Suppression of NADPH oxidase- and mitochondrion-derived superoxide by Notoginsenoside R1 protects against cerebral ischemia–reperfusion injury through estrogen receptor-dependent activation of Akt/Nrf2 pathways

References

• Goldstein LB, Adams R, Alberts MJ, Appel LJ, Brass LM, Bushnell CD, et al. Primary prevention of ischemic stroke: a guideline from the American Heart Association/American Stroke Association Stroke Council: cosponsored by the Atherosclerotic Peripheral Vascular Disease Interdisciplinary Working Group; Cardiovascular Nursing Council; Clinical Cardiology Council; Nutrition, Physical Activity, and Metabolism Council; and the Quality of Care and Outcomes Research Interdisciplinary Working Group: the American Academy of Neurology affirms the value of this guideline. Stroke 2006;37:1583–1633.
   PubMed Web of Science ®Google Scholar
• Donnan GA, Fisher M, Macleod M, Davis SM. Stroke. Lancet 2008;371:1612–1623.
   PubMed Web of Science ®Google Scholar
• Rodrigo R, Fernandez-Gajardo R, Gutierrez R, Matamala JM, Carrasco R, Miranda-Merchak A, Feuerhake W. Oxidative stress and pathophysiology of ischemic stroke: novel therapeutic opportunities. CNS Neurol Disord Drug Targets 2013;12: 698–714.
   PubMed Web of Science ®Google Scholar
• O’Collins VE, Macleod MR, Donnan GA, Horky LL, van der Worp BH, Howells DW. 1,026 experimental treatments in acute stroke. Ann Neurol 2006;59:467–477.
   PubMed Web of Science ®Google Scholar
• Radermacher KA, Wingler K, Kleikers P, Altenhöfer S, Jr Hermans J, Kleinschnitz C, Hhw Schmidt H. The 1027th target candidate in stroke: Will NADPH oxidase hold up?. Exp Transl Stroke Med 2012;4:11.
   PubMedGoogle Scholar
• Moskowitz MA, Lo EH, Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron 2010;67: 181–198.
   PubMed Web of Science ®Google Scholar
• Serrano-Pozo A, Frosch MP, Masliah E, Hyman BT. Neuropathological alterations in Alzheimer disease. Cold Spring Harb Perspect Med 2011;1:a006189.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Li HQ, Lu L, Fu DL, Liu AJ, Li JH, Zheng GQ. Ginsenoside Rg1 provides neuroprotection against blood brain barrier disruption and neurological injury in a rat model of cerebral ischemia/reperfusion through downregulation of aquaporin 4 expression. Phytomedicine 2014. doi:10.1016/j.phymed.2013.12.005.
   Google Scholar
• Lu T, Jiang Y, Zhou Z, Yue X, Wei N, Chen Z, et al. Intranasal ginsenoside Rb1 targets the brain and ameliorates cerebral ischemia/reperfusion injury in rats. Biol Pharm Bull 2011;34:1319–1324.
   PubMed Web of Science ®Google Scholar
• Zhang HS, Wang SQ. Notoginsenoside R1 inhibits TNF-alpha-induced fibronectin production in smooth muscle cells via the ROS/ERK pathway. Free Radic Biol Med 2006;40:1664–1674.
   PubMed Web of Science ®Google Scholar
• Zhang HS, Wang SQ. Notoginsenoside R1 from Panax notoginseng inhibits TNF-alpha-induced PAI-1 production in human aortic smooth muscle cells. Vascul Pharmacol 2006; 44:224–230.
   PubMed Web of Science ®Google Scholar
• Gu B, Nakamichi N, Zhang WS, Nakamura Y, Kambe Y, Fukumori R, et al. Possible protection by notoginsenoside R1 against glutamate neurotoxicity mediated by N-methyl-D-aspartate receptors composed of an NR1/NR2B subunit assembly. J Neurosci Res 2009;87:2145–2156.
   PubMed Web of Science ®Google Scholar
• Meng X, Sun G, Ye J, Xu H, Wang H, Sun X. Notoginsenoside R1-mediated neuroprotection involves estrogen receptor-dependent crosstalk between Akt and ERK1/2 pathways: a novel mechanism of Nrf2/ARE signaling activation. Free Radic Res 2014;48:445–460.
   PubMed Web of Science ®Google Scholar
• Taille C, El-Benna J, Lanone S, Dang MC, Ogier-Denis E, Aubier M, Boczkowski J. Induction of heme oxygenase-1 inhibits NAD(P)H oxidase activity by down-regulating cytochrome b558 expression via the reduction of heme availability. J Biol Chem 2004;279:28681–28688.
   PubMed Web of Science ®Google Scholar
• Chen K, Gunter K, Maines MD. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J Neurochem 2000;75:304–313.
   PubMed Web of Science ®Google Scholar
• Datla SR, Dusting GJ, Mori TA, Taylor CJ, Croft KD, Jiang F. Induction of heme oxygenase-1 in vivo suppresses NADPH oxidase derived oxidative stress. Hypertension 2007;50:636–642.
   PubMed Web of Science ®Google Scholar
• Rupadevi M, Parasuraman S, Raveendran R. Protocol for middle cerebral artery occlusion by an intraluminal suture method. J Pharmacol Pharmacother 2011;2:36–39.
   PubMedGoogle Scholar
• Aziz MT, Al-Asmar MF, Mostafa T, Atta H, Rashed L, Sabry D, et al. Assessment of heme oxygenase-1 (HO-1) activity in the cavernous tissues of sildenafil citrate-treated rats. Asian J Androl 2007;9:377–381.
   PubMed Web of Science ®Google Scholar
• Wang YH, Du GH. Ginsenoside Rg1 inhibits beta-secretase activity in vitro and protects against Abeta-induced cytotoxicity in PC12 cells. J Asian Nat Prod Res 2009;11:604–612.
   PubMed Web of Science ®Google Scholar
• Weston RM, Lin B, Dusting GJ, Roulston CL. Targeting oxidative stress injury after ischemic stroke in conscious rats: limited benefits with apocynin highlight the need to incorporate long term recovery. Stroke Res Treat 2013;2013:648061.
   PubMedGoogle Scholar
• Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007;35:495–516.
   PubMed Web of Science ®Google Scholar
• Manzanero S, Santro T, Arumugam TV. Neuronal oxidative stress in acute ischemic stroke: sources and contribution to cell injury. Neurochem Int 2013;62:712–718.
   PubMed Web of Science ®Google Scholar
• Olmez I, Ozyurt H. Reactive oxygen species and ischemic cerebrovascular disease. Neurochem Int 2012;60:208–212.
   PubMed Web of Science ®Google Scholar
• Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 2009;7:65–74.
   PubMed Web of Science ®Google Scholar
• Wingler K, Hermans JJ, Schiffers P, Moens A, Paul M, Schmidt HH. NOX1, 2, 4, 5: counting out oxidative stress. Br J Pharmacol 2011;164:866–883.
   PubMed Web of Science ®Google Scholar
• Cos P, De Bruyne T, Apers S, Vanden Berghe D, Pieters L, Vlietinck AJ. Phytoestrogens: recent developments. Planta Med 2003;69:589–599.
   PubMed Web of Science ®Google Scholar
• Kusaka I, Kusaka G, Zhou C, Ishikawa M, Nanda A, Granger DN, et al. Role of AT1 receptors and NAD(P)H oxidase in diabetes-aggravated ischemic brain injury. Am J Physiol Heart Circ Physiol 2004;286:H2442–H2451.
   Web of Science ®Google Scholar
• Alfieri A, Srivastava S, Siow RC, Modo M, Fraser PA, Mann GE. Targeting the Nrf2-Keap1 antioxidant defence pathway for neurovascular protection in stroke. J Physiol 2011;589:4125–4136.
   PubMed Web of Science ®Google Scholar
• Kanninen K, White AR, Koistinaho J, Malm T. Targeting glycogen synthase kinase-3beta for therapeutic benefit against oxidative stress in Alzheimer's disease: involvement of the Nrf2-ARE pathway. Int J Alzheimers Dis 2011;2011:985085.
   PubMedGoogle Scholar
• Salazar M, Rojo AI, Velasco D, de Sagarra RM, Cuadrado A. Glycogen synthase kinase-3beta inhibits the xenobiotic and antioxidant cell response by direct phosphorylation and nuclear exclusion of the transcription factor Nrf2. J Biol Chem 2006;281:14841–14851.
   PubMed Web of Science ®Google Scholar
• Chen CS, Tseng YT, Hsu YY, Lo YC. Nrf2-Keap1 antioxidant defense and cell survival signaling are upregulated by 17beta-estradiol in homocysteine-treated dopaminergic SH-SY5Y cells. Neuroendocrinology 2013;97:232–241.
   PubMed Web of Science ®Google Scholar