AM, Lee PJ: Reactive oxygen species and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase mediate hyperoxia-induced cell death in lung epithelium. Am J Respir Cell Mol Biol. 2003;28:305–15.
   PubMed Web of Science ®Google Scholar
• Parinandi NL, Kleinberg MA, Usatyuk PV, Cummings RJ, Pennathur A, Cardounel AJ, Zweier JL, Garcia JG, Natarajan V: Hyperoxia-induced NAD(P)H oxidase activation and regulation by MAP kinases in human lung endothelial cells. Am J Physiol Lung Cell Mol Physio. 2003;284:L26–L38.
   PubMed Web of Science ®Google Scholar
• Cacciuttolo MA, Trinh L, Lumpkin JA, Rao G: Hyperoxia induces DNA damage in mammalian cells. Free Radic Biol Med. 1993;14:267–276.
   PubMed Web of Science ®Google Scholar
• Barazzone C, White CW: Mechanisms of cell injury and death in hyperoxia: role of cytokines and Bcl-2 family proteins. Am J Respir Cell Mol Biol. 2000;22:517–519.
   PubMed Web of Science ®Google Scholar
• Zhang GL, Zhang WG, Du Y, Yao L, Sun H, Zhang R, Liu E, Bu N, Wu HQ, Zhang L, Li TT, Guo YY: Edaravone ameliorates oxidative damage associated with Aβ25–35 treatment in PC12 cells. J Mol Neurosci. 2013;50:494–503.
   PubMed Web of Science ®Google Scholar
• Roh MI, Murakami Y, Thanos A, Vavvas DG, Miller JW: Edaravone, an ROS scavenger, ameliorates photoreceptor cell death after experimental retinal detachment. Invest Ophthalmol Vis Sci. 2011;52:3825–3831.
   PubMed Web of Science ®Google Scholar
• Zhao ZY, Luan P, Huang SX, Xiao SH, Zhao J, Zhang B, Gu BB, Pi RB, Liu J: Edaravone protects HT22 neurons from H2O2-induced apoptosis by inhibiting the MAPK signaling pathway. CNS Neurosci Ther. 2013;19:163–169.
   PubMed Web of Science ®Google Scholar
• Xu JZ, Shen BZ, Li Y, Zhang T, Xu WH, Liu XW, Lu HG: Edaravone attenuates ischemia-reperfusion injury by inhibiting oxidative stress in a canine lung transplantation model. Chin Med J (Engl). 2008;121:1583–1587.
   PubMed Web of Science ®Google Scholar
• Ryu MJ, Kang KA, Piao MJ, Kim KC, Zheng J, Yao CW, Cha JW, Hyun CL, Chung HS, Park JC, Cho SJ, Hyun JW: Effect of 7, 8-dihydroxyflavone on the up-regulation of Nrf2-mediated heme oxygenase-1 expression in hamster lung fibroblasts. In Vitro Cell Dev Biol Anim. 2014;50:549–554.
   PubMed Web of Science ®Google Scholar
• Namba F, Go H, Murphy JA, La P, Yang G, Sengupta S: Expression level and subcellular localization of heme oxygenase-1 modulates its cytoprotective properties in response to lung injury: a mouse model. PLoS One. 2014;9:e90936.
   PubMed Web of Science ®Google Scholar
• Liu K, Chen HL, Huang H, Jing H, Dong GH, Wu HW, You QS: Curcumin attenuates cardiopulmonary bypass-induced lung oxidative damage in rats. J Cardiovasc Pharmacol Ther. 2012;17:395–402.
   PubMed Web of Science ®Google Scholar
• Deng X, Rui W, Zhang F, Ding W: PM2.5 induces Nrf2-mediated defense mechanisms against oxidative stress by activating PIK3/AKT signaling pathway in human lung alveolar epithelial A549 cells. Cell Biol Toxicol. 2013;29:143–157.
   PubMed Web of Science ®Google Scholar
• Zhang T, Liang X, Shi L, Wang L, Chen J, Kang C, Zhu J, Mi M: Estrogen receptor and PI3K/Akt signaling pathway involvement in S-(−)equol-induced activation of Nrf2/ARE in endothelial cells. PLoS One. 2013;8:e79075.
   PubMed Web of Science ®Google Scholar
• Toker A, Cantley LC: Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature. 1997;387:673–676.
   PubMed Web of Science ®Google Scholar
• Seo GS, Jiang WY, Park PH, Sohn DH, Cheon JH, Lee SH: Hirsutenone reduces deterioration of tight junction proteins through EGFR/Akt and ERK1/2 pathway both converging to HO-1 induction. Biochem Pharmacol. 2014;90: 115–125.
   PubMed Web of Science ®Google Scholar
• Lu CY, Yang YC, Li CC, Liu KL, Lii CK, Chen HW: Andrographolide inhibits TNFα-induced ICAM-1 expression via suppression of NADPH oxidase activation and induction of HO-1 and GCLM expression through the PI3K/Akt/Nrf2 and PI3K/Akt/AP-1 pathways in human endothelial cells. Biochem Pharmacol. 2014;91:40–50.
   PubMed Web of Science ®Google Scholar
• Ryu MJ, Kang KA, Piao MJ, Kim KC, Zheng J, Yao CW, Cha JW, Chung HS, Kim SC, Jung E, Park D, Chae S, Hyun JW: 7,8-Dihydroxyflavone protects human keratinocytes against oxidative stress-induced cell damage via the ERK and PI3K/Akt-mediated Nrf2/HO-1 signaling pathways. Int J Mol Med. 2014;33:964–970.
   PubMed Web of Science ®Google Scholar
• Kim KM, Song JD, Chung HT, Park YC: Protein kinase CK2 mediates peroxynitrite-induced heme oxygenase-1 expression in articular chondrocytes. Int J Mol Med. 2012;29: 1039–1044.
   PubMed Web of Science ®Google Scholar
• Kim SG, Kim SO: PKC downstream of Pl3-kinase regulates peroxynitrite formation for Nrf2-mediated GSTA2 induction. Arch Pharm Res. 2004;27:757–762.
   PubMed Web of Science ®Google Scholar
• Kang KW, Lee S J, Kim SG: Molecular mechanism of nrf2 activation by oxidative stress. Antioxid Redox Signal. 2005;7:1664–1673.
   PubMed Web of Science ®Google Scholar
• Yoshida H, Yanai H, Namiki Y, Fukatsu-Sasaki K, Furutani N, Tada N: Neuroprotective effects of edaravone: a novel free radical scavenger in cerebrovascular injury. CNS Drug Rev. 2006 Spring;12:9–20.
   PubMedGoogle Scholar
• Lamoke F, Mazzone V, Persichini T, Maraschi A, Harris MB, Venema RC, Colasanti M, Gliozzi M, Muscoli C, Bartoli M, Mollace V: Amyloid β peptide-induced inhibition of endothelial nitric oxide production involves oxidative stress-mediated constitutive eNOS/HSP90 interaction and disruption of agonist-mediated Akt activation. J Neuroinflammation. 2015;12:84.
   PubMed Web of Science ®Google Scholar
• Koike A, Minamiguchi I, Fujimori K, Amano F: Nitric oxide is an important regulator of heme oxygenase-1 expression in the lipopolysaccharide and interferon-γ-treated murine macrophage-like cell line J774.1/JA-4. Biol Pharm Bull. 2015;38:7–16.
   PubMed Web of Science ®Google Scholar
• Uchiyama M, Tojo K, Yazawa T, Ota S, Goto T, Kurahashi K: Edaravone prevents lung injury induced by hepatic ischemia-reperfusion. J Surg Res. 2015;194:551–557.
   PubMed Web of Science ®Google Scholar
• Wang Z, Li R, Liu Y, Liu X, Chen W, Xu S, Guo Y, Duan J, Chen Y, Wang C: Protective effects of edaravone combined puerarin on inhalation lung injury induced by black gunpowder smog. Int Immunopharmacol. 2015;26:125–132.
   PubMed Web of Science ®Google Scholar
• Yang T, Zhang J, Sun L, Zhu X, Li J, Wang J, Chen H, Bao R, Deng X, Hou J, Liu Y: Combined effects of a neutrophil elastase inhibitor (sivelestat sodium) and a free radical scavenger (edaravone) on lipopolysaccharide-induced acute lung injury in rats. Inflamm Res. 2012;61:563–569.
   PubMed Web of Science ®Google Scholar
• Cheng ZQ, Han JY, Sun P, Weng YY, Chen J, Wu GY, Ma HX: Edaravone attenuates paraquat-induced lung injury by inhibiting oxidative stress in human type II alveolar epithelial cells. World J Emerg Med. 2012;3:55–59.
   PubMedGoogle Scholar